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Arbuscular Mycorrhizal Fungi and Tolerance of Temperature Stress in Plants

April 2017

April 2017

DOI:10.1007/978-981-10-4115-0_8

In book: Arbuscular Mycorrhizas and Stress Tolerance of Plants (pp.163-194)

Authors:

Xiancan Zhu

Anhui Normal University

Fengbin Song

Fulai Liu

University of Copenhagen

Temperature is one of the most important environmental factors that determine the growth and productivity of plants across the globe. Many physiological and biochemical processes and functions are affected by low and high temperature stresses. Arbuscular mycorrhizal (AM) symbiosis has been shown to improve tolerance to temperature stress in plants. This chapter addresses the effect of AM symbiosis on plant growth and biomass production, water relations (water potential, stomatal conductance, and aquaporins), photosynthesis (photosynthetic rate, chlorophyll, and chlorophyll fluorescence), plasma membrane permeability (malondialdehyde and ATPase), reactive oxygen species (ROS) and antioxidants, osmotic adjustment, carbohydrate metabolism, nutrient acquisition, and secondary metabolism under low or high temperature stress. The possible mechanisms of AM symbiosis improving temperature stress tolerance of the host plants via enhancing water and nutrient uptake, improving photosynthetic capacity and efficiency, protecting plant against oxidative damage, and increasing accumulation of osmolytes are discussed. This chapter also provides some future perspectives for better understanding the mechanisms of AM plant tolerance against temperature stress.

Photosynthesis Antioxidants Osmoregulation Nutrient uptake

…

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163© 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_8

Chapter 8

Arbuscular Mycorrhizal Fungi andTolerance

ofTemperature Stress inPlants

XiancanZhu, FengbinSong, andFulaiLiu

Abstract Temperature is one of the most important environmental factors that

determine the growth and productivity of plants across the globe. Many physiologi-

cal and biochemical processes and functions are affected by low and high tempera-

ture stresses. Arbuscular mycorrhizal (AM) symbiosis has been shown to improve

tolerance to temperature stress in plants. This chapter addresses the effect of AM

symbiosis on plant growth and biomass production, water relations (water potential,

stomatal conductance, and aquaporins), photosynthesis (photosynthetic rate, chloro-

phyll, and chlorophyll uorescence), plasma membrane permeability (malondial-

dehyde and ATPase), reactive oxygen species (ROS) and antioxidants, osmotic

adjustment, carbohydrate metabolism, nutrient acquisition, and secondary metabo-

lism under low or high temperature stress. The possible mechanisms of AM symbio-

sis improving temperature stress tolerance of the host plants via enhancing water

and nutrient uptake, improving photosynthetic capacity and efciency, protecting

plant against oxidative damage, and increasing accumulation of osmolytes are dis-

cussed. This chapter also provides some future perspectives for better understand-

ing the mechanisms of AM plant tolerance against temperature stress.

Keywords Mycorrhiza • Plasma membrane permeability • Secondary metabolism

• Temperature

X. Zhu (*) • F. Song

Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences,

Changchun 130102, People’s Republic of China

e-mail: zhuxiancan@neigae.ac.cn

F. Liu

Department of Plant and Environmental Sciences, Faculty of Science,

University of Copenhagen, Taastrup DK-2630, Denmark

164

8.1 Introduction

Plants often encounter a wide range of environmental perturbations including

abiotic and biotic stresses (Kaplan et al. 2004). Temperature is one of the most

important environmental factors that determine the growth and productivity of

plants across the globe (Zhu et al. 2011). In recent years, extreme temperature

events have become more frequent along with global climate change. In Northeast

China, for example, crops often suffer from the damage of low temperature during

early spring, causing signicant losses in grain yield.

Temperature stress includes both low temperature and high temperature events

occurring during the growth season of the crops. In general, low but not freezing

temperatures (i.e., 0–15 °C) is considered as low temperature stress (Theocharis etal.

2012), and the elevation in temperature beyond a threshold level (i.e., 10–15 °C

above ambient) is considered as high temperature stress (Wahid etal. 2007). When

plant is exposed to low or high temperature stress, many physiological and bio-

chemical processes and functions will be disturbed. The injuries include damage of

cell membrane structure and lipid composition, cellular leakage of electrolytes and

amino acids, peroxidation of membrane lipids, a diversion of electron ow to alter-

nate pathways, denaturation and aggregation of proteins, redistribution of intracel-

lular calcium ions, inactivation of enzymes in chloroplast and mitochondria, and

production of toxic compounds and reactive oxygen species (ROS) (Wahid etal.

2007; Ruelland and Zachowski 2010; Matteucci etal. 2011; Theocharis etal. 2012).

To overcome the temperature stress, plants have evolved some adaptive strate-

gies and triggered a cascade of events that cause changes in the expression of a large

number of temperature-induced genes and the production of various protein types,

and induce biochemical and physiological modications (Theocharis etal. 2012;

Janmohammadi etal. 2015; Sharma and Laxmi 2016). The tolerance mechanisms

involved in modication of plant cell membrane, accumulation of cytosolic calcium

ion, acclimation of photosynthesis, activation of ROS scavenger systems, accumu-

lation of compatible solutes such as proline and sugars, and induction of cold-related

gene expression (Wahid et al. 2007; Theocharis et al. 2012). For example, in

Arabidopsis, ICE-DREB1/CBF regulon plays a key role in tolerance to low tem-

perature stress. ICE1 is a MYC-type transcription factor that positively regulates

and activates CBF/DREB1 genes, and CBF/DREB1 induces and regulates COR

genes leading to tolerance to low temperature stress (Chinnusamy et al. 2007;

Thomashow 2010).

It is well accepted that arbuscular mycorrhizal (AM) symbiosis is an effective

strategy to improve tolerance to temperature stress in plants (Duhamel and

Vandenkoornhuyse 2013). AM symbioses are common in nature and have been

demonstrated to be benecial for a sustainable agricultural ecosystem due to their

functions in improving plant growth, enhancing nutrient uptake, increasing soil sta-

bility, and alleviating abiotic and biotic stress (Gianinazzi etal. 2010; Berta etal.

2014; Zhu etal. 2015). AM symbiosis can alter plant physiology to allow it to cope

with stress conditions (Miransari etal. 2008). Thus, in this chapter, the effects of

X. Zhu et al.

165

AM on plants under low and high temperature stress are discussed, and the aim is to

identify the underlying mechanisms contributing to plant tolerance to temperature

stress.

8.2 Effect ofTemperature Stress onAMFungi

Environmental conditions affect the community and development of AM fungi and

the formation of mycorrhizae (Liu etal. 2004). Using traditional morphological and

molecular methods, numerous studies have investigated the diversity of AM fungi at

varied environmental conditions (Lumini etal. 2011; Camenzind etal. 2014; Botnen

etal. 2015). However, as far as we are aware, little information is available about the

effect of temperature on AM community structure. Heinemeyer et al. (2003)

reported that an increase of temperature by 3 °C above ambient results in no signi-

cant changes in the AM fungal community in a native grassland community.

Gutknecht etal. (2012) quantied the response of soil microbial biomass and com-

munity structure from 2001 to 2006 to simulated global change at the Jasper Ridge

Global Change Experiment. These authors found that AM fungi biomarker biomass

was lower under elevated temperature (by 1 °C) only in 2006, and there was no

signicant difference in another 5 years. In addition, several studies have reported

the effect of seasonal and climate changes including temperature uctuations on

AM fungal community structure (Dumbrell et al. 2011; Torrecillas et al. 2013;

Bainard etal. 2014); however, until now there is no consensus about how AM fungal

community structure and function respond to temperature stress.

Temperature altered mycelium growth, growth pattern, and phenology of intrara-

dical and extraradical colonization of AM fungi (Gavito etal. 2005; Compant etal.

2010). Gavito etal. (2005) suggested that temperature optima for AM fungi devel-

opment were between 18 and 30 °C.But the temperature optima were depending on

the species of AM fungus. Soil warming stimulated external hyphal production and

extraradical hyphal network growth in temperate conditions (Staddon etal. 2004;

Hawkes etal. 2008). Low and high temperatures reduced AM fungal growth, inhib-

ited extraradical hyphal network structure formation and AM fungal activity,

although AM fungi response to temperature stress exist difference. Liu etal. (2004)

reported that sporulation of Glomus intraradices was reduced at 15 °C, while spore

metabolic activity was not reduced until an even lower temperature (10 °C) was

reached. Schenck etal. (1975) found the germination of spores of Glomus coral-

loidea and Glomus heterogama were reduced above 34 °C.

Root colonization was also changed by low and high temperatures. Some

researchers have reported that AM colonization of crop plants was strongly reduced

at 15 °C compared with ambient temperature, and almost completely inhibited at 10

or 5 °C (Zhang etal. 1995; Liu etal. 2004; Zhu et al. 2010a). In contrast, some

scientists found that AM colonization was unaffected by low temperature (Hayman

1974; Karasawa etal. 2012). At high temperature conditions, AM colonization was

also affected. Haugen and Smith (1992) showed that colonization of cashew

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

166

(Anacardium occidentale) roots by Glomus intraradices was reduced at 38 °C

compared to 22 °C; whereas Martin and Stutz (2004) reported that colonization of

pepper (Capsicum annuum) roots by Glomus AZ112 was increased at 32.1–38 °C

compared to 20.7–25.4 °C. Zhu etal. (2011) found that there was no signicant

change in colonization of maize (Zea mays) roots by Glomus etunicatum at 35 and

40 °C.The discrepancy of the results could be due to different AM fungi and plant

materials as well as experimental conditions among the different studies.

8.3 AM andTolerance ofTemperature Stress inPlants

In the past three decades, several studies have investigated the effect of AM fungi on

plant growth and physiology under low and high temperature stresses. Table8.1

lists the published works of AM effect on the host plants exposed to low and high

temperature stresses from 1976. Below, the AM plants’ response to temperature

stress and possible role of AM in tolerance of temperature stress are discussed.

8.3.1 Plant Growth andBiomass

Under low or high temperature stress, plant morphological features were affected

and plant growth and biomass production could be inhibited. AM symbiosis has

been shown to increase the tness of the host plants via enhancing its growth and

biomass production. It has been reported that AM plants grown better than non-AM

plants under low or high temperature stress, which partly attributed to the enhanced

photosynthesis and nutrient uptake, especially for P nutrition. Several researches

have reported that shoot and root dry weights of AM plants were higher than the

non-AM plants at low or high temperature conditions (Haugen and Smith 1992;

Martin and Stutz 2004; Zhu etal. 2010b; Abdel Latef and Chaoxing 2011; Liu etal.

2014a). Matsubara etal. (2004) found AM fungi increased leaf and root number,

crown diameter, and leaf area of strawberry (Fragaria ananassa) plants under high

temperature stress. Bunn etal. (2009) observed AM Dichanthelium lanuginosum

plants had higher root length and root diameter compared with the non-AM plants

when exposed to high temperature. Hu etal. (2015) reported increased seed number

and plant biomass of Medicago truncatula plants colonized by Rhizophagus irregu-

laris when ambient night temperature increased by 1.53 °C.

In contrast, several studies have shown that AM symbiosis had no or negative

effect on plant growth and biomass production under low and high temperature

stress. Zhu etal. (2011, 2015) reported AM-inoculated maize had a similar shoot

and root dry weights with the non-AM plants under high and low temperature stress.

Maya and Matsubara (2013) found root and tuber dry weights of AM cyclamen

(Cyclamen persicum) were lower than those of the non-AM plants under high

X. Zhu et al.

167

Table 8.1 AM effects on host plant parameters under temperature stress in reported paper since 1986

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Glomus intraradices Gossypium hirsutum 30 and 36 °C 60 Plant growth; %P, Cu, Zn,

and Mn contents

Positive Smith and Roncadori

(1986)

Gl. ambisporum

Gigaspora margarita

Gl. intraradices Gossypium hirsutum 18 °C 60 Zn and Mn contents Positive Smith and Roncadori

(1986)

Gl. ambisporum Plant growth; %P and Cu

contents

Gl. margarita Gossypium hirsutum 18 °C 60 Plant growth; %P, Cu, Zn,

and Mn contents

No Smith and Roncadori

(1986)

Gl. etunicatum Fraxinus pennsylvanica 12, 16, and 20 °C 30 Leaf area growth rate;

relative leaf area growth rate;

leaf area; plant weight; leaf

weight ratio (16 °C); mean

leaf size

Positive Andersen etal.

(1987)

Stem, leaf, and root weight

ratio; root- shoot ratio; mean

leaf size (12 °C)

Stem weight ratio (20 °C);

root weight ratio (16 °C);

root-shoot ratio (16 °C)

Negative

AMF Hordeum vulgare 12, 16, and 20 °C Shoot mass Positive Volkmar and

Woodbury (1989)

Root mass and length No

Gl. fasciculatum Sorghum bicolor 20 °C 48 Dry weight; root length;

content of P, N, S, K, Ca,

Mg, Mn, Zn, Fe, and Cu

Positive Raju etal. (1990)

Gl. intraradices

Gl. macrocarpum

(continued)

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

168

Table 8.1 (continued)

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. fasciculatum Sorghum bicolor 30 °C 48 Dry weight; root length;

content of P, N, S, K, Ca,

Mg, Mn, Zn, Fe, and Cu

Positive Raju etal. (1990)

Gl. macrocarpum

Gl. intraradices Sorghum bicolor 30 °C 48 Dry weight; root length;

content of P, N, S, K, Ca,

Mg, Mn, Zn, Fe, and Cu

Negative Raju etal. (1990)

Gl. intraradices Vigna radiata 30 and 38 °C 14 and

Plant growth Positive Haugen and Smith

(1992)

Gl. mosseae Zea mays 10 °C 7 Shoot mass; sugars; protein

of Pride 5; starch of Pioneer

3902

Positive Charest etal. (1993)

Chlorophyll concentration;

protein of Pioneer 3902;

starch of Pride 5

Negative

Gl. intraradices Hordeum vulgare 15 and 10 °C 48 Specic P uptake Positive Baon etal. (1994)

P concentration; PUE No

Plant biomass; P content Negative

Gl. mosseae Triticum aestivum

Glenlea

5 °C 7 Chlorophyll content Positive Paradis etal. (1995)

Plant growth; content of total

sugars, reducing sugars, and

proteins

Nonreducing sugar content Negative

Gl. mosseae Triticum aestivum AC

Ron

5 °C 7 Plant growth; content of

chlorophyll, total sugars,

nonreducing sugar, reducing

sugars, and proteins

No Paradis etal. (1995)

X. Zhu et al.

169

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. versiforme Glycine max 15 °C Nodule weight; N

concentration and content;

root weight

Positive Zhang etal. (1995)

Nodule number Negative

Gl. versiforme Glycine max 18.2 °C N concentration and content;

root weight

Positive Zhang etal. (1995)

Nodule number and weight Negative

Gl. versiforme Glycine max 21.6 °C Nodule number and weight;

N content; root weight

Positive Zhang etal. (1995)

N concentration Negative

Gl. intraradices Phaseolus vulgaris 4 °C 6 Leaf water potential Positive EI-Tohamy etal.

(1999)

Electrolyte leakage No

Gl. margarita Asparagus ofcinalis 15 and 30 °C 28 Plant height; number of

shoots and crowns; dry

weight; P concentration

Positive Matsubara etal.

(2000)

Gl. intraradices Allium porrum 15 and 0 °C 7 and 14 32P activity (15 °C for 14 d) Positive Wang etal. (2002)

32P activity No

Gl. intraradices Sorghum bicolor 15 and 10 °C 35, 70,

and 105

Root length and fresh

weight; shoot dry weight

No Liu etal. (2004)

Root fresh weight (15 °C for

35 d)

Negative

Gl. intraradices Capsicum annuum 32.1–38 °C 56 Plant growth; root

respiration

Positive Martin and Stutz

(2004)

Leaf P content Negative

Gl. margarita, Gl.

fasciculatum, Gl.

mosseae, Gl.

aggregatum

Fragaria ananassa ~35 °C Number of leaves and roots;

diameter of crown; leaf area;

dry weight

Positive Matsubara etal.

(2004)

P content Negative

(continued)

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

170

Table 8.1 (continued)

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. claroideum Gnaphalium

norvegicum

15 °C 30 Plant growth; N content; Pn;

PNUE;

Positive Ruotsalainen and

Kytöviita (2004)

gemination; SLA No

N concentration Negative

Gl. claroideum Gnaphalium

norvegicum

8 °C 37 Gemination; plant growth; N

content; Pn; PNUE; SLA

No Ruotsalainen and

Kytöviita (2004)

N concentration Negative

Gl. intraradices Phaseolus vulgaris 4 °C 2 Expression of PvPIP1;3;

abundance of PIP protein

Positive Aroca etal. (2007)

RWC; Tr; osmotic root

hydraulic properties;

expression of PvPIP1;1,

PvPIP2;1 and PvPIP1;2;

Gl. claroideum Potentilla crantzii 17 °C 56 PPUE; P concentration Positive Kytöviita and

Ruotsalainen (2007)

Ranunculus acris 49 Pn; plant growth; PPUE; N

concentration; N and P

content

Gl. hoi Plantago lanceolata 7 °C 10 Proportion of respiratory

capacity of roots;

cytochrome c oxidase

activity

No Atkin etal. (2009)

Abundance of cytochrome c

oxidase subunit II and

alternative oxidase

Negative

X. Zhu et al.

171

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

AMF mixture Agrostis scabra, From 30 to 50 °C

at the surface to

base of the pot

70 and

Total biomass; root length

and diameter

No Bunn etal. (2009)

Mimulus guttatus

AMF mixture Dichanthelium From 30 to 50 °C

at the surface to

base of the pot

80 Total biomass; root length

and diameter

Positive Bunn etal. (2009)

lanuginosum

Gl. mosseae Citrus tangerine 15 °C 55 Root length; Ca content Positive Wu and Zou (2010)

Plant growth; Pn, Tr, gs; root

area, diameter, and volume;

content of P, K, Mg, Fe, Cu,

Mn, and Zn

Gl. etunicatum Zea mays 15 and 5 °C 7 Root dry weight; WUE;

chlorophyll content; Fm;

Fv/Fm; Fv/Fo; Pn; Tr; gs

Positive Zhu etal. (2010a)

Shoot dry weight; RWC;

WSD; Fo

Ci Negative

Gl. etunicatum Zea mays 5, 15, 35, and

40 °C

7 Plant growth; root proline

content (5 and 15 °C); root

soluble sugar content;

activity of SOD and CAT

and root POD

Positive Zhu etal. (2010b)

Leaf soluble sugar content;

root proline content (35 and

40 °C); leaf POD activity

Membrane relative

permeability; MDA; leaf

proline content

Negative

(continued)

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

172

Table 8.1 (continued)

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. mosseae Lycopersicon

esculentum

8 °C 7 Plant growth; content of

chlorophyll and soluble

sugar; activity of SOD, POD,

and APX

Positive Abdel Latef and

Chaoxing (2011)

Content of total sugar and

soluble protein; CAT activity

Content of insoluble sugar,

proline, and MDA

Negative

Gl. hoi Plantago lanceolata 12 °C N and 15N content Positive Barrett etal. (2011)

Gl. etunicatum Zea mays 35 and 40 °C 7 Pn; Tr; gs; Fm; Fv/Fm;

Fv/Fo; chlorophyll and

carotenoid contents; RWC;

WUE

Positive Zhu etal. (2011)

Plant growth; Fo;

chlorophyll a/b

Ci Negative

Gl. margarita Poa pratensis Ambient +3 °C Community plant biomass

and P stock

Positive Büscher etal. (2012)

Gl. intraradices Lolium perenne Community N stock No

Medicago lupulina

Lotus corniculatus

Rumex acetosa

Plantago

lanceolata

X. Zhu et al.

173

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. mosseae Plantago lanceolata Ambient +2.7 °C 16 P content Positive Karasawa etal.

(2012)

Plant growth; content of 13C,

N, K, Ca, Mg, and Zn; plant

CO2 uptake

Gl. versiforme Tectona grandis 6, 3, and 0 °C 0.5 Content of chlorophyll,

soluble protein; activity of

SOD and POD

Positive Zhou etal. (2012)

MDA Negative

Funneliformis

mosseae

Cucumis sativus 15 °C 25 Plant growth; content of

phenols, avonoids, lignin,

and phenolic acids; activity

of DPPH, G6PDH, SKDH,

PAL, CAD, PPO, and POD;

expression of PR-1,

CCOMT, G6PDH, CAD,

LPO, PAL, WRKY30,

and C4H

Positive Chen etal. (2013)

H2O2 content Negative

Gl. mosseae Oryza sativa 15 °C 10 Root length; fresh weight; N

and P content; NUE; soluble

sugar content; activity of

NR, GS, SPS, and SS; JA

and NO contents

Positive Liu etal. (2013)

Dry weight No

(continued)

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

174

Table 8.1 (continued)

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. fasciculatum Cyclamen persicum 30 °C 28 Shoot dry weight; activity of

leaf and tuber SOD, APX

and DPPH and root SOD

and DPPH; leaf, root, and

tuber ascorbic acid and

polyphenol contents

Positive Maya and Matsubara

(2013)

Root and tuber dry weight;

activity of root APX

Acaulospora

scrobiculata

Zea mays 15 °C 7 Leaf soluble sugar and

proline content; CAT and

POD activities

Positive Chen etal. (2014)

Gl. tortuosum

Plant growth; MDA content;

SOD activity

Gl. etunicatum Zea mays 15 °C 7 Leaf soluble sugar, proline,

and MDA content; CAT and

POD activities

Positive Chen etal. (2014)

Plant growth; SOD activity No

Gl. intraradices Zea mays 15 °C 7 Leaf soluble sugar, proline,

and MDA content; CAT

activity

Positive Chen etal. (2014)

Plant growth; SOD activity No

POD activity Negative

X. Zhu et al.

175

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Funneliformis

mosseae

Cucumis sativus 15 °C 39 Plant growth; root activity;

ATPase activity and

concentration; plasma

membrane protein content;

expression of proton pump

and calcium-transporting

ATPase-related genes

Positive Liu etal. (2014a)

Water content No

H2O2 content; NADPH

oxidase activity

Negative

Gl. intraradices Oryza sativa 15 °C 7 RWC; root length;

expression of PIP1;1,

PIP1;3, PIP2;1, PIP2;5,

TPS1, TPS2, and TPP1

Positive Liu etal. (2014b)

Expression of PIP1;1 and

PIP2;3

Rhizophagus

irregularis

Medicago truncatula Ambient night

temperature +

1.53 °C

58 Seed number; plant weight;

shoot Zn, root P, Ca, glucose,

and fructose concentration;

expression of MtSucS2

Positive Hu etal. (2015)

Flower number; shoot P and

K, root K and Zn, leaf

sucrose, glucose, and

fructose, and stem sucrose,

glucose and fructose

concentration; expression of

MtSucS3 and MtSucS5

Shoot Ca, and root sucrose

concentration; expression of

MtSucS1 and MtSucS4

Negative

(continued)

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

176

Table 8.1 (continued)

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. tortuosum Zea mays 15 °C 14 Root dry weight; content of

N, leaf soluble sugar and

reducing sugar, root reducing

sugar, sucrose, and fructose;

activity of GS, GOT, GPT,

SPS, and AMS; Pn

Positive Zhu etal. (2015)

Plant height; shoot dry

weight; SS activity

Content of leaf sucrose and

fructose, root soluble sugar

Negative

AMF mixture: R.

irregularis (isolate

Triticum aestivum 35 °C 7 Number of grains;

concentration of Tiller K and

Ca and spike C; spike

biomass

Positive Cabral etal. (2016)

Grain weight; concentration

of Tiller C, N, Mg, B and

Mn, spike N, grain C, P, and

K; tiller biomass; light-use

efciency

BEG140), R. irregularis,

Funneliformis mosseae

(isolate BEG95), F.

geosporum,

Claroideoglomus

claroideum Concentration of Tiller P, K/

Ca, Cu, Zn, and Fe, grain N

Negative

X. Zhu et al.

177

AM fungi Host plants Temperature

Length

of stress Parameters AM effect References

Gl. tortuosum Zea mays 15 °C 14 Concentration of shoot N,

NO3

−-N, NH4+-N, P, K, Cu,

and root N, P, Ca, Zn; NR

activity

Positive Liu etal. 2016

Plant growth; concentration

of shoot Ca, S, Mg, Na, Al,

Fe, Mn, Zn, and root K, S,

Mg, Na, Al, Fe, Mn, Cu

Gl. tortuosum Zea mays 15 °C 14 Concentration of Thr, Gly,

His, Lys, total amino acid,

and leaf Ile, Leu, Phe, Agr,

and root Val

Positive Zhu etal. (2016)

Plant growth; concentration

of Asp, Ser, Glu, Ala, Met,

Tyr, Pro, and leaf Val and

root Ile, Leu, Phe, Arg

AMS amylase, APX ascorbate peroxidase, CAD cinnamyl alcohol dehydrogenase, CAT catalase, Ci intercellular CO2 concentration, Fm maximal uorescence,

Fo primary uorescence, Fv/Fm maximum quantum efciency of photosystem II primary photochemistry, Fv/Fo potential photochemical efciency, G6PDH

glucose-6-phosphate dehydrogenase, Gi Gigaspora, Gl Glomus, GOT glutamate oxaloacetate transaminase, GPT glutamate pyruvate transaminase, gs stomatal

conductance, GS glutamine synthetase, H2O2 hydrogen peroxide, JA jasmonic acid, MDA malondialdehyde, NR nitrate reductase, NUE nitrogen use efciency,

PAL phenylalanine ammonia-lyase, PIP plasma membrane intrinsic protein, Pn net photosynthetic rate, PNUE photosynthetic nitrogen use efciency, POD

peroxidase, PPO polyphenol oxidase, PPUE photosynthetic phosphorus use efciency, RWC relative water content, SKDH shikimate dehydrogenase, SLA

specic leaf area, SOD superoxide dismutase, SPS sucrose phosphate synthase, SS sucrose synthase, Tr transpiration rate, WSD water saturation decit, WUE

water use efciency

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

178

temperature stress. These results could be attributed to the high carbon cost-benet

ratio of AM fungi with the host plants or AM fungi failed to deliver P and other

nutrition to the host plants (Martin and Stutz 2004; Chen etal. 2014).

8.3.2 Water Relations

Water status plays a great role in growth and physiological processes of plants. Plant

water status is an important variable under changing ambient temperatures (Mazorra

etal. 2002). AM and non-AM plants also often display different water status (Augé

2001). Under temperature stress, AM maize plants had higher water conservation,

water holding capacity, and relative water content (Zhu etal. 2010a, 2011; Liu etal.

2014b). EI-Tohamy etal. (1999) reported that AM bean (Phaseolus vulgaris) plants

had higher leaf water potential during chilling stress. These studies suggested that

AM symbiosis could improve plant water status at low or high temperature stress,

although several authors found water content in AM plants was similar to the non-

AM plants under low temperature stress (Aroca etal. 2007; Liu etal. 2014a).

Under low or high temperature stress, the ability of roots to take up water was

reduced. Root water uptake depends on root hydraulic conductivity. AM plants are

found to have better water status which could be due to the enhanced water extrac-

tion by the external hyphae (Faber etal. 1991) and higher activity and hydraulic

conductivity of the roots (Augé and Stodola 1990). Moreover, AM symbiosis was

benecial for stomatal opening in leaves and water ow through the plants to the

evaporating surfaces in the leaves (Nelsen and Sar 1982). Zhu etal. (2010a, 2011)

found that stomatal conductance and transpiration rate of AM maize plants were

higher than the corresponding non-AM plants under low and high temperature

stress, indicating that AM colonization could improve the gas exchange capacity

through maintaining opened stomata, decreased stomatal resistances, and increased

transpiration rates.

Water uptake and hydraulic conductance of roots are governed by aquaporins

(Luu and Maurel 2005). Aquaporins belong to membrane intrinsic protein family

that facilitating the passive water ow through membranes (Kruse et al. 2006).

Plasma membrane intrinsic proteins (PIPs) have been shown to regulate the whole

water transport through plant tissues (Aroca etal. 2007). Liu etal. (2014b) demon-

strated that AM fungi not only transport more water to the host plant by regulating

their own aquaporin activities but also regulate the expression of plant aquaporin

genes to improve water transport of the host. Under low temperature stress,

PvPIP1;3 gene expression and PIP protein abundance were increased in AM plants

(Aroca et al. 2007). Liu et al. (2014b) also found PIP1;1, PIP1;3, PIP2;1, and

PIP2;5 gene expression were upregulated in AM rice (Oryza sativa) plants. All

these improved plant water status facilitated by AM colonization enable plants to

use water more efciently (Evelin etal. 2009; Zhu etal. 2010b, 2011).

X. Zhu et al.

179

8.3.3 Photosynthesis

It is well documented that photosynthesis is one of the most sensitive processes to

temperature stress and can be depressed before other symptoms of the stress are

detected (Berry and Björkman 1980). Any constraint in photosynthesis can limit

plant growth at low or high temperatures (Wahid etal. 2007). AM plants often show

different photosynthetic performances from the non-AM plants (Augé 2001). It has

been reported that AM plants had higher net photosynthetic rate (Pn) than the non-

AM plants under temperature stress (Ruotsalainen and Kytöviita 2004; Zhu etal.

2010a, 2011, 2015). Higher Pn implied greater CO2 assimilation capacity in plants.

Thus, AM colonization usually stimulated plant growth, although AM fungi cost

excess carbon for its own growth. However, Wu and Zou (2010) observed AM inoc-

ulation did not affect Pn of citrus (Citrus tangerine) seedlings under low tempera-

ture stress.

Adverse temperature stress causes a decrease in chlorophyll concentration indi-

cating a suppression of chlorophyll biosynthesis or higher rate of chlorophyll deg-

radation. Several authors reported AM plants had higher chlorophyll concentration

compared with the non-AM plants at suboptimal temperatures (Paradis etal. 1995;

Zhu etal. 2010a, 2011). The results suggest that temperature stress interferes less

with chlorophyll synthesis and light harvesting in AM than in non-AM plants, and

AM symbiosis alleviates the damage of the mesophyll chloroplasts, thereby improv-

ing photosynthetic efciency (Evelin etal. 2009). In contrast, Charest etal. (1993)

found that chlorophyll concentration of AM maize plants was lower than the non-

AM plants. Furthermore, carotenoid acts as accessory light harvesting pigments and

plays an essential role in the photoprotection of photosynthetic apparatus (Young

1991). Zhu etal. (2011) reported AM maize plants had higher carotenoid concentra-

tion than the non-AM plants implying AM colonization stabilizes the lipid phase of

the thylakoid membranes and provide photoprotection to cellular structures and

photosynthetic apparatus (Karim etal. 1999; Wahid etal. 2007).

Photosystems, mainly photosystem II (PSII) with its oxygen-evolving complex

is one of three primary site of injury to the photosynthetic machinery at low and

high temperature stresses (Allakhverdiev etal. 2008). PSII photochemical reactions

in thylakoid lamellae would inevitably be affected by temperature stress. Chlorophyll

uorescence has been used in physiological and ecophysiological studies to probe

and elucidate the changes in the function of PSII and to reect the primary photo-

synthetic processes under abiotic stress (Maxwell and Johnson 2000; Baker 2008;

Hajiboland etal. 2010). The ratio of Fv/Fm (maximum quantum efciency of PSII

primary photochemistry) and of Fv/Fo (potential photochemical efciency of PSII)

is useful relative measurements of the capacity of primary photochemistry of PSII,

which are reliable diagnostic indicators of damage caused by environmental stresses

(Krause and Weis 1991; Maxwell and Johnson 2000). It has been shown that Fv/Fm

and Fv/Fo of AM maize plants was signicantly higher than that of the non-AM

plants under low and high temperature stresses (Zhu et al. 2010a, 2011). This

implies that AM symbiosis mitigates the toxic inuence of temperature stress on the

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

180

PSII reaction center and the structural and functional disruption of photosynthetic

apparatus. An increase in Fv/Fm may be due to the decrease in primary uorescence

(Fo) or increase in maximal uorescence (Fm). Zhu etal. (2010a, 2011) found that

AM maize plants had higher Fm and lower Fo compared with the non-AM plants

when subjected to temperature stress. Temperature stress could destroy the PSII

reaction center, reduce the number of open PSII units, inactive the PSII photochemi-

cal reaction, and disrupt electron transport in photosynthetic apparatus (Camejo

etal. 2005; Baker 2008). This detrimental effect of temperature stress on PSII reac-

tion center could be alleviated by AM symbiosis, consequently improving the PSII

photochemistry efciency and photosynthetic performance of AM plants. However,

a recent study by Cabral etal. (2016) showed that there was no inuence of AM on

the effective quantum yield, electron transfer rate, and non-photochemical quench-

ing in wheat (Triticum aestivum) plants under high temperature stress.

8.3.4 Plasma Membrane Permeability

The plasma membrane is considered to be the primary site of injury when plant

subjected to temperature stress. There are many alterations in the composition,

structure, and function of plasma membrane responding to temperature stress

(Uemura etal. 2006). Such alterations increase the membrane permeability, as evi-

dent from increased loss of electrolytes (Wahid etal. 2007). Studies have shown that

AM plants maintain higher electrolyte concentration than non-AM plants by keep-

ing improved integrity and stability of the membrane (Evelin etal. 2009). EI-Tohamy

etal. (1999) found no signicant effects on electrolyte leakage in AM and non-AM

bean plants under low temperature stress. However, Zhu etal. (2010b) opined that

the membrane relative permeability in the leaves and roots of AM maize plants was

lower than non-AM plants under low and high temperature stresses, which suggests

AM symbiosis can decrease membrane electrolyte permeability and alleviate the

adverse effects of temperature stress on cell membrane.

The plasma membrane lipids seem to be responsible for the fate of plasma mem-

brane at temperature stresses (Uemura etal. 2006). Temperature stress causes the

peroxidation of membrane lipids. The level of malondialdehyde (MDA) reects the

degree of membrane lipid peroxidation (Ali etal. 2005). Several studies have dem-

onstrated that MDA content in AM plants was lower than that in the non-AM plants

(Zhu etal. 2010b; Abdel Latef and Chaoxing 2011; Zhou etal. 2012; Chen etal.

2014), which indicates that AM symbiosis could alleviate the peroxidation of mem-

brane lipids and maintain the uidity of membrane.

Under low temperature stress, AM colonization induced plasma membrane

ATPase activities and ATP accumulation in cucumber (Cucumis sativus) plants (Liu

etal. 2014a). ATPase can regulate intracellular pH and generate an electrochemical

gradient for secondary active transport (Kim etal. 2013). H+-ATPase is active in the

plant membrane around arbuscules in arbuscular mycorrhizae and plays a crucial

role in plant-fungal interactions at the symbiotic interface (Gianinazzi-Pearson

X. Zhu et al.

181

etal. 1995; Liu etal. 2014a). Liu etal. (2014a) also observed that the expression of

proton pump and calcium-transporting ATPase-related genes (CsHA2, CsHA3,

CsHA4, CsHA8, CsHA9, CsHA10, CA1, and CA9) in cucumber roots was signi-

cantly upregulated by AM inoculation under low temperature stress.

8.3.5 ROS andAntioxidants

When plants are exposed to low or high temperature stress, a variety of ROS such

as superoxide anion radical (O2

∙−), hydroxyl radicals (OH∙), and hydrogen peroxide

(H2O2) are induced, causing unbalance between production and detoxication in the

cell or organism (Apel and Hirt 2004; Lenoir et al. 2016). The oxidative stress

caused by ROS is one of the main damaging factors in plants (Wahid etal. 2007).

An excess of ROS can react with DNA, lipids, and proteins, resulting in damage of

cell structure and function, such as DNA/RNA nicking, membrane lipid peroxida-

tion, protein denaturation, and enzyme inhibition (Maya and Matsubara 2013).

A large number of studies have investigated the effect of AM inoculation on ROS in

unstressed and stressed conditions. However, little information is known about the

relation between AM and ROS under temperature stress. Only Chen etal. (2013)

and Liu etal. (2014a) found AM colonization signicantly reduced H2O2 content in

cucumber leaves under low temperature stress. It is assumed that reduction in H2O2

is one of the mechanisms by which AM fungi protect host plants against tempera-

ture stress (Zhang etal. 2013). Low level of H2O2 induced by AM symbiosis may be

acts as a signaling molecule in defense and adaptive responses (Chen etal. 2013).

Moreover, Liu etal. (2014a) reported NADPH oxidase activity in AM cucumber

plants was lower than the non-AM plants. The O2

∙− produced by NADPH oxidase

can be converted to H2O2 by superoxide dismutase (SOD) in the plant apoplast. AM

symbiosis could lessen H2O2 accumulation and enhance temperature tolerance via

suppression of NADPH oxidase activity (Liu etal. 2014a).

To alleviate or prevent temperature stress induced oxidative injury, plant has

evolved a cellular defense mechanism to scavenge these ROS by antioxidant sys-

tems (Zhou etal. 2012). The antioxidant systems involving antioxidative enzymes,

such as SOD, ascorbate peroxidase (APX), peroxidase (POD), catalase (CAT),

dehydroascorbate reductase or glutathione reductase, and low molecular weight

antioxidant, such as ascorbic acid, glutathione, tocopherols, or polyphenols (Evelin

etal. 2009; Zhu etal. 2010b; Maya and Matsubara 2013). For example, SOD will

help detoxify O2

− to H2O2, and the H2O2 produced will be detoxied by CAT, POD,

or APX.The increased glutathione reductase will serve plant to minimize the pro-

duction of O2

− (Evelin et al. 2009). Several studies have demonstrated that AM

fungi could assist host plant to alleviate temperature stress by increasing the activi-

ties of antioxidant enzymes. Zhu etal. (2010b) found that AM maize plants had

higher SOD and CAT activities than the non-AM plants under low and high tem-

perature stresses. Abdel Latef and Chaoxing (2011) reported the activities of SOD,

POD, and APX in AM tomato (Lycopersicon esculentum) plants were higher than

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

182

the non-AM plants under low temperature stress. Zhou etal. (2012) showed that

AM colonization increased SOD and POD activity of teak (Tectona grandis) seed-

lings under low temperature stress. Maya and Matsubara (2013) observed activities

of SOD and APX in leaf and tuber of cyclamen plants which were greater compared

with those of the non-AM plants under high temperature stress. However, zero or

negative effects of AM symbiosis on some enzymatic activities also were observed

under temperature stress (Zhu etal. 2010b; Abdel Latef and Chaoxing 2011; Maya

and Matsubara 2013; Chen etal. 2014). The aforementioned results suggest that

AM plants possess higher antioxidant enzyme activities, but the response of the

individual enzymes varies with respect to the AM fungal and the host plant species

(Evelin etal. 2009). This variation may also be due to some enzymes such as SOD,

CAT, and APX which are metalloenzymes whose activities can be determined by

the availability of the metals they utilize (Evelin etal. 2009).

In addition to these enzymatic systems, AM symbiosis can induce accumulation

of nonenzymatic antioxidant components to scavenge ROS. Chen et al. (2013)

showed that production of phenols and avonoids was enhanced in AM cucumber

plants compared with that in the non-AM plants under low temperature stress. Maya

and Matsubara (2013) also reported AM cyclamen plants had higher ascorbic acid

and polyphenol contents than the non-AM plants under high temperature stress.

8.3.6 Osmotic Adjustment

Osmotic adjustment is considered a key tolerance mechanism in higher plants grown

under low and high temperature stresses. In response to temperature stress, plants

accumulate a variety of certain organic compounds of low molecular solutes, gener-

ally referred to as compatible osmolytes, such as sugars, proline, polyamines, beta-

ines, and acylatedsterols (Wahid etal. 2007; Theocharis etal. 2012). The accumulation

of these solutes could lower the osmotic potential in the cytosol, hereby maintaining

positive turgor pressure of the cells.

Proline is known to accumulate in many plants as a nontoxic and protective

osmolyte to maintain osmotic balance under temperature and osmotic stresses.

Proline also serves as a sink for energy to regulate redox potentials, as a hydroxyl

radical scavenger, as a solute that protects macromolecules against denaturation,

and as a means of reducing acidity in the cell (Kishor etal. 2005; Sharma and Dietz

2006; Theocharis etal. 2012). Proline accumulation has been shown to increase

when plant is colonized by AM fungi. Under low temperature stress, AM maize

plants were found to have higher root proline content than the non-AM plants (Zhu

etal. 2010b). Chen et al. (2014) also reported proline content in the AM maize

leaves was higher compared with that in the non-AM plants at low temperature

condition. However, Zhu et al. (2010b) reported proline content was lower in

the AM maize leaves than that in the non-AM plants under low and high tempera-

ture stresses, and no signicant difference between the AM and the non-AM maize

roots was found under high temperature stress. Abdel Latef and Chaoxing (2011)

X. Zhu et al.

183

also found AM tomato plants accumulated less proline than the non-AM plants

under low temperature stress. Zhu etal. (2010b) suggested that the change of leaf

proline level reects the degree of injury of mycorrhizal plants by the stress, and if

the stress was moderate, there was no need to synthesize more proline for osmotic

adjustment protection.

Soluble sugars have been reported to have multiple roles in temperature toler-

ance and contributed to the preservation of water within plant cells as typical com-

patible osmolytes (Theocharis et al. 2012). It is well documented that plant

accumulates soluble sugars to adjust the osmotic potential during temperature stress

(Evelin etal. 2009). Many studies have reported that plants inoculated with AM

fungi had higher levels of soluble sugars than the non-AM plants under unstressed

and stressed conditions (Paradis et al. 1995; Zhu et al. 2010b, Abdel Latef and

Chaoxing 2011; Liu et al. 2013; Chen et al. 2014). Moreover, increased soluble

protein is also often associated with temperature tolerance. An alternation of protein

content in AM plants under low temperature stress has been observed by Charest

etal. (1993), Abdel Latef and Chaoxing (2011), and Zhou etal. (2012).

8.3.7 Carbohydrate Metabolism

In addition to acting as osmolytes, sugars may have a role as cryoprotectants to

protect plant cell membrane, replacing water molecules in establishing hydrogen

bonds with lipid molecules. They also serve as scavengers of ROS and contribute to

increased membrane stabilization. As signaling molecules, they contribute to the

regulation of growth and development and stress responses in plants associated with

hormone signaling (Uemura etal. 2006; Zeng etal. 2011; Theocharis etal. 2012).

Both AM inoculation and temperature stress could inuence the accumulation of

sugars in plants. Charest etal. (1993) reported that AM symbiosis increased sugar

contents of maize plants under low temperature stress. Zhu etal. (2010b) found the

root soluble sugar content in AM maize plants was higher than that in the non-AM

plants. However, some authors also reported zero or even negative effect of AM

inoculation on sugar accumulation in host plants under temperature stress (Paradis

etal. 1995; Zhu etal. 2010b, 2015). The different alternations of the contents of

reducing sugars, nonreducing sugars, glucose, fructose, and sucrose of plants inocu-

lated with AM fungi under low or high temperature stress were also observed

(Paradis etal. 1995; Hu etal. 2015; Zhu etal. 2015). Depending on the AM fungal

and the host plant species, various forms of sugars are found to be involved in physi-

ological reactions to temperature stress. Koide and Schreiner (1992) stressed that

control over the activity of AM fungi by the host could occur via a regulation of

carbohydrate transfer, one way being by the regulation of arbuscule number. The

changes of carbohydrate contents could refer to carbohydrate sink-source relation-

ship of AM fungi and plants. AM fungi are able to facilitate sugar transport and

metabolism between source and sink organs via an increased exchange of carbohy-

drates and nutrients (Dodd and Perez-Alfocea 2012). Heinemeyer et al. (2006)

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

184

found that AM fungi can consume up to 20% photosynthates of the host plant.

Photosynthates are transported via the phloem to the root and, subsequently, into the

intraradical and extraradical mycelium, as well as in the spores of AM fungi.

Temperature stress may activate and enhance expression of genes encoding

specic enzymes involved in the sink-source transition and sucrose metabolism in

plants, such as sucrose synthase (SS) and sucrose phosphate synthase (SPS)

(Li etal. 2008). Generally, SS plays an important role in sucrose hydrolysis rather

than synthesis in sink tissues (Verma etal. 2011). In AM plants, sucrose is usually

hydrolyzed to monosaccharide by SS or invertase prior to utilizing by AM fungi (Hu

etal. 2015). Liu etal. (2013) reported AM rice plants had higher SS activity than the

non-AM plants under low temperature stress. Hu etal. (2015) also found AM colo-

nization enhanced expression of gene encoding SS, MtSucS2 of M. truncatula

plants grown at night warming condition. However, Zhu etal. (2015) showed that

the SS activity was unaffected by low temperature stress and AM colonization. Hu

etal. (2015) also reported that no or even negative AM effect on four genes encod-

ing SS expression of M. truncatula plants under night warming. Hawkes et al.

(2008) speculated that AM fungi consumed more sucrose and the resulting decrease

in sucrose ultimately led to lower SS and downregulated the expression of gene

encoding SS.Moreover, SPS, a key enzyme for sucrose synthesis, controls the ux

of photosynthetic carbon into sucrose (Verma etal. 2011). Under low temperature

stress, SPS activity was enhanced by AM fungi in rice and maize plants as reported

by Liu etal. (2013) and Zhu etal. (2015), indicating that AM symbiosis enhanced

sucrose metabolism under low temperature stress.

It is worth mentioning that trehalose is the main storage carbohydrate in AM

fungi and plays an important role in stress tolerance by stabilizing dehydrated

enzymes and membranes and protecting biological structures from desiccation

damage (Evelin etal. 2009). In response to temperature stress, fungal cells react by

activating transcriptionally and/or posttranscriptionally the trehalose metabolism

enzymes, which results in trehalose accumulation (Lenoir etal. 2016). Liu et al.

(2014b) reported that rice plants colonized by AM fungi had higher trehalose phos-

phate synthase (TPS) and trehalose phosphate phosphatase (TPP) transcript levels

compared with the non-AM plants under low temperature stress. The increase in the

expression of OsTPS1, OsTPS2, and OsTPP1 could result in an increased trehalose

biosynthesis and higher trehalose concentration in the AM rice plants under low

temperature stress (Liu etal. 2014b). The nding suggests that AM symbiosis could

enhance plant tolerance against temperature stress. Increases in trehalose concentra-

tion may also be involved in starch accumulation (Fernandez etal. 2010).

Starch accumulation is affected by AM symbiosis and temperature stress. Charest

etal. (1993) reported that AM colonization altered starch content in maize plants

under low temperature stress. Zhu etal. (2015) found that the activity of amylase

was higher in AM maize than that in the non-AM plants under low temperature

stress. Amylase is able to catalyze the hydrolysis of starch into sugars. The result

suggests that AM roots require more carbohydrates by AM fungi and/or synthesize

more sugar to cope with low temperature stress via the breakdown of leaf starch.

X. Zhu et al.

185

8.3.8 Nutrient Uptake

Improved nutrient uptake is one of the most important functions in AM symbiosis.

AM symbioses are generally recognized to be involved in bidirectional nutrient

exchange: AM fungi receive organic carbon from the plants, and in return, the hosts

obtain a nutritional benet from AM fungi by taking up P, N, and other macro- and

micronutrients from the soil (Smith and Read 2008). Nutrients are mobilized and

transported to the plants via direct pathway from the rhizosphere by root epidermal

cells and root hairs and AM uptake pathway by the huge intraradical and extraradi-

cal mycorrhizal network (Smith and Smith 2012). It is well documented that the

acquisition of soil nutrients by plant is suppressed by temperature stress, and several

studies have indicated that AM symbiosis could improve nutrient uptake of the host

plant under low and high temperature stresses.

N is one of the major limiting macronutrients for plant growth and development.

It serves as a constituent of many plant cell components and the synthesis of pro-

teins, nucleic acids, coenzymes, and many products and by-products of secondary

metabolism (Evelin etal. 2009). Several studies have demonstrated that AM fungi

can take up and transfer signicant amounts of N (accounting for 20 to 50% of the

total root N) to the host plant (Govindarajulu et al. 2005; Ngwene et al. 2013).

A large body of evidence indicates that AM fungi have a potential to improve plant

N acquisition under low or high temperature stress (Raju etal. 1990; Zhang etal.

1995; Ruotsalainen and Kytöviita 2004; Barrett etal. 2011; Liu etal. 2013, 2016

Zhu etal. 2015). On the contrary, some studies have reported that the N uptake was

not enhanced by AM symbiosis under temperature stress (Raju etal. 1990; Kytöviita

and Ruotsalainen 2007; Büscher etal. 2012; Karasawa etal. 2012). The differential

AM effect on N uptake has been reported to be specic to the combination of geno-

types of AM fungi and host plants, which may explain the different contributions of

the symbiosis (Cabral etal. 2016).

The extraradical mycelium of AM fungi has been shown to take up and assimi-

late organic and inorganic N resources from the soil and to transfer N to the host

plants (Govindarajulu etal. 2005). For both AM fungi and plants, the readily avail-

able inorganic N are NO3

− and NH4+, and NO3

− is the predominant form of N avail-

able in most agricultural soils (He etal. 2003). Under low temperature stress, AM

maize plants had higher NO3

−-N and NH4+-N contents compared with the non-AM

plants (Liu etal. 2016). NO3

− reduction, the most important stage of N assimilation

in plants, is rst catalyzed by nitrate reductase (NR). Low temperature stress acti-

vated NR in wheat leaves via protein dephosphorylation (Yaneva etal. 2002). NR

activity was found to be higher in AM rice and maize plants than in the non-AM

plants under low temperature stress (Liu etal. 2013, 2016), indicating that an spe-

cial capability of AM symbiosis to take up N and to reduce and assimilate NO3

−.

Arginine is synthesized in the extraradical mycelium of AM fungi and is trans-

ported to the intraradical mycelium, where it is broken down to release N for trans-

fer to the host plant (Govindarajulu etal. 2005). In plant, N metabolism involved in

different pathways, such as glutamine synthetase (GS) and glutamate synthase

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

186

cycles (Javaid 2009). Genetic and molecular approaches have demonstrated that GS

plays a key role in N metabolism, which is essential for plant N uptake and use

efciency (Martin etal. 2006). Liu etal. (2013) reported AM rice plants had higher

GS activity compared with the non-AM plants grown at low temperature condition.

Zhu etal. (2015) also found the GS activity in AM maize plants was greater than the

non-AM plants under low temperature stress. Furthermore, Zhu etal. (2015) showed

that AM symbiosis increased glutamate oxaloacetate transaminase and glutamate

pyruvate transaminase activities of maize plants under low temperature stress.

These transaminases are involved in amino acid metabolism and are linked to the

ornithine cycle. Increased amino acid content in maize plants inoculated AM fungus

under low temperature stress was observed by Zhu etal. (2016), which indicates

that the AM fungi facilitated the uptake and synthesis of amino acids.

P is an essential macronutrient for plant growth and crop production: forms an

integral component of the key structure element in nucleic acids, phospholipids,

and enzymes; and is also involved in the metabolism of matter and energy and

signal transduction cascades (Karandashov and Bucher 2005). Plant P uptake,

translocation, and metabolism are inhibited by temperature stress. However, AM

symbiosis is able to sustain plant P acquisition by the hyphal network of AM fun-

gus and the increased surface of plant roots (Karasawa etal. 2012). AM symbiosis

can increase the inorganic P gradient from root to leaves because AM plants

enhance the conversion of P from inorganic to organic forms in the leaves, conse-

quently increasing the P sink and then enhancing P uptake (Javaid 2009). AM

hyphae also can store larger amounts of absorbed P than the roots, facilitating the

continued movement of P into the hyphae. The kinetics of P uptake into hyphae

differ from those of roots because of its higher afnity for P ions or lower threshold

concentration for uptake (Evelin etal. 2009). To date, most of studies have reported

that AM plants had higher P content compared with the non-AM plant under low

or high temperature stress (Smith and Roncadori 1986; Matsubara et al. 2000;

Wang etal. 2002; Büscher etal. 2012; Karasawa etal. 2012; Liu etal. 2013, 2016;

Hu etal. 2015), suggesting that AM symbiosis enhanced the availability and uptake

of P under adverse conditions. However, some studies have demonstrated that the

contribution of AM symbiosis to P uptake maybe small because the P content in

AM plants was lower than the non- AM plants (Baon etal. 1994; Matsubara etal.

2004; Kytöviita and Ruotsalainen 2007).

In addition to N and P, other nutrients also play a key role in plant growth and

development and are involved in all physiological metabolic processes and cellular

functions. Plants show different needs for these nutrients (Hänsch and Mendel

2009). Several studies have reported the effect of AM symbiosis on these nutrients

under low or high temperature stress, though the effect varies among different nutri-

ents. Wu and Zou (2010) found only Ca content in AM citrus plants was higher than

the non-AM plants, whereas no effect of AM on the content of K, Mg, Fe, Cu, Mn,

and Zn was noticed under low temperature stress. Karasawa etal. (2012) reported

contents of K, Ca, Mg, and Zn in AM Plantago lanceolata plants that were similar

with those of the non-AM plants under lowered soil temperature. AM inoculation

increased shoot Zn and root Ca contents, decreased shoot Ca content, and has no

X. Zhu et al.

187

effect on K and root Zn content in M. truncatula plants under increased night tem-

perature (Hu etal. 2015). AM wheat plants had higher tiller K and Ca; lower tiller

Cu, Zn, and Fe concentrations; and similar tiller Mg, B and Mn, and grain K com-

pared with the non-AM plants under high temperature stress (Cabral etal. 2016).

Liu etal. (2016) also observed AM colonization had a positive effect on the concen-

trations of shoot K and Cu and root Ca and Zn, but no effect on the concentrations

of shoot Ca, S, Mg, Na, Al, Fe, Mn and Zn and root K, S, Mg, Na, Al, Fe, Mn, and

Cu of maize plants under low temperature stress. Moreover, the nutrient uptake of

the host plants has been shown to vary with the isolates of AM fungi. Smith and

Roncadori (1986) reported that contents of Cu, Zn, and Mn were not signicantly

changed in cotton plants inoculated with Gigaspora margarita, contents of Zn and

Mn were increased when plants were inoculated with Glomus intraradices and

Glomus ambisporum mixtures under low temperature stress, and the contents of Cu,

Zn, and Mn were both increased when plants were inoculated with these three AM

fungal mixtures under high temperature stress. Raju etal. (1990) also found that

sorghum plants colonized by Glomus intraradices had lower S, K, Ca, Mg, Mn, Zn,

Fe, and Cu contents than the non-AM plants under high temperature stress, but

when sorghum plants were colonized by Glomus fasciculatum and Glomus macro-

carpum mixtures, the contents of S, K, Ca, Mg, Mn, Zn, Fe, and Cu were increased.

The different effects of AM on nutrient uptake in these studies may be due to the

variations of experimental design and biological materials.

8.3.9 Secondary Metabolism

Plant secondary metabolism produces a large number of specialized compounds

that are required for the interaction of plant with its environment, for example, in

defense reactions against herbivores and microbial pathogens as well as in mutual-

istic symbiotic associations, such as with AM (Strack and Fester 2006). There is an

increasing evidence that plant secondary metabolites play an important role in the

development and functional regulation of AM symbiosis, such as avonoids and

strigolactones involved in spore germination and hyphal branching in AM fungi

(Akiyama 2007). AM fungi have also been shown to increase secondary metabolites

contents in the host plants, such as phenolics, triterpenoids, and spermine (Evelin

etal. 2009; Chen etal. 2013). However, the information about AM symbiosis inu-

ence on secondary metabolism under environmental stress is limited. Under low

temperature stress, only Chen etal. (2013) reported that AM inoculation induced

the accumulation of phenolics, avonoids, and lignin in cucumber leaves. They also

observed that activities of glucose-6-phosphate dehydrogenase (G6PDH), shikimate

dehydrogenase, phenylalanine ammonia-lyase (PAL), cinnamyl alcohol dehydroge-

nase (CAD), polyphenol oxidase, guaiacol peroxidase, caffeic acid peroxidase, and

chlorogenic acid peroxidase of AM cucumber plants were greater than the non- AM

plants under low temperature stress. These enzymes are involved in secondary

metabolism and are the key enzymes of the pentose phosphate pathway, the

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

188

phenylpropanoid pathway, and the biosynthesis of secondary metabolites. In addi-

tion, Chen etal. (2013) also reported AM cucumber seedlings had higher expression

levels of WRKY30, PR-1, C4H, CCOMT, CAD, G6PDH, PAL , LPO, and POD

encoding genes compared with the non-AM plants grown in low temperature. These

genes related to the regulation of the phenylpropanoid pathway and plant defense.

The activation of these secondary metabolism genes is important for successful

plant growth under low temperature stress (Chen etal. 2013). Thus, accumulation

of secondary metabolites and activation of secondary metabolism related enzymes

are linked to plant antioxidants system and defence system which inferred that AM

symbiosis enhanced plant tolerance to temperature stress.

8.4 Conclusions andFuture Perspectives

Based on the described above, the possible mechanism of AM symbiosis in improv-

ing plant tolerance to temperature stress includes enhancing water and nutrient

uptake, improving photosynthetic capacity and efciency, protecting plant against

oxidative damage, and increasing accumulation of osmolytes (Fig.8.1). To date,

however, knowledge about AM plants’ response to temperature stress is not suf-

cient. Most of the aforementioned studies have investigated the effect of AM fungi

on plant growth under temperature stress; little attention is paid on the physiologi-

cal, biochemical, and molecular effects. For example, it remains largely unknown

about the effect of AM on plant endogenous hormones and AM plants’ responses to

application of exogenous hormones under temperature stress. Also, the ultrastruc-

tural changes in AM plants under temperature stress have not been addressed by far.

Thus, the underlying physiological mechanisms of AM symbiosis that protect plant

against temperature stress remain yet to be elucidated.

Our knowledge of the molecular mechanisms involved in AM plants’ responses

to temperature stress is very rare. The roles of temperature-tolerant related genes

with respect to AM symbiosis and AM-induced signaling and symbiotic genes by

temperature stress need to be explored. Applications of genomics, transcriptomics,

SOIL

Water

Temperature stress

Temperature tolerance

Nutrient

FUNGI PLANT

Y, gs, RWC, PIPs

Pn, chlorophyll

fluorescence

ROS

Water status

Photosynthesis

Antioxidants

Osmoregulation

Nutrient uptake

Proline, sugars

protein

N, P

Fig. 8.1 Possible mechanisms of AM fungi improving plant tolerance to temperature stress

X. Zhu et al.

189

and proteomics approaches to a better understanding of the molecular basic of AM

plant response to temperature stress and AM plant tolerance against temperature

stress are imperative.

Although AM fungi are widespread in nature and are not specic to its host

plants, the effectiveness of AM symbiosis is different in adverse temperature-

stressed conditions. Thus, it is of great important to screen indigenous and presum-

ably temperature-stressed-tolerant AM fungi isolates for the inoculation of plants

adapted to temperature stress in future research.

Global climate change scenarios reveal temperature will increase and extremes

of temperature will be occurring more frequently, so the chance of crops being

exposed to adverse temperatures will be more likely. AM symbiosis has been shown

to provide a superior road in the adaption of adverse environmental conditions in the

future agriculture. However, numerous challenges of AM application in agriculture

remain to be met, such as large-scale cultivation of AM fungi, and hypercompetition

from other organisms in the complex soil environment.

Acknowledgements We are very grateful for the support by the “One-Three-Five” Strategic

Planning Program of Chinese Academy of Sciences (IGA-135-04), the Science Foundation of

Chinese Academy of Sciences (XDB15030103), and the National Natural Science Foundation of

China (31370144; 41571255).

References

Abdel Latef AA, Chaoxing H (2011) Arbuscular mycorrhizal inuence on growth, photosynthetic

pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low tempera-

ture stress. Acta Physiol Plant 33:1217–1225

Akiyama K (2007) Chemical identication and functional analysis of apocarotenoids involved in

the development of arbuscular mycorrhizal symbiosis. Biosci Biotechnol Biochem

71(6):1405–1414

Ali MB, Hahn E, Paek K (2005) Effects of temperature on oxidative stress defense systems, lipid

peroxidation and lipoxygenase activity in Phalaenopsis. Plant Physiol Biochem 43:213–223

Allakhverdiev SI, Kreslavski VD, Klimov VV etal (2008) Heat stress: an overview of molecular

responses in photosynthesis. Photosynth Res 98:541–550

Andersen CP, Sucoff EI, Dixon RK (1987) The inuence of low soil temperature on the growth of

vesicular-arbuscular mycorrhizal Fraxinus pennsylvanica. Can JFor Res 17:951–956

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduc-

tion. Annu Rev Plant Biol 55:373–399

Aroca R, Porcel R, Ruiz-Lozano JM (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

Atkin OK, Sherlock D, Fitter AH etal (2009) Temperature dependence of respiration in roots colo-

nized by arbuscular mycorrhizal fungi. New Phytol 182:188–199

Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis.

Mycorrhiza 11:3–42

Augé RM, Stodola JW (1990) An apparent increase in symplastic water contributes to greater

turgor in mycorrhizal roots of droughted Rosa plants. New Phytol 115:285–295

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

190

Bainard LD, Bainard JD, Hamel C et al (2014) Spatial and temporal structuring of arbuscular

mycorrhizal communities is differentially inuenced by abiotic factors and host crop in a semi-

arid prairie agroecosysten. FEMS Microbiol Ecol 88:333–344

Baker NR (2008) Chlorophyll uorescence: a probe of photosynthesis invivo. Annu Rev Plant

Biol 59:89–113

Baon JB, Smith SE, Alston AM (1994) Phosphorus uptake and growth of barley as affected by soil

temperature and mycorrhizal infection. JPlant Nutr 17:479–492

Barrett G, Campbell CD, Fitter AH etal (2011) The arbuscular mycorrhizal fungus Glomus hoi can

capture and transfer nitrogen from organic patches to its associated host plant at low tempera-

ture. Appl Soil Ecol 48:102–105

Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in high plants.

Annu Rev Plant Physiol 31:491–543

Berta G, Copetta A, Gamalero E etal (2014) Maize development and grain quality are differen-

tially affected by mycorrhizal fungi and a growth-promoting pseudomonad in the eld.

Mycorrhiza 24:161–170

Botnen S, Kauserud H, Carlsen T etal (2015) Mycorrhizal fungal communities in coastal sand

dunes and heaths investigated by pyrosequencing analyses. Mycorrhiza 25(6):447–456

Bunn R, Lekberg Y, Zabinski C (2009) Arbuscular mycorrhizal fungi ameliorate temperature stress

in thermophilic plants. Ecology 90(5):1378–1388

Büscher M, Zavalloni C, de Boulois HD etal (2012) Effects of arbuscular mycorrhizal fungi on

grassland productivity are altered by future climate and below-ground resource availability.

Environ Exp Bot 81:62–71

Cabral C, Ravnskov S, Tringovska I et al (2016) Arbuscular mycorrhizal fungi modify nutrient

allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil

408(1):385–399

Camejo D, Rodríguez P, Morales MA et al (2005) High temperature effects on photosynthetic

activity of two tomato cultivars with different heat susceptibility. JPlant Physiol 162:281–289

Camenzind T, Hempel S, Homeier Jetal (2014) Nitrogen and phosphorus additions impact arbus-

cular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global

Change Biol 20(12):3646–3659

Charest C, Dalpé Y, Brown A (1993) The effect of vesicular-arbuscular mycorrhizae and chilling

on two hybrids of Zea mays L.Mycorrhiza 4:89–92

Chen S, Jin W, Liu A etal (2013) Arbuscular mycorrhizal fungi (AMF) increase growth and sec-

ondary metabolism in cucumber subjected to low temperature stress. Sci Hortic 160:222–229

Chen XY, Song FB, Liu FL etal (2014) Effect of different arbuscular mycorrhizal fungi on growth

and physiology of maize at ambient and low temperature regimes. Sci World J2014:956141

Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends

Plant Sci 12:444–451

Compant S, van der Heijden MGA, Sessitsch A (2010) Climate change effects on benecial plant-

microorganism interactions. FEMS Microbial Ecol 73:197–214

Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot

63:3415–3428

Duhamel M, Vandenkoornhuyse P (2013) Sustainable agriculture: possible trajectories from mutu-

alistic symbiosis and plant neodomestication. Trends Plant Sci 18:597–600

Dumbrell AJ, Ashton PD, Aziz N etal (2011) Distinct seasonal assemblages of arbuscular mycor-

rhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804

EI-Tohamy W, Schnitzler WH, EI-Behairy U etal (1999) Effect of VA mycorrhiza on improving

drought and chilling tolerance of bean plants (Phaseolus vulgaris). JAppl Bot 73:178–183

Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a

review. Ann Bot 104:1263–1280

Faber BA, Zasoski RJ, Munns DN etal (1991) A method for measuring hyphal nutrient and water

uptake in mycorrhizal plants. Can JBot 69:87–94

Fernandez O, Bethencourt L, Quero A etal (2010) Trehalose and plant stress responses: friend or

foe? Trends Plant Sci 15:409–417

X. Zhu et al.

191

Gavito ME, Olsson PA, Rouhier H etal (2005) Temperature constraints on the growth and func-

tioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytol 168:179–188

Gianinazzi-Pearson V, Gollotte A, Tisserant B etal (1995) Cellular and molecular approaches in

the characterization of symbiotic events in functional arbuscular mycorrhizal associations. Can

JBot 73:526–532

Gianinazzi S, Gollotte A, Binet M etal (2010) Agroecology: the key role of arbuscular mycorrhi-

zas in ecosystem services. Mycorrhiza 20:519–530

Govindarajulu M, Pfeffer PE, Jin HR etal (2005) Nitrogen transfer in the arbuscular mycorrhizal

symbiosis. Nature 435:819–823

Gutknecht JLM, Field CB, Balser TC (2012) Microbial communities and their responses to simu-

lated global change uctuate greatly over multiple years. Global Change Biol 18:2256–2269

Hajiboland R, Aliasgharzadeh N, Laiegh SF etal (2010) Colonization with arbuscular mycorrhizal

fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil

331:313–327

Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe,

Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

Haugen LM, Smith SE (1992) The effect of high temperature and fallow period on infection of

mung bean and cashew roots by the vesicular-arbuscular mycorrhizal fungus Glomus intrara-

dices. Plant Soil 145:71–80

Hawkes CV, Hartley IP, Ineson P et al (2008) Soil temperature affects carbon allocation within

arbuscular mycorrhizal networks and carbon transport from plant to fungus. Global Change

Biol 14:1181–1190

Hayman DS (1974) Plant growth responses to vesicular-arbuscular mycorrhiza. VI.Effect of light

and temperature. New Phytol 73:71–80

He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through com-

mon mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567

Heinemeyer A, Ridgway KP, Edwards EJ etal (2003) Impact of soil warming and shading on colo-

nization and community structure of arbuscular mycorrhizal fungi in roots of a native grassland

community. Global Change Biol 10:52–64

Heinemeyer A, Ineson P, Ostle N etal (2006) Respiration of the external mycelium in the arbuscu-

lar mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation

to temperature. New Phytol 171:159–170

Hu Y, Wu S, Sun Y etal (2015) Arbuscular mycorrhizal symbiosis can mitigate the negative effects

of night warming on physiological traits of Medicago truncatula L. Mycorrhiza

25(2):131–142

Janmohammadi M, Zolla L, Rinalducci S (2015) Low temperature tolerance in plants: changes at

the protein level. Phytochemistry 117:76–89

Javaid A (2009) Arbuscular mycorrhizal mediated nutrition in plant. J Plant Nutr 32:1595–1618

Kaplan F, Kopka J, Haskell DW et al (2004) Exploring the temperature-stress metabolome of

Arabidopsis. Plant Physiol 136:4159–4168

Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas.

Trends Plant Sci 10:22–29

Karasawa T, Hodge A, Fitter AH (2012) Growth, respiration and nutrient acquisition by the arbus-

cular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled

soil. Plant Cell Environ 35:819–828

Karim MA, Fracheboud Y, Stamp P (1999) Photosynthetic activity of developing leaves of Zea

mays is less affected by heat stress than that of developed leaves. Physiol Plant 105:685–693

Kim HS, Oh JM, Luan S etal (2013) Cold stress causes rapid but differential changes in properties

of plasma membrane H+-ATPase of camelina and rapeseed. JPlant Physiol 170:828–837

Kishor PBK, Sangama S, Amrutha RN etal (2005) Regulation of proline biosynthesis degradation,

uptake and transport in higher plants: its implications in plant growth and abiotic stress toler-

ance. Curr Sci 88:424–438

Koide RT, Schreiner RP (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis.

Annu Rev Plant Physiol Plant Mol Biol 43:557–581

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

192

Krause G, Weis E (1991) Chlorophyll uorescence and photosynthesis: the basics. Annu Rev Plant

Physiol Plant Mol Biol 42:313–349

Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7:206

Kytöviita M, Ruotsalainen AL (2007) Mycorrhizal benet in two low arctic herbs increases with

increasing temperature. Am JBot 94(8):1309–1315

Lenoir I, Fontaine J, Sahraoui AL (2016) Arbuscular mycorrhizal fungal responses to abiotic

stresses: a review. Phytochemistry 123:4–15

Li JY, Liu XH, Cai QS etal (2008) Effects of elevated CO2 on growth, carbon assimilation, photo-

synthate accumulation and related enzymes in rice leaves during sink-source transition. JIntegr

Plant Biol 50:723–732

Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at subopti-

mal root zone temperature. Mycorrhiza 14:93–101

Liu ZL, Li YJ, Hou HY etal (2013) Differences in the arbuscular mycorrhizal fungi-improved rice

resistance to low temperature at two N levels: aspects of N and C metabolism on the plant side.

Plant Physiol Biochem 71:87–95

Liu A, Chen S, Chang R etal (2014a) Arbuscular mycorrhizae improve low temperature tolerance

in cucumber via alterations in H2O2 accumulation and ATPase activity. J Plant Res

127:775–785

Liu ZL, Ma LN, He XY et al (2014b) Water strategy of mycorrhizal rice at low temperature

through the regulation of PIP aquaporins with the involvement of trehalose. Appl Soil Ecol

84:185–191

Liu N, Chen X, Song F etal (2016) Effects of arbuscular mycorrhiza on growth and nutrition of

maize plants under low temperature stress. Philipp Agric Sci 99(3):246–252

Lumini E, Vallino M, Alguacil MM etal (2011) Different farming and water regimes in Italian rice

elds affect arbuscular mycorrhizal fungal soil communities. Ecol Appl 21(5):1696–1707

Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting

plant water status. Plant Cell Environ 28:85–96

Martin CA, Stutz JC (2004) Interactive effects of temperature and arbuscular mycorrhizal fungi on

growth, P uptake and root respiration of Capsicum annuum L.Mycorrhiza 14:241–244

Martin A, Lee J, Kichey T etal (2006) Two cytosolic glutamine synthetase isoforms of maize (Zea

mays L.) are specically involved in the control of grain production. Plant Cell 18:3252–3274

Matsubara Y, Kayukawa Y, Fukui H (2000) Temperature-stress tolerance of asparagus seedling

through symbiosis with arbuscular mycorrhizal fungus. JJapan Soc Hort Sci 69(5):570–575

Matsubara Y, Hirano I, Sassa D etal (2004) Alleviation of high temperature stress in strawberry

plants infected with arbuscular mycorrhizal fungi. Environ Control Biol 42(2):105–111

Matteucci M, D’Angeli S, Errico S etal (2011) Cold affects the transcription of fatty acid desatu-

rases and oil quality in the fruit of Olea europaea L, genotypes with different cold hardiness.

JExp Bot 62:3403–3420

Maxwell K, Johnson GN (2000) Chlorophyll uorescence-a practical guide. J Exp Bot

51:659–668

Maya MA, Matsubara Y (2013) Inuence of arbuscular mycorrhiza on the growth and antioxida-

tive activity in cyclamen under heat stress. Mycorrhiza 23:381–390

Mazorra LM, Nunez M, Echerarria E etal (2002) Inuence of brassinosteriods and antioxidant

enzymes activity in tomato under different temperatures. Plant Biol 45:593–596

Miransari M, Bahrami HA, Rejali F etal (2008) Using arbuscular mycorrhiza to alleviate the stress

of soil compaction on wheat (Triticum aestivum L.) growth. Soil Biol Biochem 40:1197–1206

Nelsen CE, Sar GR (1982) The water relations of well-watered, mycorrhizal and non- mycorrhizal

onion plants. JAm Soc Hortic Sci 107:271–274

Ngwene B, Gabriel E, George E (2013) Inuence of different mineral nitrogen sources (NO3

−-N

vs. NH4+-N) on arbuscular mycorrhiza development and N transfer in a Glomus intraradices-

cowpea symbiosis. Mycorrhiza 23:107–117

Paradis R, Dalpé Y, Charest C (1995) The combined effect of arbuscular mycorrhizas and short-

term cold exposure on wheat. New Phytol 129:637–642

X. Zhu et al.

193

Raju PS, Clark RB, Ellis JR etal (1990) Effects of species of VA-mycorrhizal fungi on growth and

mineral uptake of sorghum at different temperatures. Plant Soil 121:165–170

Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232

Ruotsalainen AL, Kytöviita M (2004) Mycorrhiza does not alter low temperature impact on

Gnaphalium norvegicum. Oecologia 140:226–233

Schenck NC, Graham SO, Green NE (1975) Temperature and light effects on contamination and

spore germination of vesicular-arbuscular mycorrhizal fungi. Mycologia 67:1189–1192

Sharma SS, Dietz KJ (2006) The signicance of amino acids and amino-acid derived molecules in

plant responses and adaptation to heavy metal stress. JExp Bot 57:711–726

Sharma M, Laxmi A (2016) Jasmonates: emerging players in controlling temperature stress toler-

ance. Front Plant Sci 6:1129

Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

Smith GS, Roncadori RW (1986) Responses of three vesicular-arbuscular mycorrhizal fungi at

four soil temperatures and their effects on cotton growth. New Phytol 104:89–95

Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in

plant nutrition and growth. Mycologia 104(1):1–13

Staddon PL, Gregersen R, Jakobsen I (2004) The response of two Glomus mycorrhizal fungi and

a ne endophyte to elevated atmospheric CO2, soil warming and drought. Global Change Biol

10:1909–1921

Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycor-

rhizal roots. New Phytol 172:22–34

Theocharis A, Clement C, Barka EA (2012) Physiological and molecular changes in plants grown

at low temperatures. Planta 235:1091–1105

Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying

the CBF cold response pathway. Plant Physiol 154:571–577

Torrecillas E, Torres P, Alguacil MM etal (2013) Inuence of habitat and climate variables on

arbuscular mycorrhizal fungus community distribution, as revealed by a case study of faculta-

tive plant epiphytism under semiarid conditions. Appl Environ Microbiol 79(23):7203–7209

Uemura M, Tominaga Y, Nakagawara C etal (2006) Responses of the plasma membrane to low

temperatures. Physiol Plant 126:81–89

Verma AK, Upadhyay SK, Verma PC et al (2011) Functional analysis of sucrose phosphate syn-

thase (SPS) and sucrose synthase (SS) in sugarcane (Saccharum) cultivars. Plant Biol

13:325–332

Volkmar KM, Woodbury W (1989) Effects of soil temperature and depth on colonization and root

and shoot growth of barley inoculated with vesicular-arbuscular mycorrhizae indigenous to

Canadian prairie soil. Can JBot 67:1702–1707

Wahid A, Gelani S, Ashraf M etal (2007) Heat tolerance in plants: an overview. Environ Exp Bot

61:199–223

Wang B, Funakoshi DM, Dalpé Y etal (2002) Phosphorus-32 absorption and translocation to host

plants by arbuscular mycorrhizal fungi at low root-zone temperature. Mycorrhiza 12:93–96

Wu QS, Zou YN (2010) Benecial roles of arbuscular mycorrhizas in citrus seedlings at tempera-

ture stress. Sci Hortic 125:289–293

Yaneva IA, Hoffmann GW, Tischner R (2002) Nitrate reductase from winter wheat leaves is

activated at low temperature via protein dephosphorylation. Physiol Plant 114:65–72

Young A (1991) The photoprotective role of carotenoids in higher plants. Physiol Plant

83:702–708

Zeng Y, Yu J, Cang Jetal (2011) Detection of sugar accumulation and expression levels of correla-

tive key enzymes in winter wheat (Triticum aestivum) at low temperatures. Biosci Biotechnol

Biochem 75:681–687

Zhang F, Hamel C, Kianmehr H etal (1995) Root-zone temperature and soybean [Glycine max.

(L.) Merr.] vesicular-arbuscular mycorrhizae: development and interactions with the nitrogen

xing symbiosis. Environ Exp Bot 35:287–298

8 Arbuscular Mycorrhizal Fungi andTolerance ofTemperature Stress inPlants

194

Zhang RQ, Zhu HH, Zhao HQ etal (2013) Arbuscular mycorrhizal fungal inoculation increases

phenolic synthesis in clover roots via hydrogen peroxide, salicylic acid and nitric oxide signal-

ing pathways. JPlant Physiol 170:74–79

Zhou Z, Ma H, Liang K etal (2012) Improved tolerance of teak (Tectona grandis L.f.) seedlings to

low-temperature stress by the combined effect of arbuscular mycorrhiza and paclobutrazol.

JPlant Growth Regul 31:427–435

Zhu XC, Song FB, Xu HW (2010a) Arbuscular mycorrhizae improves low temperature stress in

maize via alterations in host water status and photosynthesis. Plant Soil 331:129–137

Zhu XC, Song FB, Xu HW (2010b) Inuence of arbuscular mycorrhizae on lipid peroxidation and

antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza

20:325–332

Zhu XC, Song FB, Liu SQ etal (2011) Effects of arbuscular mycorrhizal fungus on photosynthesis

and water status of maize under high temperature stress. Plant Soil 346:189–199

Zhu XC, Song FB, Liu FL etal (2015) Carbon and nitrogen metabolism in arbuscular mycorrhizal

maize plants under low-temperature stress. Crop Pasture Sci 66(1):62–70

Zhu XC, Song FB, Liu FL (2016) Altered amino acid prole of arbuscular mycorrhizal maize

plants under low temperature stress. JPlant Nutr Soil Sci 179:186–189

X. Zhu et al.

Nano-Biofortified Crop Plants with Zinc for Human Health

Chapter

Aug 2023

Rapidly growing human populations and constantly deteriorating human health due largely to malnutrition is a major global concern. Attempt is therefore made by scientists working in different disciplines like agriculture, food, medical, and other related industries to improve the human health across the globe. The improvement in human health may be achieved by providing nutrient-rich and contaminant-free foods to circumvent many diseases arising due to malnutrition or supply of poor-quality foods to people at global scale. In this context, a recent concept “biofortification” a process which is used to supplement some vital nutrients to many food crops in order to enhance human health via food chain is promoted. The conventional/traditional “biofortification” even though has shown significant success, yet the global scientists working in this area suggest that this process of enriching food crops with essential nutrients can further be improved by adopting/employing biotechnological tool, nanotechnology. Using this technology, edible crops are enriched with indispensable micronutrients in the form of nanoparticles to enhance the quality of human dietary systems with balanced diet via “nano-biofortification.” Among micronutrients, zinc has been recognized as one of the greatest elemental deficiencies that severely destruct growth, production, and nutritional quality of many edible crops. Due to this and many other reasons, like poor consumption, low bioavailability, and several human health problems linked with zinc deficiency, researchers are working to find an economical and sustainable solution to preclude this problem. In this direction, many fortification strategies including nano-biofortification have been found useful in alleviating the zinc deficiency in plants. Broadly, nano-biofortification provides a platform for the utilization of an efficient micronutrient delivery system which is safe, quick, target specific, and sustainable. Realizing the importance of nano-biofortification and impact of zinc deficiency on human health, an attempt is made herein to better understand this process and how this process could alleviate malnutrition in order to enhance human health while supplying zinc using nanoparticles.KeywordsNano-biofortificationCrop nutritionZincNanoparticlesCerealsVegetables

Promising Role of Fungal Symbiosis for Eco-friendly Green Technology for Environmental Health

Chapter

Aug 2023

Fungi are organisms that resemble plants but lack chlorophyll. They are also recognized for their mutualistic relationships with plants. Due to their mutualistic nature and technological advancement, fungi have recently gained substantial interest around the world. Green technologies are those that are both affordable and non-detrimental to the natural world, as well as readily available in the communities in which they are implemented and generally well received by society. By combining fungal symbiosis with environmentally friendly technology, we hope to lessen the harmful effects of human activities, synthetic processes, and the chemicals and byproducts they produce. Soil and plant quality are both diminished by the widespread use of synthetic pesticides and fertilizers. A beneficial strategy in green technology is the use of biological resources including fungi, bacteria, plants, and composting fertilizer to create low-cost, energy-efficient, nontoxic plant products. By aiding in salinity, drought, nutrient water uptake, and heavy metal contamination, fungal symbiosis paves the way for a cleaner environment, which can be useful for agricultural progress. Our natural environment is being destroyed at an alarming rate as the world continues its developmental phase. This review summarizes the current state of knowledge regarding the relationship between fungal symbiosis and environmentally friendly technology.KeywordsFungusSymbiosisGreen technologyHeavy metalEnvironmentally friendly

Arbuscular Mycorrhizal Fungi (AMF) and Climate‐Smart Agriculture: Prospects and Challenges

Chapter

Jul 2023

Climate-smart agriculture (CSA) integrates the connected challenges of food security and climate change. CSA differs by integrating climate change mitigation and adaptation in planning and development of sustainable agricultural systems. The three major objectives of CSA are sustainable increase in agricultural productivity and farmer incomes, adaptation and building resilience to climate change; and reducing agricultural greenhouse gas emissions. Microbial biofertilizers are an integral component of CSA. The need to increase sustainable food production shifts focus to the role of soil biodiversity in general and arbuscular mycorrhizal fungi (AMF) in particular. AMF are most abundant symbionts in both natural and agricultural landscapes and contribute immensely to sustainable agriculture. However, conventional agriculture practices such as, low crop diversity (monocropping), intensive tillage, and extensive use of agrochemicals compromise the benefits of AMF inoculation due to their negative effects on diversity of AMF in agricultural soils.

The Co-Inoculation Effect of Mycorrhizae Fungi and PGPR for Stress Tolerance

Chapter

Dec 2023

Synergistic Influence of Arbuscular mycorrhizal Fungi Inoculation with Nanoparticle Foliar Application Enhances Chili (Capsicum annuum L.) Antioxidant Enzymes, Anatomical Characteristics, and Productivity under Cold-Stress Conditions

Article

Full-text available

Feb 2024

In this study, we aimed to evaluate the effects of Arbuscular mycorrhiza fungus (AMF) inoculation, foliar application of zinc oxide and selenium nanoparticles (ZnO-NPs and Se-NPs), and their combined interactions on the growth and productivity of chili pepper under cold-stress conditions. Two field experiments were successfully conducted during the winter seasons of 2021 and 2022 in an experimental field at the Faculty of Agriculture, Cairo University, Giza, Egypt. The results showed that, under cold stress, the combination of AMF inoculation and ZnO-NPs + Se-NPs as a foliar spray increased the average fruit weight by 92.4% and 98.7%, and the number of fruits by 34.6% and 54.8 compared to control treatment in the 2021 and 2022 seasons, respectively. Additionally, the combination of AMF and a mixture of nanoparticles (ZnO-NPs + Se-NPs) significantly increased the total marketable yield by 95.8% and 94.7% compared to the control, which recorded values of 2.4 and 1.9 kg m −2 in the 2021 and 2022 seasons, respectively. Furthermore, the combination of AMF and a mixture of nanoparticles (ZnO-NPs + Se-NPs) showed the highest total content of ascorbic acid and capsaicin in chili fruits compared to the other treatments. The combination of AMF and a mixture of nanoparticles (ZnO-NPs + Se-NPs) stimulated the accumulation of peroxidase (POD) and nitrogen glutamate dehydrogenase (GDH) while decreasing hydrogen peroxide (H 2 O 2) and lipid peroxidation (MDA) contents. SDS analysis revealed that the application of ZnO-NPs, Se-NPs, AMF + ZnO-NPs, and AMF + ZnO-NPs + Se-NPs induced the emergence of new protein bands and reconstitution of those damaged by cold stress. Regarding histological structure, the combination of AMF inoculation and ZnO-NPs + Se-NPs as a foliar spray showed an enhancement in the thickness of grana thylakoids and increased the number of chloroplasts. Intriguingly, the findings showed that AMF and a mixture of nanoparticles (ZnO-NPs + Se-NPs) could offer guidance for increasing plant development and productivity under cold-stress conditions.

Effects of Cold Stress on the Hemolymph of the Pacific White Shrimp Penaeus vannamei

Article

Full-text available

Jan 2024

Temperature is an important factor in the physiological processes of aquatic organisms and can seriously affect several chemical and biological processes in their bodies, including respiratory metabolism, antioxidant capacity, immune capacity, and signal transduction. In this study, physiological, transcriptomic, and metabolomic analyses were used to investigate the response of Penaeus vannamei to cold stress. The results indicated that cold stress disrupted nucleotide metabolism and inhibited gluconeogenesis. However, shrimp exhibited response mechanisms in order to enhance cold tolerance, regulating changes in key genes and metabolites in amino acid and lipid metabolism to increase energy supply and protect cell membrane stability. In addition, the response included regulating Ca2+ pumps and ion channels to maintain intracellular ion homeostasis and osmotic balance. When the temperature dropped further, oxidative damage occurred due to overwhelming of the antioxidant defense system, and immune function was inhibited. This research provides some references regarding the molecular mechanisms involved in responding to cold stress and potential strategies to improve cold tolerance in P. vannamei; these are important references for studying the cold stress response of shrimp.

Arbuscular Mycorrhizal Fungi in Plant Tolerance to Organic Pollutants and Associated Food Safety

Chapter

Full-text available

Jan 2024

Industrialization and the modern world have led to environmental contamination by organic pollutants, many of which are persistent and could engender hazardous disorders in ecosystems and living organisms including humans. Organic pollutants are phytotoxic compounds and affect the plant biochemical and physiological processes. However, plants can uptake these compounds leading to inclusion of pollutants into food chains. Nowadays, several studies have been carried out to explore and develop novel strategies that could lessen or eradicate pollution while posing no deleterious effects on the environment. Bioremediation (including phytoremediation) is green technology for the remediation of contaminated soils and water. The majority of plant species form symbiosis with mycorrhizal fungi which usually leads to improved plant resistance to organic contaminations. Therefore, plant root inoculation with mycorrhizal fungi could be a biological solution for the problem of organic pollutants.

Maize and Wheat Responses to the Legacies of Different Cover Crops under Warm Conditions

Article

Full-text available

Jun 2023

: Cover crops (CC) have great potential to enhance the sustainability of agroecosystems. However, the wide range of possible rotations of CC and cash crops (CaC) means that important knowledge gaps persist on how CC affects CaC. We investigated the legacy effects of five common CC (three monocultures: vetch, melilotus, and barley, and two mixtures: barley-vetch and barley-melilotus) on two of the most important CaC, maize and wheat. A microcosm, semi-controlled experiment was established simulating warm, low-income Mediterranean conditions. After two cycles, soil physicochemical and microbial properties, as well as plant growth and nutrition variables, were measured at the CC early growth CaC stage. In maize, barley CC had the best soil microbial and nutritional legacy effects, which resulted in the highest biomass and nutrient status. In contrast, barley produced the worst results on wheat, showing the disadvantages of growing two crops from the same tribe consecutively. CC mixtures also did not offer a productive advantage over pure CC. Additionally, our findings suggest that archaea seem to play a role in increasing N and Zn content in maize shoots. Furthermore, shoot B contents showed highly significant regressions with the CaC biomass. These results can help select the appropriate CC in each case.

Role of Arbuscular Mycorrhizal (AM) fungi in crop plants – A review

Article

Dec 2023

Wendy Francisca Xavier Martins

Aquaporin LjNIP1;5 positively modulates drought tolerance by promoting arbuscular mycorrhizal symbiosis in Lotus japonicus

Article

Feb 2024
PLANT SCI

Effects of arbuscular mycorrhiza on growth and nutrition of maize plants under low temperature stress

Article

Full-text available

Sep 2016
PHILIPP AGRIC SCI

Low temperature is one of the major environmental factors influencing crop growth. The effect of arbuscular mycorrhizal (AM) fungus on the growth and nutrient concentration of maize (Zea mays L.) plants in pot culture under low temperature stress was investigated. Low temperature resulted in a decrease in the root colonization of AM, plant height and biomass. N, P, K, Ca, Mg, Zn, NO3⁻-N and NH4⁺-N concentration in the shoot, and N, P, K, Ca, Al, Zn and Cu concentration in the root were all lowered by low temperature stress. Under low temperature, however, mycorrhizal plants had higher concentrations of N, P, K and Cu in the shoot, and of N, P, Ca, Zn in the root compared with the non-mycorrhizal plants. Moreover, low temperature increased the nitrate reductase (NR) activity, and mycorrhizal plants had higher NR activity than non-mycorrhizal plants. In conclusion, the results suggest that AM inoculation improves the nutritional status of maize plants and enhances their performance under low temperature condition.

Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress

Article

Full-text available

Nov 2016
PLANT SOIL

Aims To evaluate the role of the AM symbiosis on nutrient allocation in Triticum aestivum L. cv. 1110 at different growth stages before and after heat-stress at anthesis. Methods Measurements of plant biomass and grain yield at anthesis, grain-filling and maturity; determination of macro- and micronutrient concentrations in aboveground biomass; evaluation of AM fungal structures in roots and assessment of light-use efficiency of plants. Results AM increased grain number in wheat under heat-stress, and altered nutrient allocation and tiller nutrient composition. Heat increased number of arbuscules in wheat root, whereas number of vesicles and total colonization were unaffected. Heat increased photosystem II yield and the electron transfer rate, whereas non-photochemical quenching decreased during the first 2 days of heat-stress. Conclusions Nutrient allocation and –composition in wheat grown under heat-stress were altered by AM symbiosis, which lowered the K/Ca ratio, whereas it was increased by heat-stress. The increased carbon availability in spikes at this developmental stage, related to the C sink strength of the AM symbiosis and its influence on source-sink relationships in the host-plant, resulted in increased number of grains in heat-stressed AM plants.

Altered amino acid profile of arbuscular mycorrhizal maize plants under low temperature stress

Article

Full-text available

Jan 2016
J PLANT NUTR SOIL SC

We investigated the effect of arbuscular mycorrhiza (AM) on amino acid concentration and composition of maize plants under low-temperature stress. The AM plants had higher amino acid concentrations than the non-AM pants. The concentrations of Thr, Lys, Gly, Ala, His, and Ile of the AM plants were higher than non-AM plants. The results show that low-temperature stress decreased the concentrations of amino acids and altered their composition.

Jasmonates: Emerging Players in Controlling Temperature Stress Tolerance

Article

Full-text available

Jan 2016

The sedentary life of plants has forced them to live in an environment that is characterized by the presence of numerous challenges in terms of biotic and abiotic stresses. Phytohormones play essential roles in mediating plant physiology and alleviating various environmental perturbations. Jasmonates are a group of oxylipin compounds occurring ubiquitously in the plant kingdom that play pivotal roles in response to developmental and environmental cues. Jasmonates (JAs) have been shown to participate in unison with key factors of other signal transduction pathway, including those involved in response to abiotic stress. Recent findings have furnished large body of information suggesting the role of jasmonates in cold and heat stress. JAs have been shown to regulate C-repeat binding factor (CBF) pathway during cold stress. The interaction between the integrants of JA signaling and components of CBF pathway demonstrates a complex relationship between the two. JAs have also been shown to counteract chilling stress by inducing ROS avoidance enzymes. In addition, several lines of evidence suggest the positive regulation of thermotolerance by JA. The present review provides insights into biosynthesis, signal transduction pathway of jasmonic acid and their role in response to temperature stress.

The Water Relations of Weil-watered, Mycorrhizal, and Non-mycorrhizal Onion Plants1

Article

Full-text available

Mar 1982

The water relations of mycorrhizal onions ( Allium cepa L.) were compared with those of non-mycorrhizal controls grown under low and high soil phosphorus conditions. Mycorrhizal plants had higher leaf water potentials, higher transpiration rates, higher hydraulic conductivities and lower leaf resistances than did non-mycorrhizal plants grown in low soil phosphorus conditions. When controls were grown under high soil phosphorus conditions, all 4 parameters were not different from those of mycorrhizal plants. The magnitude of the effect of mycorrhizal fungi on the water relations of the host may, in part, be a function of phosphorus nutrition. The differences in leaf water potentials, transpiration rates and leaf resistances are considered to be the result of the differences found in hydraulic conductivities.

Temperature and Light Effect on Contamination and Spore Germination of Vesicular-Arbuscular Mycorrhizal Fungi

Article

Nov 1975

Chlorophyll fluorescence---a practical guide

Article

Apr 2000

Chlorophyll fluorescence analysis has become one of the most powerful and widely used techniques available to plant physiologists and ecophysiologists. This review aims to provide an introduction for the novice into the methodology and applications of chlorophyll fluorescence. After a brief introduction into the theoretical background of the technique, the methodology and some of the technical pitfalls that can be encountered are explained. A selection of examples is then used to illustrate the types of information that fluorescence can provide.

Mycorrhizal Symbiosis

Book

Jan 2008

The roots of most plants are colonized by symbiotic fungi to form mycorrhiza, which play a critical role in the capture of nutrients from the soil and therefore in plant nutrition. Mycorrhizal Symbiosis is recognized as the definitive work in this area. Since the last edition was published there have been major advances in the field, particularly in the area of molecular biology, and the new edition has been fully revised and updated to incorporate these exciting new developments. . Over 50% new material . Includes expanded color plate section . Covers all aspects of mycorrhiza . Presents new taxonomy . Discusses the impact of proteomics and genomics on research in this area.

Effects of species of VA-mycorrhizal fungi on growth and mineral uptake of sorghum at different temperatures

Article

Mar 1990

Arbuscular mycorrhizal fungal responses to abiotic stresses: A review

Article

Jan 2016

Arbuscular Mycorrhizal Fungi and Tolerance of Temperature Stress in Plants

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