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Plant–Fungi Association: Role of Fungal Endophytes in Improving Plant Tolerance to Water Stress

  • Khondoker M. G. DastogeerEmail author
  • Stephen J. Wylie
Chapter

Abstract

Plants are constantly being challenged with various biotic and abiotic stresses throughout their life cycle that exert profound deleterious effects on growth, development and health. Plants employ various physiological, biochemical and molecular mechanisms to combat these stress factors. Microorganism-mediated plant stress tolerance, particularly plant drought tolerance, is important in the study of plant–microbe interactions. Although relatively less well-known, fungal endophyte-mediated plant drought tolerance has been described for several cases. Unlike mycorrhizal fungi, non-mycorrhizal fungi may mediate the effects of water stress by adjusting, regulating or modifying plant physiological, biochemical and metabolic activities. We review the evidence for fungal endophyte-mediated plant drought tolerance and mechanisms.

Keywords

Abiotic stress Water deficit Endophyte Growth Photosynthesis ROS Osmotic adjustment 

References

  1. Andrew M, Barua R, Short SM, Kohn LM et al (2012) Evidence for a common toolbox based on necrotrophy in a fungal lineage spanning necrotrophs, biotrophs, endophytes, host generalists and specialists. PLoS One 7:e29943PubMedPubMedCentralCrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  3. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fung Biol Rev 21:51–66Google Scholar
  4. Asensio D, Rapparini F, Peñuelas J et al (2012) AM fungi root colonization increases the production of essential isoprenoids vs nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application. Phytochemistry 77:149–161PubMedCrossRefGoogle Scholar
  5. Ashmore M, Toet S, Emberson L et al (2006) Ozone-a significant threat to future world food production? New Phytol 170:201–204PubMedCrossRefGoogle Scholar
  6. Augé RM, Moore JL (2005) Arbuscular mycorrhizal symbiosis and plant drought resistance. In: Mehrotra VS (ed) Mycorrhiza: role and applications. Allied Publishers Limited, New Delhi, pp 136–157Google Scholar
  7. Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68(1):73–78. doi: 10.1007/s13199-015-0370-y
  8. Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL et al (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295. http://dx.doi.org/10.1093/jxb/erp165 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Janeczko A, Kogel KH, Schäfer P, Schwarczinger I, Zuccaro A, Skoczowski et al (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180(2):501–510. doi: 10.1111/j.1469-8137.2008.02583.x PubMedCrossRefGoogle Scholar
  10. Bao X, Roossinck MJ (2013) Multiplexed interactions: viruses of endophytic fungi. Adv Virus Res 86:37–58. doi: 10.1016/B978-0-12-394315-6.00002-7 PubMedCrossRefGoogle Scholar
  11. Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. J Exp Bot 50:375–385CrossRefGoogle Scholar
  12. Baslam M, Goicoechea N (2012) Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiza 22:347–359PubMedCrossRefGoogle Scholar
  13. Battisti DS, Naylor RL (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323:240–244PubMedCrossRefGoogle Scholar
  14. Bayat F, Mirlohib A, Khodambashic M et al (2009) Effects of endophytic fungi on some drought tolerance mechanisms of tall fescue in a hydroponics. Russ J Plant Physiol 56(4):510–516CrossRefGoogle Scholar
  15. Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148CrossRefGoogle Scholar
  16. Boyer JS (1982) Plant productivity and environment. Science 218:443–448PubMedCrossRefGoogle Scholar
  17. Bray EA, Bailey-Serres J, Weretilnyk E et al (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. Am Soc Plant Physiol, Rockville, pp 1158–1249Google Scholar
  18. Brundrett MC (2004) Diversity and classification of mycorrhizal associations. Biol Rev 79:473–495PubMedCrossRefGoogle Scholar
  19. Chaves MM, Maroco JP, Pereira JS et al (2003) Understanding plant responses to drought- from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  20. Cheplick GP (2004) Recovery from drought stress in Lolium perenne (Poaceae): are fungal endophytes detrimental? Am J Bot 91:1960–1968PubMedCrossRefGoogle Scholar
  21. Cheplick GP (2006) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ Exp Bot 60:202–210CrossRefGoogle Scholar
  22. Cheplick GP, Perera A, Koulouris K et al (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14:657–667CrossRefGoogle Scholar
  23. Clay K (1988) Fungal endophytes of grasses-a defensive mutualism between plants and fungi. Ecology 69:10–16CrossRefGoogle Scholar
  24. Cong GQ, Yin CL, He BL, Li L, Gao KX et al (2015) Effect of the endophytic fungus Chaetomium globosum ND35 on the growth and resistance to drought of winter wheat at the seedling stage under water stress. Acta Ecol Sin 35:6120–6128Google Scholar
  25. Davies FT, Potter JR, Linderman RG et al (1993) Drought resistance of mycorrhizal pepper plants independent of leaf P concentration response in gas exchange and water relations. Physiol Plant 87:45–53CrossRefGoogle Scholar
  26. De Battista JP, Bacon CW, Severson RF, Plattner RD, Bouton JH et al (1990) Indole acetic acid production by the fungal endophyte of tall fescue. Agron J 82:878e880Google Scholar
  27. Deckert RJ, Melville LH, Peterson L et al (2001) Structural features of a Lophodermium endophyte during the cryptic life-cycle phase in the foliage of Pinuss trobus. Mycol Res 105:991–997CrossRefGoogle Scholar
  28. Del Rio D, Steward AJ, Pellegrini N et al (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15:316–328PubMedCrossRefGoogle Scholar
  29. Desclaux D, Roumet P (1996) Impact of drought stress on the phenology of two soybean (Glycine max L. Merril) cultivars. Field Crops Res 46:61–70Google Scholar
  30. Dhargalkar S, Bhat DJ (2009) Echinosphaeria pteridis sp. and its Vermiculariopsiella anamorph. Mycotaxon 108:115–122CrossRefGoogle Scholar
  31. Eerens JPJ, Lucas RJ, Easton S, White JGH et al (1998) Influence of the endophyte (Neotyphodium lolii) on morphology, physiology, and alkaloid synthesis of perennial ryegrass during high temperature and water stress. N Z J Agric Res 41(2):219–226. doi: 10.1080/00288233.1998.9513305 CrossRefGoogle Scholar
  32. Elmi AA, West CP (1995) Endophyte effects on tall fescue stomatal response, osmotic adjustment, and tiller survival. New Phytol 131:61–67CrossRefGoogle Scholar
  33. Fisher PJ (1996) Survival and spread of the endophyte Stagonospora pteridiicola in Pteridium aquilinum, other ferns and some flowering plants. New Phytol 132:119–122CrossRefGoogle Scholar
  34. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189PubMedPubMedCentralCrossRefGoogle Scholar
  35. Frohlich J, Hyde KD (1999) Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodivers Conserv 8:97Z–1004CrossRefGoogle Scholar
  36. Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE et al (2006) Climate change effects of plant disease: genomes to ecosystems. Annu Rev Phytopathol 44:489–509PubMedCrossRefGoogle Scholar
  37. Geber MA, Dawson TE (1990) Genetic variation in and covariation between leaf gas exchange, morphology and development in Polygonum arenastrum, an annual plant. Oecologia 85:153–158PubMedCrossRefGoogle Scholar
  38. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C et al (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101PubMedCrossRefGoogle Scholar
  39. Ghannoum O, Conroy JP, Driscoll SP, Paul MJ, Foyer CH, Lawlor DW et al (2003) Non-stomatal limitations are responsible for drought-induced photosynthetic inhibition in four C4 grasses. New Phytol 159:835–844CrossRefGoogle Scholar
  40. Gill S, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochim 48:909–930CrossRefGoogle Scholar
  41. Grover A, Kapoor A, Laksmi OS, Agarwal S, Sahi C, Katiyar-Agarwal S, Agarwal M, Dubey H et al (2001) Understanding molecular alphabets of the plant abiotic stress responses. Curr Sci 80(2):206–216Google Scholar
  42. Hawksworth DL (1988) The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot J Linn Soc 96:3–20CrossRefGoogle Scholar
  43. Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101PubMedCrossRefGoogle Scholar
  44. IPCC (2007) Climate change 2007: synthesis report. In: Pachauri RK, Reisinger A (eds) Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. IPCC, GenevaGoogle Scholar
  45. Jackson RB, Sperry JS, Dawson TE et al (2000) Root water uptake and transport: using physiological processes in global predictions. Trends Plant Sci 5:482–488PubMedCrossRefGoogle Scholar
  46. Kane KH (2011) Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region. Environ Exp Bot 71(3):337–344Google Scholar
  47. Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J Atmos Chem 33:23–88CrossRefGoogle Scholar
  48. Khan AL, Shinwari ZK, Kim Y, Waqas M, Hamayun M, Kamran M, Lee IJ et al (2012) Role of endophyte Chaetomium globosum lk4 in growth of Capsicum annuum by production of gibberellins and indole acetic acid. Pak J Bot 44:1601–1607Google Scholar
  49. Khan AL, Waqas M, Khan AR, Hussain J, Kang SM, Gilani SA, Hamayun M, Shin JH, Kamran M, Al-Harrasi A, Yun BW, Adnan M, Lee IJ et al (2013) Fungal endophyte Penicillium janthinellum LK5 improves growth of ABA-deficient tomato under salinity. World J Microbiol Biotechnol 29(11):2133–2144. doi: 10.1007/s11274-013-1378-1 PubMedCrossRefGoogle Scholar
  50. Khan AL, Waqas M, Lee IJ et al (2014) Resilience of Penicillium resedanum LK6 and exogenous gibberellin in improving Capsicum annuum growth under abiotic stresses. J Plant Res 128(2):259–268. doi: 10.1007/s10265-014-0688-1 PubMedCrossRefGoogle Scholar
  51. Kirkham MB (2005) Principles of soil and plant water relations. Elsevier Academic Press, BurlingtonGoogle Scholar
  52. Krings M, Taylor TN, Dotzler N et al (2012) Fungal endophytes as a driving force in land plant evolution: evidence from the fossil record. In: Southworth D (ed) Biocomplexity of plant-fungal interactions. Wiley, New York, pp 5–28Google Scholar
  53. Kwak JM, Nguyen V, Shroeder JI et al (2006) The role of active oxygen species in hormonal responses. Plant Physiol 141:323–329PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lewis GC, Clements RO (1986) A survey of ryegrass endophyte (Acremonium loliae) in the U.K. and its apparent ineffectuality on a seedling pest. J Agric Sci 107:633–638CrossRefGoogle Scholar
  55. Li WC, Zhou J, Guo SY, Guo LD et al (2007) Endophytic fungi associated with lichens in Baihua mountain of Beijing, China. Fungal Divers 25:69–80Google Scholar
  56. Lopez-Ráez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R et al (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874PubMedCrossRefGoogle Scholar
  57. Maherali H, Caruso CM, Sherrard ME, Latta RG et al (2010) Adaptive value and costs of physiological plasticity to soil moisture limitation in recombinant inbred lines of Avena barbata. Am Nat 175:211–224PubMedCrossRefGoogle Scholar
  58. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940CrossRefGoogle Scholar
  59. Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52(1):1–14. doi:10.1111/j.1744-697X.2006. 00041.xCrossRefGoogle Scholar
  60. Malinowski DP, Zuo H, Belesky DP et al (2004) Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant Soil 267(1):1–12. doi: 10.1007/s11104-005-2575-y CrossRefGoogle Scholar
  61. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R et al (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467PubMedCrossRefGoogle Scholar
  62. Morgan JM (1984) Osmoregulation and water stress in higher plants. Ann Rev Plant Physiol 35:299–319CrossRefGoogle Scholar
  63. Morse LJ, Day TA, Faeth SH et al (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environ Exp Bot 48:257–268CrossRefGoogle Scholar
  64. Nagabhyru P, Dinkins RD, Wood CL, Bacon CW, Schardl CL et al (2013) Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol 13:127PubMedPubMedCentralCrossRefGoogle Scholar
  65. Okcu G, Kaya DM, Atak M et al (2005) Effects of salt and drought stresses on germination and seedling growth of pea (Pisum sativum L.) Turk J Agric For 29:237–242Google Scholar
  66. Parry MA, Andralojc PJ, Khan S, Lea PJ, Keys AJ et al (2002) Rubisco activity: effects of drought stress. Ann Bot 89:833–839PubMedPubMedCentralCrossRefGoogle Scholar
  67. Peñuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci 10:166–169PubMedCrossRefGoogle Scholar
  68. Petrini O, Fisher PJ (1986) Fungal endophytes in Salicornia perennis. Trans Br Mycol Soc 87(4):647–651CrossRefGoogle Scholar
  69. Picone C (2003) Managing mycorrhizae for sustainable agriculture in the tropics. In: Vandermeer JH (ed) Tropical agroecosystems. CRC, Boca Raton, pp 95–132Google Scholar
  70. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15CrossRefGoogle Scholar
  71. Pryor WA, Stanley JP (1975) Letter: a suggested mechanism for the production of malonaldehyde during the autoxidation of polyunsaturated fatty acids. Non-enzymatic production of prostaglandin endoperoxides during autoxidation. J Org Chem 40:3615–3617PubMedCrossRefGoogle Scholar
  72. Purahong W, Hyde KD (2011) Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7CrossRefGoogle Scholar
  73. Rapparini F, Llusià J, Peñuelas J et al (2008) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua. Plant Biol 10:108–122PubMedCrossRefGoogle Scholar
  74. Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716CrossRefGoogle Scholar
  75. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty S, Rodriguez RJ et al (2011) Increased fitness and adaptation of rice plants to cold, drought and salt stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:E14823PubMedPubMedCentralCrossRefGoogle Scholar
  76. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM et al (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581PubMedCrossRefGoogle Scholar
  77. Reid A, Greene SE (2012) How microbes can help feed the world. Report on an American Academy of Microbiology Colloquium. Washington, DCGoogle Scholar
  78. Ren A, Clay K (2008) Impact of a horizontally transmitted endophyte, Balansia henningsiana, on growth and drought tolerance of Panicum rigidulum. Int J Plant Sci 170:599e608Google Scholar
  79. Rodriguez RJ, Redman RS (1997) Fungal life-styles and ecosystem dynamics: biological aspects of plant pathogens, plant endophytes and saprophytes. In: Andrews JH, Tommerup L (eds) Advances in botanical research. Academic, LondonGoogle Scholar
  80. Rodriguez RJ, Redman RS, Henson JM et al (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9(3):261–272CrossRefGoogle Scholar
  81. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefGoogle Scholar
  82. Rodriguez RJ, White JF, Arnold AE, Redman RS et al (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedCrossRefGoogle Scholar
  83. Ruiz-Sánchez M, Aroca R, Muñoz Y, Armada E, Polón R, Ruiz-Lozano JM et al (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869PubMedCrossRefGoogle Scholar
  84. Sanchez-Marquez S, Bills GF, Herrero N, Zabalgogeazcoa I et al (2012) Nonsystemic fungal endophytes of grasses. Fungal Ecol 5:289–297CrossRefGoogle Scholar
  85. Sanders GJ, Arndt SK (2012) Osmotic adjustment under drought conditions. In: Aroca R (ed) Plant responses to drought stress. Springer, New York, pp 199–229CrossRefGoogle Scholar
  86. Schardl CL, Clay K (1997) Evolution of mutualistic endophytes from plant pathogens. In: Carroll, Tudzynski (eds) The mycota V: Part B. Springer, Berlin, pp 1–17Google Scholar
  87. Schardl CL, Leuchtmann A, Spiering MJ et al (2004a) Annu Rev Plant Biol 55:315–340PubMedCrossRefGoogle Scholar
  88. Schardl CL, Leuchtmann A, Spiering MJ et al (2004b) Symbioses of grasses with seed borne fungal endophytes. Ann Rev Plant Biol 55:315–340CrossRefGoogle Scholar
  89. Scheibe R, Beck E (2011) Drought, desiccation, and oxidative stress. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance, Ecological studies, vol 215. Springer, Heidelberg, pp 209–232CrossRefGoogle Scholar
  90. Schenk PM, Carvalhais LC, Kazan K et al (2012) Unraveling plant–microbe interactions: can multi-species transcriptomics help? Trends Biotechnol 30(3):177–184PubMedCrossRefGoogle Scholar
  91. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedCrossRefGoogle Scholar
  92. Schulz B, Guske S, Dammann U, Boyle C et al (1998) Endophyte-host interactions. II Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227Google Scholar
  93. Schulze ED (1986) Carbon dioxide and water vapor exchange in response to drought in the atmosphere and the soil. Ann Rev Plant Physiol 37:247–274CrossRefGoogle Scholar
  94. Sherameti I, Tripathi S, Varma A, Oelmuller R et al (2008) The root-colonizing endophyte Piriformospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol Plant-Microbe Interact 21:799–807. doi: 10.1094/MPMI-21-6-0799 PubMedCrossRefGoogle Scholar
  95. Sherrard ME, Maherali H, Latta RG et al (2009) Water stress alters the genetic architecture of functional traits associated with drought adaptation in Avena barbata. Evolution 63:702–715PubMedCrossRefGoogle Scholar
  96. Singh LP, Gill SS, Tuteja N (2011) Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signal Behav 6:175–191Google Scholar
  97. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58CrossRefGoogle Scholar
  98. Sun CA, Johnson J, Cai DG, Sherameti I, Oelmuller R, Lou BG et al (2010) Piriformosapora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017. doi: 10.1016/j.jplph.2010.02.013 PubMedCrossRefGoogle Scholar
  99. Swarthout D, Harper E, Judd S, Gonthier D, Shyne R, Stowe T, Bultman T et al (2009) Measures of leaf-level water-use efficiency in drought stressed endophyte infected and non-infected tall fescue grasses. Environ Exp Bot 66(1):88–93CrossRefGoogle Scholar
  100. Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates, SunderlandGoogle Scholar
  101. Vadassery J, Ranf S, Drzewiecki C, Mithöfer A, Mazars C, Scheel D, Lee J, Oelmüller R (2009) A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J 59:193–206Google Scholar
  102. Vassey TL, Sharkey TD (1989) Mild water stress leads to reduced extractable sucrose-phosphate synthase activity in leaves of Phaseolus vulgaris L. Plant Physiol 89:1066–1070PubMedPubMedCentralCrossRefGoogle Scholar
  103. Vickers CE, Gershenzon J, Lerdau MT, Loreto F et al (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Ecol 5:283–291CrossRefGoogle Scholar
  104. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, Wettstein D, Franken P, Kogel KH et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391. doi: 10.1073/pnas.0504423102 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692PubMedCrossRefGoogle Scholar
  106. Wang Y, Frei M (2011) Stressed food—the impact of abiotic environmental stresses on crop quality. Agric Ecosyst Environ 141:271–286CrossRefGoogle Scholar
  107. Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ et al (2012) Endophytic fungi produce gibberellins and indole acetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773. doi: 10.3390/molecules170910754 PubMedCrossRefGoogle Scholar
  108. Xu P, Chen F, Mannas JP, Feldman T, Sumner LW et al (2008) Virus infection improves drought tolerance. New Phytol 180:911–921PubMedCrossRefGoogle Scholar
  109. Xu ZZ, Zhou GS, Shimizu H (2009) Effects of soil drought with nocturnal warming on leaf stomatal traits and mesophyll cell ultrastructure of a perennial grass. Crop Sci 49:1843–1851CrossRefGoogle Scholar
  110. Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, Jin D et al (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172(2):1213–1228PubMedPubMedCentralCrossRefGoogle Scholar
  111. Zabalgogeazcoa I (2008) Fungal endophytes and their interaction with plant pathogens. Span J Agric Res 6:138–146CrossRefGoogle Scholar
  112. Zaurov DE, Bonos S, Murphy JA, Richardson M, Belanger FC et al (2001) Endophyte infection can contribute to aluminium tolerance in fine fescues. Crop Sci 41:1981–1984CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Khondoker M. G. Dastogeer
    • 1
    • 2
    Email author
  • Stephen J. Wylie
    • 1
  1. 1.Plant Biotechnology Research Group, Western Australian State Agricultural Biotechnology Centre (SABC)Murdoch UniversityPerthAustralia
  2. 2.Bangladesh Agricultural UniversityMymensinghBangladesh

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