Arbuscular Mycorrhizal Fungi and Tolerance of Drought Stress in Plants

Abstract

Drought stress has strong inhibition in plant growth and crop production. Arbuscular mycorrhizal fungi (AMF) can colonize the roots of 80% of land’s plants to establish arbuscular mycorrhizal symbiosis. A relative short-term soil drought did not appear to discourage root AMF colonization, whereas a long-term soil drought intensity considerably decreased root colonization and hyphal growth in the soil. Such change in mycorrhizal development still strongly stimulated the improvement of plant growth and increased plant survival under drought stress. AMF had shown to enhance drought tolerance in various plants. Firstly, mycorrhizal plants could adapt the drought stress in morphology, especially leaf epicuticular wax and root morphology. And mycorrhizal plants possessed direct pathway of water uptake by extraradical hyphae. In addition, AMF enhanced drought tolerance of the host plant through physiological mechanisms in nutrient uptake and biochemical mechanisms regarding hormones, osmotic adjustment, and antioxidant systems. AMF also released glomalin into soil, defined as glomalin-related soil protein, to improve soil structure, thereby regulating water relations of plant/soil. Molecule mechanisms about expression of relevant stressed genes were clarified a bit more detail. Future perspectives in this field are provided.

Full text

25© Springer Nature Singapore Pte Ltd. 2017
Q.-S. Wu (ed.), Arbuscular Mycorrhizas and Stress Tolerance of Plants,
DOI10.1007/978-981-10-4115-0_2
Chapter 2
Arbuscular Mycorrhizal Fungi andTolerance
ofDrought Stress inPlants
Qiang-ShengWu andYing-NingZou
Abstract Drought stress has strong inhibition in plant growth and crop production.
Arbuscular mycorrhizal fungi (AMF) can colonize the roots of 80% of land’s plants
to establish arbuscular mycorrhizal symbiosis. A relative short-term soil drought did
not appear to discourage root AMF colonization, whereas a long-term soil drought
intensity considerably decreased root colonization and hyphal growth in the soil.
Such change in mycorrhizal development still strongly stimulated the improvement
of plant growth and increased plant survival under drought stress. AMF had shown
to enhance drought tolerance in various plants. Firstly, mycorrhizal plants could
adapt the drought stress in morphology, especially leaf epicuticular wax and root
morphology. And mycorrhizal plants possessed direct pathway of water uptake by
extraradical hyphae. In addition, AMF enhanced drought tolerance of the host plant
through physiological mechanisms in nutrient uptake and biochemical mechanisms
regarding hormones, osmotic adjustment, and antioxidant systems. AMF also
released glomalin into soil, dened as glomalin-related soil protein, to improve soil
structure, thereby regulating water relations of plant/soil. Molecule mechanisms
about expression of relevant stressed genes were claried a bit more detail. Future
perspectives in this eld are provided.
Keywords Extraradical hyphae • Mycorrhizas • Mycorrhizal colonization • Water
stress • Water uptake
Q.-S. Wu (*)
College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
Institute of Root Biology, Yangtze University, Jingzhou, Hubei 434025, China
Department of Chemistry, Faculty of Science, University of Hradec Kralove,
Hradec Kralove 50003, Czech Republic
e-mail: wuqiangsh@163.com
Y.-N. Zou
College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
Institute of Root Biology, Yangtze University, Jingzhou, Hubei 434025, China
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2.1 Introduction
Drought stress is considered as one of the most serious abiotic stresses that limits
plant growth and reduces crop production in numerous regions worldwide. It is
estimated that near one-third of soils are subjected to drought stress, thus, for sup-
porting normal plant development (Calvo-Polanco etal. 2016). Many factors includ-
ing a lack of rainfall capacity, irregular rainfall distribution, drought intensity and
duration, and progression rate of stress are response for water scarcity (Kolenc etal.
2016). Drought stress often causes lower soil water potential, inducing cell dehydra-
tion, ultimately resulting in inhibiting cell expansion and division, leaf size, stem
elongation, root proliferation, disturbed stomatal oscillations, plant water, nutrient
uptake, and water use efciency (Kaushai and Wani 2016). Certainly, plants also
develop sophisticated and complex mechanisms in morphological, physiological,
and biochemical characteristics, dividing into escape, avoiding, and drought toler-
ance, to cope with drought stress (Khoyerdi etal. 2016).
Arbuscular mycorrhizal fungi, belonging to phylum Glomeromycota, are soil
inhabitants, where AMF can colonize the roots of 80% of land’s plants. Mycorrhizal
characteristics are dened as the mutual benets: AMF provide the host plant with
essential nutrients (especially P) and water, and photosynthates are transported into
endosymbiotic AMF for its development. As stated by Requena etal. (2007), com-
patible roots are colonized by the hyphae, produced by soil propagules of AMF,
asexual spores, or mycorrhizal roots. In general, mycorrhizal hyphae colonize roots
by means of an appressorium and then penetrate into the root cortex, nally forming
distinct morphological structures: intercellular and intracellular hyphae, coils, and
arbuscules (Fig.2.1). Moreover, extraradical mycorrhizal of colonized roots will
further explore the soil in mineral nutrients and even also colonize the roots of other
neighbor plants, establishing common mycorrhizal network (CMN).
The AM symbiosis has shown many benecial roles in plant growth, nutrition
absorption, root architecture, owering, and stress tolerance (Pozo et al. 2015).
Studies indicated that AM symbiosis is able to enhance drought tolerance of plants
(Augé 2001; Augé and Moore 2005), but the exact mechanisms are not fully known.
This work was begun rstly by Sar etal. (1971), who found that AMs reduced the
resistance to water uptake by soybean, possibly attributable to changes in root resis-
tance. Sar’s works initiated the research between AM fungi and water relations of
plants. In the next 40 years, new perspectives are achieved recently in terms of
advances in molecular, biochemical, and physiological techniques.
The objectives of this chapter are to highlight the effects of drought stress on
mycorrhizal development and to discuss these possible mechanisms regarding
AMF-induced drought tolerance enhancement in plants.
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2.2 Effects ofDrought Stress onMycorrhizal Development
Drought stress strongly affects mycorrhizal development in roots and soils. Augé
(2001) proposed, based on >150 literatures, that relative short-term soil drought did
not appear to favor or discourage root AMF colonization and longer-term soil
drought decreased AMF colonization. So it is more common in increased levels of
root AMF colonization in response to soil drought stress than in decreased levels,
which is related to reductions in plant P levels (Finlay etal. 2008).
In fact, spores of AMF live in soils, and soil moisture can affect spore germina-
tion and development. Studies had conrmed that soil water status strongly altered
spore behavior. Spores are surrounded by soils, where soil water availability is one
of the important factors modulating the contact zone between the spore and the soil
(Tommerup 1984). Tiny changes in the matric potential of the soil surrounding a
spore result in either recession of water from smaller spores or movement into larger
spores with consequential changes in the degree of contact between spores and soil
water, and in the conductivity of water in the capillaries at the spore-soil interface.
So spore germination is favored in soil at or above eld capacity but is decreased
with decreasing soil water potentials below eld capacity (Daniels and Trappe
1980). As reported by Grifn (1972), spore germination increased with the time
lapsing before hydration (<1.4 Mpa, soil water potential), then decreased between
−1.4 and −5 Mpa, and stopped between −5 and −10 Mpa. As reviewed by Wu etal.
(2013), drought stress considerably inhibited the root mycorrhizal development in
citrus plants. Root AMF colonization in adult pomelo (Citrus grandis Osbeck cv.
Shatianyou) trees increased from a drying soil to well-watered soil and decreased
with the increase of soil water status, due to low O2 concentration (Xue 2004). As a
result, soil waterlogging generally inhibited mycorrhizal development in roots and
soil (Wu etal. 2013).
Fig. 2.1 Arbuscules in
white clover colonized by
Rhizoglomus intraradices
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Moreover, part of AMF species can quickly adapt to soil drought and thus still
keep relatively higher root AMF colonization, which is benecial for survival and
growth of the host plant (Nasim 2010). For example, three Glomus species, G. mac-
rocarpum, G. clarum, and G. etunicatum, exhibited considerable tolerance to soil
drying (Sylvia and Schenck 1983). If the spores of AMF were treated by storage in
different soil water potentials, Glomus mosseae and G. deserticola under −0.04
Mpa showed better infectivity than G. fasciculatum under −0.8 Mpa, indicating that
surrounding of spores would have strong function on its efciency in root coloniza-
tion (Wu etal. 2013). Douds and Schenck (1991) reported that spore germination of
Gigaspora margarita was independent on soil water content, while germination of
G. intraradices, G. mosseae, and Acaulospora longula was inhibited by matric
potentials between −0.50 and −2.20 Mpa. In a word, soil wetting and drying cycles
are the most factors affecting spore survival and germination and subsequent infec-
tivity of AMF (Giovannetti etal. 2010).
However, other studies also showed an increased AMF colonization on Sorghum
bicolor with drier soils (Sieverding 1981) or no differences of root AMF coloniza-
tion for winter wheat between wet and dry treatments (Allen and Boosalis 1983).
Besides root mycorrhizal colonization, low soil moisture also strongly inhibits soil
extraradical hyphal length (Neumann etal. 2009).
2.3 AM Effects onPlant Growth andTransplanted Survival
UnderDrought Stress
2.3.1 Plant Growth
In general, soil drought stress strongly inhibited plant growth, while AMF inocula-
tion considerably mitigated the negative effects by drought stress in various plants,
including sugarcane, citrus, mung bean, apple, tomato, maize, wheat, wild jujube,
trifoliate orange (Fig.2.2), etc. As reported by He etal. (1999), inoculation with G.
mosseae, G. spp., and G. caledonium showed 1.99, 1.95, and 1.80 times higher
biomass of mung bean than non-AMF treatment under 12% soil water content con-
ditions. Moreover, the AMF-stimulated plant growth enhancement may be more
important in the host plant under drought stress than under well-watered conditions
(Sánchez-Díaz and Honrubia 1994; Zou etal. 2015a). As outlined by Pozo etal.
(2015), stress-induced abscisic acid (ABA) and strigolactones may participate in the
promotion of AM functioning. In addition, other explanations including increase of
P nutrition (Bethlenfalvay etal. 1988; Sweatt and Davies 1984), water uptake by
hyphae (Zou etal. 2015b), and increase of root length (Bryla and Duniway 1997)
should be included.
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2.3.2 Plant Survival at Transplanting
Plant survival at transplanting is an important factor in crop production. Earlier
studies showed that AMF inoculation strongly enhanced plant survival at transplant-
ing under drought stress conditions. In Casuarina equisetifolia seedlings grown in
the condition of greenhouse, plant survival of the seedlings inoculated with Glomus
caledonium Gc90068, G. versiforme Gv9004, and G. caledonium Gc90036
increased by 37%, 23%, and 17%, respectively, compared with non-AMF seedlings
exposed to drought stress without watering for 7 days (Zhang etal. 2010). Wu etal.
(2006) also found 8% higher plant survival in trifoliate orange colonized by F. mos-
seae than non-AMF colonization after water stress and rewatering. Similar results
were reported in Wyoming big sagebrush (Artemisia tridentata Nutt. ssp. wyomin-
gensis Beetle and Young) seedlings grown in the process of −2.5 to −3.8 Mpa soil
environment (Stahl etal. 1998). In a word, the increase of plant survival in trans-
planting by AMF will help to rebuild ecosystems under drought stress.
At weaning and hardening stages of micropagated Syngonium podophyllum
plantlets, inoculation with a mixed AMF inocula relatively increased plant survival
than non-AMF inoculation, while the AMF effect was high in weaning stage than in
Fig. 2.2 Plant growth of trifoliate orange inoculated with Diversispora versiformis (AMF) under
well-watered (WW) and drought stress (DS)
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hardened stage (Gaur and Adholeya 1999). This may be due to a more effective root
architecture for water and nutritional absorption and the developed external hyphae
in the soil (Graham etal. 1982; Berta etal. 1990; Wu etal. 2011b).
2.4 Potential Mechanisms RegardingAMF-Enhanced
Drought Tolerance inPlants
Since Sar etal. (1971) reported AMF effects on water uptake of soybean, investi-
gations of AM symbiosis in plant species under drought stress conditions have
lasted for 45 years, and many mechanisms have been outlined to clarify AMF roles
in drought tolerance in the levels of morphology, physiology, biochemistry, and
molecule.
2.4.1 Morphological Adaptation
Studies showed that AMF colonization can modulate morphological adaptation to
enhance drought tolerance of the host plant. Earlier studies revealed that less epicu-
ticular wax and lower cuticle weight were found in leaves of AM rose plants than
non-AM plants during drought acclimation (Henderson and Davies 1990). The lack
of wax in AM rose during drought acclimation would be ascribed to the tendency to
abscise leaves. Another explanation is an increased ability of AM plants to absorb
water. Morphological studies further showed more starch storage in palisade meso-
phyll in AM rose under low P, while less starch quantity was found in palisade layer,
near vascular bundle in non-AM rose under high P (Augé etal. 1987). Mycorrhizal
plants would recover more quickly from wilting than non-mycorrhizal plants after
drought recovery (Gemma etal. 1997). Even so, AMF inoculation did not consider-
ably affect stomatal density and guard cell size than non-AMF treatment (Henderson
and Davies 1990).
In addition to leaf morphological adaptation, root morphological adaptation is
also a strategy by mycorrhization under drought stress. Recently, Liu etal. (2016)
analyzed the changes in root morphology of trifoliate orange infected with or with-
out F. mosseae. The results showed signicantly higher root total length, projected
area, surface area, average diameter, volume, and number of rst-, second-, and
third-order lateral roots in AMF trifoliate orange seedlings under well-watered and
drought stress conditions, as compared with non-AMF seedlings (Fig.2.3). Such
better root morphological adaptation caused by mycorrhization can provide more
exploration of soil volume to absorb water and nutrients from the soil (Comas etal.
2013), thereby potentially enhancing drought tolerance of the host plant. The AMF-
induced root morphological changes may be due to the regulation of endogenous
polyamine metabolism and phytohormone equilibrium, especially root putrescine
synthetases by activation of arginine decarboxylase and ornithine decarboxylase, as
well as root indole-3-acetic acid (IAA) (Wu etal. 2012; Liu etal. 2016).
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2.4.2 Water Uptake Directly byMycorrhizal Extraradical
Hyphae
Mycorrhizal hyphae have an important function on uptake and transport of water
from the bulk soil to the host plant (Egerton-Warburton etal. 2007). George etal.
(1992) reported that mycorrhizal hyphae had the ability to transport considerable
quantities of phosphate and nitrogen to the plant from soil zones but no evidence for
a signicant direct water transport by AM hyphae to plants. To examine the long-
distance transport of water through mycorrhizal hyphae, Faber etal. (1991) designed
a rhizobox system, consisting of plant + hyphae chamber and hyphae chamber,
which conrmed an active role in water transport by mycorrhizal hyphae.
Subsequently, Ruiz-Lozano and Azcón (1995) designed a simple split-root-hyphae
system chamber to evaluate water uptake by extraradical hyphae. Zou etal. (2015b)
also reported that disruption of mycorrhizal hyphae in a two-chambered rootbox
resulted in a decrease in leaf water potential in trifoliate orange. It is well known
that mycorrhizal hyphae have a diameter of 2–5 μm that penetrates soil pores inac-
cessible to root hairs (Sánchez-Díaz and Honrubia 1994), thereby extending root
contacted zones more access to available water (Khan 2003). Due to the few or no
septa in mycorrhizal hyphae, mycorrhizal hyphae can be used as a highway to trans-
port water from hyphae to plant cells, in company with phosphate (Wu and Zou
2009c). It is estimated that water transport in 10-mm-diameter hyphae would be 5.4
nl/h under a 0.5MPa gradient conditions (Allen 2006).
Drought stress–Funneliformis mosseae Drought stress+Funneliformis mosseae
Fig. 2.3 Root morphology of trifoliate orange inoculated with Funneliformis mosseae under
drought stress
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As proposed by Allen (2007), mycorrhizal hyphae have bidirectional ows. In
addition to water uptake, mycorrhizal hyphae also contributed to water redistribu-
tion with rhizosphere through reverse ow, namely, transfer of water from the root
to AMF (Egerton-Warburton etal. 2007).
2.4.3 Physiological Mechanisms inNutrient Uptake
Earlier studies showed that the increase in water uptake by AM was a consequence
of P increase, an indirect response (Sar etal. 1972). Subsequently, many studies
also conrmed the correlation of drought tolerance with improved nutrition, espe-
cially P (Nelsen and Sar 1982a; Bethlenfalvay etal. 1988; Fitter 1988; Yano-Melo
etal. 1999). For instance, addition of P fertilizer to non-AM control plants essen-
tially eliminated the differences in resistance to water transport (Nelsen and Sar
1982a, b). The increases in transpiration rate and stomatal conduction in AMF-
inoculated sunower plants ascribed to P-mediated improvement (Koide 1993).
Interestingly, mycorrhizal effect responses to N, P, K, Ca, Fe, Mn, and Zn were
higher under drought stress than under well-watered conditions (Wu and Zou
2009b). It seems that mycorrhizal effect on nutrient uptake is more important under
drought stress than under well-watered conditions. The study of Wu etal. (2011a)
reported that though active, functional and total hyphae were decreased by drought
stress in trifoliate orange; these hyphal activities under drought stress still helped
host plants to sustain greater nutritional (especially P) uptake and water transport.
Hence, AMF-enhanced nutrient absorption is an important physiological mecha-
nism in drought tolerance of the host plant caused by mycorrhization.
Other researches considered that AM plants had different sizes than non-AM
plants under drought stress, which did not directly judge the results originated from
nutrient differences. They proposed equal in size between AM and non-AM plants
(Davies etal. 1992). Graham etal. (1987) conrmed no signicant difference in
water relations between AM citrus plants and non-AM plants fertilized with soluble
P.So AMF-induced enhancement of nutrient absorption may be an indirect mecha-
nism in AMF functioning on drought tolerance of plants.
2.4.4 Biochemical Mechanisms RegardingHormones,
Osmotic Adjustment, andAntioxidant Systems
Studies indicated higher Spd and Spm levels in Glomus fasciculatum-infected
Medicago sativa under drought stress than in non-AMF-infected plants. Meanwhile,
Spd level was considerably correlated with proline accumulation (Goicoechea
et al. 1998). AMF inoculation with Gigaspora margarita signicantly decreased
ethylene level and 1-aminocyclopropane-1-carboxylic acid (precursor of ethylene)
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concentration in the root of papaya under drought stress conditions (Cruz et al.
2000). This suggests that AMF would postpone consenescence of the host plants. In
trifoliate orange seedlings, AMF inoculation with F. mosseae signicantly increased
the levels of indole-3-acetic acid (IAA), abscisic acid (ABA), methyl jasmonate
(MeJA), and zeatin riboside (ZR) levels under well-watered conditions and IAA,
ABA, MeJA, ZR, and brassinosteroids (BRs) levels under drought stress conditions,
respectively (Liu etal. 2016). Such changes in phytohormones by AMF would pro-
vide the clue to enhance drought tolerance in the host plant.
In addition to phytohormones, enhancement of osmotic adjustment is considered
to be an important component of drought tolerance in AM plants. Earlier, Augé
etal. (1986) reported that AMF decreased leaf osmotic potential at both the full-
turgor and turgor-loss points, in company with an increase in pressure potential at
full turgor, thereby maintaining greater leaf water status of the host plant. Wu and
his collaborators further analyzed the changes regarding osmolytes under drought
stress (Wu and Xia 2006; Wu et al. 2007). These results revealed that AM citrus
plants under drought stress had higher soluble sugar in leaf, soluble starch and total
nonstructural carbohydrate in leaf and root, glucose in root, sucrose in leaf and root,
and K+ and Ca2+ in leaf and root, as compared with non-AM plants (Wu etal. 2007).
These positive responses of osmolytes to AMF colonization protect and stabilize
macromolecules and structures from damage by greater capacity of osmotic adjust-
ment, contributing to maintaining a water potential gradient and water absorption
from soil into roots, thereby enhancing drought tolerance of plants (Martinez etal.
2004; Zhang etal. 2015).
Proline, a primary osmolyte in the process of osmotic adjustment, induced two
diverse changes by AMF inoculation under drought stress. Higher proline accumu-
lation in Lactuca sativa (Azcón etal. 1996), Macadamia tetraphylla (Yooyongwech
etal. 2013), and Oryza sativa (Ruíz-Sánchez etal. 2011) under drought stress and
Prunes persica (Tuo etal. 2015) under waterlogged stress was found in AMF plants
than non-AMF plants. More proline accumulation in AMF plants would provide
greater capacity of osmotic adjustment to cope with drought stress. However, lower
accumulation of proline in Erythrina variegata (Manoharan etal. 2010), Knautia
arvensis (Doubková etal. 2013), pistachio (Abbaspour etal. 2012), and Poncirus
trifoliata (Zou etal. 2013) was often found in AMF than in non-AMF seedlings
under drought stress. The lower proline level in AMF plants is derived from the
integration of an inhibition of glutamate synthetic pathway of proline but not orni-
thine pathway, with an enhancement of proline degradation (Zou etal. 2013). Such
lower proline in AMF plants also reects the less damage by drought stress, because
of greater water status in AMF plants, thereby providing an avoidance of drought
stress. It concludes that proline changes by mycorrhization would be a response for
tolerance or avoidance of drought (Augé and Moore 2005).
Changes in reactive oxygen species (ROS) and antioxidant-protected systems by
mycorrhization have been reviewed by Wu etal. (2014) in details, as well as in
Chap. 10. AM plants possessed higher antioxidant enzyme activities and nonenzy-
matic antioxidant concentrations, which may serve to protect the organism against
oxidative damage, thereby enhancing drought tolerance (Wu etal. 2006). Here, our
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team reported that AMF inoculation with F. mosseae induced signicantly higher
net H2O2 efuxes in roots, especially in the root meristem zone of trifoliate orange
under drought stress (Zou etal. 2015a). Possibly, mycorrhizal extraradical hyphae
participate in the H2O2 efux, because mycorrhizal hyphae possess functional aqua-
porins, which can transport H2O and H2O2 (Zou etal. 2015a). On the other hand,
AMF colonization signicantly increased net Ca2+ inuxes in root elongation zone
of trifoliate orange under drought stress, which is a downstream component in the
H2O2 signaling pathway. The Ca2+ inuxes were signicantly correlated with root
H2O2 efuxes/concentrations, suggesting that AMF-mediated Ca2+ inuxes can
result in less H2O2 production.
In another work conducted by Huang etal. (2014), AMF colonization resulted in
an enhancement of calmodulin (CaM) levels, which might participate in regulation
of superoxide dismutase (SOD) activity with a CaM-binding protein, as well as
CAT activity. The study of Huang etal. (2014) also showed that leaf Cu/Zn-SOD
and Mn-SOD activity was stimulated in an increased trend by mycorrhization under
drought stress, but not well-watered conditions, suggesting that drought stress pro-
foundly stimulated AM to trigger the overexpression of SOD isozymes, potentially
leading to a low accumulation of ROS in the host plant.
Correlation studies revealed that root colonization and arbuscule, but not entry
point and vesicle, were signicantly correlated with ROS metabolism (Wu and
Zou 2009a).
2.4.5 Improvement ofSoil Structure byAMF-Released
Glomalin-Related Soil Protein
Glomalin, an immunoreactive glycoprotein, is released exclusively by mycorrhizal
hyphae and spores of AMF (Wright etal. 1996). In nature, glomalin is very stable
and high persisted in the soil and also an alkaline-soluble protein, dened as
glomalin- related soil protein (GRSP) by the Bradford assay (Rillig et al. 2001;
Rillig 2004). The study of Augé etal. (2001) revealed that AM soils possessed better
water-stable aggregates, conferring a higher soil moisture. The work conducted by
Wu et al. (2008) further indicated relatively higher distribution of water-stable
aggregates in citrus rhizosphere, which is highly correlated with total glomalin-
related soil protein concentration. As reported by Zou etal. (2014), in total gloma-
lin-related soil protein (T-GRSP) and easily extractable glomalin-related soil protein
(EE-GRSP), only T-GRSP was signicantly negatively correlated with soil and leaf
soil potential, indicating that T-GRSP is more active under drought stress than
EE-GRSP (Zou etal. 2016). GRSP generally coats on fungal hyphae and forms a
hydrophobic layer in the aggregate surface, thereby reducing water loss within soil
aggregates (Nichols 2008). Therefore, mycorrhizal soils possessed well-structured
soils through AMF-released GRSP production, thereby keeping comparatively
higher available water than poorly structured non-mycorrhizal soils under drought
stress (Augé 2001). Moreover, GRSP-induced aggregate stability was more con-
spicuous under drought stress than under salinity stress (Kohler etal. 2009).
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2.4.6 Molecule Mechanisms
Drought stress generally regulated two groups of stressed inducible genes to respond
to the stress. Meanwhile, rst group functions in stress tolerance, including late
embryogenesis abundant (LEA) proteins, osmotin, mRNA-binding proteins, key
enzymes for osmolyte biosynthesis, water and ion channels, ROS-scavenging
enzymes, etc. (Yokota et al. 2006). The second group contains protein factors
involved in the regulation of signal transduction and gene expression that probably
function in stress response: protein kinases, transcription factors, and enzymes in
phospholipid metabolism (Shinozaki and Yamaguchi-Shinozaki 1999). Studies
showed two regulated patterns in AMF-induced stressed genes that responded to
drought stress: downregulation or upregulation. Ruiz-Lozano etal. (2001) rstly
reported downregulated expression in Mn-sods and Fe-sod genes under ample water
conditions and upregulated expression in Mn-sod II gene under drought stress. A
downregulated pattern in plasma membrane aquaporins gene and ∆1-pyrroline- 5-
carboxylate synthetase (p5cs, a key proline synthetase) gene in soybean and lettuce
was found in AM plants under drought stress conditions (Porcel etal. 2004, 2006a).
Another work also revealed that the combination of exogenous ABA and AM sym-
biosis strongly inhibited the expression of plasma membrane intrinsic proteins (PIP)
aquaporin gene as water conservation in the host plant, allowing the host plant to
maintain higher leaf relative water status (Ruiz-Lozano etal. 2009). In Robinia
pseudoacacia seedlings, root expression of RpTIP1;1 was induced by AMF under
well-watered condition but was downregulated by AMF under drought stress condi-
tion (He etal. 2016). This indicates the expression of RpAQP genes in mycorrhizal
plants dependent on soil water condition and plant tissue. Alternatively, reduction of
PIP gene expression could be compensated by changing the abundance or the activ-
ity of other aquaporins. However, the PIP gene expression was increased under salt
stress, suggesting that effect of AM on PIP gene expression depends on the intrinsic
properties of the osmotic stress itself (Ruiz-Lozano and Aroca 2010).
Other studies showed upregulated expression in relevant genes by mycorrhiza-
tion. A gene from G. intraradices encoding a binding protein (GiBiP, a molecular
chaperone) (Porcel etal. 2007) or cloned from an aquaporin (water channel) gene
(Aroca etal. 2007) was upregulated by drought stress in some mycorrhizal plants.
Porcel etal. (2006b) showed the involvement of a group of proteins (G. intraradices
14-3-3 gene) under drought stress by mycorrhization to regulate signaling pathways
and effector proteins. In trifoliate orange, mRNA abundance of four genes involved
in reactive oxygen species homeostasis and oxidative stress battling was higher in
the AM plants when compared with the NAM plants (Fan and Liu 2011).
Liu etal. (2007) used a 16,000-feature oligonucleotide array to explore transcrip-
tional changes triggered in Medicago truncatula by Gigaspora gigantea and G.
intraradices. In roots, Gigaspora gigantea upregulated 107 genes and downregu-
lated 50 genes, and 56 genes were induced in the two AMF species. Such changes
in gene expression provide clear clue to screen differential genes and understand
molecule mechanisms.
2 Arbuscular Mycorrhizal Fungi andTolerance ofDrought Stress inPlants
wuqiangsh@163.com

36
2.5 Future Perspectives
Future research in this eld will have to concern the mechanisms as the following:
1. Using the noninvasive micro-test technique (NMT) to monitor dynamic changes
in specic ions/molecules (including K+, Na+, Ca2+, H+, Cl−, Mg2+, H2O2, IAA,
and glucose) noninvasively after AMF inoculation.
2. Detecting ROS accumulation in roots and AM structure to further conrm the
functioning of AM on ROS accumulation, as well as the functioning of ROS on
AM development.
3. Combining of AMF with other plant growth-promoting rhizobacteria can be
used in further works to clarify the synergy effect on drought tolerance of the
host plant.
4. Analyzing the role of GRSP in soil structure and subsequent improving soil/
plant water relations.
5. Utilizing RNA-seq technique to understand changes in metabolic pathways and
to screen differentiated expressed genes in whole genes, which are conrmed by
qRT-PCR for the relative expression.
6. Clarifying the perspectives in the study of aquaporins under drought stress, as
well as other stress conditions in both drought tolerance and AM symbiosis.
Acknowledgments This study was supported by the Plan in Scientic and Technological
Innovation Team of Outstanding Young, Hubei Provincial Department of Education (T201604)
and the National Natural Scientic Foundation of China (31101513).
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