Skip to main content
SpringerLink
Log in

Arbuscular Mycorrhizal Fungi in Alleviation of Cold Stress in Plants

  • Chapter
  • First Online:
Book cover Advancing Frontiers in Mycology & Mycotechnology

Abstract

Cold stress is an important abiotic factor that adversely affects the growth and productivity of different agricultural crops globally. It leads to slower plant metabolism, cell membrane rigidification and loss of function, solute leakage, protein disintegration, depletion in sugar metabolism, and reproductive loss. The ever-increasing population and yet decrease in agricultural productivity is a global concern. So, there is a need for developing strategies that can help plants tolerate the harsh environmental condition and still not affect their productivity. In this context, utilization of arbuscular mycorrhizal fungi (AMF) for alleviation of cold stress in plants has gained much attention. Formation of AMF is reported to improve the performance of plants under both normal and stressful conditions. Although at low temperature (<15 °C) colonization of roots by AMF is often restrained, studies have reported improved tolerance in mycorrhizal plants to cold stress. Symbiotic association of plant roots with AMF improves cold tolerance through reduction of lipid peroxidation and maintenance of membrane integrity, enhancement of antioxidative potential, optimization of osmolytes accumulation and regulation of root hydraulic conductance, improvement of photosynthetic activity and respiration rate, and integrated transcriptional regulation of cold-responsive genes. This chapter discusses various mechanisms that AMF-colonized plants employ to mitigate the detrimental effects caused by low temperature.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adam S, Murthy SDS (2014) Effect of cold stress on photosynthesis of plants and possible protection mechanisms. In: Gaur RK, Sharma P (eds) Approaches to plant stress and their management. Springer, New Delhi, pp 219–226

    Chapter  Google Scholar 

  • Amir H, Jourand P, Cavaloc Y, Ducousso M (2014) Role of mycorrhizal fungi in the alleviation of heavy metal toxicity in plants. In: Solaiman ZM, Abott LK, Varma A (eds) Mycorrhizal Fungi: use in sustainable agriculture and land restoration. Springer, Berlin/Heidelberg, pp 241–258

    Chapter  Google Scholar 

  • Amthor JS (1995) Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle. Glob Change Biol. 1:243–274

    Article  Google Scholar 

  • Antunes PM, De Varennes A, Rajcan I, Goss MJ (2006) Accumulation of specific flavonoids in soybean (Glycine max (L.) Merr.) as a function of the early tripartite symbiosis with arbuscular mycorrhizal fungi and Bradyrhizobium japonicum (Kirchner) Jordan. Soil Biol Biochem 38:1234–1242

    Article  CAS  Google Scholar 

  • Aroca R, Tognoni F, Irigoyen JJ, Sánchez-Díaz M, Pardossi A (2001) Different root low temperature response of two maize genotypes differing in chilling sensitivity. Plant Physiol Biochem 39:1067–1073

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Atkin OK, Sherlock D, Fitter AH, Jarvis S, Hughes JK, Campbell C, Hurry V, Hodge A (2009) Temperature dependence of respiration in roots colonized by arbuscular mycorrhizal fungi. New Phytol 182:188–199

    Article  CAS  PubMed  Google Scholar 

  • Bagnall DJ, King RW, Farquhar GD (1988) Temperature-dependent feedback inhibition of photosynthesis in peanut. Planta 175:348–354

    Article  CAS  PubMed  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balestrini R, Lumini E, Borriello R, Bianciotto V (2015) Plant-soil biota interactions. Soil Microbiol Ecol Biochem:311–338

    Google Scholar 

  • Barrett G, Campbell CD, Fitter AH, Hodge A (2011) The arbuscular mycorrhizal fungus Glomus hoi can capture and transfer nitrogen from organic patches to its associated host plant at low temperature. Appl Soil Ecol 48:102–105

    Article  Google Scholar 

  • Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45

    Article  Google Scholar 

  • Beck EH, Heim R, Hansen J (2004) Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci 29:449–459

    Article  PubMed  Google Scholar 

  • Bowler C, Montagu MV, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116

    Article  CAS  Google Scholar 

  • Bucher M, Hause B, Krajinski F, Küster H (2014) Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 204:833–840

    Article  CAS  PubMed  Google Scholar 

  • Byun MY, Lee J, Cui LH, Kang Y, Oh TK, Park H, Lee H, Kim WT (2015) Constitutive expression of DaCBF7, an Antarctic vascular plant Deschampsia antarctica CBF homolog, resulted in improved cold tolerance in transgenic rice plants. Plant Sci 236:61–74

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530

    Article  CAS  Google Scholar 

  • Candido V, Campanelli G, D’Addabbo T, Castronuovo D, Perniola M, Camele I (2015) Growth and yield promoting effect of artificial mycorrhization on field tomato at different irrigation regimes. Sci Hortic 187:35–43

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Jin W, Liu A, Zhang S, Liu D, Wang F, Lin X, He C (2013) Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Sci Hortic 160:222–229

    Article  CAS  Google Scholar 

  • Chen X, Song F, Liu F, Tian C, Liu S, Xu H, Zhu X (2014) Effect of different arbuscular mycorrhizal fungi on growth and physiology of maize at ambient and low temperature regimes. Sci World J 2014:1–7

    Google Scholar 

  • Chen S, Zhao H, Zou C, Li Y, Chen Y, Wang Z, Jiang Y, Liu A, Zhao P, Wang M, Ahammed GJ (2017) Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front Microbiol 8:2516–2527

    Article  PubMed  PubMed Central  Google Scholar 

  • Chu XT, Fu JJ, Sun YF, Xu YM, Miao YJ, Xu YF, Hu TM (2016) Effect of arbuscular mycorrhizal fungi inoculation on cold stress-induced oxidative damage in leaves of Elymus nutans Griseb. S Afr J Bot 104:21–29

    Article  CAS  Google Scholar 

  • Cooper AJ (1973) Root temperature and plant growth. Commonwealth Agricultural Bureaux, Farnham Royal

    Google Scholar 

  • Crifò T, Puglisi I, Petrone G, Recupero GR, Piero ARL (2011) Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476:1–9

    Article  PubMed  CAS  Google Scholar 

  • Danneberg G, Latus C, Zimmer W, Hundeshagen B, Schneider-Poetsch HJ, Bothe H (1993) Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J Plant Physiol 141:33–39

    Article  CAS  Google Scholar 

  • Del-Saz NF, Romero-Munar A, Cawthray GR, Aroca R, Baraza E, Flexas J, Lambers H, Ribas-Carbó M (2017a) Arbuscular mycorrhizal fungus colonization in Nicotiana tabacum decreases the rate of both carboxylate exudation and root respiration and increases plant growth under phosphorus limitation. Plant Soil 416:97–106

    Article  CAS  Google Scholar 

  • Del-Saz NF, Romero-Munar A, Alonso D, Aroca R, Baraza E, Flexas J, Ribas-Carbó M (2017b) Respiratory ATP cost and benefit of arbuscular mycorrhizal symbiosis with Nicotiana tabacum at different growth stages and under salinity. J Plant Physiol 218:243–248

    Article  CAS  PubMed  Google Scholar 

  • Devi BSR, Kim YJ, Selvi SK, Gayathri S, Altanzul K, Parvin S, Yang DU, Lee OR, Lee S, Yang DC (2012) Influence of potassium nitrate on antioxidant level and secondary metabolite genes under cold stress in Panax ginseng. Russ J Plant Physiol 59:318–325

    Article  CAS  Google Scholar 

  • Dinakar C, Raghavendra AS, Padmasree K (2010) Importance of AOX pathway in optimizing photosynthesis under high light stress: role of pyruvate and malate in activating AOX. Physiol Plant 139:13–26

    Article  CAS  PubMed  Google Scholar 

  • Ensminger I, Busch F, Huner NP (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • Eremina M, Rozhon W, Poppenberger B (2016) Hormonal control of cold stress responses in plants. Cell Mol Life Sci 73:797–810

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2012) Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22:203–217

    Article  CAS  PubMed  Google Scholar 

  • Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86

    Article  CAS  PubMed  Google Scholar 

  • Ferullo JM, Griffith M (2001) Mechanisms of cold acclimation. In: Basra AS (ed) Crop responses & adaptations to temperature stress. Food Products Press, New York, pp 109–150

    Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu J, Miao Y, Shao L, Hu T, Yang P (2016) De novo transcriptome sequencing and gene expression profiling of Elymus nutans under cold stress. BMC Genomics 17:870–889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gavito ME, Bruhn D, Jakobsen I (2002) Phosphorus uptake by arbuscular mycorrhizal hyphae does not increase when the host plant grows under atmospheric CO2 enrichment. New Phytol 154:751–760

    Article  CAS  PubMed  Google Scholar 

  • Gavito ME, Olsson PA, Rouhier H, Medina-Peñafiel A, Jakobsen I, Bago A, Azcón-Aguilar C (2005) Temperature constraints on the growth and functioning of root organ cultures with arbuscular mycorrhizal fungi. New Phytol 168:179–188

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Balestrini R, Volpe V, Guether M, Straub D, Costa A, Ludewig U, Bonfante P (2012) Two putative-aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 12:186–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  CAS  PubMed  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  CAS  PubMed  Google Scholar 

  • Gregory PJ (1988) Growth and functioning of plant roots. Russell’s soil conditions and plant growth. Longman Scientific and Technical. Inglaterra, pp 113–67

    Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Biol 41:187–223

    Article  CAS  Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327

    Article  CAS  Google Scholar 

  • Hakerlerler H, Oktay M, Eryuce N, Yagmur B (1997) Effect of potassium sources on the chilling tolerance of some vegetable seedlings grown in hotbeds. In: Johnston AE (ed) Food security in the WANA region, the essential need for balanced fertilization. International Potash Institute, Basel, pp 353–359

    Google Scholar 

  • Hamburger D, Rezzonico E, Petétot JMC, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1:26–44

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicagotruncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinemeyer A, Fitter AH (2004) Impact of temperature on the arbuscular mycorrhizal (AM) symbiosis: growth responses of the host plant and its AM fungal partner. J Exp Bot 55:525–534

    Article  CAS  PubMed  Google Scholar 

  • Hetrick BD, Bloom J (1984) The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76:953–956

    Article  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression–c-repeat binding factor/DRE binding factor 1 cascade and freezing tolerance in Arabidopsis. Plant Cell 113:1–19

    Google Scholar 

  • Jan N, Andrabi KI (2009) Cold resistance in plants: a mystery unresolved. EJB 12:14–15

    Google Scholar 

  • Janicka-Russak M, Kabała K, Wdowikowska A, Kłobus G (2012) Response of plasma membrane H+-ATPase to low temperature in cucumber roots. J Plant Res 125:291–300

    Article  CAS  PubMed  Google Scholar 

  • Jewell MC, Campbell BC, Godwin ID (2010) Transgenic plants for abiotic stress resistance. In: Kole C, Michler CH, Abbott AG, Hall TC (eds) Transgenic crop plants. Springer, Berlin, Heidelberg, pp 67–132

    Chapter  Google Scholar 

  • Kapoor R, Singh N (2016) Arbuscular mycorrhiza and reactive oxygen species. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer Nature, Singapore, pp 225–243

    Google Scholar 

  • Karasawa T, Hodge A, Fitter AH (2012) Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil. Plant Cell Environ 35:819–828

    Article  CAS  PubMed  Google Scholar 

  • Kaur G, Kumar S, Thakur P, Malik JA, Bhandhari K, Sharma KD, Nayyar H (2011) Involvement of proline in response of chickpea (Cicer arietinum L.) to chilling stress at reproductive stage. Sci Hortic 128:174–181

    Article  CAS  Google Scholar 

  • Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712

    Article  CAS  PubMed  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • Kishor PK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci:424–438

    Google Scholar 

  • Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2015) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Rev Biotechnol 35:461–474

    Article  PubMed  CAS  Google Scholar 

  • Kurimoto K, Millar AH, Lambers H, Day DA, Noguchi K (2004) Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production. Plant Cell Physiol 45:1015–1022

    Article  CAS  PubMed  Google Scholar 

  • Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 84:692–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Labate CA, Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Planta 173:519–527

    Article  CAS  PubMed  Google Scholar 

  • Latef AAHA, Chaoxing H (2011) Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol Plant 33:1217–1225

    Article  CAS  Google Scholar 

  • Lázaro JJ, Jiménez A, Camejo D, Martí MC, Lázaro-Payo A, Barranco-Medina S, Sevilla F (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 460:1–20

    Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stress, chilling, freezing, and high temperature stresses. Academic:1–497

    Google Scholar 

  • Li CR, Liang DD, Li J, Duan YB, Hao L, Yang YC, Qin RY, Li LI, Wei PC, Yang JB (2013) Unravelling mitochondrial retrograde regulation in the abiotic stress induction of rice alternative oxidase 1 genes. Plant Cell Environ 36:775–788

    Article  CAS  PubMed  Google Scholar 

  • Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. Mycorrhiza 14:93–101

    Article  CAS  PubMed  Google Scholar 

  • Liu ZL, Li YJ, Hou HY, Zhu XC, Rai V, He XY, Tian CJ (2013a) 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

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Yu K, He T, Li F, Zhang D, Liu J (2013b) The low temperature induced physiological responses of Avena nuda L., a cold-tolerant plant species. Sci World J 2013:1–8

    Google Scholar 

  • Liu Z, Li Y, Wang J, He X, Tian C (2015) Different respiration metabolism between mycorrhizal and non-mycorrhizal rice under low-temperature stress: a cry for help from the host. J of Agric Sci 153:602–614

    Article  CAS  Google Scholar 

  • Liu A, Chen S, Wang M, Liu D, Chang R, Wang Z, Lin X, Bai B, Ahammed GJ (2016) Arbuscular mycorrhizal fungus alleviates chilling stress by boosting redox poise and antioxidant potential of tomato seedlings. J Plant Growth Regul 35:109–120

    Article  CAS  Google Scholar 

  • Locato V, De Pinto MC, De Gara L (2009) Different involvement of the mitochondrial, plastidial and cytosolic ascorbate-glutathione redox enzymes in heat shock responses. Physiol Plant 135:296–306

    Article  CAS  PubMed  Google Scholar 

  • Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • Ma J, Janoušková M, Li Y, Yu X, Yan Y, Zou Z, He C (2015) Impact of arbuscular mycorrhizal fungi (AMF) on cucumber growth and phosphorus uptake under cold stress. Funct Plant Biol 42:1158–1167

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Sun C, Bai L, Dong R, Yan Y, Yu X, He C, Zou Z, Li Y (2018) Transcriptome analysis of cucumber roots reveals key cold-resistance genes induced by AM fungi. Plant Mol Biol Report 36:135–148

    Article  CAS  Google Scholar 

  • Mandal S, Upadhyay S, Wajid S, Ram M, Jain DC, Singh VP, Abdin MZ, Kapoor R (2015) Arbuscular mycorrhiza increase artemisinin accumulation in Artemisia annua by higher expression of key biosynthesis genes via enhanced jasmonic acid levels. Mycorrhiza 25:345–357

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, New York

    Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102

    Article  CAS  Google Scholar 

  • Marulanda A, Azcon R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533

    Article  CAS  Google Scholar 

  • Marulanda-Aguirre A, Azcón R, Ruiz-Lozano JM, Aroca R (2008) Differential effects of a Bacillus megaterium strain on Lactuca sativa plant growth depending on the origin of the arbuscular mycorrhizal fungus coinoculated: physiologic and biochemical traits. J Plant Growth Regul 27:10–18

    Article  CAS  Google Scholar 

  • Matsubara Y, Kayukawa Y, Fukui H (2000) Temperature-stress tolerance of asparagus seedlings through symbiosis with arbuscular mycorrhizal fungus. J Jpn Soc Hortic Sci 69:570–575

    Article  Google Scholar 

  • Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotech Adv 29:645–653

    Article  CAS  Google Scholar 

  • Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol 17:625–631

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170–176

    Article  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez-Garcia BELEN, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • O’Leary BM, Plaxton WC (2016) Plant respiration. eLS, pp 1–11

    Google Scholar 

  • Oliver SN, Lunn JE, Urbanczyk-Wochniak E, Lytovchenko A, Van Dongen JT, Faix B, Schmälzlin E, Fernie AR, Geigenberger P (2008) Decreased expression of cytosolic pyruvate kinase in potato tubers leads to a decline in pyruvate resulting in an in vivo repression of the alternative oxidase. Plant Physiol 148:1640–1654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ordoñez NM, Marondedze C, Thomas L, Pasqualini S, Shabala L, Shabala S, Gehring C (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS Lett 588:1008–1015

    Article  PubMed  CAS  Google Scholar 

  • Otgonsuren B, Rewald B, Godbold DL, Göransson H (2016) Ectomycorrhizal inoculation of Populus nigra modifies the response of absorptive root respiration and root surface enzyme activity to salinity stress. Flora 224:123–129

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Paredes M, Quiles MJ (2015) The effects of cold stress on photosynthesis in Hibiscus plants. PLoS One 10:e0137472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 99:13324–13329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavithra D, Yapa N (2018) Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundw Sustain Dev 7:490–494

    Article  Google Scholar 

  • Pedranzani H, Tavecchio N, Gutiérrez M, Garbero M, Porcel R & Ruiz-Lozano JM (2015). Differential effects of cold stress on the antioxidant response of mycorrhizal and non-mycorrhizal Jatropha curcas (L.) plants. J Agric Sci 7:35

    Google Scholar 

  • Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750

    Article  CAS  PubMed  Google Scholar 

  • Porcel R, Redondo-Gómez S, Mateos-Naranjo E, Aroca R, Garcia R, Ruiz-Lozano JM (2015) Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. J Plant Physiol 185:75–83

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of arbuscular mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 193–207

    Chapter  Google Scholar 

  • Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM (2017) Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci 8:1056

    Article  PubMed  PubMed Central  Google Scholar 

  • Raju PS, Clark RB, Ellis JR, Maranville JW (1990) Effects of species of VA-mycorrhizal fungi on growth and mineral uptake of sorghum at different temperatures. Plant Soil 121:165–170

    Article  CAS  Google Scholar 

  • Rao ASVC, Reddy AR (2008) Glutathione reductase: a putative redox regulatory system in plant cells. In: Khan NA, Singh S, Umar S (eds) Sulfur assimilation and abiotic stresses in plants. Springer, Dordrecht, pp 111–147

    Chapter  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–470

    Article  CAS  PubMed  Google Scholar 

  • Rewald B, Holzer L, Göransson H (2015) Impact of arbuscular mycorrhiza inoculum on biomass accumulation and root respiration of salt-stressed Ulmusglabra seedlings. Urban For Urban Green 14:432–437

    Article  Google Scholar 

  • Robinson SA, Ribas-Carbo M, Yakir D, Giles L, Reuveni Y, Berry JA (1995) Beyond SHAM and cyanide: opportunities for studying the alternative oxidase in plant respiration using oxygen isotope discrimination. Funct Plant Biol 22:487–496

    Article  CAS  Google Scholar 

  • Ruelland E, Zachowsk A (2010) How plants sense temperature? EEB 69:225–232

    Google Scholar 

  • Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    Article  CAS  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawers RJ, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97

    Article  CAS  PubMed  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Anand G, Singh N, Kapoor R (2017) Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Front Plant Sci 8:906–927

    Article  PubMed  PubMed Central  Google Scholar 

  • Silsbury JH, Smith SE, Oliver AJ (1983) A comparison of growth efficiency and specific rate of dark respiration of uninfected and vesicular-arbuscular mycorrhizal plants of Trifolium subterraneum L. New Phytol 93:555–566

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    Article  CAS  PubMed  Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    Article  CAS  PubMed  Google Scholar 

  • Staddon PL, Thompson K, Jakobsen I, Grime JP, Askew AP, Fitter AH (2003) Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob Change Biol 9:186–194

    Article  Google Scholar 

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Takabatake R, Hata S, Taniguchi M, Kouchi H, Sugiyama T, Izui K (1999) Isolation and characterization of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice and Arabidopsis. Plant Mol Biol 40:479–486

    Article  CAS  PubMed  Google Scholar 

  • Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39:1–83

    Article  CAS  PubMed  Google Scholar 

  • Tayal P, Kapoor R, Bhatnagar AK (2011) Functional synergism among Glomus fasciculatum, Trichoderma viride and Pseudomonas fluorescens on Fusarium wilt in tomato. J Plant Pathol 93:745–750

    Google Scholar 

  • Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599

    Article  CAS  Google Scholar 

  • Tindall JA, Mills HA, Radcliffe DE (1990) The effect of root zone temperature on nutrient uptake of tomato. J Plant Nutr 13:939–956

    Article  CAS  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, ColardA CD, Da Silva C, Gomez SK, Koul R, Ferrol N (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–202

    Article  CAS  PubMed  Google Scholar 

  • Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2; 1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14:1751–1766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Wang H, Shao H, Tang X (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67–80

    PubMed  PubMed Central  Google Scholar 

  • Wani SH, Sandhu JS, Gosal SS (2008) Genetic engineering of crop plants for abiotic stress tolerance. In: Malik CP, Kaur B, Wadhwani C (eds) Advanced topics in plant biotechnology and plant biology. MD Publications, New Delhi, pp 149–183

    Google Scholar 

  • Waraich EA, Ahmad R, Ashraf MY, Saifullah, Ahmad M (2011) Improving agricultural water use efficiency by nutrient management in crop plants. Acta Agr Scan B-S P 61:291–304

    CAS  Google Scholar 

  • Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181

    Article  CAS  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771

    Article  CAS  PubMed  Google Scholar 

  • Wu QS, Zou YN (2010) Beneficial roles of arbuscular mycorrhizas in citrus seedlings at temperature stress. Sci Hortic 125:289–293

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Abd-Allah EF (2014) Mycorrhizal association and ROS in plants. In: Ahmad P (ed) Oxidative damage to plants. Elsevier, Amsterdam, pp 453–475

    Chapter  Google Scholar 

  • Xin Z, Browse J (2001) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902

    Article  Google Scholar 

  • Xin Z, Li PH (1993) Relationship between proline and abscisic acid in the induction of chilling tolerance in maize suspension-cultured cells. Plant Physiol 103:607–613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Article  CAS  Google Scholar 

  • Yadav SK (2011) Cold stress tolerance mechanisms in plants. In: Gaba S, Smith B, Lichtfouse E (eds) Sustainable agriculture. Springer, Dordrecht, pp 605–620

    Google Scholar 

  • Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One 10:e0145726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeng Y, Yu J, Cang J, Liu L, Mu Y, Wang J, Zhang D (2011) Detection of sugar accumulation and expression levels of correlative key enzymes in winter wheat (Triticum aestivum) at low temperatures. Biosci Biotechnol Biochem 75:681–687

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Hamel C, Kianmehr H, Smith DL (1995) Root-zone temperature and soybean [Glycine max.(L.) Merr.] vesicular-arbuscularmycorrhizae: development and interactions with the nitrogen fixing symbiosis. Environ Exp Bot 35:287–298

    Article  Google Scholar 

  • Zhu X, Song F, Xu H (2010a) Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20:325–332

    Article  CAS  PubMed  Google Scholar 

  • Zhu XC, Song FB, Xu HW (2010b) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331:129–137

    Article  CAS  Google Scholar 

  • Zhu XC, Song FB, Liu SQ, Liu TD, Zhou X (2012) Arbuscular mycorrhizae improves photosynthesis and water status of Zea mays L. under drought stress. Plant Soil Environ 58:186–191

    Article  CAS  Google Scholar 

  • Zhu XC, Song FB, Liu FL, Liu SQ, Tian CJ (2015) Carbon and nitrogen metabolism in arbuscular mycorrhizal maize plants under low-temperature stress. Crop Pasture Sci 66:62–70

    Article  CAS  Google Scholar 

  • Zhu X, Song F, Liu F (2017) Arbuscular mycorrhizal fungi and tolerance of temperature stress in plants. In: Wu QS (ed) Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 163–194

    Chapter  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, University of Delhi, New Delhi, Delhi, India

    Thokchom Sarda Devi, Samta Gupta & Rupam Kapoor

Authors
  1. Thokchom Sarda Devi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samta Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rupam Kapoor
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Division of Biological Science and Engineering, Netaji Subhas University of Technology, New Delhi, Delhi, India

    Tulasi Satyanarayana

  2. Biotech & Management of Bioresources Div, The Energy and Resources Institute, New Delhi, Delhi, India

    Sunil Kumar Deshmukh

  3. Division of Biological Sciences, CSIR-National Chemical Laboratory, Pune, Maharashtra, India

    Mukund V. Deshpande

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Devi, T.S., Gupta, S., Kapoor, R. (2019). Arbuscular Mycorrhizal Fungi in Alleviation of Cold Stress in Plants. In: Satyanarayana, T., Deshmukh, S., Deshpande, M. (eds) Advancing Frontiers in Mycology & Mycotechnology. Springer, Singapore. https://doi.org/10.1007/978-981-13-9349-5_17

Download citation

Publish with us

Policies and ethics

Search

Navigation