Access to this full-text is provided by Frontiers.
Content available from Frontiers in Plant Science
This content is subject to copyright.
fpls-08-00172 February 8, 2017 Time: 16:13 # 1
REVIEW
published: 09 February 2017
doi: 10.3389/fpls.2017.00172
Edited by:
Raquel Esteban,
University of the Basque Country,
Spain
Reviewed by:
Rudra Deo Tripathi,
National Botanical Research Institute
(CSIR), India
Zhenzhu Xu,
Institute of Botany (CAS), China
*Correspondence:
Kamlesh K. Meena
kkmeenamicro@gmail.com
†These authors have combined first
authors.
Specialty section:
This article was submitted to
Functional Plant Ecology,
a section of the journal
Frontiers in Plant Science
Received: 07 September 2016
Accepted: 27 January 2017
Published: 09 February 2017
Citation:
Meena KK, Sorty AM, Bitla UM,
Choudhary K, Gupta P, Pareek A,
Singh DP, Prabha R, Sahu PK,
Gupta VK, Singh HB, Krishanani KK
and Minhas PS (2017) Abiotic Stress
Responses and Microbe-Mediated
Mitigation in Plants: The Omics
Strategies. Front. Plant Sci. 8:172.
doi: 10.3389/fpls.2017.00172
Abiotic Stress Responses and
Microbe-Mediated Mitigation in
Plants: The Omics Strategies
Kamlesh K. Meena1*†, Ajay M. Sorty1†, Utkarsh M. Bitla1, Khushboo Choudhary1,
Priyanka Gupta2, Ashwani Pareek2, Dhananjaya P. Singh3, Ratna Prabha3,
Pramod K. Sahu3, Vijai K. Gupta4,5 , Harikesh B. Singh6, Kishor K. Krishanani1and
Paramjit S. Minhas1
1Department of Microbiology, School of Edaphic Stress Management, National Institute of Abiotic Stress Management,
Indian Council of Agricultural Research, Baramati, India, 2Stress Physiology and Molecular Biology Laboratory, School of Life
Sciences, Jawaharlal Nehru University, New Delhi, India, 3Department of Biotechnology, National Bureau of Agriculturally
Important Microorganisms, Indian Council of Agricultural Research, Kushmaur, India, 4Molecular Glyco-Biotechnology
Group, Discipline of Biochemistry, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland,
5Department of Chemistry and Biotechnology, ERA Chair of Green Chemistry, School of Science, Tallinn University of
Technology, Tallinn, Estonia, 6Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu
University, Varanasi, India
Abiotic stresses are the foremost limiting factors for agricultural productivity. Crop
plants need to cope up adverse external pressure created by environmental and
edaphic conditions with their intrinsic biological mechanisms, failing which their growth,
development, and productivity suffer. Microorganisms, the most natural inhabitants
of diverse environments exhibit enormous metabolic capabilities to mitigate abiotic
stresses. Since microbial interactions with plants are an integral part of the living
ecosystem, they are believed to be the natural partners that modulate local and systemic
mechanisms in plants to offer defense under adverse external conditions. Plant–
microbe interactions comprise complex mechanisms within the plant cellular system.
Biochemical, molecular and physiological studies are paving the way in understanding
the complex but integrated cellular processes. Under the continuous pressure of
increasing climatic alterations, it now becomes more imperative to define and interpret
plant–microbe relationships in terms of protection against abiotic stresses. At the same
time, it also becomes essential to generate deeper insights into the stress-mitigating
mechanisms in crop plants for their translation in higher productivity. Multi-omics
approaches comprising genomics, transcriptomics, proteomics, metabolomics and
phenomics integrate studies on the interaction of plants with microbes and their
external environment and generate multi-layered information that can answer what
is happening in real-time within the cells. Integration, analysis and decipherization
of the big-data can lead to a massive outcome that has significant chance for
implementation in the fields. This review summarizes abiotic stresses responses in plants
in-terms of biochemical and molecular mechanisms followed by the microbe-mediated
stress mitigation phenomenon. We describe the role of multi-omics approaches
in generating multi-pronged information to provide a better understanding of
Frontiers in Plant Science | www.frontiersin.org 1February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 2
Meena et al. Microbe-Mediated Management of Abiotic Stress
plant–microbe interactions that modulate cellular mechanisms in plants under extreme
external conditions and help to optimize abiotic stresses. Vigilant amalgamation of these
high-throughput approaches supports a higher level of knowledge generation about
root-level mechanisms involved in the alleviation of abiotic stresses in organisms.
Keywords: abiotic stress, genomics, metabolomics, microbes, multi-omics, plant–microbe interactions
INTRODUCTION
Adverse climatic conditions creating abiotic stresses are among
the principal limiting factors for decline in agricultural
productivity (Padgham, 2009;Grayson, 2013). As per the FAO
report (2007), only 3.5% of the global land area has left
unaffected by any environmental constraint1. Dominant abiotic
stresses comprise drought, low/high temperature, salinity and
acidic conditions, light intensity, submergence, anaerobiosis and
nutrient starvation (Wang et al., 2003;Chaves and Oliveira,
2004;Agarwal and Grover, 2006;Nakashima and Yamaguchi-
Shinozaki, 2006;Hirel et al., 2007;Bailey-Serres and Voesenek,
2008). Water deficit (drought) has affected 64% of the global
land area, flood (anoxia) 13% of the land area, salinity 6%,
mineral deficiency 9%, acidic soils 15% and, cold 57% (Mittler,
2006;Cramer et al., 2011). Out of the world’s 5.2 billion ha of
dryland agriculture, 3.6 billion ha is affected by the problems
of erosion, soil degradation and salinity (Riadh et al., 2010).
Ruan et al. (2010) estimated salt affected soils to impact upon
50% of total irrigated land in the world costing US$12 billion
in terms of loss (Flowers et al., 2010). Similarly, global annual
cost of land degradation by salinity in irrigated lands could
be US$ 27.3 billion due to loss in crop production (Qadir
et al., 2014). The detrimental effect of salinity on plant growth
is well established. The area under ever-increasing salinization
has almost reached 34 million irrigated hectares (FAO, 2012)2.
Although any accurate estimation of agricultural loss (reduction
of crop production and soil health) in terms of agro-ecological
disturbances due to abiotic stresses could not be made, it is
evident that such stresses affect large land areas and significantly
impact qualitative and quantitative loss in crop production
(Cramer et al., 2011).
Plants frequently cope up with the rapid fluctuations and
adversity of environmental conditions because of their intrinsic
metabolic capabilities (Simontacchi et al., 2015). Variations in
the outside environment could put the plant metabolism out
of homeostasis (Foyer and Noctor, 2005), and create necessity
for the plant to harbor some advanced genetic and metabolic
mechanisms within its cellular system (Apel and Hirt, 2004;
Gill and Tuteja, 2010). Plants possess an array of protective
mechanisms acquired during the course of evolution to combat
adverse environmental situations (Yolcu et al., 2016). Such
mechanisms cause metabolic re-programming in the cells (Heil
and Bostock, 2002;Swarbrick et al., 2006;Shao et al., 2008;
Bolton, 2009;Massad et al., 2012) to facilitate routine bio-
physico-chemical processes irrespective of the external situations
1http://www.fao.org/docrep/010/a1075e/a1075e00.htm
2http://www.fao.org/docrep/meeting/024/md324e.pdf
(Mickelbart et al., 2015). Many times plants get facilitated in
reducing the burden of environmental stresses with the support
of the microbiome they inhabit (Turner et al., 2013a;Ngumbi and
Kloepper, 2014).
Microbial life is the most fundamental and live system
on the earth. Being important living component of the soils,
they naturally become integral part of the crop production
system as soon as a seed comes into the soil to start
its life cycle. Microorganisms are important inhabitants of
seeds also, and proliferate as the seeds grow in the soils
to form symbiotic associations at the surface or endophytic
interactions inside the roots, stems or leaves. Plant microbiome
provides fundamental support to the plants in acquiring
nutrients, resisting against diseases and tolerating abiotic
stresses (Turner et al., 2013a). Microbial intrinsic metabolic
and genetic capabilities make them suitable organisms to
combat extreme conditions of the environment (Sessitsch
et al., 2012;Singh et al., 2014). Their interactions with the
plants evoke various kinds of local and systemic responses
that improve metabolic capability of the plants to fight
against abiotic stresses (Nguyen et al., 2016). A testament
to the important attributes of the microbial interactions
with plants is significant number of accumulating pieces
of evidence that suggest in-depth mechanisms based on
plant–microbe interactions that offer modulation of cellular,
biochemical and molecular mechanisms connected with stress
tolerance (Bakker et al., 2012;Onaga and Wydra, 2016).
Growing interest in uncultured microbes, especially from the
rhizosphere of the crop plants, depleted and degraded soils,
soils with disturbed fertility status and endophytic communities
that potentially represent ‘obligate endophytes’ inhabiting
plant tissues deciphered multi-phasic functions associated
with the stress tolerance in microbial communities. The
advent of next-generation sequencing (NGS) facilities supported
gradually increasing metagenomic work and consequently led
to the accumulation of greater amount of data for functional
characterization of microbial communities in the soils (Bulgarelli
et al., 2012).
Work on plant–microbe interactions at biochemical,
physiological and molecular levels established that microbial
associations largely direct plant responses toward stresses (Farrar
et al., 2014). For dissecting deeper interaction mechanisms
and connecting the changes at molecular levels with the
tolerance responses against stresses, biological data based
on the multi-omics approaches were generated (Kissoudis
et al., 2014). The data generation and analysis was supported
by the advancements in the high-end instrumentation and
computational integration which helped to decipher individual
signal molecules, proteins, genes and gene cascades to connect
Frontiers in Plant Science | www.frontiersin.org 2February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 3
Meena et al. Microbe-Mediated Management of Abiotic Stress
them with the gene networks/pathways for their function
description. Technological developments also facilitated
understanding of gene editing systems, RNAi-mediated
gene silencing, mutant technology, proteomic analysis
and metabolite profiling to reveal voluminous molecular
information that helped in improving our understanding of
microbe-mediated mitigation strategies of abiotic stresses
in plants (Yin et al., 2014;Luan et al., 2015). Multi-omics
approaches have emerged as a holistic and integrated analytical
strategies for the dissection of one of the most complex and
dynamic living system of microbial interactions with plants
and modulating the consequences developed in the plants
to help them overcome stresses. In this review, we aim at
summarizing the implications of abiotic stresses and plant
responses generated thereafter in terms of biochemical and
molecular mechanisms followed by the microbe-mediated
stress mitigation processes. We further describe the role of
multi-omics approaches in establishing understanding of
plant–microbe interactions that help plants optimize abiotic
stresses.
HOW DO ABIOTIC STRESSES AFFECT
PLANTS?
Plants need light, water, carbon and mineral nutrients for
their optimal growth, development and reproduction. Extreme
conditions (below or above the optimal levels) limit plant growth
and development. An unfavorable environment comprising
extreme high or low of temperature, salinity and drought
pose a complex set of stress conditions. Plants can sense and
react to stresses in many ways that favor their sustenance
(Crane et al., 2011;Ahmad et al., 2015;Jiang et al., 2016).
They remember past exposure to abiotic stresses and even
mechanisms to overcome them in such a way that responses
to repeated stresses can be modified accordingly (Hilker et al.,
2015). However, the underlying molecular mechanisms are
primarily unknown. The most obvious effect of unfavorable
conditions initially appear at the cellular levels after that,
physiological symptoms are observable. Water stress adversely
affects physiological status of plants including the photosynthetic
capability (Xu and Zhou, 2006). Prolonged water stress
decreases leaf water potential and stomatal opening, reduces
leaf size, suppresses root growth, reduces seed number, size,
and viability, delays flowering and fruiting and limits plant
growth and productivity (Osakabe et al., 2014;Xu et al.,
2016) (Figure 1). Therefore, plants have smartly evolved
different mechanisms to minimize consumption of optimal
water resources and manage their growth till they face adverse
conditions (Osakabe et al., 2013). Exposure to low or high
light intensities diminishes physiological process and adversely
influences growth and development of plants. Excess light
induces photooxidation that increases the production of highly
reactive oxygen intermediates to manipulate biomolecules and
enzymes (Figure 1). Under severe conditions, loss in plant
productivity is observed (Li et al., 2009). Both freezing (cold)
injury and/or an increase in temperature are major cause of
crop loss (Koini et al., 2009;Pareek et al., 2010). Various
edaphic factors like acidity, salinity, and alkalinity of soils
(Bromham et al., 2013;Bui, 2013), pollutant contamination
and anthropogenic perturbations (Emamverdian et al., 2015)
severely affect plant development and adversely influence crop
production (Figure 1). Different levels of acidic conditions badly
influence soil nutrients and limit their ease of availability due
to which plants become nutrient deficient and lose their normal
physiological pattern of growth and development (Rorison,
1986). Early exposure to salinity leads to ion toxicity within
the cell followed by disruption of osmotic balance when stress
prolonged for longer duration. Combined effect of these ionic
as well as osmotic shocks result into altered plant growth and
development (Munns and Tester, 2008). Tolerance to salinity
stress needs to maintain or quickly adjust both osmotic and
ionic homeostasis within the cells. For combating salinity,
plants usually try to avoid high saline environments by keeping
sensitive plant tissues away from the zone of high salinity or
by exuding ions from roots or compartmentalize ions away
from the cytoplasm of physiologically active cells (Silva et al.,
2010). Plants under extreme cold conditions survive either
through avoiding super cooling of tissue water or through
freezing tolerance. Certain species of plants have developed
an ability to tolerate super-cooling or freezing temperatures
by increasing their anti-freezing response within a short
photoperiod, a process called cold acclimation (Thomashow,
2010).
After sensing the stress stimuli, plants exhibit an immediate
and effective response to initiate a complex stress-specific
signaling cascade (Chinnusamy et al., 2004;Andreasson and
Ellis, 2010). Synthesis of phytohormone like abcisic acid,
jasmonic acid, salicylic acid and ethylene (Spoel and Dong,
2008;Qin et al., 2011;Todaka et al., 2012), accumulation of
phenolic acids and flavonoids (Singh et al., 2011;Tiwari et al.,
2011), elaboration of various antioxidants and osmolytes and
activation of transcription factors (TFs), are initiated along with
the expression of stress-specific genes to mount appropriate
defense system (Koussevitzky et al., 2008;Atkinson et al.,
2013;Prasch and Sonnewald, 2013). Though many of the
mechanisms related to stress tolerance in plants are known,
our knowledge regarding ‘on-field response’ of the plants to
simultaneous exposure to multiple stresses is still in quite an
infancy.
The most crucial aspect in mitigating stress in plants
is to understand fine level molecular machinery and its
networks operative under stress conditions. This includes
elaborative elucidation of abundance of metabolic pathways
and their regulatory genes in the plant varieties. Identification
of multigenic traits involved in stress responses, exploration
of linked markers for such genes, and investigation of the
probabilities to pool out important genes through breeding
programs is the current focus of stress mitigation strategies.
Other strategies that have put forward for the alleviation of
abiotic stresses in plants include the use of various biomolecules
of plant and microbial origin. These approaches are opening new
gateways for scientists to dig out novel methods to alleviate the
abiotic stresses in field grown plants.
Frontiers in Plant Science | www.frontiersin.org 3February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 4
Meena et al. Microbe-Mediated Management of Abiotic Stress
FIGURE 1 | Diverse abiotic stresses and the strategic defense mechanisms adopted by the plants. Though the consequences of heat, drought, salinity and
chilling are different, the biochemical responses seem more or less similar. High light intensity and heavy metal toxicity also generate similar impact but
submergence/flood situation leads to degenerative responses in plants where aerenchyma are developed to cope with anaerobiosis. It is therefore, clear that
adaptive strategies of plants against variety of abiotic stresses are analogous in nature. It may provide an important key for mounting strategic tolerance to combined
abiotic stresses in crop plants.
PHYSIOLOGICAL AND MOLECULAR
RESPONSES OF PLANTS AGAINST
STRESSES
Plants smartly sense, manage, maintain or escape changing
environmental conditions (Figure 1). Their perception to
environmental stimuli and responses to abiotic stresses involve
an interactive metabolic crosstalk within diverse biosynthetic
networks and pathways. Root architecture is thought to be more
sensitive in sensing abiotic stimuli and reacting accordingly
in the soils (Khan M.A. et al., 2016). It is a complex
phenomenon that involves dynamic and real-time changes at
genetic, transcriptomic, cellular, metabolic and physiological
levels (Atkinson and Urwin, 2012). The foremost and direct
impact of drought stress, frost, salinity and heat is creation
of water deficient conditions within cells followed by a
parallel development of biochemical, molecular and phenotypic
responses against stresses (Cushman et al., 1990;Almoguera
et al., 1995;Xu and Zhou, 2006). In the environment, the
stresses experienced by the plants may be many, so as the
complexity of their responses to multiple stresses in comparison
to individual stress. The complexity lies in activating specific
gene expression followed by metabolic programming in cells in
response to individual stresses encountered. Tolerance, defense
Frontiers in Plant Science | www.frontiersin.org 4February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 5
Meena et al. Microbe-Mediated Management of Abiotic Stress
or susceptibility to stresses is a dynamic event involving multiple
stages of plant’s development. Rather than imposing an additive
effect on plants, abiotic stress responses may reduce or enhance
susceptibility of plants toward biotic stresses caused due to
pests or pathogens (Rizhsky et al., 2004). This becomes more
important when we take into account agricultural crops because,
in many agricultural systems, most crops grow in suboptimal
environmental conditions that are limiting to the genetic
potential of the plants for growth and development (Bray et al.,
2000). Defense, repair, acclimation and adaptation are the major
components of resistance responses toward stresses.
Plants are vulnerable to water stress. Environmental changes
like rewatering or cycled water conditions are created most
frequently in the globally changing climatic conditions (Xu
et al., 2010). Under severe water deficit conditions, peroxidation
may be induced leading to negative impact on antioxidant
metabolism (Bian and Jiang, 2009;Xu et al., 2014). Rewatering
further decreases the level of peroxidation and restores growth
and development of new plant parts and stomatal opening. In
roots, both drought and rewatering lead to high accumulation
of H2O2(Bian and Jiang, 2009). Drought responses vary
from plant to plant in terms of the activity of superoxide
dismutase (SOD) enzyme that plays a central role in antioxidant
metabolism (Xu Z. et al., 2015). In bluegrass, SOD activity
remains unaffected by drought conditions and gene expression
of FeSOD and Cu/ZnSOD is down-regulated. In Alfalfa nodules,
FeSOD and CU/ZnSOD are up-regulated by moderate drought,
implicating that responses differ from species and tissues (Foyer
and Noctor, 2005;Naya et al., 2007). An elevated level of
salts present in the soil is detrimental to the plant cells, and
different cells in a tissue respond differently to the stresses
caused due to salinity (Voesenek and Pierik, 2008). Stressed
cells irrespective of their location, whether at the root surface
or within internal tissues, influence their neighbors and cause
a change in their gene expression pattern over the stress
duration (Dinneny et al., 2008). A drastic decrease in the
osmotic potential of the soil occurs due to the elevated salt
levels, the ultimate result of which is ion toxicity coupled
with water stress in the plants. This situation can affect the
vitality of the plants by suppressing seed germination and
growth of the seedlings, hamper senescence of the plants
and finally cause death (McCue and Hanson, 1990). The
role of Salt Overly Sensitive (SOS) stress signaling pathway
consisting of three majorly involved proteins SOS1, SOS2, and
SOS3 is well demonstrated (Hasegawa et al., 2000). Salinity
conditions cause decrease in the levels of aromatic amino acids
like cysteine, arginine and methionine. Proline accumulation
within the cells is a well-known alleviation strategy from
salinity stress (Matysik et al., 2002). Similarly, generation
of nitric oxide (NO), activation of antioxidant enzymes and
compounds, modulation of hormones, accumulation of glycine
betaine and polyols are some other changes within plants due
to salinity stress (Gupta and Huang, 2014). This principally
happens due to unavailability of water and mutilation in the
nutrient availability caused due to high salt concentrations
that create much damage to plant tissues and ultimately affect
productivity.
Due to continued rise in global temperature, heat stress is
becoming an important agricultural problem as it badly affects
crop production. Rising temperature has an adverse impact
on morpho-anatomical, physiological, biochemical and genetic
changes in plants. A thorough understanding of physiological
responses of plants to heat and mechanisms of tolerance could
lead to strategic development of better approaches for crop
production management (Wahid et al., 2007). Heat affects
plants at different developmental levels, and high temperature
causes reduced seed germination, loss in photosynthesis and
respiration and decrease in membrane permeability (Xu et al.,
2014). Alterations in the level of phytohormones, primary
and secondary metabolites, enhancement in the expression of
heat shock and related proteins and production of reactive
oxygen species (ROS) are some prominent responses of
plants against heat stress (Iba, 2002) (Figure 1). Mitigation
strategies in plants against heat stress involve activation of
mechanisms that support maintenance of membrane stability
and induction of mitogen-activated protein kinase (MAPK)
and calcium-dependent protein kinase (CDPK) cascades (Wang
and Li, 2006). Besides, scavenging of ROS, accumulation
of antioxidant metabolites and compatible solutes, chaperone
signaling and transcriptional modulation are certain parallel
activities that help cells to sustain heat stress (Wahid et al.,
2007).
Multiple stress conditions impose more beneficial impacts on
plants compared to that posed in presence of individual stress
alone. Combination of stresses ultimately reduce the detrimental
effect of each other thereby, increasing the probability of better
survival of plants. Iyer et al. (2013) demonstrated that the
cumulative impact of drought and accumulation of ozone (O3)
in plants resulted in better tolerance. The combined affect
was attributed to decreased values of stomatal conductance.
Elevated concentration of reduced glutathione and ascorbic acid
effectively scavenge ROS, thereby causing a considerable drop
in the total ROS content. However, it is a difficult task to infer
response pattern of a plant against any single stress, particularly
when it is growing in the field from the cumulative impact of
environmental stresses. Multiple stresses occur simultaneously
in field conditions and so, multifaceted mechanisms exist in the
plants to cope-up with rapidly fluctuating adverse situations.
Although much efforts have been made to assess plant responses
toward single stress conditions (Rizhsky et al., 2002, 2004;
Mittler, 2006;Mittler and Blumwald, 2010;Alameda et al., 2012;
Atkinson and Urwin, 2012;Kasurinen et al., 2012;Srivastava
et al., 2012;Perez-Lopez et al., 2013;Rivero et al., 2013),
attempts to assess the impact of combined stress conditions
on crop plants under simulated laboratory trials are limited.
This particularly limits our knowledge and understanding
of plant responses to combined stresses and prediction of
cumulative stress tolerance mechanisms in laboratory or field
conditions.
Phytohormones are crucial for the plant growth and
development but they critically play role in the abiotic stress
tolerance (Wani et al., 2016). Gene expression profiling revealed
that prioritization of signals done by protein switches like
kinases, TFs and G-proteins are mostly regulated by hormones
Frontiers in Plant Science | www.frontiersin.org 5February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 6
Meena et al. Microbe-Mediated Management of Abiotic Stress
(Depuyd and Hardtke, 2011;Yao et al., 2011). Plants typically
channel their physiological resources toward adapting to abiotic
stress which makes them more susceptible to biotic stresses
like herbivory and disease attack (Zabala et al., 2009;Hey
et al., 2010). ABA-dependent abiotic stress response pathways are
predominant. Other defense pathways rooted through salicylic
acid, jasmonic acid or ethylene also trigger plants for abiotic
stress response. For example, triggering ROS production to
minimize loss during abiotic stress may prevent plants from
biotrophic pathogen attack, but it makes plants more prone
for necrotrophic pathogens. The other hormone, JA is effective
for defense responses to necrotrophic pathogens and associated
to ISR by beneficial microbes (Matilla et al., 2010). Study of
omics may help in understanding these complex plant–microbe
interactions and harvesting associated and linked understanding.
MICROBE-MEDIATED MITIGATION OF
ABIOTIC STRESSES
Microbial interactions with crop plants are key to the adaptation
and survival of both the partners in any abiotic environment.
Induced Systemic Tolerance (IST) is the term being used for
microbe-mediated induction of abiotic stress responses. The role
of microorganisms to alleviate abiotic stresses in plants has been
the area of great concern in past few decades (de Zelicourt et al.,
2013;Nadeem et al., 2014;Souza et al., 2015). Microbes with their
potential intrinsic metabolic and genetic capabilities, contribute
to alleviate abiotic stresses in the plants (Gopalakrishnan et al.,
2015). The role of several rhizospheric occupants belonging to
the genera Pseudomonas (Grichko and Glick, 2001;Ali et al.,
2009;Sorty et al., 2016), Azotobacter (Sahoo et al., 2014a,b),
Azospirillum (Creus et al., 2004;Omar et al., 2009), Rhizobium
(Alami et al., 2000;Remans et al., 2008;Sorty et al., 2016),
Pantoea (Amellal et al., 1998;Egamberdiyeva and Höflich, 2003;
Sorty et al., 2016), Bacillus (Ashraf et al., 2004;Marulanda et al.,
2007;Tiwari et al., 2011;Vardharajula et al., 2011;Sorty et al.,
2016), Enterobacter (Grichko and Glick, 2001;Nadeem et al.,
2007;Sorty et al., 2016), Bradyrhizobium (Fugyeuredi et al.,
1999;Swaine et al., 2007;Panlada et al., 2013), Methylobacterium
(Madhaiyan et al., 2007;Meena et al., 2012), Burkholderia
(Barka et al., 2006;Oliveira et al., 2009), Trichoderma (Ahmad
et al., 2015) and cyanobacteria (Singh et al., 2011) in plant
growth promotion and mitigation of multiple kinds of abiotic
stresses has been documented. Recently, Pandey et al. (2016)
have demonstrated the role of Trichoderma harzianum on
stress mitigation in rice genotypes due to upregulation of
aquaporin, dehydrin and malonialdehyde genes along with
various other physiological parameters. Rhizobacteria-induced
drought endurance and resilience (RIDER) that includes changes
in the levels of phytohormones, defense-related proteins and
enzymes, antioxidants and epoxypolysaccharide have been
observed for microbe-mediated plant responses. Such strategies
make plants tougher toward abiotic stresses (Kaushal and
Wani, 2016). The selection, screening and application of stress-
tolerant microorganisms, therefore, could be viable options
to help overcome productivity limitations of crop plants in
stress-prone areas. Enhanced oil content in NaCl affected
Indian mustard (Brassica juncea) was reported by Trichoderma
harzianum application which improved the uptake of essential
nutrients, enhanced accumulation of antioxidants and osmolytes
and decreased Na+uptake (Ahmad et al., 2015). Parallel to
such reports, up-regulation of monodehydroascorbate reductase
in Trichoderma treated plants was demonstrated. It was also
confirmed by mutant studies that Trichoderma ameliorates
salinity stress by producing ACC-deaminase (Brotman et al.,
2013). In barley and oats, Pseudomonas sp. and Acinetobacter
sp. were reported to enhance production of IAA and ACC-
deaminase in salt affected soil (Chang et al., 2014). Palaniyandi
et al. (2014) reported alleviation of salt stress and growth
promotion by Streptomyces sp. strain PGPA39 in ‘Micro-Tom’
tomato plants. Burkholderia phytofirmans strain PsJN mitigates
drought stress in maize (Naveed et al., 2014b), wheat (Naveed
et al., 2014a) and salt stress in Arabidopsis (Pinedo et al., 2015).
The rhizosphere comprises the fraction of soil in vicinity
of the plant roots. It constitutes a soil microenvironment
in the proximity of root region where the average count of
microorganisms is very high than rest of the bulk soil. It is,
therefore, obvious that plant roots with a diversity of their
nutrient, mineral and metabolite composition, could be a major
factor responsible for attracting microorganisms to accumulate
and associate alongside. The secretion of root exudates by plants
is a vital factor for microbial colonization within the rhizosphere.
Chemotactic movement of microorganisms toward the root
exudates plays the role of dragging force for the microbial
communities to colonize on the roots. While utilizing the
rhizosphere-microenvironment around plant roots, the PGPRs
may act as biofertilizers, phytostimulators or biocontrol agents
depending upon their inherent capabilities, mode of interaction
and competitive survival conditions. Growth promoting bacteria
stimulate plant growth by employing several broadly categorized
direct and indirect mechanisms (Braud et al., 2009;Hayat
et al., 2010). Direct mechanisms include synthesis of bacterial
compounds which facilitate uptake of essential nutrients and
micronutrients from the soil along with the production of plant
growth regulators, e.g., iron and zinc sequestration, siderophore
production, phosphorus and potassium solubilisation, plant
hormone production, and atmospheric nitrogen fixation. On the
other hand, indirect mechanisms involve antagonistic activity
toward plant pathogenic organisms, production of HCN and
antifungal compounds and tolerance against abiotic stresses.
Besides this, the bacteria can induce systemic resistance in
plants by their metabolites acting as extracellular signals, which
subsequently trigger a series of internal processes. Eventually,
the translocated signal is perceived by the distant plant cells
triggering the activation of the defense mechanism. Besides
bacteria, fungi particularly the mycorrhiza are also important
plant growth promoters. These are principally divided into
mycorrhizal fungi and vesicular-arbuscular mycorrhizal (VAM)
fungi. These fungi remain associated with the host plant
externally (ectomycorrhizae) or they may form endosymbiotic
associations (VAM). These fungi form extensive networking
of very fine hyphae, thus increasing overall nutrient uptake
by the roots. The root fungal endophyte Piriformospora indica
Frontiers in Plant Science | www.frontiersin.org 6February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 7
Meena et al. Microbe-Mediated Management of Abiotic Stress
induces salt tolerance in barley (Baltruschat et al., 2008) and
drought tolerance in Chinese cabbage (Sun et al., 2010) by
increasing the levels of antioxidants and improving many
other aspects (Franken, 2012). The potential of microbial
interactions with the plants have, therefore, multipronged
role. At one end, microbes induce local or systemic stress
alleviation response mechanisms in plants to sustain under
abiotic stress conditions while at the other end, they help plants
to maintain their growth and development through fixation,
mobilization and/or production of nutrients, hormones and
organic phytostimulant compounds. Such multifaceted action of
microorganisms or their communities makes them strong, viable
and vital options for abiotic stress mitigation strategies in crop
plants.
Several mechanisms highlighting the role of microbes in
abiotic stress alleviation have been proposed. Soil-inhabiting
microbes belonging to genera Achromobacter, Azospirillum,
Variovorax, Bacillus, Enterobacter, Azotobacter, Aeromonas,
Klebsiella and Pseudomonas have been shown to enhance
plant growth even under unfavorable environmental conditions
(Pishchik et al., 2002;Hamdia et al., 2004;Mayak et al., 2004;
Arkhipova et al., 2007;Barriuso et al., 2008a,b;Dardanelli
et al., 2008;Belimov et al., 2009;Ortiz et al., 2015; Kaushal
and Wani, 2016;Sorty et al., 2016). Literature relating to the
involvement of microbes for the alleviation of abiotic stressors
signifies the importance of microbes in this area (Table 1).
All such soil bacteria that are capable of inducing plant
growth under variety of physicochemical and environmental
conditions are classified cumulatively as plant growth promoters
(PGP). There exists different mechanisms by which microbes
induce plant growth. The plant-growth regulating molecules
predominantly, indole acetic acid (IAA) are synthesized in
shoot and accumulated in the actively growing regions of roots.
The IAA and other auxins have growth-stimulating effect in
terms of cell elongation resulting in root growth initiation.
Moreover, these molecules also promote the development of
lateral roots. Higher concentrations of auxins, on the other
hand, are known to have a negative impact on root growth
(Jackson, 1991;Sorty et al., 2016). A similar situation can also
happen due to increased synthesis of ethylene (Jackson, 1991).
The rhizosphere colonizing bacteria were reported to perform
in a similar manner, and produce phytohormones to enhance
plant growth (Bowen and Rovira, 1991;Timmusk and Wagner,
1999;German et al., 2000;Belimov et al., 2007). Evidences from
recent agricultural practices witness that the PGPRs not just
help in mitigation of environmental stresses, but also improve
yield of diverse crop plants including rice, maize, barley and
soybean (Tapias et al., 2012;Sharma et al., 2013;Sen and
Chandrasekhar, 2014;Suarez et al., 2015). A mechanism of salt
tolerance imposed by Pseudomonas sp. PMDzncd2003 on rice
germination under salinity stress is demonstrated. Better root
colonizing capability of Pseudomonas sp. along with its ability
to produce exopolysaccharides (EPS) leads to enhanced tolerance
toward salinity (Sen and Chandrasekhar, 2014). Similarly, Khan
A. et al. (2016) have shown that inoculation of Bacillus pumilus
improved rice growth in response to salinity and high boron
stresses. A possible mechanism was suggested, that higher
expression of antioxidant enzyme machinery in the presence
of bacterial inoculant may lead to cell protection in stress
conditions. More efforts are now needed to dissect molecular
mechanisms involved in the communication between plant and
bacterial colonizers.
MULTI-OMICS APPROACHES TO
ADDRESS ALLEVIATION OF ABIOTIC
STRESS
The ecology of plant–microbe interaction is very complicated
and interwoven system. It is important to understand the
fine-tuning and integration of diverse signals generated by
microbial interactions in the plants for advantage in crop
improvement. A plant has to combat multiple biotic and
abiotic stresses in the environment. Multiple stress factors
produce complex defense signals in plants and therefore,
the result of plant–microbe interaction can be decided by
prioritization of physiological pathways in plants (Schenk
et al., 2012). Interaction of microbes with plant roots evoke
multipronged responses in local and/or in distal plant parts at
physiological, biochemical and molecular level. Such responses
at all levels have their interconnections with the stress; many
are parallel to stress responses while others are adverse. For
dissecting the mechanisms, multi-omics approaches can be
applied to address the challenging task of deciphering changes
in plants at genetic, proteomic or metabolomic level (Figure 2).
Entwined with the advances in bioinformatics, the data-
driven science of multi-omics has improved our knowledge in
understanding the microbial community composition and their
functional behavior in complex environments like rhizosphere,
where inter-connections among microbial communities
direct plant responses toward stresses. Recently, meta-omics
approaches including metagenomics, metatranscriptomics
and metaproteomics have emerged as promising tools to
address microbial communities and functions within a given
environment at a deeper level (de Castro et al., 2013).
GENOMICS
Abiotic stress alleviation by altering crop genetics is of paramount
importance and is a challenging issue that requires extensive
breeding programs (Grainger and Rajcan, 2013). Low heritability
and environmental variations make such breeding programs even
more challenging (Manavalan et al., 2009). Strategic marker-
assisted breeding is efficient in accelerating tolerance in cultivars.
Understanding about genomic loci governing traits responsible
for tolerance and availability of molecular markers tightly linked
with it is a prerequisite for marker assisted selection (Xu et al.,
2012). A large amount of genomic data in the form of sequenced
genomes and expression profiles are thus, impetuous for breeding
for stress alleviation (Sonah et al., 2011;Tomar et al., 2014).
Use of genomics-based technologies has made a great impact
in crop improvement programs. Use of molecular markers in
crop improvement for the accumulation of silicon (Si) in rice
Frontiers in Plant Science | www.frontiersin.org 7February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 8
Meena et al. Microbe-Mediated Management of Abiotic Stress
TABLE 1 | Microbe-mediated abiotic stress tolerance in plants.
Abiotic stress Microbe inoculation Plant Tolerance strategy Reference
Salt Bacillus subtilis GB03 Arabidopsis thaliana Tissue-specific regulation of sodium
transporter HKT1
Zhang et al., 2008
Salt Pseudomonas simiae Glycine max 4-nitroguaiacol and quinoline promote
soybean seed germination
Vaishnav et al., 2016
Salt Pseudomonas syringae
DC3000, Bacillus sp. strain
L81, Arthrobacter oxidans
Arabidopsis thaliana SA-dependent pathway Barriuso et al., 2008b
Salt Root-associated plant
growth-promoting rhizobacteria
(PGPR)
Oryza sativa Expression of salt stress-related RAB18
plant gene
Jha et al., 2014
Salt Cyanobacteria and
cyanobacterial extracts
Oryza sativa,Triticum
aestivum,Zea mays,
Gossypium hirsutum
Phytohormones as elicitor molecule Singh, 2014
Salt Pseudomonas koreensis strain
AK-1
Glycine max L. Merrill Reduction in Na+level and increase in
K+level
Kasotia et al., 2015
Osmotic stress Bacillus megaterium Zea mays High hydraulic conductance, increased
root expression of two ZmPIP isoforms
Marulanda et al., 2010
Osmotic stress Glomus intraradices BEG 123 Phaseolus vulgaris High osmotic root hydraulic
conductance due to increased active
solute transport through roots
Aroca et al., 2007
Salt Glomus etunicatum Glycine max Increased root but decreased shoot
proline concentrations
Sharifi et al., 2007
Salt Burkholderia, Arthrobacter and
Bacillus
Vitis vinifera,Capsicum
annuum
Increased accumulation of proline Barka et al., 2006
Drought Rhizobium tropici and
Paenibacillus polymyxa
(Co-inoculation)
Phaseolus vulgaris Upregulation of genes involved in stress
tolerance
Figueiredo et al., 2008
Salt Glomus fasciculatum Phragmites australis Accumulation of carbohydrates Al-Garni, 2006
Salt Glomus intraradices Glycine max Accumulation of carbohydrates Porcel and Ruiz-Lozano, 2004
Salinity Azospirillum brasilense and
Pantoea dispersa
(Co-inoculation)
Capsicum annuum High stomatal conductance and
photosynthesis
del Amor and Cuadra-Crespo
(2012)
Salinity Glomus intraradices BAFC
3108
Lotus glaber Decreased root and shoot Na+
accumulation and enhanced root K+
concentrations
Sannazzaro et al., 2006
Salinity Glomus clarum
Glomus etunicatum
Vigna radiata,
Capsicum annuum,
Triticum aestivum
Decreased Na+in root and shoot and
incesaed concentration of K+in root
Rabie, 2005;Daei et al., 2009;
Kaya et al., 2009
Salinity Bacillus subtilis Arabidopsis Decreased root transcriptional
expression of a high-affinity K+
transporter (AtHKT1) decreasing root
Na+import
Zhang et al., 2008
Salinity Glomus intraradices BEG121 Lactuca sativa Reduced concentration of ABA Aroca et al. (2008)
Salinity Pseudomonas putida Rs-198 Gossypium hirsutum Prevented salinity-induced ABA
accumulation in seedlings
Yao et al., 2010
Salinity Azospirillum brasilense strain
Cd
Phaseolus vulgaris Stimulation of persistent exudation of
flavonoids
Dardanelli et al., 2008
Salinity Bacillus subtilis Lactuca sativa Root-to-shoot cytokinin signalling and
stimulation of shoot biomass
Arkhipova et al., 2007
Drought Burkholderia phytofirmans
Enterobacter sp. FD17
Zea mays Increased photosynthesis, root and
shoot biomass under drought
conditions
Naveed et al., 2014b
Drought Bacillus thuringiensis AZP2 Triticum aestivum Production of volatile organic
compounds
Timmusk et al., 2014
Drought Pseudomonas chlororaphis O6 Arabidopsis thaliana Production of 2R,3R butanediol- a
volatile compound
Cho et al., 2008
Drought Pseudomonas putida strain
GAP-P45
Helianthus annuus Epoxypolysaccharide production Sandhya et al., 2009
Drought Bacillus licheformis strain K11 Capsicum annum Stress related genes and proteins Lim and Kim, 2013
(Continued)
Frontiers in Plant Science | www.frontiersin.org 8February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 9
Meena et al. Microbe-Mediated Management of Abiotic Stress
TABLE 1 | Continued
Abiotic stress Microbe inoculation Plant Tolerance strategy Reference
Drought Bacillus cereus AR156,
B. subtilis SM21 and Serratia
sp. XY21
Cucumis sativa Production of monodehydro ascorbate,
proline, and antioxidant enzyme,
expression of genes
Wang et al., 2012
Heat Bacillus amyloliquefaciens,
Azospirillum brasilence
Triticum aestivum Reduced regeneration of reactive
oxygen species, preactivation of heat
shock transcription factors, changes in
metabolome
El-Daim et al., 2014
Heat and drought Curvularia proturberata isolate
Cp4666D
Dichanthelium
lanuginosum, Solanum
lycopersicum
Colonization of roots de Zelicourt et al., 2013
Arsenic toxicity Staphylococcus arlettae Brassica juncea Increased soil dehydrogenase,
phosphatase and available phosphorus
Srivastava et al., 2013
Pb/Zn toxicity Phyllobacterium
myrsinacearum
Sedum plumbizincicola Resistance to 350mg/L Cd, 1000 mg/L
Zn, 1200 mg/L Pb
Ma et al., 2013
Zn toxicity Pseudomonas aeruginosa Triticum aestivum Improved biomass, N and P uptake
and total soluble protein
Islam et al., 2014
Zn toxicity Enterobacter intermedius
MH8b
Sinapis alba ACC deaminase, IAA, hydrocyanic acid,
P solubilization
Plociniczak et al., 2013
Cd, AS, Cu, Pb and
Zn toxicity
Pseudomonas koreensis
AGB-1
Miscanthus sinensis ACC deaminase, IAA production Babu et al., 2015
Zn toxicity Pseudomonas brassicacearum,
Rhizobium leguminosarum
Brassica juncea Metal-chellating molecules Adediran et al., 2016
Hg toxicity Photobacterium spp. Phragmites australis IAA, mercury reductase activity Mathew et al., 2015
to enhance the tolerance of plant for abiotic stress is in vogue.
Ma et al. (2004) used PCR-based markers for microsatellite
(RM5303) and expressed sequence tag (EST, E60168) in mapping
Si transporter gene during a bulk segregant experiments.
Besides crop breeding programs, a significant level of
abiotic stress alleviation in plants can be achieved through
the manifestations of plant-microbe interaction also. Omics
approaches help to have deep insight into the mechanisms of
established plant–microbe interactions (Figure 2). In a study of
Trichoderma-plant interaction (T. atroviride and T. harzianum
with tomato), Tucci et al. (2011) reported the impact of
genotypic characteristics of plants for modulation of microbe–
plant interaction leading to its effect on plant growth and stress
alleviation. Growth promoting and stress alleviating activity of
T. atroviride on tomato is demonstrated through degradation
of IAA in the rhizosphere and ACC deaminase activity (Gravel
et al., 2007). A putative sequence of ACC-deaminase found in
Trichoderma genome was confirmed by gene silencing through
RNAi (Viterbo et al., 2010;Kubicek et al., 2011). Expression of
dicarboxylate transporter LjALMT4 responsible for carbohydrate
translocation in plants was reported in Lotus japonicas genome by
Takanashi et al. (2016). The gene silencing strategy of Hb1 gene
to enhance NO production and up-regulation of CBF regulon
could be a way to engineer crops in improving cold tolerance
(Sehrawat et al., 2013). Kumari et al. (2015) reported IST to
salinity in soybean by Pseudomonas sp. AK-1 and Bacillus sp. SJ-5
inoculation. Results indicated that superior tolerance to salt stress
may be observed due to proline accumulation and lipoxygenase
activity.
Koussevitzky et al. (2008) reported that Apx1, a gene coding
for cytosolic ascorbate peroxidase 1 is specifically required for
tolerance to drought and heat stress in Arabidopsis. Ectoine is a
compatible osmolyte responsible for salt tolarance in Halomonas
elongata OUT30018. Three genes for ectoine biosynthesis were
cloned and transferred to tobacco plant (Nicotiana tabacum L.)
cv Bright Yellow 2 (BY2) which caused increase in tolerance to
hyperosmotic shock by accumulation of ectoine and exhibited
normal growth under such conditions (Nakayama et al., 2000).
Identifying the genes and their regulation helps breeders in
generating better varieties for stress tolerance. Use of multi-omics
strategies yield highly efficient and reliable outcome that are
useful to facilitate methodical experiments (Figure 2). Chilling
tolerance in Miscanthus grass is a desirable trait that often varies
in different cultivars. Molecular expression of relevant genes for
the accumulation of carbohydrates creates differentiation among
varieties for chilling tolerance. The impairment of tolerance
among varieties can be predicted by molecular marker of sensitive
genes like TF MsCBF3 expressed in sensitive genotypes (Purdy
et al., 2013).
Stress due to submergence affects more than 15 million
hectares of rainfed lowland rice in different parts of Asia (Neeraja
et al., 2007). Thirteen percent of the total land area of the world is
affected by problems of flooding or anoxia (Cramer et al., 2011).
In rice, submergence tolerance is governed by a single major
quantitative trait locus (QTL) found on chromosome 9 (Toojinda
et al., 2003). Neeraja et al. (2007) used molecular markers for
Sub1 gene in backcross breeding program with recurrent parant
Swarna. This Sub1 provides tolerance in sensitive mega varieties.
Sub1A is now confirmed of being the primary contributor to
submergence tolerance (Septiningsih et al., 2009). This QTL has
provided a great opportunity for marker assisted backcrossing
(MAB) for developing submergence tolerance in mega varieties.
Frontiers in Plant Science | www.frontiersin.org 9February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 10
Meena et al. Microbe-Mediated Management of Abiotic Stress
FIGURE 2 | Cellular level components, multi-omics approaches to address different levels and the strategies that help identify the outcome of the
impact of abiotic stresses or impact of microbial-interactions.
Genomic analysis of both the host and associated microbial
communities especially phyllosphere-associated microbial
communities permits to access the system involved for the
smooth functioning of associative interactions (Figure 2).
Several studies have outlined the role of different genes from
associated bacteria. Plants donate indispensible moleculr
counterparts to facilitate and maintain the biological system
involved at the associative interface. The genotypic diversity of
plants has significant influence on the interactive process. The
response of the roots of SUNN1 Medicago truncatula toward
elevated levels of nitrate gets markedly affected with the advent of
associative rhizobia because SUNN1 exhibited no impact showing
the response of SUNN1 under limiting nitrogen environment
in presence of associative rhizobia (Jin et al., 2012). There are
evidences on the influence of Nod factors from associative
microbes on the pattern of root development and smooth
functioning of symbiotic association (Olah et al., 2005;Oldroyd,
2013). Unlike nodulating plants, widely cultivated cereals lack
a system to acquire nitrogen with the help of nodulation. Some
diazotrophic microbes manage to enter and colonize root tissues
via mechanical injuries caused during root growth (Gaiero et al.,
2013). However, knowledge of such interactions is scarce.
Frontiers in Plant Science | www.frontiersin.org 10 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 11
Meena et al. Microbe-Mediated Management of Abiotic Stress
FIGURE 3 | Meta-omics approaches to exploit yet-unexplored environmental population of microbial communities that have major impact on plant
roots and support plants against stresses. Metatranscriptomics and metaproteomics are relatively new approaches to characterize functional attributes of
microbial communities that have not yet been cultured. The approach could generate a deeper snapshot of major metabolic pathways and interactions and
dominance of functional microbial communities in the rhizosphere of crop plants facing multiple environmental stresses. (∗Enrichment techniques in metagenomics.
In order to trace out less abundant genes from the environment, these techniques are usually employed. In induced enrichment approach, the physico-chemical
factors such as nutrients, temperature, acidity/alkalinity, xenobiotic compounds, etc. (Eyers et al., 2004;Bertrand et al., 2005) are used to enrich the respective
populations in situ. These factors are either directly implemented in the microbial habitat itself or used in simulated in situ laboratory conditions. The natural sample
enrichment is mainly dependent on executing fine criteria while proceeding for sampling of an environment. The naturally predominating bio-geo-physico-chemical
situations need to be considered, as they are the key factors for selective natural enrichment of genes, e.g., sites contaminated with xenobiotic compounds and
habitats with extreme environments can be expected to yield the genes participating in the metabolism of xenobiotic compounds and the genes participating in
environmental stress tolerance respectively. The enrichment of nucleic acids from natural environment is principally carried out for the samples containing insufficient
quantities of nucleic acids. It involves techniques such as affinity capture, differential expression analysis, stable isotope probing, e.g., addition of 13 C labeled carbon
source in the habitat. For the samples with low density of biomass, whole genome amplification technique is recommended to yield relatively larger quantity of
nucleic acids (Abulencia et al., 2006;Binga et al., 2008). These approaches may work better with the samples collected from highly saline/sodic/drought affected,
barren soils, where it is virtually difficult to cultivate the crop. The stress-genes of the little microbial community thriving in such harsh environments may provide novel
guidelines for stress alleviation strategies in the crop).
Frontiers in Plant Science | www.frontiersin.org 11 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 12
Meena et al. Microbe-Mediated Management of Abiotic Stress
METAGENOMICS
The culture-independent approach for the analysis of microbial
communities has been a powerful tool for resolution of yet-
uncultured, unseen microbial diversity that plays various role
in the plant rhizosphere (Chen and Pachter, 2005) (Figure 3).
The approach referred to as metagenomics enables the user
to acquire data related to the habitat-specific distribution of
microbial communities with plant growth promoting (PGP),
biocontrol, antibiotic producing and xenobiotic degrading traits.
The approach helps to elevate likelihood of successfully directed
attempts made to explore novel culturable flora from particular
niches (Handelsman et al., 2007). High-throughput metagenomic
sequencing is proving to be an extremely useful tool for improved
understanding of PGP rhizobacterial communities (Figure 3).
In a study on potato endophytes, two types of ACC-deaminase
genes (acdS) homologous to that of Pseudomonas fluorescens
for stress alleviation were found from PCR analysis. Analysis of
clones present in metagenomic libraries helped in identifying
entire acdS operon from uncultivated endophyte and revealed
a transcriptional regulator gene acdR at upstream of acdS.
This operon was found prominently in the genus Burkholderia
(Nikolic et al., 2011). Escherichia coli clones from a pond water
metagenomic library were studied to identify salt tolerance
genes in uncultivable bacteria by growing at inhibitory NaCl
concentrations of 750 mM. Genes from two clones encoding
for proteins similar to a putative general stress protein (GspM)
having GsiB domain with a putative enoyl-CoA hydratase (EchM)
identified to have a role in salt tolerance. After purification, EchM
was found to have crotonyl-CoA hydratase activity (Kapardar
et al., 2010). These genes are of great utility in developing
salt tolerant recombinant bacteria and also transgenic plants.
Metagenomic study of an acid mine drainage 250 m belowground
revealed the presence of mechanisms of adaptation to cold. Genes
related with the survival at low temperature like anti-freeze
protein, cold-shock proteins, compatible solutes production
pathways and pH homeostasis were found in the metagenome of
acid mine drainage (Liljeqvist et al., 2015). Such metagenomics
data help to finding out new genes and mechanisms for cold stress
alleviation. The role of bacterial endophytes that reside inside
roots is largely unexplored because endophytic microbes which
are cultured successfully represent only a fraction of the whole
bacterial community that inhabit root interiors. Sessitsch et al.
(2012) described endophytic bacterial residents of rice roots with
the help of metagenomics approach. Metagenomic sequences
obtained from endophytic cell extracts revealed that metabolic
processes pertaining to the endophytic life style and functional
features like quorum sensing and detoxification of ROS have
their role in improving plant stress resistance (Sessitsch et al.,
2012). Microbial communities have a fundamental impact on
plant health and productivity. As a community, microbes interact
with each other and with the host. This is a key phenomenon
that increases resistance to diseases and stresses. To know the
microbiome composition and describe its diversity and function,
global approaches like metagenomics, metatranscriptomics and
metaproteomics are being applied (Figure 3). Metagenomics
also reveals functional potential of microbial communities in
terms of the abundance of the genes involved in particular
metabolic processes linked with stresses or stress alleviation
mechanism. Similarly, metatranscriptomics can reveal kingdom-
level changes in rhizosphere microbiome structure (Turner et al.,
2013b) and metaproteomics can reflect community-wide gene
expression, protein abundance and putative proteins that can
be linked with functions after bioinformatics analysis (Turner
et al., 2013b). Diversity profiling and colonization studies using
metagenomics can also reveal quantitative colonization of a
given host under the influence of stressor. This can yield
valuable knowledge regarding stressor-induced alterations in the
taxonomic and functional diversity of colonizing population if
coupled with metatranscriptomic analysis (Turner et al., 2013b)
(Figure 3). The coupled analysis thus achieved significantly
help in understanding mitigation of stressor-influence over
colonization process.
TRANSCRIPTOMICS
Comparison of transcriptome profiles is helpful in identifying
different sets of transcripts responsible for differences between
two biologically different expressions in various conditions
(Bräutigam and Gowik, 2010). Use of mRNA sequencing analysis
and microarray technique to generate transcriptome level
information is one of the important methodologies employed for
studying plant-microbe interactions (Akpinar et al., 2015;Budak
and Akpinar, 2015;Wang et al., 2016). Next-generation RNA
sequencing study on Sinorhizobium meliloti revealed induction
of genes for stress response in IAA overproducing strains
(Defez et al., 2016). This study compared transcription profile
of two S. meliloti strains, wild-type strain-1021 and an IAA
overproducing derivative RD64. The genes coding for sigma
factor RpoH1 and other stress responses were found to induce
IAA overproducing strain of S. meliloti.Alavi et al. (2013)
identified spermidine as a novel plant growth regulator during
abiotic stress by transcriptome analysis of rapeseed and its
symbiont Stenotrophomonas rhizophila.
Different miRNAs in rice, Medicago, Phaseolus, Arabidopsis
and other plants have a regulatory role under abiotic stresses
like drought, salinity and cold (Trindade et al., 2010). miRNAs
are non-coding RNAs of 19–23 nucleotide length having
regulatory role in several biological processes (Budak et al.,
2015). Regulatory role of miR393 was found for salinity tolerance
in Arabidopsis overexpressing osaMIR393 exhibit tolerant to
salt excess (Gao et al., 2011). Zhao et al. (2009) reported
miR169 alleviating salinity and drought stress in rice by
modulating expression of a nuclear transcription factor YA
(NF-YA). In tomato, plants overexpressing miR169c which
controls expression of gene(s) involved in stomatal activity confer
drought tolerance (Zhang et al., 2011). Bvu-miR13 regulates WD-
repeat proteins which plays crucial role in stress tolerance in
cucumber (Li et al., 2014). Apart from regulating TFs, miRNAs
also target stress signaling pathways which are responsible
for root development, leaf morphogenesis and stress response
(Curaba et al., 2014). Thirteen mature miRNAs were identified
using in silico approach in B. vulgaris plants (Li et al., 2015).
Frontiers in Plant Science | www.frontiersin.org 12 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 13
Meena et al. Microbe-Mediated Management of Abiotic Stress
The activity of superoxide dismutases SOD1 and SOD2 mRNAs
are targeted by miR398 that has a role in reducing ROS and
secondary effects of abiotic stress (Kantar et al., 2011). Diverse
classes of miRNAs alleviate stress by regulating differential
cellular responses and metabolic processes like transcriptional
regulation, auxin homeostasis, ion transport and apoptosis (Li
et al., 2010). miRNA is also found to regulate aluminum stress
response in plants (Lima et al., 2011). Comparison of miRNA
expression in two different rice subspecies, japonica and indica
differing in aluminum tolerance was done. RT-qPCR approach
revealed 16 different kinds of responses of miRNA indicating a
complex response under aluminum stress.
UV-B radiation and flooding (hypoxia) affects plants by
inducing irreversible damage by generation of ROS (Blokhina
and Fagerstedt, 2010). The up-regulation of SOD proteins and
miR398 down-regulation is crucial under oxidative stress in
Arabidopsis (Sunkar et al., 2006). Induction of miR398 and
down-regulation of miR395 was observed in alleviating UV-B
stress in Populus tremula (Jia et al., 2009). Low temperature
severely affects sugar beet seedlings and sugar recovery from
final harvest. Transcriptome profile of cold stressed plants was
done by high throughput RNA sequencing from leaves and roots
(Moliterni et al., 2015). Up-regulation of CBF3 was reported from
root tissues faster than the leaf tissues. Genes from AP2/ERF
family that were known to participate in jasmonic acid mediated
responses were also upregulated during cold stress (Licausi et al.,
2013).
PROTEOMICS
Proteins play a crucial role in expressing plant stress responses
since they directly reflect shaping of a phenotypic trait. Proteomic
studies therefore, have become powerful tools for the exploration
of physiological metabolism and protein–protein interactions
in microbes and plants (Figures 2 and 3). The implications
of proteomics is important for intra- and inter-microbial
species and host–microbe interactions, where host-mediated
signaling and tactic responses of related microorganisms are
involved (Kosova et al., 2015). Such studies lead to generate a
deeper understanding of the regulation of biological system by
identifying several proteins as signal of changes in physiological
status due to stress or factors responsible for stress alleviation
(Silva-Sanchez et al., 2015). Therefore, a comparative analysis
in stressed, non-stressed and microbe-associated plants can help
to identify protein targets and networks. Proteomic studies
for stress responses in crops have been studied extensively
in plants including Arabidopsis, wheat (Triticum aestivum),
durum wheat (Triticum durum), barley (Hordeum vulgare),
maize (Zea maize), rice (Oryza sativa), soybean (Soybean max),
common bean (Phaseolus vulgaris), pea (Pisum sativum), oilseed
rape (Brassica napus), potato (Solanum tuberosum) and tomato
(Lycopersicon esculentum) (Liu et al., 2015;Kosova et al., 2015;Xu
J. et al., 2015;Wang et al., 2016). Such studies reflected dynamic
alternations in protein functional groups, proteins of signaling
and regulatory pathways, TFs, protein metabolism, protein–
protein interactions at interface, proteins and enzymes conferring
several stress-related compounds, functions of structural proteins
associated with the cell wall and cytoskeleton and identification
of putative proteins using bioinformatics tools (Kosova et al.,
2015).
Chen et al. (2015) assessed mechanisms of cold acclimation
in alfalfa by proteomic analysis in cold tolerant (ZD7) and
cold sensitive lines (W5). Cassava, a tropical crop sensitive
to low temperature can modify its metabolism and growth
to adapt to the cold stress. Proteomic study was carried out
to understand the mechanism behind cold-tolerant process.
Twenty differential proteins were found to have similar patterns
in apical expanded leaves of cultivars SC8 and Col1046.
Expression of proteome profile was found to link closely with
changes in photosynthetic activity and peroxiredoxin expression
levels. Principle component analysis reflected that electrolyte
leakage (EL), chlorophyll content, and malondialdehyde (MDA)
accumulation were the physiological indexes in determining cold
tolerance in cassava (An et al., 2016).
A leucine-rich repeat receptor kinase (Srlk) was reported to
function as an upstream regulator of salinity responsive genes
in Medicago truncatula. It was found to be involved in sensing
salinity stress and its response (de Lorenzo et al., 2009). This
study revealed an interesting mechanism of sensing salinity stress.
Based on proteome profile of barley at different water stress
conditions, Ghabooli et al. (2013) proposed that P. indica mitigate
drought stress by photosynthesis stimulation releasing energy
and higher antioxidant production. Wang et al. (2016) screened
a novel gene Ds-26-16 from the cDNA library of 4M salt-stressed
Dunaliella salina. This gene was found to confer salt tolerance
in E.coli,Haematococcus pluvialis and tobacco. Proteomics data
by iTRAQ studies reflected that Ds-26-16 up-regulates TFs for
stress responses like ROS alleviation, osmotic balance, and energy
metabolism in E.coli.
The diversity of metabolic pathways existing amongst the
microbes makes them more responsive toward stress conditions.
It is important in the protocols implemented for the elucidation
of plant-elaborated responses against stress. Unlike routine
proteomics approaches which are more focused toward a
single organism, the role of metaproteomics that deals with
multiple metabolic interactions occurring simultaneously in an
ecosystem is the need of the time (Figure 3). This could help to
resolve better significance of interdependence between various
microbial communities in an agro-ecosystem alongwith their
interactions with the host plant. The protocols for protein
extraction from the environmental samples are most important
success-milestone in the area of metaproteomics (Figure 3).
Recent advancements in protein sequencing are the key step
for the identification of proteins from diverse species (Cordwell
et al., 1995, 1997;Shevchenko et al., 2001). The complexity
of metaproteome makes resolution and analysis quite difficult.
However, recent approaches in extraction and analysis of
successful environmental metaproteome could yield decisive
output and establish a better correlation among the omics data
and response mechanisms among organisms toward stresses
(Schulze, 2005;Schweder et al., 2008).
Most of the environmental proteomic experiments are limited
to model organisms cultured. They particularly highlight the
Frontiers in Plant Science | www.frontiersin.org 13 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 14
Meena et al. Microbe-Mediated Management of Abiotic Stress
exceptional ability of the organisms, e.g., tolerance to salinity,
sodicity, temperature, low water availability, toxic metals and
radiation etc. The proteomic studies of the organisms lead toward
better understanding of fine mechanisms being executed by them.
Moreover, the same also stands helpful for the confirmation of the
probability of their exploitation for expected induction of the said
metabolism in diverse environments. The laboratory experiments
allow a better grasp of the protein profile in a controlled
environment, however, it contrasts the fact that the expression
profile varies with changes in environmental conditions.
The Haloarchea and Halobacteria are gaining strong attention
in present era due to their ability to thrive in high salt
environments. PGP ability of organisms can be implemented
conveniently in saline and sodic soils for the alleviation
of respective stresses encountered by the crops. This will
prove beneficial for yield improvement in stress-prone areas.
Harvesting and implementing metabolites that can confer
halotolerance from microorganisms growing in the area of high
salt stress with other combined stresses may find important
applications in the crop improvement programs. Culturing of
these organisms under in situ stress conditions in laboratory
is the simplest approach to induce the production of effective
metabolites that when applied on plants, could impart tolerance
against stresses. Similarly, to cope with the most agonizing
problem of xenobiotic compounds, the genus Pseudomonas is
the best considered one, particularly because of its unique
ability to degrade enormous amount of carbon sources,
especially of xenobiotic nature. The hydrocarbon degradation
by Pseudomonas is well known. The proteomic experiments
for Pseudomonas have been designed principally to focus on
the recalcitrant, xenobiotic compounds in addition to the toxic
organic pollutants (Lupi et al., 1995;Reardon and Kim, 2002;Kim
et al., 2007). Species of Pseudomonas have been well characterized
for their PGP traits such as siderophore production (Ferret et al.,
2014;Cunrath et al., 2015), secretion of plant growth stimulating
substances (Pereira and Castro, 2014;Balcazar et al., 2015;Sorty
et al., 2016), and biocontrol against phytopathogenic organisms
(Chet and Inbar, 1994;Natsch et al., 1994;Acebo-Guerrero et al.,
2015;Wang et al., 2015). Characteristic versatile metabolic scope
and unique biofilm forming ability of the members of this genus
(Kertesz et al., 1993;Sauer et al., 2002, 2004;Arevalo-Ferro et al.,
2005;VerBerkmoes et al., 2006) permits these species to thrive
well under diverse environmental conditions, thus making them
most effective inoculants for field application.
The proteomic exploration of methylotrophic bacteria is
also an active area of interest today. Methylotrophs constitute
a major portion of phylosphere community, typically leaf
surface, where one-carbon substrate, methanol is easily
available via transpiration activity. Pink-pigmented facultative
methylotrophic (PPFM) bacteria are predominant and explored
largely for their ability to release plant-growth regulation
molecules (Meena et al., 2012;Araujo et al., 2015;Dourado
et al., 2015). Many studies have successfully demonstrated PGP
potential of these organisms under various conditions (Tani
et al., 2012;Yim et al., 2013). Detailed investigations about
the proteomic insights of these characteristic phyllosphere-
community members helped to get novel ideas regarding
involvements of proteins in survival mechanism of organisms
under relatively harsh environments, generally encountered
on leaf surfaces, where in addition to intense radiation, there
exists frequent scarcity of nutrients. Additionally, their potential
to secrete plant-growth regulators may come to a large-scale
execution. It is, therefore, needful to elucidate deep molecular
insights of PGP microbial communities, chiefly involved in stress
alleviation to acquire the data regarding mechanisms involved
in such processes. The identification of proteins involved in
these processes is sufficient to create a boom in stress alleviation
strategies at the molecular level where direct implementation of
active molecules were thought upon instead of employing the
whole organism.
In plants, the study of protein expression of different lines
is helpful in selecting cold-tolerant lines for crop improvement.
It is evident from earlier studies that cold-tolerant lines showed
14 differential proteome expressions in cold acclimation of
sunflower (Balbuena et al., 2011). Proteome analysis also reveals
possible mechanisms for chilling mitigation in plants and cross
tolerance mechanisms (Yuan et al., 2015;Meng et al., 2016).
Once the database of responsive and blocked genotypes is
made for particular abiotic stress, it can be used as a marker
in differentiating stress responsive genotypes. Santos et al.
(2016) has made GeLC–MS/MS based proteomic profiling for
large-scale identification of proteins from Araucaria angustifolia
embryogenic cell lines. In total, 106 proteins were differentially
expressed between the responsive and blocked type lines for
abiotic stress. Two proteins at early stage were identified to be
related with blocked cell lines only. These proteins can be an
indicative to blocked cell lines at early stage of plant development.
METABOLOMICS
The scope of metabolomics involves characterization of all the
metabolites elaborated by an organism under the influence
of given environmental conditions. The metabolome of an
organism directly correlates with diverse pathways being
operated inside the cell which in turn reflects the availability
of corresponding genetic information. The metabolome varies
largely with alterations in surrounding environment that induce
direct physiological alterations in an organism (Bundy et al.,
2005). Similar situations of physiological state are expected in
those organisms which are supposed to thrive well under the
stress conditions. It is, therefore, important to acquire detailed
knowledge of metabolome of an organism both in normal and
under-stress physiological status, the subtraction of which will
yield the presence/absence of typical signature metabolites of
interest. This will be helpful in identifying alterations induced
within the pathways and induction of typical stress-inducible
genes (Figure 2). Metabolomics is increasingly being used for
generating deep insights into abiotic stress responses (Jorge et al.,
2015;Jia et al., 2016). Recent high throughput developments in
the area of molecular detection techniques have given boost to
metabolomics studies (Hollywood et al., 2006;Morrow, 2010).
Studies highlight the presence of different bioactive chemicals
(Burns et al., 2003;Ketchum et al., 2003) in plant metabolome.
Frontiers in Plant Science | www.frontiersin.org 14 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 15
Meena et al. Microbe-Mediated Management of Abiotic Stress
This observation correlates with the reports pertaining to the
identification of various signal molecules secreted by plants to
attract and induce important biochemical pathways in colonizing
microbial population (Zhang and Cheng, 2006;Micallef et al.,
2009).
Trichoderma spp. produce auxins which stimulate plant
growth by alleviating stress (Contreras-Cornejo et al., 2009).
Two secondary metabolites, harzianolide and 6-pentyl-a-pyrone
of Trichoderma was reported to exhibit auxin-like effects in
etiolated pea stem (Vinale et al., 2008) and enhance plant growth.
Variations induced by changing environmental situations in
plant metabolism also affect secretion pattern and nature
of secreted molecules (Martínez-Cortés et al., 2014) thereby
affecting the level of root colonization. Microbial molecular
signaling mechanisms in the rhizosphere are also affected in a
similar manner but this is yet to be explored.
Plants accumulate different metabolites like trehalose, glycine
betain, IAA etc. in response to abiotic stresses. Allen et al.
(2009) reported that mere accumulation of a specific compound
does not indicate stress tolerance, but it is the adjustment
of flux to different pathways of defense and growth which
decides tolerance. Modulation of stoichiometry and metabolism
is reported as mechanisms to maintain optimum fitness in
plants (Rivas-Ubach et al., 2012). Time-series experiments with
Arabidopsis thaliana indicated that metabolic activities respond
more quickly than that of transcriptional activities to abiotic
alterations (Caldana et al., 2011).
The conditions, available within surrounding environment
influence pathways operating in the microbial cell, thereby
affecting the metabolome. It is evident that the same must affect
their overall performance in surrounding microenvironment and
within the ecosystem to a greater extent (Tringe et al., 2005;Raes
and Bork, 2008;Jiao et al., 2010) in terms of the interactions
evident within and between the inhabitants therein. Microbial
metabolic products have been involved in both direct as well as
indirect plant growth promotion. It is well known that many
of the rhizosphere bacteria show the ability to produce plant
growth stimulating biomolecules like cytokinins, gibberelins,
etc. (Williams and de Mallorca, 1982;Robin et al., 2006).
Variety of microbial metabolites including IAA, gibberelins,
siderophores serve the purpose. Recently the IAA produced
by Pseudomonas sp., Rhizobium sp., Enterobacter sp., Pantoea
sp., Marinobacterium sp., Acinetobacter sp., and Sinorhizobium
sp., has been shown to influence the germination and seedling
growth in wheat under saline conditions (Sorty et al., 2016).
Similarly, the strains of Bacillus sp. having phosphate solubilizing
potential successfully improved the yield and quality of fennel
in semiarid saline soil (Mishra et al., 2016). The solubilization
of phosphate is mainly attributed to the low molecular weight
organic acids produced by the microbes. Microbial siderophores
also play an important role toward the biological availability
of iron to plant roots, for instance, the siderophores produced
by Pseudomonas fluorescens C7 successfully supplemented the
iron to Arabidopsis thaliana (Vansuyt et al., 2007). Although
the siderophore production by the microbes seems influenced
by biogeochemical factors, they also help in the alleviation
of the stress imposed by heavy metals (Diels et al., 2002).
Many microbes show high degree of environmental dependency
for optimal siderophore production. Sorty and Shaikh (2015)
reported reduced iron uptake by both sediment as well as soil
magnetotactic bacteria under acidic conditions and the probable
cause was attributed to the conversion of Fe+++ to Fe++
under acidic conditions that could have interfered with the
siderophore mediated iron uptake system. This signifies the need
of keen evaluation of in situ mechanisms influencing microbial
metabolism. Moreover, the majority of these metabolites are
yet to be identified. The cutting edge metabolomics technology
could serve as a powerful tool for the evaluation of these
metabolites and environmental interventions in the microbial
metabolism in situ. Many microbes from the ecosystem show
interdependence with respect to the substrate utilization and
metabolite exchange forming the basis of succession. Moreover,
the same is applicable in the area of biodegradation of
recalcitrant as well as xenobiotic compounds too, where co-
metabolism is shown to play the principle role. This involves
simultaneous oxidation of non-substrate compounds with that of
true substrates during vigorous growth of bacteria. The members
belonging to the genera Pseudomonas, Flavobacterium, Bacillus,
Azotobacter, Microbacterium, Hydrogenomonas, Achromobacter
and Xanthomonas are predominant co-metabolisers in the
ecosystem (Beam and Perry, 1973). This property of co-
metabolism has significant implications in the studies depicting
biochemical pathways, particularly involved in the metabolism
of polycyclic and polyaromatic compounds (Horvath, 1972;
Chauhan et al., 2008). Metabolomics studies of these processes
provide the information on the enzymes involved in the
conversion and pathways they participate in, thereby raising the
probability of their large-scale exploitation to the sites where
the native ecosystems have encountered the stress conditions
due to the accumulation and/or contamination of xenobiotic
and recalcitrant compounds. Many hydrocarbons such as
p-isopropyltoulene, n-butylcyclohexane, n-butylbenzene, ortho
and para xylene etc. are actively co-metabolized by the members
of genus Nocardia (Davis and Raymond, 1961;Raymond et al.,
1967). The inimitable metabolic power of such organisms
highlight strong implementable ability of PGP members of such
genera to remediate stresses imposed by contaminated soils on
crop and thus pave the way for bioremediation.
The quantitative metabolomics studies also permit
measurements of cellular processes with high accuracy and
precision (Noack and Wiechert, 2014). The high-throughput
mass spectrometric profiling of cellular metabolites of plant-
associated microbes under the influence of stressors could
reveal the level of interference by the stressor in the overall
cellular homeostasis (Figure 2). The communication between
plants and soil microbial community represents a bilateral
process involving root exudates and microbial-elaborated
signal response molecules (Oldroyd and Downie, 2008;
Inceoglu et al., 2011;Peiffer et al., 2013). The augmentation of
rhizosphere with exogenous microbial metabolites also needs
prior insights into the microbial metabolism. This includes
the ratio of cellular abundance, biomolecules elaborated under
normal and optimal circumstances, quantitative leakage,
participation of plant signals in the cascade and resulting counter
Frontiers in Plant Science | www.frontiersin.org 15 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 16
Meena et al. Microbe-Mediated Management of Abiotic Stress
response of microbes. It could be thoughtful to enrich such
biomolecules in the rhizosphere that are down-regulated due to
the influence of the stressor. Similar is applicable to the probable
management of stressor-responsive biomolecules influencing
overall communication process between the host and microbe.
The altered plant root exudation under the influence of stressor
fails to induce cascades described above in microbial systems that
transpire otherwise.
The accessibility of nucleotide data has been one of
the value additions for metabolomics studies (NCBI).
This ensures smoothening of future experiments targeting
systems biological perspectives. The recruitment of microbial-
originated biomolecules and/or in vitro synthesized metabolites
under simulated conditions in the phyllosphere have been
demonstrated recently (Sorty et al., 2016). This mainly deals
with the fact that live microbes, under stressed environment
fail to express vital genes for PGP activity. However, the impact
of enrichment of rhizosphere with the appropriate quantity
of such metabolites needs thorough evaluation. The insights
to host metabolomics are also beneficial to acquire knowledge
regarding the influence of host on post-colonization metabolism
of microbes. This could open the gateway for simulation of highly
complex endophytic environment.
Rhizosphere community also represents multifaceted system
involving biogeochemical cycling and exchange of nutrients,
leaving an excellent platform for gaining deep insights in to the
systems microbiology. Enormous pathways are simultaneously
operated by diverse members of microbial community.
Environmental factors have maximum influence on the
smooth operation of such pathways. Arrival of stressor/altered
environmental situation ultimately diverts overall functionality of
microbial system, thereby inducing variation in the community
structure. The understanding of biochemical links within and
between the members of an ecosystem is necessary to acquire the
phenotype-level knowledge in a given biogeochemical state of
event (Breitling et al., 2008).
CONCLUSION
Plant responses toward various abiotic stresses and microbe-
mediated stress mitigation strategies in plants have been
studied on sound grounds of molecular, biochemical,
physiological and ultrastructural parameters. Such studies have
been carried out encompassing different omics approaches
(genomics, metagenomics, metatranscriptomics, proteomics,
metaproteomics and metabolomics) that strengthened our
understanding behind the mechanisms of microbial interactions,
gene cascades and metabolic pathways, accumulation and
enhancement of various metabolites, proteins, enzymes and
up- and down regulation of different genes. Such studies could
yield dynamic data related to combined responses of plants
to multiple stresses, and the same is also pertinent with the
naturally associated or artificially inoculated microorganisms.
These studies provide new directions for improvising the existing
protocols in the field of plant–microbe interactions under stress,
and use of microorganisms and microbial metabolite molecules
for alleviation of diverse stresses encountered by plants.
The expected outcomes are facilitating germination, superior
sustenance, enhanced ability to combat adverse conditions of
environment and superior yield in plants because of the use of
microbe-elaborated molecules. Due to limitations regarding the
sustenance of microbes in diversity of stress environments and
variable responses at phenotypic level, it is always suitable to
implement microbe-derived natural products that are capable
of performing expected job of stress mitigation irrespective
of the environmental situations. To conclude, we strongly
advocate that there is a need to put greater attention on in-
depth studies pertaining to identification, trait characterization,
compatibility assessment, delivery methods and impact of
application of microbes isolated from diverse environmental
conditions for the mitigation of abiotic stresses in crop plants.
We need to find out new roles for microbial metabolites that
are being produced under stressed environmental conditions.
Established evidences exist to support the role of microbe-
mediated plant interactions in stress mitigation under diverse
climatic and edaphic conditions. However, more focused
omics-based research data generation following integrated
approaches encompassing genomics, metagenomics, proteomics
and metabolomics studies on specific plant–microbe-abiotic
stress system will be needed to resolve many facts behind precise
mechanisms of stress tolerance/mitigation in the crop plants.
AUTHOR CONTRIBUTIONS
KM proposed concept, KM and AS collected data and wrote the
manuscript, KC and UB collected data, AP and PG added abiotic
stress in plants, DS, RP, PS, HS, KK, VG, and PM contributed for
omics data and edited the manuscript.
ACKNOWLEDGMENTS
Financial assistance from Indian Council of Agricultural
Research (ICAR), India under Application of Microorganisms in
Agriculture and Allied Sectors (AMAAS-NBAIM/AMAAS/2014-
15/1a(6)/223) and DST-SERB Young Scientist scheme
(SB/YS/LS-218/2013) is gratefully acknowledged.
REFERENCES
Abulencia, C. B., Wyborski, D. L., Garcia, J. A., Podar, M., Chen, W., Chang,
S. H., et al. (2006). Environmental whole-genome amplification to access
microbial populations in contaminated sediments. Appl. Environ. Microbiol. 72,
3291–3301. doi: 10.1128/AEM.72.5.3291-3301.2006
Acebo-Guerrero, Y., Hernández-Rodríguez, A., Vandeputte, O.,
Miguélez-Sierra, Y., Heydrich-Pérez, M., Ye, L., et al. (2015).
Characterization of Pseudomonas chlororaphis from Theobroma
cacao L. rhizosphere with antagonistic activity against Phytophthora
palmivora (Butler). J. Appl. Microbiol. 119, 1112–1126. doi: 10.1111/jam.
12910
Frontiers in Plant Science | www.frontiersin.org 16 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 17
Meena et al. Microbe-Mediated Management of Abiotic Stress
Adediran, G. A., Ngwenya, B. T., Mosselmans, J. F. W., and HealK, V. (2016).
Bacteria–zinc co-localization implicates enhanced synthesis of cysteine-rich
peptides in zinc detoxification when Brassica juncea is inoculated with
Rhizobium leguminosarum.New Phytol. 209, 280–293. doi: 10.1111/nph.
13588
Agarwal, S., and Grover,A. (2006). Mole cular biology, biotechnology and genomics
of flooding-associated low O2 stress response in plants. Crit. Rev. Plant Sci. 25,
1–21. doi: 10.1080/07352680500365232
Ahmad, P., Hashem, A., Abd-Allah, E. F., Alqarawi, A. A., John, R.,
Egamberdieva, D., et al. (2015). Role of Trichoderma harzianum in mitigating
NaCl stress in Indian mustard (Brassica juncea L) through antioxidative defense
system. Front. Plant Sci. 6:868. doi: 10.3389/fpls.2015.00868
Akpinar, B. A., Kantar, M., and Budak, H. (2015). Root precursors of microRNAs
in wild emmer and modern wheats show major differences in response to
drought stress. Funct. Integr. Genomics 15, 587–598. doi: 10.1007/s10142-015-
0453-0
Alameda, D., Anten, N. P. R., and Villar, R. (2012). Soil compaction effects on
growth and root traits of tobacco depend on light, water regime and mechanical
stress. Soil Tillage Res. 120, 121–129. doi: 10.1016/j.still.2011.11.013
Alami, Y., Achouak, W., Marol, C., and Heulin, T. (2000). Rhizosphere soil
aggregation and plant growth promotion of sunflowers by exopolysaccharide
producing Rhizobium sp. strain isolated from sunflower roots. Appl. Environ.
Microbiol. 66, 3393–3398. doi: 10.1128/AEM.66.8.3393-3398.2000
Alavi, P., Starcher, M. R., Zachow, C., Müller, H., and Berg, G. (2013). Root-
microbe systems: the effect and mode of interaction of stress protecting agent
(SPA) Stenotrophomonas rhizophila DSM14405T. Front. Plant Sci. 4:141. doi:
10.3389/fpls.2013.00141
Al-Garni, S. M. S. (2006). Increasing NaCl-salt tolerance of a halophytic plant
Phragmites australis by mycorrhizal symbiosis. Am. Eurasian J. Agric. Environ.
Sci. 1, 119–126.
Ali, S. Z., Sandhya, V., Grover, M., Kishore, N., Rao, L. V., and Venkateswarlu, B.
(2009). Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum
seedlings to elevated temperatures. Biol. Fertil. Soil 46, 45–55. doi: 10.1007/
s00374-009-0404-9
Allen, D. K., Libourel, I. G., and Shachar-Hill, Y. (2009). Metabolic flux analysis
in plants: coping with complexity. Plant Cell Environ. 32, 1241–1257. doi:
10.1111/j.1365-3040.2009.01992.x
Almoguera, C., Coca, M. A., and Jouanin, L. (1995). Differential accumulation
of sunflower tetraubiquitin mRNAs during zygotic embryogenesis and
developmental regulation of their heat shock response. Plant Physiol. 107,
765–773. doi: 10.1104/pp.107.3.765
Amellal, N., Burtin, G., Bartoli, F., and Heulin, T. (1998). Colonization of wheat
rhizosphere by EPS producing Pantoea agglomerans and its effect on soil
aggregation. Appl. Environ. Microbiol. 64, 3740–3747.
An, F., Li, G., Li, Q. X., Li, K., Carvalho, L. J., Ou, W., et al. (2016). The
Comparatively proteomic analysis in response to cold stress in Cassava
Plantlets. Plant Mol. Biol. Report. 34, 1095–1110. doi: 10.1007/s11105-016-
0987-x
Andreasson, E., and Ellis, B. (2010). Convergence and specificity in the Arabidopsis
MAPK nexus. Trends Plant Sci. 15, 106–113. doi: 10.1016/j.tplants.2009.
12.001
Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress,
and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. doi: 10.1146/
annurev.arplant.55.031903.141701
Araujo, W. L., Santos, D. S., Dini-Andreote, F., Salgueiro-London˜o, J. K.,
Camargo-Neves, A. A., Andreote, F. D., et al. (2015). Genes related to
antioxidant metabolism are involved in Methylobacterium mesophilicum-
soybean interaction. Antonie Van Leeuwenhoek 108, 951–963. doi: 10.1007/
s10482-015-0548-6
Arevalo-Ferro, C., Reil, G., Gorg, A., Eberl, L., and Riedel, K. (2005). Biofilm
formation of Pseudomonas putida IsoF: the role of quorum sensing as assessed
by proteomics. Syst. Appl. Microbiol. 28, 87–114. doi: 10.1016/j.syapm.2004.10.
005
Arkhipova, T. N., Prinsen, E., Veselov, S. U., Martinenko,E. V., Melentie v, A. I., and
Kudoyarova, G. R. (2007). Cytokinin producing bacteria enhance plant growth
in drying soil. Plant Soil 292, 305–315. doi: 10.1007/s11104-007- 9233-5
Aroca, R., Porcel, R., and Ruiz-Lozano, J. M. (2007). How does arbuscular
mycorrhizal symbiosis regulate root hydraulic properties and plasma
membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity
stresses? New Phytol. 173, 808–816. doi: 10.1111/j.1469-8137.2006.01961.x
Aroca, R., Vernieri, P., and Ruiz-Lozano, J. M. (2008). Mycorrhizal and non-
mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous
ABA during drought stress and recovery. J. Exp. Bot. 59, 2029–2041. doi: 10.
1093/jxb/ern057
Ashraf, M., Hasnain, S., Berge, O., and Mahmood, T. (2004). Inoculating wheat
seeds with exopolysaccharide-producing bacteria restricts sodium uptake and
stimulates plant growth under salt stress. Biol. Fertil. Soil 40, 157–162. doi:
10.1007/s00374-004-0766-y
Atkinson, N. J., Lilley, C. J., and Urwin, P. E., (2013). Identification of
genes involved in the response of arabidopsis to simultaneous biotic
and abiotic stresses. Plant Physiol. 162, 2028–2041. doi: 10.1104/pp.113.
222372
Atkinson, N. J., and Urwin, P. E. (2012). The interaction of plant biotic and abiotic
stresses: from genes to the field. J. Exp. Bot. 63, 3523–3543. doi: 10.1093/jxb/
ers100
Babu, A. G., Shea, P. J., Sudhakar, D., Jung, I. B., and Oh, B. T. (2015). Potential
use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to
remediate heavy metal(loid)-contaminated mining site soil. J. Environ. Manage.
151, 160–166. doi: 10.1016/j.jenvman.2014.12.045
Bailey-Serres, J., and Voesenek, L. A. (2008). Flooding stress: acclimations and
genetic diversity. Annu. Rev. Plant Biol. 59, 313–339. doi: 10.1146/annurev.
arplant.59.032607.092752
Bakker, M. G., Manter, D. K., Sheflin, A. M., Weir, T. L., and Vivanco, J. M.
(2012). Harnessing the rhizosphere microbiome through plant breeding and
agricultural management. Plant Soil 360, 1–13. doi: 10.1007/s11104-012- 1361-x
Balbuena, T. S., Salas, J. J., Martínez-Force, E., Garcés, R., and Thelen, J. J.
(2011). Proteome analysis of cold acclimation in sunflower J. Proteome Res. 10,
2330–2346. doi: 10.1021/pr101137q
Balcazar, W., Rondón, J., Rengifo, M., Ball, M. M., Melfo, A., Gómez, W.,
et al. (2015). Bioprospecting glacial ice for plant growth promoting bacteria.
Microbiol. Res. 177, 1–7. doi: 10.1016/j.micres.2015.05.001
Baltruschat, H., Fodor, J., Harrach, B. D., Niemczyk, E., Barna, B., Gullner, G., et al.
(2008). Salt tolerance of barley induced by the root endophyte Piriformospora
indica is associated with a strong increase in anti-oxidants. New Phytol. 180,
501–510. doi: 10.1111/j.1469-8137.2008.02583.x
Barka, E. A., Nowak, J., and Clément, C. (2006). Enhancement of chilling
resistance of inoculated grapevine plantlets with a plant growth-promoting
rhizobacterium Burkholderia phytofirmans strain PsJN. Appl. Environ.
Microbiol. 72, 7246–7252. doi: 10.1128/AEM.01047-06
Barriuso, J., Solano, B. R., Fray, R. G., Camara, M., Hartmann, A., and Manero,
F. J. G. (2008a). Transgenic tomato plants alter quorum sensing in plant growth-
promoting rhizobacteria. Plant Biotechnol. J. 6, 442–452. doi: 10.1111/j.1467-
7652.2008.00331.x
Barriuso, J., Solano, B. R., and Mañero, F. J. G. (2008b). Protection against pathogen
and salt stress by four plant growth-promoting rhizobacteria isolated from
Pinus sp. on Arabidopsis thaliana.Phytopathology 98, 666–672. doi: 10.1094/
PHYTO-98- 6-0666
Beam, H. W., and Perry, J. J. (1973). Co-Metabolism as a factor in microbial
degradation of cycloparaffinic hydrocarbons. Arch. Microbiol. 91, 87–90.
Belimov, A. A., Dodd, I. C., Hontzeas, N., Theobald, J. C., Safronova, V. I., and
Davies, W. J. (2009). Rhizosphere bacteria containing 1-aminocyclopropane-
1-carboxylate deaminase increase yield of plants grown in drying soil via both
local and systemic hormone signalling. New Phytol. 181, 413–423. doi: 10.1111/
j.1469-8137.2008.02657.x
Belimov, A. A., Dodd, I. C., Safronova, V. I., Hontzeas, N., and Davies,W. J. (2007).
Pseudomonas brassicacearum strain Am3 containing 1-aminocyclopropane-
1-carboxylate deaminase can show both pathogenic and growth-promoting
properties in its interaction with tomato. J. Exp. Bot. 58, 1485–1495. doi: 10.
1093/jxb/erm010
Bertrand, H., Poly, F., Van, V. T., Lombard, N., Nalin, R., Vogel, T. M., et al.
(2005). High molecular weight DNA recovery from soils prerequisite for
biotechnological metagenomic library construction. J. Microbiol. Methods 62,
1–11. doi: 10.1016/j.mimet.2005.01.003
Bian, S., and Jiang, Y. (2009). Reactive oxygen species, antioxidant enzyme activities
and gene expression patterns and recovery. Sci. Hortic. 120, 264–270. doi:
10.1016/j.chemosphere.2016.02.072
Frontiers in Plant Science | www.frontiersin.org 17 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 18
Meena et al. Microbe-Mediated Management of Abiotic Stress
Binga, E. K., Lasken, R. S., and Neufeld, J. D. (2008). Something from (almost)
nothing: the impact of multiple displacement amplification on microbial
ecology. ISME J. 2, 233–241. doi: 10.1038/ismej.2008.10
Blokhina, O., and Fagerstedt, K. V. (2010). Reactive oxygen species and nitric oxide
in plant mitochondria: origin and redundant regulatory systems. Physiol. Plant.
138, 447–462. doi: 10.1111/j.1399-3054.2009.01340.x
Bolton, M. V. (2009). Primary metabolism and plant defense-Fuel for the fire. Mol.
Plant Microbe Interact. 22, 487–497. doi: 10.1094/MPMI-22-5- 0487
Bowen, G. D., and Rovira, A. D. (1991). “The rhizosphere: the hidden half of the
hidden half,” in Plant Roots: The Hidden Half, eds Y. Waisel, A. Eshel, and U.
Kalkafi (New York, NY: Marcel Dekker), 641–669.
Braud, A., Jezequel, K., Bazot, S., and Lebeau, T. (2009). Enhanced phytoextraction
of an agricultural Cr-, Hg- and Pb-contaminated soil by bioaugmentation
with siderophoreproducing bacteria. Chemosphere 74, 280–286. doi: 10.1016/
j.chemosphere.2008.09.013
Bräutigam, A., and Gowik, U. (2010). What can next generation sequencing do for
you? Next generation sequencing as a valuable tool in plant research. Plant Biol.
12, 831–841. doi: 10.1111/j.1438-8677.2010.00373.x
Bray, E. A., Bailey-Serres, J., and Weretilnyk, E. (2000). “Responses to abiotic
stresses,” in Biochemistry and Molecular Biology of Plants, eds W. Gruissem,
B. Buchannan, and R. Jones (Rockville, MD: American Society of Plant
Physiologists), 1158–1203.
Breitling, R., Vitkup, D., and Barrett, M. P. (2008). New surveyor tools for
charting microbial metabolic maps. Nat. Rev. Microbiol. 6, 156–161. doi: 10.
1038/nrmicro1797
Bromham, L., Saslis-Lagoudakis, C. H., Bennett, T. H., and Flowers, T. J. (2013).
Soil alkalinity and salt tolerance: adapting to multiple stresses. Biol. Lett.
9:20130642. doi: 10.1098/rsbl.2013.0642
Brotman, Y., Landau, U., Cuadros-Inostroza, Á, Takayuki, T., Fernie, A. R.,
Chet, I., et al. (2013). Trichoderma-plant root colonization: escaping early
plant defense responses and activation of the antioxidant machinery for
saline stress tolerance. PLoS Pathog. 9:e1003221. doi: 10.1371/journal.ppat.100
3221
Budak, H., and Akpinar, B. A. (2015). Plant miRNAs: biogenesis, organization
and origins. Funct. Integr. Genomics 15, 523–531. doi: 10.1007/s10142-015-
0451-2
Budak, H., Kantar, M., Bulut, R., and Akpinar, B. A. (2015). Stress responsive
miRNAs and isomiRs in cereals. Plant Sci. 235, 1–13. doi: 10.1016/j.plantsci.
2015.02.008
Bui, E. N. (2013). Soil salinity: a neglected factor in plant ecology and biogeography.
J. Arid Environ. 92, 14–25. doi: 10.1016/j.jaridenv.2012.12.014
Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E.,
Ahmadinejad, N., and Assenza, F. (2012). Revealing structure and assembly
cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95.
doi: 10.1038/nature11336
Bundy, J. G., Willey, T. L., Castell, R. S., Ellar, D. J., and Brindle, K. M. (2005).
Discrimination of pathogenic clinical isolates and laboratory strains of Bacillus
cereus by NMR-based metabolomic profiling. FEMS Microbiol. Lett. 242,
127–136. doi: 10.1016/j.femsle.2004.10.048
Burns, J., Fraser, P. D., and Bramley, P. M. (2003). Identification and quantification
of carotenoids, tocopherols and chlorophylls in commonly consumed fruits
and vegetables. Phytochemistry 62, 939–947. doi: 10.1016/S0031-9422(02)
00710-0
Caldana, C., Degenkolbe, T., Cuadros-Inostroza, A., Klie, S., Sulpice, R.,
Leisse, A., et al. (2011). High-density kinetic analysis of the metabolomic
and transcriptomic response of Arabidopsis to eight environmental conditions.
Plant J. 67, 869–884. doi: 10.1111/j.1365-313X.2011.04640.x
Chang, P., Gerhardt, K. E., Huang, X.-D., Yu, X.-M., Glick, B. R., Gerwing,
P. D., et al. (2014). Plant growthpromoting bacteria facilitate the growth of
barley and oats in saltimpacted soil: implications for phytoremediation of saline
soils. Int. J. Phytoremediation 16, 1133–1147. doi: 10.1080/15226514.2013.
821447
Chauhan, A., Faziurrahman, Oakeshott, J. G., and Jain, R. K. (2008). Bacterial
metabolism of polycyclic aromatic hydrocarbons: strategies for bioremediation.
J. Ind. Microbiol. 48, 95–113. doi: 10.1007/s12088-008-0010- 9
Chaves, M. M., and Oliveira, M. M. (2004). Mechanisms underlying plant resilience
to waterdeficits: prospects for water-saving agriculture. J. Exp. Bot. 55, 2365–
2384. doi: 10.1093/jxb/erh269
Chen, J., Han, G., Shang, C., Li, J., Zhang, H., Liu, F., et al. (2015). Proteomic
analyses reveal differences in cold acclimation mechanisms in freezing-tolerant
and freezing-sensitive cultivars of alfalfa. Front. Plant Sci. 6:105. doi: 10.3389/
fpls.2015.00105
Chen, K., and Pachter, L. (2005). Bioinformatics for whole genome shotgun
sequencing of microbial communities. PLoS Comput. Biol. 1, 106–112. doi:
10.1371/journal.pcbi.0010024
Chet, I., and Inbar, J. (1994). Biological control of fungal pathogens. Appl. Biochem.
Biotechnol. 48, 37–43. doi: 10.1007/BF02825358
Chinnusamy, V., Schumaker, K., and Zhu, J. K. (2004). Molecular genetics
perspectives on cross-talk and specifcity in abiotic stress signalling in plants.
J. Exp. Bot. 55, 225–236. doi: 10.1093/jxb/erh005
Cho, S. M., Kang, B. R., Han, S. H., Anderson, A. J., Park, J. Y., Lee, Y. H.,
et al. (2008). 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas
chlororaphis O6, is involved in induction of systemic tolerance to drought in
Arabidopsis thaliana.Mol. Plant Microbe Interact. 21, 1067–1075. doi: 10.1094/
MPMI-21-8-1067
Contreras-Cornejo, H. A., Macías-Rodríguez, L., Cortés-Penagos, C., and López-
Bucio, J. (2009). Trichoderma virens, a plant beneficial fungus, enhances
biomass production and promotes lateral root growth through an auxin-
dependent mechanism in Arabidopsis.Plant Physiol. 149, 1579–1592. doi: 10.
1104/pp.108.130369
Cordwell, S. J., Basseal, D. J., and Humphery-Smith, I. (1997). Proteome
analysis of Spiroplasma melliferum (A56) and protein characterisation across
species boundaries. Electrophoresis 18, 1335–1346. doi: 10.1002/elps.11501
80809
Cordwell, S. J., Wilkins, M. R., Cerpa-poljak, A., Gooley, A. A., Duncan, M.,
Williams, K. L., et al. (1995). Cross species identification of proteins separated
by 2-dimensional gel-electrophoresis using matrix-assisted laser-desorption
ionization time-of-flight mass-spectrometry and aminoacid-composition.
Electrophoresis 16, 438–443. doi: 10.1002/elps.1150160171
Cramer, G. R., Urano, K., Delrot, S., Pezzotti, M., and Shinozaki, K. (2011). Effects
of abiotic stress on plants: a systems biology perspective. BMC Plant Biol.
11:163. doi: 10.1186/1471-2229- 11-163
Crane, T. A., Roncoli, C., and Hoogenboom, G. (2011). Adaptation to climate
change and climate variability: the importance of understanding agriculture
as performance. NJAS –Wag. J. Life Sci. 57, 179–185. doi: 10.1016/j.njas.2010.
11.002
Creus, C. M., Sueldo, R. J., and Barassi, C. A. (2004). Water relations and yield in
Azospirillum-inoculated wheat exposed to drought in the field. Can. J. Bot. 82,
273–281. doi: 10.1139/b03-119
Cunrath, O., Gasser, V., Hoegy, F., Reimmann, C., Guillon, L., Schalk, I. J., et al.
(2015). A cell biological view of the siderophore pyochelin iron uptake pathway
in Pseudomonas aeruginosa.Environ. Microbiol. 17, 171–185. doi: 10.1111/
1462-2920.12544
Curaba, J., Singh, M. B., and Bhalla, P. L. (2014). miRNAs in the crosstalk between
phytohormone signalling pathways. J. Exp. Bot. 65, 1425–1438. doi: 10.1093/
jxb/eru002
Cushman, J. C., De Rocher,E. J., and Bohnert, H. J. (1990). “Gene expression during
adaptation to salt stress,” in Environmental Injury of Plants, ed. F. Kalterman
(San Diego, CA: Academic Press), 173–203.
Daei, G., Ardekani, M. R., Rejali, F., Teimuri, S., and Miransari, M. (2009).
Alleviation of salinity stress on wheat yield, yield components, and nutrient
uptake using arbuscular mycorrhizal fungi under field conditions. J. Plant
Physiol. 66, 617–625. doi: 10.1016/j.jplph.2008.09.013
Dardanelli, M. S., Fernández de Córdoba, F. J., Espuny, M. R., Rodríguez Carvajal,
M. A., Soria Díaz, M. E., Gil Serrano, A. M., et al. (2008). Effect of Azospirillum
brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and
Nod factor production under salt stress. Soil Biol. Biochem. 40, 2713–2721.
doi: 10.1016/j.soilbio.2008.06.016
Davis, J. B., and Raymond, R. L. (1961). Oxidation of alkyl-substituted cyclic
hydrocarbons by a nocardia during growth on n-alkanes. Appl. Microbiol. 9,
383–388.
de Castro, A. P., Sartori, A., Silva, M. R., Quirino, B. F., and Kruger, R. H.
(2013). Combining "omics" strategies to analyze the biotechnological potential
of complex microbial environments. Curr. Protein Pept. Sci. 14, 447–458.
de Lorenzo, L., Merchan, F., Laporte, P., Thompson, R., Clarke, J., Sousa, C.,
et al. (2009). A novel plant leucine-rich repeat receptor kinase regulates the
Frontiers in Plant Science | www.frontiersin.org 18 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 19
Meena et al. Microbe-Mediated Management of Abiotic Stress
response of Medicago truncatula roots to salt stress. Plant Cell 21, 668–680.
doi: 10.1105/tpc.108.059576
de Zelicourt, A., Al-Yousif, M., and Hirt, H. (2013). Rhizosphere microbes as
essential partners for plant stress tolerance. Mol. Plant. 6, 242–245. doi: 10.1093/
mp/sst028
Defez, R., Esposito, R., Angelini, C., and Bianco, C. (2016). Overproduction of
indole-3-acetic acid in free-living rhizobia induces transcriptional changes
resembling those occurring in nodule bacteroids. Mol. Plant Microbe Interact.
29, 484–495. doi: 10.1094/MPMI-01- 16-0010-R
del Amor, F., and Cuadra-Crespo, P. (2012). Plant growth-promoting bacteria as a
tool to improve salinity tolerance in sweet pepper. Funct. Plant Biol. 39, 82–90.
doi: 10.1071/FP11173
Depuyd, S., and Hardtke, C. S. (2011). Hormone signalling crosstalk in plant
growth regulation. Curr. Biol. 21, 365–373. doi: 10.1016/j.cub.2011.03.013
Diels, L., van der Lelie, N., and Bastiaens, L. (2002). New developments in treatment
of heavy metal contaminated soils. Rev. Env. Sci. Biotechnol. 1, 75–82. doi:
10.1023/A:1015188708612
Dinneny, J. R., Long, T. A., Wang, J. Y., Jung, J. W., Mace, D., Pointer, S., et al.
(2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress.
Science 320, 942–945. doi: 10.1126/science.1153795
Dourado, M. N., Camargo Neves, A. A., Santos, D. S., and Araújo, W. L. (2015).
Biotechnological and agronomic potential of endophytic pink-pigmented
methylotrophic Methylobacterium spp. Biomed. Res. Int. 2015:909016. doi: 10.
1155/2015/909016
Egamberdiyeva, D., and Höflich, G. (2003). Influence of growth-promoting on
the growth of wheat in different soils and temperatures. Soil Biol. Biochem. 35,
973–978. doi: 10.1016/S0038-0717(03)00158- 5
El-Daim, I. A. A., Bejai, S., and Meijer, J. (2014). Improved heat stress tolerance
of wheat seedlings by bacterial seed treatment. Plant Soil 379, 337–350. doi:
10.1007/s11104-014-2063-3
Emamverdian, A., Ding, Y., Mokhberdoran, F., and Xie, Y. (2015). Heavy
metal stress and some mechanisms of plant defense response. Sci. World J.
2015:756120. doi: 10.1155/2015/756120
Eyers, L., George, I., Schuler, L., Stenuit, B., Agathos, S. N., and El, F. S. (2004).
Environmental genomics: exploring the unmined richness of microbes to
degrade xenobiotics. Appl. Microbiol. Biotechnol. 66, 123–130. doi: 10.1007/
s00253-004-1703-6
Farrar, K., Bryant, D., and Cope-Selby, N. (2014). Understanding and engineering
beneficial plant–microbe interactions: plant growth promotion in energy crops.
Plant Biotechnol. J. 12, 1193–1206. doi: 10.1111/pbi.12279
Ferret, C., Sterckeman, T., Cornu, J. Y., Gangloff, S., Schalk, I. J., and Geoffroy,
V. A. (2014). Siderophore-promoted dissolution of smectite by fluorescent
Pseudomonas.Environ. Microbiol. Rep. 6, 459–467. doi: 10.1111/1758-2229.
12146
Figueiredo, M. V. B., Burity, H. A., Martinez, C. R., and Chanway, C. P. (2008).
Alleviation of drought stress in common bean (Phaseolus vulgaris L.) by co-
inoculation with Paenibacillus polymyxa and Rhizobium tropici.Appl. Soil Ecol.
40, 182–188. doi: 10.1016/j.apsoil.2008.04.005
Flowers, T. J., Galal, H. K., and Bromham, L. (2010). Evolution of halophytes:
multiple origins of salt tolerance in land plants. Funct. Plant Biol. 37, 604–612.
doi: 10.1007/s10142-011- 0218-3
Foyer, C. H., and Noctor, G. (2005). Oxidant and antioxidant signalling in plants: a
re-evaluation of the concept of oxidative stress in a physiological context. Plant
Cell Environ. 28, 1056–1071. doi: 10.1111/j.1365-3040.2005.01327.x
Franken, P. (2012). The plant strengthening root endophyte Piriformospora indica:
potential application and the biology behind. Appl. Microbiol. Biotechnol. 96,
1455–1464. doi: 10.1007/s00253-012- 4506-1
Fugyeuredi, M. V. B., Vilhar, J. J., Burity, H. A., and de Franca, F. P. (1999).
Alleviation of water stress effects in cowpea by Bradyrhizobium spp. inoculation.
Pant Soil 207, 67–75.
Gaiero, J. R., McCall, C. A., Thompson, K. A., Day, N. J., Best, A. S., and Dunfield,
K. E. (2013). Inside the root microbiome: bacterial root endophytes and plant
growth promotion. Am. J. Bot. 100, 1738–1750. doi: 10.3732/ajb.1200572
Gao, P., Bai, X., Yang, L., Lv, D., Pan, X., Li, Y., et al. (2011). osa-MIR393: a
salinity and alkaline stress-related microRNA gene. Mol. Biol. Rep. 38, 237–242.
doi: 10.1007/s11033-010- 0100-8
German, M. A., Burdman, S., Okon, Y., and Kigel, J. (2000). Effects of Azospirillum
brasilense on root morphology of common bean (Phaseolus vulgaris L.)
under different water regimes. Biol. Fertil. Soils 32, 259–264. doi: 10.1007/
s003740000245
Ghabooli, M., Khatabi, B., Ahmadi, F. S., Sepehri, M., Mirzaei, M., Amirkhani, A.,
et al. (2013). Proteomics study reveals the molecular mechanisms underlying
water stress tolerance induced by Piriformospora indica in barley. J. Proteomics
94, 289–301. doi: 10.1016/j.jprot.2013.09.017
Gill, S. S., and Tuteja, N. (2010). Reactive oxygen species and antioxidant
machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48,
909–930. doi: 10.1016/j.plaphy.2010.08.016
Gopalakrishnan, S., Sathya, A., Vijayabharathi, R., Varshney, R. K., Gowda, C. L.,
and Krishnamurthy, L. (2015). Plant growth promoting rhizobia: challenges and
opportunities. 3Biotech 5, 355–377.
Grainger, C. M., and Rajcan, I. (2013). Characterization of the genetic changes in a
multi-generational pedigree of an elite Canadian soybean cultivar. Theor. Appl.
Genet. 127, 211–229. doi: 10.1007/s00122-013-2211-9
Gravel, V., Antoun, H., and Tweddell, R. J. (2007). Growth stimulation and
fruit yield improvement of greenhouse tomato plants by inoculation with
Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic
acid (IAA). Soil Biol. Biochem. 39, 1968–1977. doi: 10.1016/j.soilbio.2007.
02.015
Grayson, M. (2013). Agriculture and drought. Nature 501:S1. doi: 10.1038/501S1a
Grichko, V. P., and Glick, B. R. (2001). Amelioration of flooding stress by ACC
deaminase containing plant growth promoting bacteria. Can. J. Microbiol. 47,
77–80.
Gupta, B., and Huang, B. (2014). Mechanism of salinity tolerance in plants:
physiological, biochemical, and molecular characterization. Int. J. Genomics
2014:701596. doi: 10.1155/2014/701596
Hamdia, A. B. E., Shaddad, M. A. K., and Doaa, M. M. (2004). Mechanisms of salt
tolerance and interactive effects of Azospirillum brasilense inoculation on maize
cultivars grown under salt stress conditions. Plant Growth Regul. 44, 165–174.
doi: 10.1023/B:GROW.0000049414.03099.9b
Handelsman, J., Tiedje, J., Alvarez-Cohen, L., Ashburner, M., Cann, I. K. O.,
Delong, E. F., et al. (2007). The New Science of Metagenomics: Revealing the
Secrets of Our Microbial Planet. Washington, DC: National Academy of Science.
Hasegawa, P. M., Bressan, R. A., Zhu, J.-K., and Bohnert, H. J. (2000). Plant cellular
and molecular responses to high salinity. Annu. Rev. Plant Biol. 51, 463–499.
doi: 10.1146/annurev.arplant.51.1.463
Hayat, R., Ali, S., Amara, U., Khalid, R., and Ahmed, I. (2010). Soil beneficial
bacteria and their role in plant growth promotion: a review. Ann. Microbiol.
60, 579–598. doi: 10.1007/s13213-010- 0117-1
Heil, M., and Bostock, R. M. (2002). Induced systemic resistance (ISR) against
pathogens in the context of induced plant defences. Ann. Bot. 89, 503–512.
doi: 10.1093/aob/mcf076
Hey, S. J., Byrne, E., and Halford, N. G. (2010). The interface between metabolic
and stress signalling. Ann. Bot. 105, 197–203. doi: 10.1093/aob/mcp285
Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt, S., et al.
(2015). Priming and memory of stress responses in organisms lacking a nervous
system. Biol. Rev. 91, 1118–1133. doi: 10.1111/brv.12215
Hirel, B., Le Gouis, J., Ney, B., and Gallais, A. (2007). The challenge of improving
nitrogenuse efficiency in crop plants: towards a more central role for genetic
variability andquantitative genetics within integrated approaches. J. Exp. Bot.
58, 2369–2387. doi: 10.1093/jxb/erm097
Hollywood, K., Brison, R. D., and Goodacre, R. (2006). Metabolomics: current
technologies and future trends. Proteomics 6, 4716–4723. doi: 10.1002/pmic.
200600106
Horvath, R. S. (1972). Microbial co-metabolism and the degradation of organic
compounds in nature. Bacteriol. Rev. 36, 146–155.
Iba, K. (2002). Acclimative response to temperature stress in higher plants:
approaches of gene engineering for temperature tolerance. Annu. Rev. Plant
Biol. 53, 225–245. doi: 10.1146/annurev.arplant.53.100201.160729
Inceoglu, O. L., Al-Soud, W. A., Salles, J. F., Alexander, V. S., and Elsas, J. D. V.
(2011). Comparative analysis of bacterial communities in a potato field as
determined by pyrosequencing. PLoS ONE 6:e23321. doi: 10.1371/journal.pone.
0023321
Islam, F., Yasmeen, T., Ali, Q., Ali, S., Arif, M. S., Hussain, S., et al. (2014). Influence
of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat
under Zn stress. Ecotoxicol. Environ. Saf. 104, 285–293. doi: 10.1016/j.ecoenv.
2014.03.008
Frontiers in Plant Science | www.frontiersin.org 19 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 20
Meena et al. Microbe-Mediated Management of Abiotic Stress
Iyer, N. J., Tang, Y., and Mahalingam, R. (2013). Physiological, biochemical
and molecular responses to combination of drought and ozone in
Medicago truncatula.Plant Cell Environ. 2013, 706–720. doi: 10.1111/pce.
12008
Jackson, M. B. (1991). “Regulation of water relationships in flooded plants by ABA
from leaves, roots and xylem sap,” in Abscisic Acid. Physiology and Biochemistry,
eds W. J. Davis and H. G. Jones (Oxford: Bios Scientific), 217–226.
Jha, Y., Sablok, G., Subbarao, N., Sudhakar, R., Fazil, M. H. U. T., Subramanian,
R. B., et al. (2014). Bacterial-induced expression of RAB18 protein in Orzya
sativa salinity stress and insights into molecular interaction with GTP ligand.
J. Mol. Recognit. 27, 521–527. doi: 10.1002/jmr.2371
Jia, X., Sun, C., Zuo, Y., Li, G., Li, G., Ren, L., et al. (2016). Integrating
transcriptomics and metabolomics to characterise the response of Astragalus
membranaceus Bge. var. mongolicus (Bge.) to progressive drought stress. BMC
Genomics 17:188. doi: 10.1186/s12864-016- 2554-0
Jia, X., Wang, W.-X., Ren, L., Chen, Q.-J., Mendu, V., Willcut, B., et al. (2009).
Differential and dynamic regulation of miR398 in response to ABA and salt
stress in Populus tremula and Arabidopsis thaliana.Plant Mol. Biol. 71, 51–59.
doi: 10.1007/s11103-009- 9508-8
Jiang, Q.-Y., Zhuo, F., Long, S.-H., Zhao, H.-D., Yang, D.-J., Ye, Z.-H., et al.
(2016). Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd
toxicity of Lonicera japonica grown in Cd-added soils? Sci. Rep. 6:21805. doi:
10.1038/srep21805
Jiao, N., Herndl, G. J., Hansell, D. A., Benner, R., Kattner, G., Wilhelm, S. W.,
et al. (2010). Microbial production of recalcitrant dissolved organic matter:
long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599.
doi: 10.1038/nrmicro2386
Jin, J., Watt, M., and Mathesius, U. (2012). The auto regulation gene SUNN
mediates changes in root organ formation in response to nitrogen through
alteration of shoot-to-root auxin transport. Plant Physiol. 159, 489–500. doi:
10.1104/pp.112.194993
Jorge, T. F., Rodrigues, J. A., Caldana, C., Schmidt, R., van Dongen, J. T.,
Thomas-Oates, J., et al. (2015). Mass-spectrometry-based plant metabolomics:
metabolite responses to abiotic stress. Mass Spectrom. Rev. 35, 620–649. doi:
10.1002/mas.21449
Kantar, M., Lucas, S. J., and Budak, H. (2011). miRNA expression patterns of
Triticum dicoccoides in response to shock drought stress. Planta 233, 471–484.
doi: 10.1007/s00425-010- 1309-4
Kapardar, R. K., Ranjan, R., Grover, A., Puri, M., and Sharma, R. (2010).
Identification and characterization of genes conferring salt tolerance to
Escherichia coli from pond water metagenome. Bioresour. Technol. 101, 3917–
3924. doi: 10.1016/j.biortech.2010.01.017
Kasotia, A., Varma, A., and Choudhary, D. K. (2015). Pseudomonas-mediated
mitigation of salt stress and growth promotion in Glycine max.Agric. Res. 4,
31–41. doi: 10.1007/s40003-014- 0139-1
Kasurinen, A., Biasi, C., Holopainen, T., Rousi, M., Maenpaa, M., and
Oksanen, E. (2012). Interactive effects of elevated ozone and temperature
on carbon allocation of silver birch (Betula pendula) genotypes in an
open-air field exposure. Tree Physiol. 32, 737–751. doi: 10.1093/treephys/
tps005
Kaushal, M., and Wani, S. P. (2016). Plant-growth-promoting rhizobacteria:
drought stress alleviators to ameliorate crop production in drylands. Ann.
Microbiol. 66, 35–42. doi: 10.1007/s13213-015-1112- 3
Kaya, C., Ashraf, M., Sonmez, O., Aydemir, S., Tuna, A. L., and Cullu, M. A. (2009).
The influence of arbuscular mycorrhizal colonisation on key growth parameters
and fruit yield of pepper plants grown at high salinity. Sci. Hortic. 121, 1–6.
doi: 10.1016/j.scienta.2009.01.001
Kertesz, M. A., Leisinger, T., and Cook, A. M. (1993). Proteins induced by
sulfate limitation in Escherichia coli,Pseudomonas putida, or Staphylococcus
aureus.J. Bacteriol. 175, 1187–1190. doi: 10.1128/jb.175.4.1187-1190.
1993
Ketchum, R. E., Rithner, C. D., Qiu, D., Kim, Y. S., Williams, R. M., and
Croteau, R. B. (2003). Taxus metabolomics: methyl jasmonate preferentially
induces production of taxoids oxygenated at C-13 in Taxus x media
cell cultures. Phytochemistry 62, 901–909. doi: 10.1016/S0031-9422(02)
00711-2
Khan, A., Sirajuddin, Zhao, X. Q., Javed, M. T., Khan, K. S., Bano, A.,
et al. (2016). Bacillus pumilus enhances tolerance in rice (Oryza sativa
L.) to combined stresses of NaCl and high boron due to limited uptake
of Na+.Environ. Exp. Bot. 124, 120–129. doi: 10.1016/j.envexpbot.2015.
12.011
Khan, M. A., Gemenet, D. C., and Villordon, A. (2016). Root system architecture
and abiotic stress tolerance: current knowledge in root and tuber crops. Front.
Plant Sci. 7:1584. doi: 10.3389/fpls.2016.01584
Kim, S. I., Choi, J. S., and Kahng, H. Y. (2007). A proteomics strategy for the
analysis of bacterial biodegradation pathways. OMICS 11, 280–294. doi: 10.
1089/omi.2007.0019
Kissoudis, C., van de Wiel, C., Visser, R. G. F., and van der Linden, G. (2014).
Enhancing crop resilience to combined abiotic and biotic stress through the
dissection of physiological and molecular crosstalk. Front. Plant Sci. 5:207.
doi: 10.3389/fpls.2014.00207
Koini, M. A., Alvey, L., Allen, T., Tilley, C. A., Harberd, N. P., Whitelam, G. C., et al.
(2009). High temperature-mediated adaptations in plant architecture require
the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413. doi: 10.1016/j.cub.
2009.01.046
Kosova, K., Vitamvas, P., Urban, M. O., Klima, M., Roy, A., and Prasil, I. T.
(2015). Biological networks underlying abiotic stress tolerance in temperate
crops- a proteomic perspective. Int. J. Mol. Sci. 16, 20913–20942. doi: 10.3390/
ijms160920913
Koussevitzky, S., Suzuki, N., Huntington, S., Armijo, L., Sha, W., Cortes, D., et al.
(2008). Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis
thaliana to stress combination. J. Biol. Chem. 283, 34197–34203. doi: 10.1074/
jbc.M806337200
Kubicek, C. P., Herrera-Estrella, A., Seidl-Seiboth, V., Martinez, D. A., Druzhinina,
I. S., Thon, M., et al. (2011). Comparative genome sequence analysis
underscores mycoparasitism as the ancestral life style of Trichoderma.Genome
Biol. 12:R40. doi: 10.1186/gb-2011-12-4- r40
Kumari, S., Vaishnav, A., Jain, S., Varma, A., and Choudhary, D. K.
(2015). Bacterial-mediated induction of systemic tolerance to salinity with
expression of stress alleviating enzymes in soybean (Glycine max L.
Merrill). J. Plant Growth Regul. 34, 558–573. doi: 10.1007/s00344-015-
9490-0
Li, J. L., Cui, J., and Cheng, D. Y. (2015). Computational identification
and characterization of conserved miRNAs and their target genes in
beet (Beta vulgaris) Genet. Mol. Res. 14, 9103–9108. doi: 10.4238/2015.
August.7.19
Li, Q., Zhao, P., Li, J., Zhang, C., Wang, L., and Ren, Z. (2014). Genome-
wide analysis of the WD-repeat protein family in cucumber and
Arabidopsis.Mol. Genet. Genomics 289, 103–124. doi: 10.1007/s00438-013-
0789-x
Li, Y. F., Zheng, Y., Addo-Quaye, C., Zhang, L., Saini, A., Jagadeeswaran, G., et al.
(2010). Transcriptome-wide identification of microRNA targets in rice. Plant J.
62, 742–759. doi: 10.1111/j.1365-313X.2010.04187.x
Li, Z., Setsuko, W., Fischer, B. B., and Niyogi, K. K. (2009). Sensing and responding
to excess light. Annu. Rev. Plant Biol. 60, 239–260. doi: 10.1146/annurev.
arplant.58.032806.103844
Licausi, F., Ohme-Takagi, M., and Perata, P. (2013). APETALA2/Ethylene
Responsive Factor (AP2/ERF) transcription factors: mediators of stress
responses and developmental programs. New Phytol. 199, 639–649. doi: 10.
1111/nph.12291
Liljeqvist, M., Ossandon, F. J., Gonzalez, C., Rajan, S., Stell, A., Valdes, J., et al.
(2015). Metagenomic analysis reveals adaptations to a cold-adapted lifestyle in
a low-temperature acid mine drainage stream. FEMS Microbiol. Ecol. 91:fiv011.
doi: 10.1093/femsec/fiv011
Lim, J. H., and Kim, S. D. (2013). Induction of drought stress resistance by multi-
functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol. J. 29,
201–208. doi: 10.5423/PPJ.SI.02.2013.0021
Lima, J. C., Arenhart, R. A., Margis-Pinheiro, M., and Margis, R. (2011). Aluminum
triggers broad changes in microRNA expression in rice roots. Genet. Mol. Res.
10, 2817–2832. doi: 10.4238/2011.November.10.4
Liu, Z., Li, Y., Cao, H., and Ren, D. (2015). Comparative phospho-proteomics
analysis of salt-responsive phosphoproteins regulated by the MKK9-MPK6
cascade in Arabidopsis.Plant Sci. 241, 138–150. doi: 10.1016/j.plantsci.2015.
10.005
Luan, Y., Cui, J., Zhai, J., Li, J., Han, L., and Meng, J. (2015). High-throughput
sequencing reveals differential expression of miRNAs in tomato inoculated
Frontiers in Plant Science | www.frontiersin.org 20 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 21
Meena et al. Microbe-Mediated Management of Abiotic Stress
with Phytophthora infestans.Planta 241, 1405–1416. doi: 10.1007/s00425-015-
2267-7
Lupi, C. G., Colangelo, T., and Mason, C. A. (1995). Two-dimensional gel
electrophoresis analysis of the response of Pseudomonas putida KT2442 to
2-Chlorophenol. Appl. Environ. Microbiol. 61, 2863–2872.
Ma, J. F., Mitani, N., Nagao, S., Konishi, S., Tamai, K., Iwashita, T., et al. (2004).
Characterization of the Silicon uptake system and molecular mapping of the
Silicon transporter gene in rice. Plant Physiol. 136, 3284–3289. doi: 10.1104/pp.
104.047365
Ma, Y., Rajkumar, M., Luo, Y., and Freitas, H. (2013). Phytoextraction of
heavy metal polluted soils using Sedum plumbizincicola inoculated with metal
mobilizing Phyllobacterium myrsinacearum RC6b. Chemosphere 93, 1386–1392.
doi: 10.1016/j.chemosphere.2013.06.077
Madhaiyan, M., Poonguzhali, S., and Sa, T. (2007). Metal tolerating methylotrophic
bacteria reduces nickel and cadmium toxicity and promotes plant growth of
tomato (Lycopersicon esculentum L.). Chemosphere 69, 220–228. doi: 10.1016/j.
chemosphere.2007.04.017
Manavalan, L. P., Guttikonda, S. K., Tran, L. S. P., and Nguyen, H. T.
(2009). Physiological and molecular approaches to improve drought
resistance in soybean. Plant Cell Physiol. 50, 1260–1276. doi: 10.1093/pcp/
pcp082
Martínez-Cortés, T., Pomar, F., Merino, F., and Novo-Uzal, E. (2014). A proteomic
approach to Physcomitrella patens rhizoid exudates. J. Plant Physiol. 171,
1671–1678. doi: 10.1016/j.jplph.2014.08.004
Marulanda, A., Azcón, R., Chaumont, F., Ruiz-Lozano, J. M., and Aroca, R.
(2010). Regulation of plasma membrane aquaporins by inoculation with a
Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed
and salt-stressed conditions. Planta 232, 533–543. doi: 10.1007/s00425-010-
1196-8
Marulanda, A., Porcel, R., Barea, J. M., and Azcon, R. (2007). Drought tolerance
and antioxidant activities in lavender plants colonized by native drought
tolerant or drought sensitive Glomus species. Microb. Ecol. 54, 543–552. doi:
10.1007/s00248-007-9237-y
Massad, T. J., Dyer, L. A., and Vega, C. G. (2012). Cost of defense and a test of the
carbon-nutrient balanceand growth-differentation balance hypotheses for two
co-occurring classes of plant defense. PLoS ONE 7:7554. doi: 10.1371/journal.
pone.0047554
Mathew, D. C., Ho, Y.-N., Gicana, R. G., Mathew, G. M., Chien, M.-C., and
Huang, C.-C. (2015). A rhizosphere-associated symbiont, Photobacterium spp.
strain MELD1, and its targeted synergistic activity for phytoprotection
against mercury. PLoS ONE 10:e0121178. doi: 10.1371/journal.pone.
0121178
Matilla, M. A., Ramos, J. L., Bakker, P. A., Doornbos, R., Badri, D. V., Vivanco,J. M.,
et al. (2010). Pseudomonas putida KT2440 causes induced systemic resistance
and changes in Arabidopsis root exudation. Environ. Microbiol. Rep.2, 381–388.
doi: 10.1111/j.1758-2229.2009.00091.x
Matysik, J., Alia, A., Bhalu, B., and Mohanty, P. (2002). Molecular mechanisms of
quenching of reactive oxygen species by proline under stress in plants. Curr. Sci.
82, 525–532.
Mayak, S., Tirosh, T., and Glick, B. R. (2004). Plant growth-promoting bacteria
confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 42,
565–572. doi: 10.1016/j.plaphy.2004.05.009
McCue, K. F., and Hanson, A. D. (1990). Salt-inducible betaine aldehyde
dehydrogenase from sugar beet: cDNA cloning and expression. Trends
Biotechnol. 8, 358–362. doi: 10.1016/0167-7799(90)90225-M
Meena, K. K., Kumar, M., Kalyuzhnaya, M. G., Yandigeri, M. S., Singh, D. P.,
Saxena, A. K., et al. (2012). Epiphytic pink-pigmented methylotrophic bacteria
enhance germination and seedling growth of wheat (Triticum aestivum) by
producing phytohormone. Antonie Van Leeuwenhoek 101, 777–786. doi: 10.
1007/s10482-011-9692-9
Meng, C., Zeleznik, O. A., Thallinger, G. G., Kuster, B., Gholami, A. M., and
Culhane, A. C. (2016). Dimension reduction techniques for the integrative
analysis of multi-omics data. Brief. Bioinform. 17, 628–641. doi: 10.1093/bib/
bbv108
Micallef, S. A., Channer, S., Shiaris, M. P., and Colón-Carmona, A. (2009). Plant
age and genotype impact the progression of bacterial community succession in
the Arabidopsis rhizosphere. Plant Signal. Behav. 4, 777–780. doi: 10.1093/jxb/
erp053
Mickelbart, M. V., Paul, M., Hasegawa, P. M., and Bailey-Serres, J. (2015). Genetic
mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat.
Rev. Genet. 16, 237–251. doi: 10.1038/nrg3901
Mishra, B. K., Meena, K. K., Dubey, P. N., Aishwath, O. P., Kant, K., Sorty,
A. M., et al. (2016). Influence on yield and quality of fennel (Foeniculum
vulgare Mill.) grown under semi-arid saline soil, due to application of native
phosphate solubilizing rhizobacterial isolates. Ecol. Eng. 97, 327–333. doi: 10.
1016/j.ecoleng.2016.10.034
Mittler, R. (2006). Abiotic stress, the field environment and stress combination.
Trends Plant Sci. 11, 15–19. doi: 10.1016/j.tplants.2005.11.002
Mittler, R., and Blumwald, E. (2010). Genetic engineering for modern agriculture:
challenges and perspectives. Annu. Rev. Plant Biol. 61, 443–462. doi: 10.1146/
annurev-arplant- 042809-112116
Moliterni, V. M. C., Paris, R., Onofri, C., Orrù, L., Cattivelli, L., Pacifico, D.,
et al. (2015). Early transcriptional changes in Beta vulgaris in response
to low temperature. Planta 242, 187–201. doi: 10.1007/s00425-015-
2299-z
Morrow, K. J. Jr. (2010). Mass spec central to metabolomics. Gen. Eng. Biotechnol.
News 30, 1–3.
Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev.
Plant Biol. 59, 651–681. doi: 10.1146/annurev.arplant.59.032607.092911
Nadeem, S. M., Ahmad, M., Zahir, Z. A., Javaid, A., and Ashraf, M. (2014). The
role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in
improving crop productivity under stressful environments. Biotechnol. Adv. 32,
429–448. doi: 10.1016/j.biotechadv.2013.12.005
Nadeem, S. M., Zahir, Z. A., Naveed, M., and Arshad, M. (2007). Preliminary
investigations on inducing salt tolerance in maize through inoculation with
rhizobacteria containing ACC deaminase activity. Can. J. Microbiol. 53, 1141–
1149. doi: 10.1139/W07-081
Nakashima, K., and Yamaguchi-Shinozaki, K. (2006). Regulons involved in osmotic
stress-responsive and cold stress-responsive gene expression in plants. Physiol.
Plant. 126, 62–71. doi: 10.1111/j.1399-3054.2005.00592.x
Nakayama, H., Yoshida, K., and Ono, H. (2000). Ectoine, the compatible solute of
Halomonas elongata, confers hyperosmotic tolerance in cultured tobacco cells.
Plant Physiol. 122, 1239–1247. doi: 10.1104/pp.122.4.1239
Natsch, A., Keel, C., Pfirter, H. A., Haas, D., and Défago, G. (1994).
Contribution of the global regulator gene gacA to persistence and dissemination
of Pseudomonas fluorescens biocontrol strain CHA0 introduced into soil
microcosms. Appl. Environ. Microbiol. 60, 2553–2560.
Naveed, M., Hussain, M. B., Zahir, Z. A., Mitter, B., and Sessitsch, A. (2014a).
Drought stress amelioration in wheat through inoculation with Burkholderia
phytofirmans strain PsJN. Plant Growth Regul. 73, 121–131. doi: 10.1007/
s10725-013-9874-8
Naveed, M., Mitter, B., Reichenauer, T. G., Wieczorek, K., and Sessitsch, A. (2014b).
Increased drought stress resilience of maize through endophytic colonization by
Burkholderia phytofirmans PsJN and Enterobacter sp FD17. Environ. Exp. Bot.
97, 30–39. doi: 10.1016/j.envexpbot.2013.09.014
Naya, L., Ladrera, R., Ramos, J., González, E. M., Arrese-Igor, C., Minchin, F. R.,
et al. (2007). The response of carbon metabolism and antioxidant defenses of
alfalfa nodules to drought stress and to the subsequent recovery of plants. Plant
Physiol. 144, 1104–1114. doi: 10.1104/pp.107.099648
Neeraja, C. N., Maghirang-Rodriguez, R., Pamplona, A., Heuer, S., Collard, B. C. Y.,
Septiningsih, E. M., et al. (2007). A marker-assisted backcross approach for
developing submergence-tolerant rice cultivars. Theor. Appl. Genet. 115, 767–
776. doi: 10.1007/s00122-007- 0607-0
Ngumbi, E., and Kloepper, J. (2014). Bacterial-mediated drought tolerance: current
and future prospects. Appl. Soil Ecol. 105, 109–125. doi: 10.1016/j.apsoil.2016.
04.009
Nguyen, D., Rieu, I., Mariani, C., and van Dam, N. M. (2016). How plants handle
multiple stresses: hormonal interactions underlying responses to abiotic stress
and insect herbivory. Plant Mol. Biol. 91, 727–740. doi: 10.1007/s11103-016-
0481-8
Nikolic, B., Schwab, H., and Sessitsch, A. (2011). Metagenomic analysis of
the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of
an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch.
Microbial. 193, 665–676. doi: 10.1007/s00203-011-0703- z
Noack, S., and Wiechert, W. (2014). Quantitative metabolomics: a phantom?
Trends Biotechnol. 5, 238–244. doi: 10.1016/j.tibtech.2014.03.006
Frontiers in Plant Science | www.frontiersin.org 21 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 22
Meena et al. Microbe-Mediated Management of Abiotic Stress
Olah, B., Briere, C., Becard, G., Denarie, J., and Gough, C. (2005). Nod factors
and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root
formation in Medicago truncatula via the DMI1/DMI2 signalling pathway.
Plant J. 44, 195–207. doi: 10.1111/j.1365-313X.2005.02522.x
Oldroyd, G. E. D. (2013). Speak, friend, and enter: signalling systems that promote
beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263.
doi: 10.1038/nrmicro2990
Oldroyd, G. E. D., and Downie, J. A. (2008). Coordinating nodule morphogenesis
with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519–546. doi:
10.1146/annurev.arplant.59.032607.092839
Oliveira, C. A., Alves, V. M. C., Marriel, I. E., Gomes, E. A., Scotti,
M. R., Carneiro, N. P., et al. (2009). Phosphate solubilizing microorganisms
isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian
Cerrado biome. Soil Biol. Biochem. 41, 1782–1787. doi: 10.1016/j.soilbio.2008.
01.012
Omar, M. N. A., Osman, M. E. H., Kasim, W. A., and Abd El-Daim, I. A. (2009).
Improvement of salt tolerance mechanisms of barley cultivated under salt stress
using Azospirillum brasiliense.Tasks Veg. Sci. 44, 133–147. doi: 10.1007/978-1-
4020-9065-3_15
Onaga, G., and Wydra, K. (2016). “Advances in plant tolerance to abiotic stresses,”
in Plant Genomics, ed. I. Y. Abdurakhmonov (Rijeka: InTech). doi: 10.5772/
64350
Ortiz, N., Armadaa, E., Duque, E., Roldánc, A., and Azcóna, R. (2015).
Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing
plant drought tolerance under natural soil conditions: effectiveness of
autochthonous or allochthonous strains. J. Plant Physiol. 174, 87–96. doi: 10.
1016/j.jplph.2014.08.019
Osakabe, Y., Arinaga, N., Umezawa, T., Katsura, S., Nagamachi, K., Tanaka, H.,
et al. (2013). Osmotic stress responses and plant growth controlled by potassium
transporters in Arabidopsis.Plant Cell 25, 609–624. doi: 10.1105/tpc.112.105700
Osakabe, Y., Osakabe, K., Shinozaki, K., and Tran, L.-S. P. (2014). Response
of plants to water stress. Front. Plant Sci. 5:86. doi: 10.3389/fpls.2014.
00086
Padgham, J. (2009). Agricultural Development Under a Changing Climate:
Opportunities and Challenges for Adaptation. Washington, DC: Agriculture and
Rural Development & Environmental Departments, The World Bank.
Palaniyandi, S. A., Damodharan, K., Yang, S. H., and Suh, J. W. (2014).
Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of
‘Micro Tom’ tomato plants. J. Appl. Microbiol. 117, 766–773. doi: 10.1111/jam.
12563
Pandey, V., Ansari, M. W., Tula, S., Yadav, S., Sahoo, R. K., Shukla, N., et al. (2016).
Dose-dependent response of Trichoderma harzianum in improving drought
tolerance in rice genotypes. Planta 243, 1251–1264. doi: 10.1007/s00425-016-
2482-x
Panlada, T., Pongdet, P., Aphakorn, L., Rujirek, N.-N., Nantakorn, B., and
Neung, T. (2013). Alleviation of the effect of environmental stresses using
co-inoculation of mungbean by Bradyrhizobium and rhizobacteria containing
stress-induced ACC deaminase enzyme. Soil Sci. Plant Nut. 59, 559–571. doi:
10.1080/00380768.2013.804391
Pareek, A., Sopory, S. K., Bohnert, H. K., and Govindjee. (eds) (2010). Abiotic
Stress Adaptation in Plants: Physiolgical, Molecular and Genomic Foundation.
Dordrecht: Springer, 526.
Peiffer, J. A., Spor, A., Koren, O., Jin, Z., Tringe, S. G., Dangl, J. L., et al. (2013).
Diversity and heritability of the maize rhizosphere microbiome under field
conditions. Proc. Natl. Acad. Sci. U.S.A. 110, 6548–6553. doi: 10.1073/pnas.
1302837110
Pereira, S. I., and Castro, P. M. (2014). Diversity and characterization of culturable
bacterial endophytes from Zea mays and their potential as plant growth-
promoting agents in metal-degraded soils. Environ. Sci. Pollut. Res. Int. 24,
14110–14123. doi: 10.1007/s11356-014- 3309-6
Perez-Lopez, U., Miranda-Apodaca, J., Munoz-Rueda, A., and Mena-
Petite, A. (2013). Lettuce production and antioxidant capacity are
differentially modified by salt stress and light intensity under ambient
and elevated CO2. J. Plant Physiol. 170, 1517–1525. doi: 10.1016/j.jplph.2013.
06.004
Pinedo, I., Ledger, T., Greve, M., and Poupin, M. J. (2015). Burkholderia
phytofirmans PsJN induces long-term metabolic and transcriptional changes
involved in Arabidopsis thaliana salt tolerance. Front. Plant Sci. 6:466. doi:
10.3389/flps.2015.00466
Pishchik, V. N., Vorobyev, N. I., Chernyaeva, I. I., Timofeeva, S. V., Kozhemyakov,
A. P., Alexeev, Y. V., et al. (2002). Experimental and mathematical
simulation of plant growth promoting rhizobacteria and plant interaction
under cadmium stress. Plant Soil 243, 173–186. doi: 10.1023/A:1019941
525758
Plociniczak, T., Sinkkonen, A., Romantschuk, M., and Piotrowska-seget, Z.
(2013). Characterization of Enterobacter intermedius MH8b and its use for the
enhancement of heavy metal uptake by Sinapsis alba L. Appl. Soil Ecol. 63, 1–7.
doi: 10.1016/j.apsoil.2012.09.009
Porcel, R., and Ruiz-Lozano, J. M. (2004). Arbuscular mycorrhizal influence on
leaf water potential, solute accumulation and oxidative stress in soybean plants
subjected to drought stress. J. Exp. Bot. 55, 1743–1750. doi: 10.1093/jxb/
erh188
Prasch, C. M., and Sonnewald, U. (2013). Simultaneous application of heat,
drought, and virus to Arabidopsis plants reveals significant shifts in signaling
networks. Plant Physiol. 162, 1849–1866. doi: 10.1104/pp.113.221044
Purdy, S. J., Maddison, A. L., Jones, L. E., Webster, R. J., Andralojc, J., Donnison, I.,
et al. (2013). Characterization of chilling-shock responses in four genotypes
of Miscanthus reveals the superior tolerance of M. x giganteus compared with
M. sinensis and M. sacchariflorus.Ann. Bot. 111, 999–1013. doi: 10.1093/aob/
mct059
Qadir, M., Quillérou, E., Nangia, V., Murtaza, G., Singh, M., Thomas, R. J.,
et al. (2014). Economics of salt-induced land degradation and restoration. Nat.
Resour. Forum. 38, 282–295. doi: 10.1111/1477-8947.12054
Qin, F., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2011). Achievements and
challenges in understanding plant abiotic stress responses and tolerance. Plant
Cell Physiol. 52, 1569–1582. doi: 10.1093/pcp/pcr106
Rabie, G. H. (2005). Influence of arbuscular mycorrhizal fungi and kinetin on
the response of mungbean plants to irrigation with seawater. Mycorrhiza 15,
225–230. doi: 10.1007/s00572-004- 0345-y
Raes, J., and Bork, P. (2008). Molecular eco-systems biology: towards an
understanding of community function. Nat. Rev. Microbiol. 6, 693–699. doi:
10.1038/nrmicro1935
Raymond, R. L., Jamison, V. W., and Hudson, J. O. (1967). Microbial hydrocarbon
co-oxidation. I. oxidation of mono- and dicyclic hydrocarbons by soil isolates
of the genus Nocardia.Appl. Microbiol. 15, 857–865.
Reardon, K. F., and Kim, K. H. (2002). Two-dimensional electrophoresis analysis
of protein production during growth of Pseudomonas putida F1 on toluene,
phenol, and their mixture. Electrophoresis 23, 2233–2241. doi: 10.1002/1522-
2683(200207)23:14<2233::AID-ELPS2233<3.0.CO;2- B
Remans, R., Ramaekers, L., Shelkens, S., Hernandez, G., Garcia, A., Reyes, G. L.,
et al. (2008). Effect of Rhizobium,Azospirillum co-inoculation on nitrogen
fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated
across different environments in Cuba. Plant Soil 312, 25–37. doi: 10.1007/
s11104-008-9606-4
Riadh, K., Wided, M., Hans-Werner, K., and Chedly, A. (2010). Responses of
halophytes to environmental stresses with special emphasis to salinity. Adv. Bot.
Res. 53, 117–145. doi: 10.1016/S0065-2296(10)53004-0
Rivas-Ubach, A., Sardans, J., Perez-Trujillo, M., Estiarte, M., and Penuelas, J.
(2012). Strong relationship between elemental stoichiometry and metabolome
in plants. Proc. Natl. Acad. Sci. U.S.A. 109, 4181–4186. doi: 10.1073/pnas.
1116092109
Rivero, R. M., Mestre, T. C., Mittler, R., Rubio, F., Garcia-Sanchez, F., and
Martinez, V. (2013). The combined effect of salinity and heat reveals a specific
physiological, biochemical and molecular response in tomato plants. Plant Cell
Environ. 37, 1059–1073. doi: 10.1111/pce.12199
Rizhsky, L., Liang, H., and Mittler, R. (2002). The combined effect of drought stress
and heat shock on gene expression in tobacco. Plant Physiol. 130, 1143–1151.
doi: 10.1104/pp.006858
Rizhsky, L., Liang, H. J., Shuman, J., Shulaev, V., Davletova, S., and Mittler, R.
(2004). When defense pathways collide. The response of Arabidopsis to a
combination of drought and heat stress. Plant Physiol. 134, 1683–1696. doi:
10.1104/pp.103.033431
Robin, A., Mougel, C., Siblot, S., Vansuyt, G., Mazurier, S., and Lemanceau, P.
(2006). Effect of ferritin overexpression in tobacco on the structure of bacterial
Frontiers in Plant Science | www.frontiersin.org 22 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 23
Meena et al. Microbe-Mediated Management of Abiotic Stress
and pseudomonad communities associated with the roots. FEMS Microbiol.
Ecol. 58, 492–502. doi: 10.1111/j.1574-6941.2006.00174.x
Rorison, I. H. (1986). The response of plants to acid soils. Experintia 42:357–362.
doi: 10.1007/BF02118616
Ruan, C. J., da Silva, J. A. T., Mopper, S., Qin, P., and Lutts, S. (2010). Halophyte
improvement for a salinized world. Crit. Rev. Plant Sci. 29, 329–359. doi: 10.
1080/07352689.2010.524517
Sahoo, R. K., Ansari, M. W., Dangar, T. K., Mohanty, S., and Tuteja, N.
(2014a). Phenotypic and molecular characterisation of efficient nitrogen-fixing
Azotobacter strains from rice fields for crop improvement. Protoplasma 251,
511–523. doi: 10.1007/s00709-013- 0547-2
Sahoo, R. K., Ansari, M. W., Pradhan, M., Dangar, T. K., Mohanty, S., and
Tuteja, N. (2014b). A novel Azotobacter vinellandii (SRIAz3) functions in
salinity stress tolerance in rice. Plant Sig. Behav. 9:e29377. doi: 10.4161/psb.
29377
Sandhya, V., Ali, S. K. Z., Minakshi, G., Reddy, G., and Venkateswarlu, B.
(2009). Alleviation of drought stress effects in sunflower seedlings by the
exopolysaccharides producing Pseudomonas putida strain GAP-P45.Biol. Fertil.
Soils 46, 17–26. doi: 10.1007/s00374-009- 0401-z
Sannazzaro, A. I., Ruiz, O. A., Alberto, E. O., and Menéndez, A. B. (2006).
Alleviation of salt stress in Lotus glaber by Glomus intraradices.Plant Soil 285,
279–287. doi: 10.1007/s11104-006- 9015-5
Santos, R. D., Patel, M., Cuadros, J., and Martins, Z. (2016). Influence of mineralogy
on the preservation of amino acids under simulated Mars conditions. Icarus
277, 342–353. doi: 10.1016/j.icarus.2016.05.029
Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., and Davies, D. G. (2002).
Pseudomonas aeruginosa displays multiple phenotypes during development as
a biofilm. J. Bacteriol. 184, 1140–1154. doi: 10.1128/jb.184.4.1140-1154.2002
Sauer, K., Cullen, M. C., Rickard, A. H., Zeef, L. A., Davies, D. G., and Gilbert, P.
(2004). Characterization of nutrient-induced dispersion in Pseudomonas
aeruginosa PAO1 biofilm. J. Bacteriol. 186, 7312–7326.
Schenk, P. M., Carvalhais, L. C., and Kazan, K. (2012). Unraveling plant–microbe
interactions: can multi-species transcriptomics help? Trends Biotechnol. 30,
177–184. doi: 10.1016/j.tibtech.2011.11.002
Schulze, W. X. (2005). Protein analysis in dissolved organic matter: what proteins
from organic debris, soil leachate and surface water can tell us–a perspective.
Biogeosciences 2, 75–86. doi: 10.5194/bg-2-75-2005
Schweder, T., Markert, S., and Hecker, M. (2008). Proteomics of marine bacteria.
Electrophoresis 29, 2603–2616. doi: 10.1002/elps.200800009
Sehrawat, A., Gupta, R., and Deswal, R. (2013). Nitric oxide-cold stress signalling
cross-talk, evolution of a novel regulatory mechanism. Proteomics 13, 1816–
1835. doi: 10.1002/pmic.201200445
Sen, S., and Chandrasekhar, C. N. (2014). Effect of PGPR on growth promotion of
rice (Oryza sativa L.) under salt stress. Asian J. Plant Sci. Res. 4, 62–67.
Septiningsih, E. M., Pamplona, A. M., Sanchez, D. L., Neeraja, C. N., Vergara, G. V.,
Heuer, S., et al. (2009). Development of submergence-tolerant rice cultivars: the
Sub1 locus and beyond. Ann. Bot. 103, 151–160. doi: 10.1093/aob/mcn206
Sessitsch, A., Hardoim, P., Döring, J., Weilharter, A., Krause, A., Woyke, T., et al.
(2012). Functional characteristics of an endophyte community colonizing roots
as revealed by metagenomic analysis. Mol. Plant Microbe Interact. 25, 28–36.
doi: 10.1094/MPMI-08- 11-0204
Shao, H. B., Chu, L. Y., Jaleel, C. A., and Zhao, C. X. (2008). Water-deficit stress—
Induced anatomical changes in higher plants. Crit. Rev. Biol. 331, 215–225.
doi: 10.1016/j.crvi.2008.01.002
Sharifi, M., Ghorbanli, M., and Ebrahimzadeh, H. (2007). Improved growth of
salinity-stressed soybean after inoculation with salt pre-treated mycorrhizal
fungi. J. Plant Physiol. 164, 1144–1151. doi: 10.1016/j.jplph.2006.06.016
Sharma, A., Shankhdhar, D., and Shankhdhar, S. C. (2013). Enhancing grain iron
content of rice by the application of plant growth promoting rhizobacteria.
Plant Soil Environ. 59, 89–94.
Shevchenko, A., Sunyaev, S., Loboda, A., Schevchenko, A., Bork, P., Ens, W., et al.
(2001). Charting the proteomes of organisms with unsequenced genomes by
MALDI-quadrupole time of flight mass spectrometry and BLAST homology
searching. Anal. Chem. 73, 1917–1926. doi: 10.1021/ac0013709
Silva, E. N., Ribeiro, R. V., Ferreira-Silva, S. L., Viégas, R. A., and Silveira, J. A. G.
(2010). Comparative effects of salinity and water stress on photosynthesis, water
relations and growth of Jatropha curcas plants. J. Arid. Environ. 74, 1130–1137.
doi: 10.1016/j.jaridenv.2010.05.036
Silva-Sanchez, C., Li, H., and Chen, S. (2015). Recent advances and challenges
in plant phosphoproteomics. Proteomics 15, 1127–1141. doi: 10.1002/pmic.
201400410
Simontacchi, M., Galatro, A., Ramos-Artuso, F., and Santa-Maria, G. E. (2015).
Plant survival in a changing environment : the role of nitric oxide in plant
responses to abiotic stress. Front. Plant Sci. 6:977. doi: 10.3389/fpls.2015.
00977
Singh, D. P., Prabha, R., Yandigeri, M. S., and Arora, D. K. (2011). Cyanobacteria-
mediated phenylpropanoids and phytohormones in rice (Oryza sativa) enhance
plant growth and stress tolerance. Antonie Van Leeuwenhoek 100, 557–568.
doi: 10.1007/s10482-011- 9611-0
Singh, R., Singh, P., and Sharma, R. (2014). Microorganism as a tool of
bioremediation technology for cleaning environment: A review. Proc. Int. Acad.
Ecol. Environ. Sci. 4, 1–6.
Singh, S. (2014). A review on possible elicitor molecules of cyanobacteria: their
role in improving plant growth and providing tolerance against biotic or abiotic
stress. J. Appl. Microbiol. 117, 1221–1244. doi: 10.1111/jam.12612
Sonah, H., Deshmukh, R. K., Sharma, A., Singh, V. P., Gupta, D. K., Gacche, R. N.,
et al. (2011). Genome-wide distribution and organization of microsatellites
in plants: an insight into marker development in Brachypodium.PLoS ONE
6:21298. doi: 10.1371/journal.pone.0021298
Sorty, A. M., Meena, K. K., Choudhary, K., Bitla, U. M., Minhas, P. S., and
Krishnani, K. K. (2016). Effect of plant growth promoting bacteria associated
with halophytic weed (Psoralea corylifolia L.) on germination and seedling
growth of wheat under saline conditions. Appl. Biochem. Biotechnol. 180,
872–882. doi: 10.1007/s12010-016- 2139-z
Sorty, A. M., and Shaikh, N. R. (2015). Novel co-enrichment method for isolation
of magnetotactic bacteria. J. Basic Microbiol. 55, 520–526. doi: 10.1002/jobm.
201400457
Souza, R. D., Ambrosini, A., and Passaglia, L. M. P. (2015). Plant growth-promoting
bacteria as inoculants in agricultural soils. Genet. Mol. Biol. 38, 401–419. doi:
10.1590/S1415-475738420150053
Spoel, S. H., and Dong, X. (2008). Making sense of hormone crosstalk during plant
immune response. Cell Host Microbe. 3, 348–351. doi: 10.1016/j.chom.2008.
05.009
Srivastava, G., Kumar, S., Dubey, G., Mishra, V., and Prasad, S. M. (2012).
Nickel and ultraviolet-B stresses induce differential growth and photosynthetic
responses in Pisum sativum L. seedlings. Biol. Trace Elem. Res. 49, 86–96.
doi: 10.1007/s12011-012- 9406-9
Srivastava, S., Verma, P. C., Chaudhry, V., Singh, N., Abhilash, P. C., Kumar, K. V.,
et al. (2013). Influence of inoculation of arsenic-resistant Staphylococcus arlettae
on growth and arsenic uptake in Brassica juncea (L.) Czern. Var. R-46. J. Hazard.
Mater. 262, 1039–1047. doi: 10.1016/j.jhazmat.2012.08.019
Suarez, C., Cardinale, M., Ratering, S., Steffens, D., Jung, S., Montoya, A. M. Z.,
et al. (2015). Plant growth-promoting effects of Hartmannibacter diazotrophicus
on summer barley (Hordeum vulgare L.) under salt stress. Appl. Soil Ecol. 95,
23–30. doi: 10.1016/j.apsoil.2015.04.017
Sun, C., Johnson, J., Cai, D., Sherameti, I., Oelmüeller, R., and Lou, B. (2010).
Piriformosporaindica confers drought tolerance in Chinese cabbage leaves by
stimulating antioxidant enzymes, the expression of drought-related genes and
the plastid-localized CAS protein. J. Plant. Physiol. 167, 1009–1017. doi: 10.
1016/j.jplph.2010.02.013
Sunkar, R., Kapoor, A., and Zhu, J. K. (2006). Posttranscriptional Induction
of Two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by
downregulation of miR398 and important for oxidative stress tolerance. Plant
Cell 18, 2051–2065. doi: 10.1105/tpc.106.041673
Swaine, E. K., Swaine, M. D., and Killham, K. (2007). Effects of drought on isolates
of Bradyrhizobium elkanii cultured from Albizia adianthifolia seedlings on
different provenances. Agroforest. Syst. 69, 135–145. doi: 10.1007/s10457-006-
9025-6
Swarbrick, P. J., Schulze-Lefert, P., and Scholes, J. D. (2006). Metabolic
consequences of susceptibility and resistance in barley leaves challenged with
powdery mildew. Plant Cell Environ. 29, 1061–1076. doi: 10.1111/j.1365-3040.
2005.01472.x
Takanashi, K., Sasaki, T., Kan, T., Saida, Y., Sugiyama, A., Yamamoto, Y., et al.
(2016). A dicarboxylate transporter, LjALMT4, mainly expressed in nodules of
Lotus japonicus. Mol. Plant Microbe Interact. 29, 584–592. doi: 10.1094/MPMI-
04-16-0071-R
Frontiers in Plant Science | www.frontiersin.org 23 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 24
Meena et al. Microbe-Mediated Management of Abiotic Stress
Tani, A., Takai, Y., Suzukawa, I., Akita, M., Murase, H., and Kimbara, K. (2012).
Practical application of methanol-mediated mutualistic symbiosis between
Methylobacterium species and a roof greening moss, Racomitrium japonicum.
PLoS ONE 7:e33800. doi: 10.1371/journal.pone.0033800
Tapias, D. R., Galvan, A. M., Diaz, S. P., Obando, M., Rivera, D., and Bonilla, R.
(2012). Effect of inoculation with plant growth-promoting bacteria (PGPB) on
amelioration of saline stress in maize (Zea mays). Appl. Soil Ecol. 61, 264–272.
doi: 10.1016/j.apsoil.2012.01.006
Thomashow, M. F. (2010). Molecular basis of plant cold acclimation: insights
gained from studying the CBF cold response pathway. Plant Physiol. 154,
571–577. doi: 10.1104/pp.110.161794
Timmusk, S., El-Daim, I. A. A., Copolovici, L., Tanilas, T., Kännaste, A.,
Behers, L., et al. (2014). Drought-tolerance of wheat improved by rhizosphere
bacteria from harsh environments: enhanced biomass production and reduced
emissions of stress volatiles. PLoS ONE 9:e96086. doi: 10.1371/journal.pone.
0096086
Timmusk, S., and Wagner, E. G. H. (1999). The plant growth-promoting
rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana
gene expression, a possible connection between biotic and abiotic stress
responses. Mol. Plant Microbe Interact. 12, 951–959. doi: 10.1094/MPMI.1999.
12.11.951
Tiwari, S., Singh, P., Tiwari, R., Meena, K. K., Yandigeri, M., Singh, D. P.,
et al. (2011). Salt-tolerant rhizobacteria-mediated induced tolerance in wheat
(Triticum aestivum) and chemical diversity in rhizosphere enhance plant
growth. Biol. Fertil. Soils 47, 907–916. doi: 10.1007/s00374-011- 0598-5
Todaka, D., Nakashima, K., Shinozaki, K., and Yamaguchi-Shinozaki, K.
(2012). Toward understanding transcriptional regulatory networks in abiotic
stress responses and tolerance in rice. Rice J. 5, 1–9. doi: 10.1186/1939-
8433-5-6
Tomar, R. S. S., Deshmukh, R. K., Naik, K., and Tomar, S. M. S. (2014).
Development of chloroplast-specific microsatellite markers for molecular
characterization of alloplasmic lines and phylogenetic analysis in wheat. Plant
Breed. 133, 12–18. doi: 10.1111/pbr.12116
Toojinda, T., Siangliw, M., Tragroonrung, S., and Vanavichit, A. (2003). Molecular
genetics of submergence tolerance in rice: QTL analysis of key traits. Ann. Bot.
91, 243–253. doi: 10.1093/aob/mcf072
Trindade, I., Capitao, C., Dalmay, T., Fevereiro, M. P., and Santos, D. M. (2010).
miR398 and miR408 are up-regulated in response to water deficit in Medicago
truncatula.Planta 231, 705–716. doi: 10.1007/s00425-009-1078- 0
Tringe, S. G., von Mering, C., Kobayashi, A., Salamov, A. A., Chen, K., Chang,
H. W., et al. (2005). Comparative metagenomics of microbial communities.
Science 308, 554–557. doi: 10.1126/science.1107851
Tucci, M., Ruocco, M., De Masi, L., De Palma, M., and Lorito, M. (2011).
The beneficial effect of Trichoderma spp. on tomato is modulated by the
plant genotype. Mol. Plant. Pathol. 12, 341–354. doi: 10.1111/j.1364-3703.2010.
00674.x
Turner, T. R., James,E. K., and Poole, P. S. (2013a). The plant microbiome. Genome
Biol. 14:209. doi: 10.1186/gb-2013-14-6- 209
Turner, T. R., Ramakrishnan, K., Walshaw, J., Heavens, D., Alston, M.,
Swarbreck, D., et al. (2013b). Comparative metatranscriptomics reveals
kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7,
2248–2258. doi: 10.1038/ismej.2013.119
Vaishnav, A., Kumari, S., Jain, S., Verma, A., Tuteja, N., and Choudhary, D. K.
(2016). PGPR-mediated expression of salt tolerance gene in soybean through
volatiles under sodium nitroprusside. J. Basic Microbiol. 56, 1274–1288. doi:
10.1002/jobm.201600188
Vansuyt, G., Robin, A., Briat, J. F., Curie, C., and Lemanceau, P. (2007). Iron
acquisition from Fe-pyoverdine by Arabidopsis thaliana.Mol. Plant Microbe
Interact. 20, 441–447. doi: 10.1094/MPMI-20-4-0441
Vardharajula, S., Ali, S. Z., Grover, M., Reddy, G., and Bandi, V. (2011). Drought-
tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and
antioxidant status of maize under drought stress. J. Plant Int. 6, 1–14.
VerBerkmoes, N. C., Shah, M. B., Lankford, P. K., Pelletier, D. A., Strader, M. B.,
Tabb, D. L., et al. (2006). Determination and comparison of the baseline
proteomes of the versatile microbe Rhodopseudomonas palustris under its major
metabolic states. J. Proteome Res. 5, 287–298. doi: 10.1021/pr0503230
Vinale, F., Sivasithamparam, K., Ghisalberti, E. L., Marra, R., Barbetti, M. J.,
Li, H., et al. (2008). A novel role for Trichoderma secondary metabolites in the
interactions with plants. Physiol. Mol. Plant Pathol. 72, 80–86. doi: 10.1016/j.
pmpp.2008.05.005
Viterbo, A., Landau, U., Kim, S., Chernin, L., and Chet, I. (2010). Characterization
of ACC deaminase from the biocontrol and plant growth-promoting agent
Trichoderma asperellum T203. FEMS Microbiol. Lett. 305, 42–48. doi: 10.1111/
j.1574-6968.2010.01910.x
Voesenek, L. A. C. J., and Pierik, R. (2008). Plant stress profiles. Science 320,
880–881. doi: 10.1126/science.1158720
Wahid, A., Gelani, S., Ashraf, M., and Foolad, M. R. (2007). Heat tolerance in
plants: an overview. Environ. Exp. Bot. 61, 199–223. doi: 10.1016/j.envexpbot.
2007.05.011
Wang, C., Yang, W., Wang, C., Gu, C., Niu, D., Liu, H., et al. (2012). Induction of
drought tolerance in cucumber plants by a consortium of three plant growth-
promoting rhizobacterium strains. PLoS ONE 7:e52565. doi: 10.1371/journal.
pone.0052565
Wang, L. J., and Li, S. L. (2006). Salicylic acid-induced heat or cold tolerance in
relation to Ca2+homeostasis and antioxidant systems in young grape plants.
Plant Sci. 170, 685–694. doi: 10.1016/j.plantsci.2005.09.005
Wang, L. Y., Xie, Y. S., Cui, Y. Y., Xu, J., He, W., Chen, H. G., et al. (2015).
Conjunctively screening of biocontrol agents (BCAs) against fusarium root rot
and fusarium head blight caused by Fusarium graminearum.Microbiol. Res. 177,
34–42. doi: 10.1016/j.micres.2015.05.005
Wang, W., Vinocur, B., and Altman, A. (2003). Plant responses to drought, salinity
andextreme temperatures: towards genetic engineering for stress tolerance.
Planta 218, 1–14. doi: 10.1007/s00425-003-1105-5
Wang, Y., Hu, B., Du, S., Gao, S., Chen, X., and Chen, D. (2016). Proteomic
analyses reveal the mechanism of Dunaliella salina Ds-26-16 gene enhancing
salt tolerance in Escherichia coli.PLoS ONE 11:e0153640. doi: 10.1371/journal.
pone.0153640
Wani, S. H., Kumar, V., Shriram, V., and Sah, S. K. (2016). Phytohormones and
their metabolic engineering for abiotic stress tolerance in crop plants. Crop J. 4,
162–176. doi: 10.1016/j.cj.2016.01.010
Williams, P. M., and de Mallorca, M. S. (1982). Abscisic acid and gibberellin-like
substances in roots and root nodules of Glycine max.Plant Soil 65, 19–26.
doi: 10.1007/BF02376799
Xu, J., Lan, H., Fang, H., Huang, X., Zhang, H., and Huang, J. (2015). Quantitative
proteomic analysis of the rice (Oryza sativa L.) salt response. PLoS ONE
10:e0120978. doi: 10.1371/journal.pone.0120978
Xu, X., Zhou, G., and Shimizu, H. (2010). Plant responses to drought
and rewatering. Plant Signal. Behav. 5, 649–654. doi: 10.4161/psb.5.6.
11398
Xu, Y., Lu, Y., Xie, C., Gao, S., Wan, J., and Prasanna, B. M. (2012). Whole-
genome strategies for marker-assisted plant breeding. Mol. Breed. 29, 833–854.
doi: 10.1007/s11032-012- 9724-9
Xu, Z., Jiang, Y., Jia, B., and Zhou, G. (2016). Elevated-CO2 response of stomata
and its dependence on environmental factors. Front. Plant Sci. 7:657. doi: 10.
3389/fpls.2016.00657
Xu, Z., Jiang, Y., and Zhou, G. (2015). Response and adaptation of photosynthesis,
respiration, and antioxidant systems to elevated CO2 with environmental stress
in plants. Front. Plant Sci. 6:701. doi: 10.3389/fpls.2015.00701
Xu, Z., Shimizu, H., Ito, S., Yagasaki, Y., Zou, C., Zhou, G., et al. (2014).
Effects of elevated CO2, warming and precipitation change on plant growth,
photosynthesis and peroxidation in dominant species from North China
grassland. Planta 239, 421–435. doi: 10.1007/s00425-013-1987-9
Xu, Z. Z., and Zhou, G. S. (2006). Combined effects of water stress and high
temperature on photosynthesis, nitrogen metabolism and lipid peroxidation
of a perennial grass Leymus chinensis.Planta 224, 1080–1090. doi: 10.1007/
s00425-006-0281-5
Yao, D., Zhang, X., Zhao, X., Liu, C., Wang, C., Zhang, Z., et al. (2011).
Transcriptome analysis reveals salt-stressregulated biological processes and key
pathways in roots of cotton (Gossypium hirsutum L.). Genomics 98, 47–55.
doi: 10.1016/j.ygeno.2011.04.007
Yao, L. X., Wu, Z. S., Zheng, Y. Y., Kaleem, I., and Li, C. (2010). Growth promotion
and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur.
J. Soil Biol. 46, 49–54. doi: 10.1016/j.ejsobi.2009.11.002
Yim, W., Seshadri, S., Kim, K., Lee, G., and Sa, T. (2013). Ethylene emission
and PR protein synthesis in ACC deaminase producing Methylobacterium
spp. inoculated tomato plants (Lycopersicon esculentum Mill.) challenged with
Frontiers in Plant Science | www.frontiersin.org 24 February 2017 | Volume 8 | Article 172
fpls-08-00172 February 8, 2017 Time: 16:13 # 25
Meena et al. Microbe-Mediated Management of Abiotic Stress
Ralstonia solanacearum under greenhouse conditions. Plant Physiol. Biochem.
67, 95–104. doi: 10.1016/j.plaphy.2013.03.002
Yin, R., Han, K., Heller, W., Albert, A., Dobrev, P. I., Zažímalová, E., et al. (2014).
Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol
inhibitor of polar auxin transport in Arabidopsis shoots. New Phytol. 201,
466–475. doi: 10.1111/nph.12558
Yolcu, S., Ozdemir, F., Güler, A., and Bor, M. (2016). Histone acetylation influences
the transcriptional activation of POX in Beta vulgaris L. and Beta maritima L.
under salt stress. Plant Physiol. Biochem. 100, 37–46. doi: 10.1016/j.plaphy.2015.
12.019
Yuan, H., Zhang, T., Liu, X., Deng, M., Zhang, W., Wen, Z., et al. (2015).
Sumoylation of CCAAT/ enhancer-binding protein a is implicated in
hematopoietic stem/progenitor cell development through regulating runx1 in
zebrafish. Sci. Rep. 5:9011. doi: 10.1038/srep09011
Zabala, M. D., Bennett, M. H., Truman, W. H., and Grant, M. R. (2009).
Antagonism between salicylic and abscisic acid reflects early host-pathogen
conflict and moulds plant defence responses. Plant J. 59, 375–386. doi: 10.1111/
j.1365-313X.2009.03875.x
Zhang, H., Kim, M. S., Sun, Y., Dowd, S. E., Shi, H., and Paré, P. W. (2008). Soil
bacteria confer plant salt tolerance by tissue-specific regulation of the sodium
transporter HKT1. Mol. Plant Microbe Interact. 21, 737–744. doi: 10.1094/
MPMI-21-6-0737
Zhang, X., Zou, Z., Gong, P., Zhang, J., Ziaf, K., Li, X., et al. (2011). Over-expression
of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol.
Lett. 33, 403–409. doi: 10.1007/s10529-010-0436-0
Zhang, X. S., and Cheng, H. P. (2006). Identification of Sinorhizobium meliloti
early symbiotic genes by use of a positive functional screen. Appl. Environ.
Microbiol. 72, 2738–2748. doi: 10.1128/AEM.72.4.2738-2748.2006
Zhao, M. G., Chen, L., Zhang, L. L., and Zhang, W. H. (2009). Nitric reductase-
dependent nitric oxide production is involved in cold acclimation and freezing
tolerance in Arabidopsis.Plant Physiol. 151, 755–767. doi: 10.1104/pp.109.
140996
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2017 Meena, Sorty, Bitla, Choudhary, Gupta, Pareek, Singh, Prabha,
Sahu, Gupta, Singh, Krishanani and Minhas. This is an open-access article
distributed under the terms of the Creative Commons Attribution License (CC BY).
The use, distribution or reproduction in other forums is permitted, provided the
original author(s) or licensor are credited and that the original publication in this
journal is cited, in accordance with accepted academic practice. No use, distribution
or reproduction is permitted which does not comply with these terms.
Frontiers in Plant Science | www.frontiersin.org 25 February 2017 | Volume 8 | Article 172
Available via license: CC BY 4.0
Content may be subject to copyright.
Content uploaded by Ratna Prabha
Author content
All content in this area was uploaded by Ratna Prabha on Feb 11, 2017
Content may be subject to copyright.
Content uploaded by Ratna Prabha
Author content
All content in this area was uploaded by Ratna Prabha on Feb 11, 2017
Content may be subject to copyright.
