Morpho-Physiological, Biochemical and Molecular Adaptation of Millets to Abiotic Stresses: A Review

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Morpho-Physiological, Biochemical and Molecular Adaptation of Millets
to Abiotic Stresses: A Review
Seerat Saleem
1
, Naveed Ul Mushtaq
1
, Wasifa Hafiz Shah
1
, Aadil Rasool
1
, Khalid Rehman Hakeem
2
,
*
and
Reiaz Ul Rehman
1
,
*
1
Department of Bioresources, School of Biological Sciences, University of Kashmir, Srinagar, 190006, India
2
Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, 21589, Saudi Arabia
*Corresponding Authors: Khalid Rehman Hakeem. Email: kur.hakeem@gmail.com; Reiaz Ul Rehman.
Email: rreaizbiores@gmail.com
Received: 02 November 2020 Accepted: 12 February 2021
ABSTRACT
Abiotic stresses such as drought, heat, cold, nutrient deficiency, excess salt and hazardous metals can hamper
plantgrowth and development. Intensive agriculture of only a few major staple food crops that are sensitive
and intolerant to environmental stresses has led to an agrarian crisis. On the other hand, nutritionally rich, gluten
free and stress tolerant plants like millets are neglected and underutilized. Millets sustain about one-third of the
world’s population and show exceptional tolerance to various abiotic and biotic stresses. Millets are C4 plants
that are adapted to marginal and dry lands of arid and semi-arid regions, and survive low rainfall and poor soils.
Abiotic stresses significantly affect plant growth which ultimately results in reduced crop yields. However, various
adaptation mechanisms have evolved in millets to withstand different stresses. This review aims at exploring
various of these morphophysiological, biochemical and molecular aspects of mechanisms in millets. Morphological
adaptations include short life span, smallplant height and leaf area, dense root system, adjusted flowering time,
increased root and decreased shoot lengths, high tillering, and leaf folding. A high accumulation of various osmo-
protectants (proline, soluble sugars, proteins) improves hyperosmolarity and enhances the activity of antioxidant
enzymes (e.g., Ascorbate peroxidase, Superoxide dismutase, Catalase, Peroxidase) providing defense against
oxidative damage. Physiologically, plants show low photosynthetic and stomatal conductance rates, and root respira-
tion which help them to escape from water stress. Molecular adaptations include the upregulation of stress-related
transcriptional factors, signalling genes, ion transporters, secondary metabolite pathways, receptor kinases, phyto-
hormone biosynthesis and antioxidative enzymes. Lack of genetic resources hampers improvement of millets.
However, several identified and characterized genes for stress tolerance can be exploited for further development
of millet resilience. This will provide them with an extra characteristic plant resistance to withstand environmental
pressures, besides their excellent nutritional value over the conventional staple crops like rice, wheat and maize.
KEYWORDS
Millets; adaptation; abiotic stress; osmoprotectants; antioxidants; transcriptomics
This work is licensed under a Creative Commons Attribution 4.0 International License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original
work is properly cited.
DOI: 10.32604/phyton.2021.014826
REVIEW
ech
T
PressScience

1 Introduction
Millets are small seeded, annual C4 grasses grown for both food and fodder [1]. They belong to the
family Poaceae, comprising Pearl millet (Pennisetum glaucum (L.) R.Br.), Foxtail millet (Setaria italica
(L.) P. Beauvois), Common millet (Panicum miliaceum L.), Finger millet (Eleusine coracana Gaertn.),
Barnyard Millet (Echinochloa utilis Ohwi & Yabuno; Echinochloa frumentacea Link), Little Millet
(Panicum sumatrense Roth. ex Roem. & Schultz), Kodo millet (Paspalum scrobiculatum L.) and Teff
millet (Eragrostis tef (Zucc.) Trotter). Millets are adapted to marginal and dry lands of arid and semi-arid
regions, and show exceptional tolerance to various abiotic stresses [2]. The total world production of
millets in 2018 was estimated to be 31,019,370 tonnes (FAO 2020) [3]. Millets account for only 2% of
the world cereal production, and 95% of the world millet production comes from Asia and Africa
(Fig. 1). Millets are a good source of energy and essential nutrients, and thus serve as the food source of
for millions of people across the globe. They are superior to cereals in various beneficial components
such as dietary fibre, micro and macro nutrients and bioactive components. Millets are the chief food of
small farmer communities of India, Africa, China, and some parts of Central America, and ensure food
security to low income generating countries of Asia and Africa [4]. To bring millets back to the
mainstream and gain benefits from their nutritious properties, 2018 was declared as the “National Year of
Millets”by the Indian Government. Also, FAO declared that the year 2023 willbe the “International Year
of Millets”to increase the production and productivity of millets throughout the globe [5]. Major cereals
such as rice, wheat, and maize have a significant global warming potential due to their high carbon
emission rates. Millets, on the other hand, have comparatively lower carbon footprints [6]. They are
considered as models for studying C4 photosynthesis, stress biology, and biofuel traits; this has led to
studies on structural and functional genomics of foxtail millet [7]. Currently, this is the age of an agrarian
crisis which has called for crop improvement under the detrimental effects of climate change. Intensive
agriculture of a few crops for food requirements has led to inadequate nutrition, and genetic erosion, and
has forced to neglect local nutritionally-rich crops. “Millets”are neglected and underutilized crops which
are nutritionally-rich and gluten free. Being the 6
th
most important crop in the world, Millets are used for
the purpose of food, feed and fodder. These are known as poor man’s crops and sustain about one-third
of the world’s population [8]. Among the various elite traits of foxtail millet are its tolerance to various
abiotic stresses (e.g., drought and salinity), less fertilizer requirement, and higher photosynthetic
efficiency than C3 plants, and its ability to grow on less fertile lands [9]. Finger millet can resist storage
pests for as long as 10 years and hence it has earned thepopular name of ‘’Famine Crop’’ [10]. Millets
provide the poor people with nutritional security in these regions, but lacks adequate scientific attention
which restricts it mainly to regions of major cereal crops. Millets, popularly known as minor cereals,
have been given very little attention for their improvement, however, this could be easily done by the
development of genetic resources [11]. Drought, temperature extremes (e.g., heat, cold), nutrient
deficiency, salinityand heavy metals are categorized as abiotic stresses. These factors threaten the food
security and plant production [12]. Abiotic stress conditions lead to the accumulation of reactive oxygen
species (ROS), causing extreme cell damage and inhibition of photosynthesis [13]. With the increasing
population, agriculture is currently facing a tough time due to the unavailability of land and water, and
climatechange. The problem can be solved to a large extent by the use of naturally stress resistant plants
(NSRP’s), which ensures yield stability, global food security and health. These NSRP’s (minor crops)
should be genetically improved for increasing their productivity [14]. Millets are agronomically beneficial
because ofthey are tolerant to drought, heat, salt and biotic stresses, and survive in marginal lands under
rainfed conditions [15]. These plants are classified as glycophytes and have an average salt tolerance
threshold of 6 (ECe) (dS/m) [16].
1364 Phyton, 2021, vol.90, no.5

Water requirements for producing 1 gm of dry biomass of maize and wheat are 470 g and 510 g,
respectively, while those of some drought tolerant varieties of Seteria italica are of only 257 g [17]. Millets
are adapted to low rainfall and poor soils. Pearl millet is probably the most drought and heat resistant
among the millets, and is preferably grown in well drained sands or sandy loams. Lighter soils are best
suited, and sometimes a mixture of black, red and light coloured gravelly soils of Deccan are well suited for
their growth. Finger millet is adapted to various temperature and moisture ranges, and is mostly grown on
reddish brown lateritic soils having good drainage and adequate water holding capacity [18]. Foxtail millet
is grown on water deficient black cotton soils, and also on loamy or alluvial or clayey soils. Kodo millet is
extremely drought resistant, and it is grown on hard-gravelly soils where other crops cannot grow. Fonio is
mainly grown on plateau savanna lands with slightly heavier soils and moist conditions [19]. Among the
millets, finger millet is the most stress resilient crop in terms of stress conditions such as high temperature,
low moisture, and poor soils. As a result, itcan be used in the improvement of other economically important
crops. So, millets are a treasure of important genes and regulatory proteins which are responsible for their
adaptive traits, and can be used in the development of stress resistant crops. Transgenic crops with desired
traits can be developed by inactivation or over-expression of transcription factor genes with desirable stress
tolerance traits. These can be identified by genome wide expression profiling [20]. The pearl millet varieties
have been reported to have a better drought tolerance capacity than maize showing a better relative water
content (RWC); photosynthetic rate; upregulated expression of CBF, PIP2;3 transcripts, and a repressed
expression of RubSc on leaves which provide drought resistance [21]. Among the minor millets, the
drought tolerance was found to be highest in barnyard millet followed by finger millet and little millet when
they are in the reproductive developmental morphology stage. Barnyard millet performed better in terms of
number of reproductive tillers, ear heads, grain weight, ear head weight, grain yield and straw yield [22].
Furthermore, pearl millet ishighly nutritious and it has been called a perfect solution under water stress
conditionsbecause of its drought tolerance [23].
2 Impact of Abiotic Stress in Millets
Salinization of arable lands due to improper water drainage systems, underlying high salt content rocks,
irrigation of crops in arid and semi-arid regions with saline water, and lack of good quality water due to
shortage of rainfall affect soil characteristics. Soil salinity has rendered in valueless agricultural lands, and
has hadhazardous impact on growth of many plants. Na
+
and Cl
-
ions present in poor quality water are at
excess levels and cause osmotic damage, ion-specific toxicity and nutritional disorders in plants leading
Figure 1: Millet production (%) in different countries of the world (FAO 2018)
Phyton, 2021, vol.90, no.5 1365

to salinity stress [24,25]. Thirty three percent of the global irrigated agricultural lands and 20% of the
cultivable land areimpacted by salinity, and this can increase up to 50% by the year 2050 [26]. Salinity
stress causes a reduction in RWC which might be due to the osmotic stress in roots caused by high salt
content. This restricts water absorption and leads to dehydration [27]. Finger millet which is moderately
tolerant to salt stress, has displayed a decrease in (1) shoot dry weight, leaf number, leaf surface area, and
leaf chlorophyll content, and an increase in (2) leaf succulence, destruction of chloroplast, leaf chlorosis,
severe damage oftissues, lignification of xylem vessels, electrolyte leakage, hydrogen peroxide and
proline content under increased salinity [28]. Also, salinity stress in finger millet resulted in reduced
germination rates, root and shoot growth, chlorophyll content, leaf relative water content, and K
+
concentration of leaves, and chlorosis, and increased salt and malonaldehyde contents [29]. Salinization
and alkalization resulted in reduction of plant dry weight, relative growth rate (RGR), net assimilation
rate (NAR), leaf area ratio (LAR), RWC and nitrogen in foxtail millet and proso millet. However, the
detrimental effects were greateron foxtail than proso millet which indicates that proso millet is more
tolerant to both stresses [30]. It was reported that the tolerant accessions of proso millet were high in
chlorophyll aunder saline conditions. Chlorophyll acontent can be related to salt tolerance in proso
millet (Panicum miliaceum). The salt tolerance of a plant species determines the degree of reduction in
total chlorophyll [31].
Drought, which leads to a severe water deficiency, has devastating effects on crop productivity. The
stomatal closure due to drought leads to an excessive accumulation of ROS leading to oxidative stress.
This stress results in lipid peroxidation and damage to other bio-molecules [32]. Abscisic Acid (ABA)
and Ethylene (ET) are among the phytohormones which are often involved in drought stress signalling
and tolerance. Salicylic acid (SA) and jasmonic acid (JA) enhance plant tolerance against drought,
salinity and heat stresses [33]. Drought stress in pearl millet has led to a significant reduction in plant
height, plant biomass, plant weight and grain number [34]. Water stress on black and brown finger millet
resulted in a decreased chlorophyll, photosynthesis, and RWC, and an increased proline content; brown
finger millet showed higher levels of tolerance than black finger millet [35]. Drought-induced oxidative
stress in finger millet led to droopy shoots, curling of leaves, increased proline and malondialdehyde
(MDA) contents, electrolyte leakage, damaged membrane integrity, and a significant increase in H
2
O
2.
Drought resulted in increased activities of antioxidant enzymes such as glutathione reductase (GR),
superoxide dismutase (SOD), ascorbate peroxidase (APX), glutathione peroxidase (GPX) and catalase
(CAT) [32]. At the sight of drought induction, this stress promoted an increase of the endophyte
Actinobacteria in roots, therhizosphere, and the bulk soil communities of millet species, which might
benefit the host [36]. Increasing atrazine herbicide concentration caused a physiological distress in pearl
millet seedlings by inhibiting photosynthesis. Furthermore, it blocked the electron acceptor in
photosynthesis and led to an excessive production of ROS causing an oxidative damage to proteins, lipids
and pigments [37]. Nickel toxicity in pearl millet and finger millet resulted in inhibition of seed
germination with supressed root and shoot length, and reduced root and shoot dry weights, and a 4-5-fold
increase in proline content, with roots and stem turning brownish [38]. Heat stress resulted in reduced
chlorophyll index, grain yield, harvest index and photosystem II activity in finger millet. Furthermore, the
maximum impact of heat stress occurredduring the booting, panicle emergence and flowering
developmental morphology stages, where genetic variability played a significant role in plant stress
tolerance [39]. Linoleate 9S-lipoxygenase (LOX) which encodes an enzyme involved in lipid
peroxidation, was induced by the water and heat stresses in foxtail millet [40]. The impact of various
abiotic stresses on different millet varieties is given in Tab. 1. The overview of the biological plant
responses tovarious abiotic stresses is depicted in Fig. 2.
1366 Phyton, 2021, vol.90, no.5

Plants have evolved various morphological, biochemical, physiological and molecular mechanisms to
withstand various environmental stresses.Stress stimuli are perceived by plant cells via various sensors
which then activate various signalling pathways. These involve various plant hormones, secondary
messengers, transcription regulators and signal transducers [41]. These adaptations affect the plant’s
vegetative growth, reproductive development, yield and quality [42].
3 Morphological Adaptations to Stress
Short life cycle, and plant heights, small leaf areas, thickened cell walls, and dense root systems are
various traits that help millets in resistingstress. Being C4 plants is highly advantageous as it increases
the water use efficiency (WUE) and nitrogen use efficiency (NUE) [43]. Flowering in pearl millet
mightchange with the rainfall pattern [44]. An increased root length and a decreased shoot length were
seen in Panicum sumatrense undergoing drought treatments [45]. It was further reported that pearl millet
is composed of a fast-growing primary root system and a rapid colonization of deeper soil horizons [46].
Table 1: Impact of abiotic stresses on millets
Species Stress (Drought/Salt/ Heat/Metal/Herbicide) Effect on plant Reference
Pearl millet Drought stress was applied by stopping irrigation for
4 weeks, after 3 weeks fromgermination
Significant reduction in plant height, biomass, panicle and
stalk lengths, no. of leaves, total grain weight and number.
Debieu
et al. [34]
Finger
millet
Induction of saline stress with various NaCl concentrations
(0, 50, 100, 150, 200 mM)
Salt concentrations above 50 mM decreased chlorophyll
contents (a,b, chlorophyll a+ chlorophyll b), , seed
germination, survival rate, plant growth, fresh and dry
weights, and shoot length and biomass, and increased
proline accumulation, chlorosis of leaves , H
2
O
2
content,
and cell death. Above 100 mM concentration of NaCl,
RWC decreased, and there was a significant increase in
electrolyte leakage, caspase like activity, and thick wall
lignification of xylem vessels.
Satish
et al. [28]
Pearl millet Atrazine stress caused by increasing concentration (0, 5,
10 and 50 mg/kg) of the herbicide atrazine
Increasing herbicide concentration caused an increase in
H
2
O
2
and MDA, and increased activity of APX, POD
antioxidant enzymes. There was a decrease of the SOD and
CAT activities, and a suppression of antioxidant gene
expression. Photosynthesis was inhibited by blocking the
electron acceptor protein PSII of the thylakoid membrane,
resulting in an inhibited electron transfer.
Erinle
et al. [37]
Pearl millet
and Finger
millet
Various concentrations of nickel (0, 15, 20, 25, 30 and
40 ppm) resulted in nickel induced stress in plants
Increased nickel concentration resulted in inhibition of
seed germination, supressed root and shoot length, and
reduced root and shoot dry weights. At higher
concentration of nickel, the stem turned brownish.
Activities of POD and SOD were increased and those of
CAT activity decreased. At 40 ppm nickel, proline content
increased 4.0–4.3-fold.
Gupta
et al. [38]
Finger
millet
Changing the temperature from optimum (32/22°C:
daytime maximum/night-time minimum) to high
temperature (HT
1
) 36/26°C and HT
2
38/28°C resulted in
high temperature stress in seedlings
High temperature stress resulted in a decreased chlorophyll
index, photosystem II activity, plant height, internode
length, no. of tillers per plant, leaf and stem dry weights,
and harvest and grain yields. Panicle emergence was
delayed by 16 days, flowering by 21 days and
physiological maturity by 28 days. Stress during booting,
panicle emergence or flowering developmental
morphology stages resulted in a maximum decrease in
grain yield.
Opole
et al. [39]
Finger
millet
Withholding irrigation to 45-day-old plants resulted in
plant water stress
Water stress led to droopy, curling leaves, a 10-fold
increase in proline leaf content, increased MDA content,
electrolyte leakage, H
2
O
2
concentration, and activity of
antioxidant enzymes (GR, SOD, APX, GPX and CAT).
Bhatt
et al. [32]
Phyton, 2021, vol.90, no.5 1367

Pearl millet yields are reduced because of water stress after flowering that effects both grain filling and seed
setting. High tillering varieties having small-size grains and small panicles minimize drought-related grain
filling impairments [47]. Foxtail millet plants produce longer and denser root hairs forming a large
rhizosheath that produces more root biomass which mighthelp in penetrating deep into dry soils [48]. It is
reported that the farmers in dry areas preferred short duration, high tillering varieties of pearl millet which
ensured better yield and fodder value. The drought escape mechanism of pearl millet is the short
“flowering time”which is completed with little available water [49]. Pearl millet has a varying root
system depending on the water limitation, with a root depth ranging from 140 cm to 3 m with lateral root
spreading. The transpiration rate is kept high by adjusting the stomatal movements with a maximisation
of carbon fixation while water is available [50]. The adaptive responses of pearl millet to drought stress
include an increase in its root length to increase water uptake [51]. Stay green is a drought tolerance trait
which is a characteristic of some genotypes where active photosynthesis is extended by delaying leaf
senescence via a complex signalling network. The pearl millet semi-dwarf, inbred lines developed in
USA have this “stay green”characteristics. This allowsplants to continue with photosynthesis regardless
of the soil water content, and maintain a good grain yield under drought stress conditions [52]. Drought
tolerant pearl millet accessions showed various morphological and physiological responses to stress such
as upright folding of leaves that reduces surface area of evaporation, greater osmotic adjustment capacity
of young leaves and stems, and higher accumulation of NO
3
–
,K
+
, amino acids, proline, sucrose, glucose
and ammonium compounds [53]. It was reported that an increased leaf tensile strength leads to an
increased drought tolerance among three species of Eragrotis [54].
Metal tolerance in finger millet was reported to be higher than that in pearl millet and oats. Finger millet
had the maximum build-up of nickel (Ni) in roots which indicates that Ni accumulation in the roots helps the
plant to mitigate the effects of metal toxicity [38]. Phosphorus (P) limitation in plants lead to a phenotypic
adaption of large root systems. In foxtail millet, phosphorus adaptation leads to lateral root proliferation by
Figure 2: Plant biological responses to various abiotic stresses. (Created with BioRender.com)
1368 Phyton, 2021, vol.90, no.5

increasing rootnumber, density and length, and thus enlarging the root absorptive surface area. Auxin and
gibberellin stimulate root development understress conditions [55].
4 Biochemical and Physiological Adaptations to Stresses in Millets
Osmoprotectants play a vital role in improving hyperosmolarity which is caused by salinity stress and
establishes cellular ionic homeostatic conditions. The biochemical adaptive response to salt stress in finger
millet included anelevated proline content, increased reduced sugar concentration and total leaf proteins [29].
Proline which is an important amino acid, plays a vital role as a compatible osmotic molecule and in osmotic
potential adjustment; it thus helps in improving drought tolerance. It also acts in antioxidative defense, metal
chelation and stress signalling [56]. Antioxidant enzymes represent the adaptive mechanism of plants
exposed to oxidative damage caused by stress. This consists of SOD, CAT, peroxidase (POD) and APX.
Metal stress in millets resulted in elevated activities of POD and SOD with a reduction in CAT activity
[38]. A pearl millet variety well-adapted to saline environments showed goodphysiological and
biochemical responses to increased salinity such as increased proline, total soluble proteins, and
epicuticular wax content [27]. It was seen that the salt tolerant varieties of finger millet and rice had
lower shoot Na
+
/K
+
ratios and much higher leaf carbohydrate contents; it was concluded that ion
regulation along with carbohydrate metabolism led to salt tolerance in rice and finger millet [57].
Ascorbate is a water-soluble antioxidant in plants that is necessary for the efficient activity of APX,
which plays an important role in the scavenging process ofconverting H
2
O
2
into H
2
O. A 200% ascorbate
increase was reported in finger millet drought tolerant varieties which implies that ascorbate increases
tolerance against drought stress [58]. A higher expression of secondary metabolite genes associated with
alkaloid, terpenoid, flavanols, lignin, wax, mevalonic acid (MVA) and Shikimic acid (SA) metabolic
pathways, was seen in drought stressed pearl millet at the flowering than at the vegetative stage; this
helped in maintaining osmotic potential and membrane integrity. A higher accumulation of secondary
metabolites was found in drought tolerant pearl millet genotypes [59]. Phytohormones such as auxin,
cytokinin, ABA, gibberellin and ethylene play a vital role in stress adaptive responses.
An increased lipoxygenase enzyme activity during water stress in millets indicate that it might provide a
better drought tolerance to plants [60]. The foremost physiological adaptations of pearl millet to drought
stress were stomatal closure to prevent transpiration water loss, reduced stomatal conductance, reduced
photosynthetic rate and ultimately decreased CO
2
and rubisco activities [61]. A total of
2474 differentially expressed proteins, identified by proteomic analysis, were found to be involved in
various plant processes (photosynthesis; stress and defense responses; ATP synthesis; carbon metabolism;
protein biosynthesis, folding and degradation; cellular organization) and had up to a 4-fold increased
expression underdrought stress, which indicates their possible role in the response and adaption of foxtail
millet todrought stress [62]. Pearl millet has expanded the gene families forwax, suberin, and cutin
biosynthesis, and transporters for secondary metabolites as compared to other cereal crops. It has been
proposed that these deposits might provide the plants with drought and heat tolerances [34]. High levels
of osmotic adjustment and transpiration were found in resistant races of millet to drought stress. Osmotic
adjustment is greater in millet races with smaller plants having small organs and cells; hence, having
smaller plants in these races is a drought adaptive trait [63]. It was concluded that higher excised leaf
water retention capacity (ELWRC), plant water relations, proline accumulation, leaf area index (LAI),
total biomass (TB) and an efficient antioxidant (AOX) system contribute to the dehydration stress
tolerance in pearl millet [61]. It was reported that the drought tolerance capacity of a finger millet
genotype included alower MDA content, higher osmolyte accumulation (proline, glycine betaine and total
soluble sugars) and an increased activity of antioxidant enzymes (SOD, CAT, APX and GPX) [64].
A drought tolerant foxtail millet variety had a moderate rate of decline RCW and chlorophyll, increased
soluble sugar and proline concentrations, and a significant increase of the stress hormones ABA and JA.
Phyton, 2021, vol.90, no.5 1369

These phytohormones are involved in drought adaptive responses such as the regulation of gene expression
whichhelp plants in the adaption to stress [65]. A high temperature tolerant variety of foxtail millet showed
low photosynthetic and stomatal conductance rates, reduced root respiration, accumulation of protective
metabolites (serine, threonine, valine, fructose, glucose, maltose, isomaltose, malate, itaconate) in roots
with a better utilization of carbon and nitrogen [66]. The effects of water stress and heat stress are
reported to be key regulators of abscisic acid (ABA) biosynthesis, and led to a 7–8 fold increase of ABA
in foxtail millet [40]. The various biochemical and physiological adaptations of millets to various abiotic
stresses are summarizedin Tab. 2.
5 Molecular Adaptations of Millets to Stresses
The plant response to various environmental factors is differentially perceived and expressed at the
molecular level. In a study on phosphorus limitation in foxtail millet the molecular adaptions include the
upregulated expression of SiPHT1;1,SiPHT1;4 in roots and that of SiPHT1;2 in roots and shoots for
anenhanced uptake and translocation of phosphorus under stress conditions [51]. Drought tolerance QTL
of pearl millet helped in a reduced salt uptake and enhanced growth undersalt stress [67]. Late
embryogenesis abundant (LEA) gene, namely SiLEA14, from foxtail millet was induced by osmotic,
NaCl stress and ABA. It increased salt tolerance in transgenic Arabidopsis and when overexpressed in
transgenic foxtail millet, it enhanced tolerance tosalt and drought stresses [68]. Stress induced EcNAC1
(NAM, ATAF1/2, and CUC2) transcription factor from finger millet, which is induced by salinity and
drought, was characterised and expressed in transgenic tobacco plants. It resulted in an increased
tolerance to various abiotic stresses such as osmotic stress and salinity stress [69]. Lipid transfer gene
(SiLTP) expressed in all foxtail millet tissues improved the drought and salt tolerance in this speciesby
increasing the proline and total soluble sugar contents. This gene can be used for anenhanced drought and
salt stress tolerance in crop plants [70]. Plasma membrane proteolipid genes in pearl millet (PgPmp3-1
and PgPmp3-2), in association with other proteins showed enhanced expression during cold, drought and
salt stresses and provided abiotic stress tolerance to plants by encoding hydrophobic proteins and
Table 2: Biochemical and physiological adaptations to stress in millets
Species Variety Trait (Drought adaptive/
Salt adaptive/High
temperature)
Adaptive mechanisms Reference
Pearl
millet
AVKB-19 Salt adaptive Accumulated, higher osmolyte (proline, soluble protein) concentration. Makarana
et al. [27]
Pearl
millet
PRLT2/89-33 Drought adaptive Higher, accumulation of secondary metabolites (flavonoids, lignin,
terpenoids)
Shivhare et al.
[56]
Finger
millet
Trichy 1 Salinity tolerant Accumulate higher levels of carbohydrates, and maintain low Na
+
/K
+
ratios under stress conditions.
Vijayalakshmi
et al. [57]
Finger
millet
PRM6107 and
PR202
Drought tolerant 200% increase in ascorbate content, which limited the accumulation of
ROS.
Bartwal et al.
[58]
Foxtail
millet
Damaomao
(DM)
Drought tolerant Moderate rate of decline of RWC and chlorophyll, increased soluble
sugar and proline concentrations, significant increase in ABA and JA
phytohormones
XU et al. [65]
Foxtail
millet
523-P1219619 High soil temperature
tolerance
Effective utilization and assimilation of membrane carbon and nitrogen,
accumulation of stress-related protective metabolites (serine, threonine,
valine, fructose, glucose, maltose, isomaltose, malate, itaconate) in
roots
Aidoo et al.
[66]
Finger
millet
FM/ST/01 Drought tolerant Significant accumulation of proline, glycine betaine and total soluble
sugars. Increased activity of antioxidant enzymes (SOD, CAT, APX,
GPX)
Mundada et al.
[64]
1370 Phyton, 2021, vol.90, no.5

maintaining cellular ion homeostasis [71]. 35 CBL-interacting protein kinase (CIPK) genes reported in
foxtail millet are involved in stress signalling pathways and play an important role in stress responses and
plant development. Most SiCIPK genes are strongly induced by salt and cold stresses, and others by
ABA and PEG treatments [72]. There are three abiotic stress-inducible promoters in pearl millet which
are induced under high temperature, drought and salt stresses that confer high abiotic stress tolerance and
can be used in developing stress tolerant crops [73]. These promoters include (1) Cytoplasmic Apx1
(Ascorbate peroxidase)- potential candidate in the elimination of H
2
O
2
; (2) Dhn (Dehydrin)-stabilization
and protection of cellular membrane and enzymes from low temperature and ROS; and (3) Hsc70 (Heat
shock cognate)-play chaperone function by proper folding and translocation of newly synthesised
proteins. The SiMYB42 (Myeloblastosis) transcription factor in foxtail millet was upregulated under low
nitrogen, salt, and drought stresses; it regulated the expression of nitrate transporter genes which
enhanced the plant tolerance to low nitrogen conditions [74]. Calcium-dependent protein kinases (CDPK)
genes of foxtail millet play a vital role in signalling pathways, and enhance drought resistance in the plant
and transgenic Arabidopsis. Foxtail millet has 29 CDPK genes, and SiCDPK24 had the highest transcript
levels underdrought conditions; it was concluded that CDPK’s play an important role in drought stress
resistance [75]. NAC (NAM, ATAF, and CUC) like transcription factor SiNAC110 in foxtail millet,
localized in the nucleus, is induced by drought, salt and other abiotic stresses. Its over expression led to
an increased drought and salt tolerance in Arabidopsis by enhancing the gene expression for proline
biosynthesis, Na
+
/K
+
transport, and aqueous transport proteins [76]. Under salt and drought stresses in
foxtail millet, NF-Y (Nuclear Factor Y) genes, SiNF-YA1 and SiNF-YB8 were highly induced by ABA
and H
2
O
2
. These led to stress tolerance by activating stress related genes, RWC, chlorophyll contents,
and SOD, POD, and CAT, thus enhancing the antioxidant system [77]. In foxtail millet, the autophagy-
related gene SiATG8a, which is localized in the membrane and cytoplasm, is involved in plant responses
to nitrogen starvation and drought stress. Overexpression of SiATG8a in transgenic Arabidopsis, resulted
in plant tolerance to nitrogen starvation and drought, as the plants having higher nitrogen content showed
higher drought tolerance [78]. The three antioxidant genes, i.e., APX, glutathione reductase (GluR) and
SOD had a higher expression level in pearl millet genotypes during polyethylene glycol (PEG)-induced
drought stress conditions, resulting in a higher osmotic stress tolerance in the seedlings [56].
Sevendrought-responsive genes may be involved in the drought tolerance of minor millets as their
expression was up regulated by water stress treatment, and can be used for the development of transgenic
drought tolerant crops [79]. These genes included (1) NAC2; (2) CDPK; (3) U2-snRNP (small nuclear
RiboNucleoProtein particles)-regulates gene expression; (4) plant synaptotagmin- maintains plasma
membrane intrigrity; (5) Aquaporin- membrane channel; (6) MPK17-1 (Mitogen activated Protein
Kinase)-signalling and (7) Scythe protein-regulates apoptosis Transcriptome analysis of finger millet
showed upregulation of various drought stress signalling cascade genes such as Protein Phosphatase 2A
(PP2A)-2 fold increase in drought stressed finger millet; Calcineurin B-Like protein (CBL) Interacting
Protein Kinase 31 (CIPK31)- highly stress responsive; Farnesyl Pyrophosphate Synthase (FPS)- which
facilitates farnesylation of proteins which are involved in ABA signalling; Signal Recognition Particle
Receptor (SRPR α); and basal regulatory gene TBP (Tata Binding Protein) Associated Factor6 (TAF6). It
was concluded that drought activates the genes associated with housekeeping or basal regulatory
processes in finger millet [80].
Terpene synthase (TPS) genes in foxtail millet especially SiTPS19 showed a significantly higher
expression under both biotic and abiotic stresses, indicating that it can improve crop resilience by having
a possible function in defense and environmental adaptation [81]. There was an abundant upregulation of
the AKR1 gene (Aldo Keto Reductases) in roots and leaves of foxtail millet with increasing drought and
salt stress; it was concluded that the AKR1 gene is associated with aphysiological defense against
oxidative stress [82]. The PgPAP18 gene onpearl millet, belonging to the purple acid phosphatase (PAP)
Phyton, 2021, vol.90, no.5 1371

family, showed a 2-3-fold upregulation underheat, drought, salt and metal stresses. In addition to having a
role in the phosphatase activity, genes of this family may play a vital role in tolerance against various
abiotic stresses by scavenging ROS and crosstalk between stress signalling pathways [83]. Ninety seven
pgWRKY genes were identified in pearl millet with the presence of 127 cis regulatory elements, specific
to various biotic and abiotic stresses. This indicated the likelyinvolvement of pearl millet WRKY
transcription factors in providing resistance against plant biotic and abiotic stresses [84]. The transcription
factor EcbZIP60 belonging to the family of basic leucine Zippers (bZIPs) from finger millet was highly
upregulated underdrought, osmotic and salinity stresses. EcbZIP60 plays an important role in adaptation
to various stresses by improving growth and upregulation of unfolded protein-protein responsive pathway
genes [85]. Ten LIM genes were reported in foxtail millet with cis acting elements related to abiotic
stresses. SiWLIM2b was highly upregulated in foxtail millet under abiotic stress; when it was
overexpressed in transgenic rice under drought conditions led to a higher survival rate with higher
relative water content and less cell damage in the plant. Therefore, it was concluded that SiWLIM2b is
involved in the phenylpropane pathway, gene regulation and enhances drought stress tolerance [86].
Increased transcription levels of the stress-induced SiARDP (ABA- responsive DREB-binding protein
gene) gene after drought, salinity, and low temperature stresses, and ABA treatment, was seen in foxtail
millet seedlings. SiARDP gene expression might be regulated by SiAREB
1
and SiAREB
2
(ABA responsive
element binding) transcription factors; SiARDP is involved in signalling pathways and plays an important
role in stress response and increased stress tolerance in plants [87]. The heat-shock protein gene
EcHSP17.8 in finger millet was induced by heat, NaCl, and oxidative stresses, and mannitol, and the
maximum expression was found in root tissues. An upregulation of up to 40-folds was found underheat
stress, and hence this gene is characterised for heat stress tolerance in plants [88]. Cold stress resulted in
upregulation of the SiSET14 gene in foxtail millet. SET [(Su(var)3–9, E(Z) and Trithorax)] domain
proteins are putative candidates for histone lysine methyltransferases. When expressed in a yeast system,
it conferred abiotic stress tolerance to transgenic yeast cells. This suggests a possible role of SiSET genes
in conferring abiotic stress tolerance in foxtail millet [89]. The Acetyl-Coenzyme A Carboxylase
(ACCase) gene in foxtail millet provides herbicide (sethoxydim) resistance, and can be used in the
development of transgenic maize with herbicide resistance and higher oil content [90].The various genes
involved in stress adaption of millets are summarized in Tab. 3. An account of the millet adaptation
mechanisms is depicted in Fig. 3.
Table 3: Genes involved in the stress adaptation of millets
Gene Source Stress Role Reference
SiLEA14 Foxtail
millet
Salt/Drought stress Improved salt tolerance of transgenic Arabidopsis; its overexpression in
transgenic Foxtail millet led to enhanced salt and drought tolerance.
Wang et al.
[68]
SiATG8a Foxtail
millet
Nitrogen starvation/
Drought stress
Overexpression in Arabidopsis conferred tolerance to nitrogen starvation and
drought stress
Li et al. [78]
SiLTP Foxtail
millet
Salt/Drought stress SiLTP expression enhanced the salt and drought tolerance in transgenic tobacco. Pan et al.
[70]
PgPmp3-
1 and
PgPmp3-2
Pearl
millet
Cold/Salt stress Upregulation of PgPm3 genes under cold/salt stress contributed to cold/salt stress
tolerance in plants.
Yeshvekar
et al. [71]
SiCDPK24 Foxtail
millet
Drought stress Overexpression in transgenic Arabidopsis enhanced its drought resistance Yu et al. [75]
ACCase Foxtail
millet
Herbicide stress Overexpression in transgenic maize resulted in an increased herbicide
(sethoxydim) resistance.
Dong et al.
[90]
SiNF-YA1 and
SiNF-YB8
Foxtail
millet
Drought/Salt
stresses
Enhanced stress tolerance in tobacco by activating stress- related genes, and
improving physiological traits.
Feng et al.
[77]
1372 Phyton, 2021, vol.90, no.5

The abiotic stress signalling cascade is activated with the recognition of stress signal by the various cell
membrane receptors and transporters including GPCR (G-Protein Coupled Receptor), Enzyme Linked
Receptor (ELR), Calcium channels and Ion transporters. The cytosolic Ca
2+
increases in response to
Table 3 (continued ).
Gene Source Stress Role Reference
SiCIPK Foxtail
millet
Salt/Cold/ABA
stresses
Involved in stress responses and signalling towards various abiotic stresses. Zhao et al.
[72]
EcHSP17.8 Finger
millet
Heat stress/NaCl
stress
40-fold upregulation underheat stress, and early responsive gene underheat stress
and tolerance.
Chopperla
et al. [88]
SiWLIM2b Foxtail
millet
Drought stress Increased drought resistance in transgenic rice, with higher RWC and less cell
damage.
Yang et al.
[86]
SiARDP Foxtail
millet
Drought/Salt stress/
Low temperature
Enhanced drought and salt tolerance in transgenic Arabidopsis. The DREB
transcription factors might regulate the expression of SiARDP
Li et al. [87]
EcbZIP60 Finger
millet
Drought/Salinity/
Oxidative stress
Expression in transgenic tobacco resulted in tolerance to drought, salinity and
oxidative stresses. This was by maintaining cellular homoeostasis via
upregulation of unfolded protein responsive pathway genes.
Babitha
et al. [85]
AKR1 Foxtail
millet
Osmotic/Salt stress Contribution in antioxidant defense related pathways. Kirankumar
et al. [82]
Figure 3: Molecular mechanism of adaptation in millets at the functional gene level (Created with
BioRender.com)
Phyton, 2021, vol.90, no.5 1373

hyperosmotic stress, and oxidative stress causes an elevation in the ROS levels. The signal is then transmitted
downstream through the relay molecules and is converted into intracellular signal by the secondary
messengers [i.e., Ca
2+
, ROS, cAMP, cGMP, Nitric oxide (NO)]. These secondary messengers further
activate the kinase cascade (protein kinases; i.e., CDPK; MAPK) and elevate phytohormone signalling
(Abscisic acid-ABA; Ethylene-ET; Salicylic acid-SA; Jasmonic acid-JA). These kinases are responsible
for the sequential phosphorylation/dephosphorylation of proteins, and activation of cascade components.
The phosphorylation/dephosphorylation of transcription factors (TF’s) results in their upregulation/
downregulation. Various upregulated TF’s from various millets include [Eleusine coracana (EcNAC1,
EcbZIP60); Setaria italica (SiMYB42, SiNAC110, SiNF-YA1, SiNF-YB8, SiAREB
1
,
SiAREB
2
); Pennisetum glaucum (pgWRKY)] which are involved inregulating the expression of stress
responsive/defensive genes in various millets [Setaria italica (SiLEA14; SiARDP; SiCDPK24, SiCIPK,
SiATG8a, SiLTP, SiWLIM2b); Pennisetum glaucum (PgApx pro, PgDhn pro, PgHsc70, PgPAP18,
PgPmp3-1, PgPmp3-2); Eleusine coracana (EcHSP17.8); APX; SOD; GlutR; U2-snRNP; MPK17-1;
AKR1]. These later genes are involved in the various abiotic stress responses and tolerance such as the
accumulation of protective metabolites, osmoregulators, decreased transpiration, reduced stomatal
conductance, reduced photosynthetic rate, increased root length and denser roots, enhanced activity of
antioxidant enzymes and phytohormones, elevated nitrogen content, maintenance of membrane integrity,
increased epicuticular wax content, increased nitrogen use efficiency (NUE) and water use efficiency (WUE).
6 Transcriptomic Analysis of Millets
Transcriptomic analysis of a salt tolerant and a susceptible foxtail millet cultivars, revealed that
159 differentially expressed transcripts produced >2-fold change in response to salinity stress. Among
these, 115 were upregulated and 44 were down regulated. It was concluded that the expression of
transcription factors and signalling genes was greater in the tolerant than in the susceptible variety which
contribute to their signal perception mechanisms under saline conditions [91]. Eighty one conserved and
14 novel differentially-regulated miRNAs were identified during a small RNA sequencing on the salinity
tolerant pearl millet genotypes. A total of 448 genes were identified as target genes, and 122 among these
encoded transcription factors. These miRNA’s and their target genes can regulate the auxin response
pathway, and hence have a role in salinity stress tolerance in pearl millet [92]. Twenty-nine upregulated
and downregulated differentially expressed proteins (involved in various energy, lipid, nitrogen,
carbohydrate, nucleotide, stress related metabolism, signal transduction, and photosynthesis) were
identified in foxtail millet seedlings, and they seemed to be involved in Providing tolerance against salt
stress [93]. The transcriptome changes in a drought tolerant foxtail millet were analysed after a PEG-
induced drought stress. Among the identified 327 differentially expressed transcripts, the reverse northern
technique identified 86 upregulated transcripts, which suggested their possible function in dehydration
adaption. Most of the upregulated transcripts were involved in metabolism, transcription regulation,
signalling, protein degradation and stress. A 5-11-fold induction of the DREB2 (Dehydration Responsive
Element Binding type) protein was seen by qRT-PCR analysis [94]. Comparative transcriptome analysis
of pearl millet salinity tolerant and susceptible cultivars identified 11,627 DEG’s, 1,287 upregulated
unigenes and 1,451 downregulated unigenes that were common in both cultivars. Among the
differentially-expressed genes, there were the genes encoding for transcription factors, ion transporters,
and metabolic pathways involved in stress responses. The tolerant line had an upregulation of the
ubiquitin-mediated proteolysis and phenylpropanoid biosynthesis pathway genes. On the other hand,
glycolysis/gluconeogenesis unigenes and ribosome genes were downregulated in the susceptible variety
[95]. Three thousand and sixty six differentially-expressed genes (DEGs) were identified
(1404 upregulated and 1,662 downregulated) in a drought tolerant variety of foxtail millet, which lead to
the formation of regulatory networks involving photosynthesis, signal transduction, osmotic regulation,
redox regulation, hormonal signalling, cuticle and wax biosynthesis and enhanced drought tolerance [96].
1374 Phyton, 2021, vol.90, no.5

Leaf transcriptome of two contrasting pearl millet varieties differing in terminal drought tolerance was
examined. A total of 40,880 genes were differentially-expressed in both varieties; 13,260 and
8,799 DEGs were significantly-expressed in the sensitive and tolerant varieties, respectively. The tolerant
variety had a higher expression than the sensitive one in receptor kinases, genes involved in regulation of
detoxification enzymes, phytohormone biosynthesis, secondary metabolites, and stress-related
transcription factors [59]. Root transcriptome of the drought tolerant and sensitive pearl millet lines led to
the identification of 6,799 and 1,253 DEGs, respectively, under both control and drought conditions. The
tolerant variety had an upregulation of 2,846 genes, and 3,169 genes were downregulated, while the
sensitive line had an upregulation of 371 genes, and 96 genes were downregulated. The upregulated
DEGs were involved in photosynthesis, plant hormone signal transduction, and mitogen-activated protein
kinase signalling [97]. Integrated transcriptomic and metabolomics of two foxtail millet cultivars implied
that salinity tolerance is attributed to higher ion channel efficiencies and the antioxidant system. A total
of 8,887 and 12,249 DEGs were identified in the salt tolerant and salt sensitive varieties, respectively.
A total of 4,830 and 4,057 genes were upregulated and downregulated, respectively, on the tolerant
cultivar. The sensitive cultivar had an upregulation of 6,339 genes, and 5,910 genes were downregulated
[98]. The transcriptome analysis of various millets is listed in Tab. 4.
7 Alleviation of Stress in Millets
One economically feasible option to tackle the effects of stress on plants is the application of plant
growth promoting bacteria (PGPB). Finger millet inoculated with 1-aminocyclopropane-1-carboxylic acid
(ACC) deaminase-producing drought tolerant Pseudomonas spp. resulted in improved growth, and
enhanced antioxidant activity in both well-watered and drought stressed plants. The ACC deaminase
converts the immediate precursor of ethylene (ACC) into α-ketobutyrate (α-KB) and ammonia, thereby
reducing the ethylene level of plants and promoting growth [102]. Florescent Pseudomonads (SPF-33,
Table 4: Transcriptomic analysis of millets
Species Transcriptome platform Link/ Reference
Foxtail millet Microarray analysis Puranik et al. [91]
https://doi.org/10.1016/j.jplph.2010.07.005
Foxtail millet ABI solid sequencing Lata et al. [94]
https://doi.org/10.1016/j.bbrc.2010.02.068
Pearl millet Illumina HiSeq 2500 Shinde et al. [95]
https://doi.org/10.1016/j.envexpbot.2018.07.008
Foxtail millet Illumina HiSeq X Ten platform using PE150 mode Shi et al. [96]
https://doi.org/10.7717/peerj.4752
Finger millet Illumina NextSeq 500 Parvathi et al. [80]
https://doi.org/10.1007/s12041-019-1087-0
Pearl millet Illumina HiSeq2300 Shivhare et al. [56]
https://doi.org/10.1007/s11103-020-01015-w
Pearl millet Illumina Hiseq Dudhate et al. [97]
https://doi.org/10.1371/journal.pone.0195908
Foxtail millet Illumina Hiseq platform X ten Pan et al. [98]
https://doi.org/10.1038/s41598-020-70520-1
Proso millet Illumina HiSeq 2000 platform Hou et al. [99]
https://doi.org/10.3732/apps.1600137
Foxtail millet Illumina HiSeq 2000 Tang et al. [100]
https://doi.org/10.1038/s41598-017-08854-6
Broomcorn millet Illumina HiSeq 4000 Shan et al. [101]
https://doi.org/10.1186/s12864-020-6479-2
Phyton, 2021, vol.90, no.5 1375

SPF-37, SPF-5), which are plant growth promoting rhizobacteria (PGPR) have been reported to alleviate salt
stress in salinity-sensitive finger millet. This was done by increasing its plant height and spikelet number,
germination, total chlorophyll, phenolics, flavonoids, proteins, activity of enzymatic antioxidants,
andproline content, and decreasing its lipid peroxidation and H
2
O
2
[103]. Millets inoculated with
halophilic rhizobacteria Enterobacter sp. PR14 showed growth promoting traits such as indole acetic acid
(IAA), aminocyclopropane-1-carboxylate deaminase (ACCD), phosphate solubilization and antioxidant
enzymes. This led to an increased seed germination, root and shoot length, and dry weight, hence
ameliorating salinity stress in millets [104]. Inoculated finger and foxtail millets with Sphingomonas faeni
bacterial mutants carrying the ACC deaminase gene, which is known to regulate ethylene, evolved during
cold stress which in turn hampered plant growth. Blocking of ethylene resulted in improved root and
shoot length, biomass content, and increased antioxidant activity, thus alleviating cold stress in finger and
foxtail millets [105]. NaCl-stressed foxtail millet had an enhanced antioxidant enzyme system when
treated with biogenic amines putrescine (Put) and spermidine (Spd). Plants of foxtail millet showed a
reduced hydrogen peroxide level and electrolyte leakage, allowing an increased biomass content, relative
water content, total chlorophyll, carotenoid levels, and a greater activity of in SOD, CAT, APX and GPX
[106]. It was reported that the endophytic, salt tolerant, plant growth promoting Bacillus
amyloliquefaciens EPP90 from pearl millet is a potential multi stress reliever and growth promoter. These
halophilic bacteria were obtained from the roots, leaves and stem of the host pearl millet [107].
Inoculation of Panicum miliaceum with the root colonising endophytic fungi Piriformospora indica,
resulted in an increased number of grains, plant height, and pinnacle length, and a greater grain nitrogen,
protein, phosphorus, and chlorophyll contents under both well-watered and drought conditions [108].
Hydrogen sulphide (H
2
S) in combination with proline alleviate cadmium (Cd) damage in foxtail millet
[109]. Nickel overloaded finger millet seedlings reduced the toxic effect of Ni when treated with sodium
nitroprusside (SNP) and Salicylic Acid (SA) by improving root and shoot length, chlorophyll content,
mineral concentration and dry mass [110]. Cadmium (Cd
2+
)-induced oxidative damage in foxtail millet
was alleviated by sulphur dioxide (SO
2
) by enhancing the activities of antioxidant enzymes, increasing
the contents of glutathione and phytochelatins, and reducing the uptake and translocation of Cd
2+
[111].
Drought tolerant, phosphorus solubilizing microbes Acinetobacter calcoaceticus and Penicillium sp.
mitigated the adverse effects of drought stress in foxtail millet by enhancing the accumulation of glycine
betaine, sugars, and proline [112]. Pearl millet seedlings improved their tolerance to salt stress when they
were inoculated with the endophyte Aspergillus terreus; this was because of increased chlorophyll
content, RWC, soluble sugar, phenol and flavonoids [113]. Fig. 4 depicts the abiotic stress amelioration in
millets by plant growth promoting bacteria (PGPB). Furthermore, the role of exogenously applied
selenium was elucidated in Seteria italica and Panicum miliaceum after exposure to salt stress. It was
concluded that Se amplified the antioxidant enzyme activities and the osmolyte concentrations, and
lowered the H
2
O
2
production. Hence, Se alleviated salt stress in millets [114,115]. Various stress
mitigants in millets are mentioned in Tab. 5.
PGPBs help plants in surviving various stress conditions because of their growth promoting traits.
Rhizobacteria associated with plants take up tryptophan and other exudates from the plant. They utilize
tryptophan (trp) to synthesise the phytohormone indole-3-acetic acid (IAA) which is utilized by plants
(along with its own synthesized IAA) to regulate plant development via cell proliferation and elongation,
and development of lateral and adventitious roots. IAA activates the transcription of the plant enzyme
1-aminocyclopropane-1-carboxylic acid (ACC) synthase which catalyses the production of ACC from
S-Adenosyl Methionine (SAM). ACC is further converted to ethylene with the aid of the enzyme ACC
oxidase (ACCO). After perceiving a stress signal, the ethylene level inside the plant is increased as a
stress response, and growth is retarded. PGPBs take up a large portion of the ACC synthesised by root
cells and limit the ethylene production by the root cells. This is accomplished by the enzyme
1376 Phyton, 2021, vol.90, no.5

1-aminocyclopropane-1-carboxylic acid deaminase (ACCD) present in the bacteria that hydrolyses ACC into
ammonia and α- Ketobutyrate. Thus, PGPB promote growth by IAA production and ACC deamination. The
various PGPB studies in millets include Pseudomonas sp., Florescent pseudomonads, Enterobacter sp. PR14,
Sphingomonas faeni mutants, Acinetobacter calcoaceticus, and Bacillus amyloliquefaciens EPP90. These
bacteria help in mitigating the effects of various abiotic stresses by an increased phosphate solubilization,
and antioxidant activity of enzymes, and accumulation of osmoprotectants, and a decreased lipid
peroxidation.)
Figure 4: Abiotic stress amelioration in millets by plant growth promoting bacteria (PGPB) (Created with
BioRender.com)
Table 5: Stress mitigants
Stress type Species Mitigant
Chemical/Biological
Reference
Drought stress Finger millet ACC deaminase- producing
Pseudomonas spp.
Chandra et al. [102]
Salinity stress Finger millet Fluorescent Pseudomonas Mahadik et al. [103]
Salinity stress Sorghum and
Finger millets
Halophilic ACC deaminase-
producing Enterobacter sp.
Sagar et al. [104]
Cold stress Finger and Foxtail
millets
Sphingomonas faeni Srinivasan et al. [105]
Salinity stress Foxtail millet Put + Spd; 0.5 + 0.5 mM Rathinapriya et al. [106]
(Continued)
Phyton, 2021, vol.90, no.5 1377

8 Conclusion
Abiotic restrains like salinity and drought are the foremost preventive factors for the development and
productivity of plants. However, millets have a broad range of adaptive measures to deal with those stresses.
Millets are well adapted to marginal regions, and thus they can be suitable crops for food security as
demanded by the year 2050. So far, we have various studies on millets like stress tolerance mechanisms,
adaptations, genetic manipulation, targeted expression of enzymes and transporters, contribution of
proline etc. However, the proteomic and metabolic investigations on millets in response to various abiotic
stresses are still limited. Additional molecular studiesand gene transfer methods are required to develop
new and proficient cultivars with boosted natural osmolytes and raised tolerance for crop production. This
will aid in attaining sustainable development efforts. The application of ‘omics’approaches can be useful
in enhancing tolerance ofabiotic stress in millets. There is a need to focus on the crosstalk between
various stress responses and signalling pathways to understand the precise mechanisms used by plants to
adjust in the fluctuating environments. This will help to obtaincrop varieties that are more resistant to
stress conditions, thus producing a better yield of increasedquality.
Funding Statement: The authors received no specific funding for this study.
Conflicts of Interest: The authors declare that they have no conflicts of interest to report the present study.
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