Arbuscular Mycorrhizal Fungi in Alleviation of Cold Stress in Plants

  • Thokchom Sarda Devi
  • Samta Gupta
  • Rupam Kapoor


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.


Arbuscular mycorrhiza fungi Cold stress Root hydraulic conductance Osmotic adjustments Transcriptional regulation 


  1. 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 219–226CrossRefGoogle Scholar
  2. 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 241–258CrossRefGoogle Scholar
  3. Amthor JS (1995) Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle. Glob Change Biol. 1:243–274CrossRefGoogle Scholar
  4. 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 38:1234–1242CrossRefGoogle Scholar
  5. 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 39:1067–1073CrossRefGoogle Scholar
  6. 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 173:808–816PubMedCrossRefPubMedCentralGoogle Scholar
  7. 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 182:188–199PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bagnall DJ, King RW, Farquhar GD (1988) Temperature-dependent feedback inhibition of photosynthesis in peanut. Planta 175:348–354PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958PubMedPubMedCentralCrossRefGoogle Scholar
  10. Balestrini R, Lumini E, Borriello R, Bianciotto V (2015) Plant-soil biota interactions. Soil Microbiol Ecol Biochem:311–338Google Scholar
  11. 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 48:102–105CrossRefGoogle Scholar
  12. Basu S, Rabara RC, Negi S (2018) AMF: the future prospect for sustainable agriculture. Physiol Mol Plant Pathol 102:36–45CrossRefGoogle Scholar
  13. Beck EH, Heim R, Hansen J (2004) Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci 29:449–459PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bowler C, Montagu MV, Inzé D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116CrossRefGoogle Scholar
  15. Bucher M, Hause B, Krajinski F, Küster H (2014) Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 204:833–840PubMedCrossRefPubMedCentralGoogle Scholar
  16. 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 236:61–74PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sci 168:521–530CrossRefGoogle Scholar
  18. 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 187:35–43CrossRefGoogle Scholar
  19. Charest C, Dalpé Y, Brown A (1993) The effect of vesicular-arbuscular mycorrhizae and chilling on two hybrids of Zea mays L. Mycorrhiza 4:89–92CrossRefGoogle Scholar
  20. Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787PubMedPubMedCentralCrossRefGoogle Scholar
  21. 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 160:222–229CrossRefGoogle Scholar
  22. 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 2014:1–7Google Scholar
  23. 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 8:2516–2527PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 104:21–29CrossRefGoogle Scholar
  25. Cooper AJ (1973) Root temperature and plant growth. Commonwealth Agricultural Bureaux, Farnham RoyalGoogle Scholar
  26. 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 476:1–9PubMedCrossRefPubMedCentralGoogle Scholar
  27. 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 141:33–39CrossRefGoogle Scholar
  28. 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 416:97–106CrossRefGoogle Scholar
  29. 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 218:243–248PubMedCrossRefPubMedCentralGoogle Scholar
  30. 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 59:318–325CrossRefGoogle Scholar
  31. 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 139:13–26PubMedCrossRefPubMedCentralGoogle Scholar
  32. Ensminger I, Busch F, Huner NP (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44CrossRefGoogle Scholar
  33. Eremina M, Rozhon W, Poppenberger B (2016) Hormonal control of cold stress responses in plants. Cell Mol Life Sci 73:797–810PubMedCrossRefPubMedCentralGoogle Scholar
  34. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280PubMedPubMedCentralCrossRefGoogle Scholar
  35. 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 22:203–217PubMedCrossRefGoogle Scholar
  36. Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86PubMedCrossRefGoogle Scholar
  37. 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 109–150Google Scholar
  38. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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 17:870–889PubMedPubMedCentralCrossRefGoogle Scholar
  40. 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 154:751–760CrossRefGoogle Scholar
  41. 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 168:179–188PubMedCrossRefPubMedCentralGoogle Scholar
  42. 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 12:186–200PubMedPubMedCentralCrossRefGoogle Scholar
  43. 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 455:189–194PubMedCrossRefPubMedCentralGoogle Scholar
  44. 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 435:819–823PubMedCrossRefPubMedCentralGoogle Scholar
  45. Gregory PJ (1988) Growth and functioning of plant roots. Russell’s soil conditions and plant growth. Longman Scientific and Technical. Inglaterra, pp 113–67Google Scholar
  46. Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Biol 41:187–223CrossRefGoogle Scholar
  47. 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 331:313–327CrossRefGoogle Scholar
  48. 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 353–359Google Scholar
  49. 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 14:889–902PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1:26–44CrossRefGoogle Scholar
  51. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  52. 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 14:2413–2429PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 55:525–534PubMedCrossRefPubMedCentralGoogle Scholar
  55. Hetrick BD, Bloom J (1984) The influence of temperature on colonization of winter wheat by vesicular-arbuscular mycorrhizal fungi. Mycologia 76:953–956CrossRefGoogle Scholar
  56. 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 113:1–19Google Scholar
  57. Jan N, Andrabi KI (2009) Cold resistance in plants: a mystery unresolved. EJB 12:14–15Google Scholar
  58. 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 125:291–300PubMedCrossRefPubMedCentralGoogle Scholar
  59. 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 67–132CrossRefGoogle Scholar
  60. 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 225–243Google Scholar
  61. 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 35:819–828PubMedCrossRefPubMedCentralGoogle Scholar
  62. 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 128:174–181CrossRefGoogle Scholar
  63. 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 7:706–712PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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 333:880–882PubMedCrossRefPubMedCentralGoogle Scholar
  65. 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:424–438Google Scholar
  66. 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 35:461–474PubMedCrossRefPubMedCentralGoogle Scholar
  67. 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 45:1015–1022PubMedCrossRefPubMedCentralGoogle Scholar
  68. Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 84:692–695PubMedPubMedCentralCrossRefGoogle Scholar
  69. Labate CA, Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Planta 173:519–527PubMedCrossRefPubMedCentralGoogle Scholar
  70. 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 33:1217–1225CrossRefGoogle Scholar
  71. 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 460:1–20Google Scholar
  72. Levitt J (1980) Responses of plants to environmental stress, chilling, freezing, and high temperature stresses. Academic:1–497Google Scholar
  73. 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 36:775–788PubMedCrossRefPubMedCentralGoogle Scholar
  74. Liu A, Wang B, Hamel C (2004) Arbuscular mycorrhiza colonization and development at suboptimal root zone temperature. Mycorrhiza 14:93–101PubMedCrossRefPubMedCentralGoogle Scholar
  75. 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 71:87–95PubMedCrossRefPubMedCentralGoogle Scholar
  76. 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 2013:1–8Google Scholar
  77. 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 153:602–614CrossRefGoogle Scholar
  78. 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 35:109–120CrossRefGoogle Scholar
  79. 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 135:296–306PubMedCrossRefPubMedCentralGoogle Scholar
  80. Luu DT, Maurel C (2005) Aquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96CrossRefGoogle Scholar
  81. 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 42:1158–1167CrossRefGoogle Scholar
  82. 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 36:135–148CrossRefGoogle Scholar
  83. 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 25:345–357PubMedCrossRefPubMedCentralGoogle Scholar
  84. Marschner H (1995) Mineral nutrition of higher plants. Academic, New YorkGoogle Scholar
  85. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102CrossRefGoogle Scholar
  86. 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 119:526–533CrossRefGoogle Scholar
  87. 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 27:10–18CrossRefGoogle Scholar
  88. Matsubara Y, Kayukawa Y, Fukui H (2000) Temperature-stress tolerance of asparagus seedlings through symbiosis with arbuscular mycorrhizal fungus. J Jpn Soc Hortic Sci 69:570–575CrossRefGoogle Scholar
  89. 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 96:8271–8276PubMedPubMedCentralCrossRefGoogle Scholar
  90. Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotech Adv 29:645–653CrossRefGoogle Scholar
  91. 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 17:625–631PubMedCrossRefPubMedCentralGoogle Scholar
  92. 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 5:170–176PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 35:454–484PubMedCrossRefPubMedCentralGoogle Scholar
  94. O’Leary BM, Plaxton WC (2016) Plant respiration. eLS, pp 1–11Google Scholar
  95. 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 148:1640–1654PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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 588:1008–1015PubMedCrossRefPubMedCentralGoogle Scholar
  97. 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 224:123–129CrossRefGoogle Scholar
  98. Paradis R, Dalpé Y, Charest C (1995) The combined effect of arbuscular mycorrhizas and short-term cold exposure on wheat. New Phytol 129:637–642CrossRefGoogle Scholar
  99. Paredes M, Quiles MJ (2015) The effects of cold stress on photosynthesis in Hibiscus plants. PLoS One 10:e0137472PubMedPubMedCentralCrossRefGoogle Scholar
  100. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefPubMedCentralGoogle Scholar
  101. 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 99:13324–13329PubMedCrossRefPubMedCentralGoogle Scholar
  102. Pavithra D, Yapa N (2018) Arbuscular mycorrhizal fungi inoculation enhances drought stress tolerance of plants. Groundw Sustain Dev 7:490–494CrossRefGoogle Scholar
  103. 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 7:35Google Scholar
  104. 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 55:1743–1750PubMedCrossRefPubMedCentralGoogle Scholar
  105. 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 185:75–83PubMedCrossRefPubMedCentralGoogle Scholar
  106. 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 193–207CrossRefGoogle Scholar
  107. 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 8:1056PubMedPubMedCentralCrossRefGoogle Scholar
  108. 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 121:165–170CrossRefGoogle Scholar
  109. 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 111–147CrossRefGoogle Scholar
  110. 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 414:462–470PubMedCrossRefPubMedCentralGoogle Scholar
  111. 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 14:432–437CrossRefGoogle Scholar
  112. 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 22:487–496CrossRefGoogle Scholar
  113. Ruelland E, Zachowsk A (2010) How plants sense temperature? EEB 69:225–232Google Scholar
  114. Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150CrossRefGoogle Scholar
  115. Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30–43PubMedPubMedCentralCrossRefGoogle Scholar
  116. Sawers RJ, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97PubMedCrossRefPubMedCentralGoogle Scholar
  117. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  118. 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 14:194–199PubMedCrossRefPubMedCentralGoogle Scholar
  119. 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 8:906–927PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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 93:555–566CrossRefGoogle Scholar
  121. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San DiegoGoogle Scholar
  122. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  123. Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic, LondonGoogle Scholar
  124. 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 62:227–250PubMedCrossRefPubMedCentralGoogle Scholar
  125. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358PubMedCrossRefPubMedCentralGoogle Scholar
  126. 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 9:186–194CrossRefGoogle Scholar
  127. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedCrossRefPubMedCentralGoogle Scholar
  128. 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 40:479–486PubMedCrossRefPubMedCentralGoogle Scholar
  129. Takata K, Matsuzaki T, Tajika Y (2004) Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39:1–83PubMedCrossRefPubMedCentralGoogle Scholar
  130. 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 93:745–750Google Scholar
  131. Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105PubMedCrossRefPubMedCentralGoogle Scholar
  132. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599CrossRefGoogle Scholar
  133. Tindall JA, Mills HA, Radcliffe DE (1990) The effect of root zone temperature on nutrient uptake of tomato. J Plant Nutr 13:939–956CrossRefGoogle Scholar
  134. 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 193:755–769PubMedCrossRefPubMedCentralGoogle Scholar
  135. 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 455:195–202PubMedCrossRefPubMedCentralGoogle Scholar
  136. Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2; 1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell 14:1751–1766PubMedPubMedCentralCrossRefGoogle Scholar
  137. 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 7:67–80PubMedPubMedCentralGoogle Scholar
  138. 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 149–183Google Scholar
  139. 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 61:291–304Google Scholar
  140. Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181CrossRefGoogle Scholar
  141. Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771PubMedCrossRefPubMedCentralGoogle Scholar
  142. Wu QS, Zou YN (2010) Beneficial roles of arbuscular mycorrhizas in citrus seedlings at temperature stress. Sci Hortic 125:289–293CrossRefGoogle Scholar
  143. 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 453–475CrossRefGoogle Scholar
  144. Xin Z, Browse J (2001) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902CrossRefGoogle Scholar
  145. Xin Z, Li PH (1993) Relationship between proline and abscisic acid in the induction of chilling tolerance in maize suspension-cultured cells. Plant Physiol 103:607–613PubMedPubMedCentralCrossRefGoogle Scholar
  146. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183CrossRefGoogle Scholar
  147. Yadav SK (2011) Cold stress tolerance mechanisms in plants. In: Gaba S, Smith B, Lichtfouse E (eds) Sustainable agriculture. Springer, Dordrecht, pp 605–620Google Scholar
  148. 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:e0145726PubMedPubMedCentralCrossRefGoogle Scholar
  149. 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 75:681–687PubMedCrossRefPubMedCentralGoogle Scholar
  150. 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 35:287–298CrossRefGoogle Scholar
  151. 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 20:325–332PubMedCrossRefPubMedCentralGoogle Scholar
  152. 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 331:129–137CrossRefGoogle Scholar
  153. 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 58:186–191CrossRefGoogle Scholar
  154. 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 66:62–70CrossRefGoogle Scholar
  155. 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 163–194CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Thokchom Sarda Devi
    • 1
  • Samta Gupta
    • 1
  • Rupam Kapoor
    • 1
  1. 1.Department of BotanyUniversity of DelhiNew DelhiIndia

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