Advertisement

Biology and Fertility of Soils

, Volume 48, Issue 5, pp 519–529 | Cite as

Exophiala sp.LHL08 association gives heat stress tolerance by avoiding oxidative damage to cucumber plants

  • Abdul Latif Khan
  • Muhammad Hamayun
  • Muhammad Waqas
  • Sang-Mo Kang
  • Yoon-Ha Kim
  • Duk-Hwan Kim
  • In-Jung Lee
Original Paper

Abstract

Exophiala sp. LHL08, a gibberellin-producing strain, was investigated to assess its effects on cucumber plant growth and heat (40°C) stress tolerance. The results reveal that Exophiala sp. associated plants had significantly higher plant growth attributes (shoot length, plant biomass, chlorophyll contents, and leaf area) than control under heat stress. Endophytic association helped the plants to obtain adequate water to reduce the leaf electrolytic leakage under stress. High-temperature-induced oxidative stress was less pronounced in Exophiala sp. associated plants as shown by enhanced levels of total polyphenol and reduced activities of glutathione, superoxide anion, and lipid peroxidation. To tolerate heat stress and rescue plant growth, the endophyte association significantly increased catalase and peroxidase activities of the host plants as compared to control plants. Contents of palmitic, stearic, oleic, and α-linolenic were significantly decreased in the Exophiala sp.-inoculated plants than control plants under heat stress. Contents of flavonoids like genistein and daidzein were produced in higher quantities, while glycitein content was almost same in endophyte-associated plants under heat stress than control plants. Contrarily, stress-responsive endogenous abscisic acid and jasmonic acid were significantly activated in non-inoculated control treatments as compared to endophyte-inoculated plants under heat stress. The findings of the study reveal that association of Exophiala sp. with cucumber host plants can modulate heat stress by influencing physiological and biochemical contents of plants under heat stress.

Keywords

Exophiala sp.LHL08 Heat stress Phytohormones Isoflavonoids Fatty acids Oxidative stress 

Notes

Acknowledgements

The research work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2011-0022027).

Supplementary material

374_2011_649_MOESM1_ESM.doc (32 kb)
Supplementary Table 1 GC-MS conditions used for analysis and quantification of the plant endogenous ABA and JA (DOC 32 kb)

References

  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–127PubMedCrossRefGoogle Scholar
  2. Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171:382–388CrossRefGoogle Scholar
  3. Antunes MDC, Sfakiotakis EM (2008) Changes in fatty acid composition and electrolyte leakage of ‘Hayward’kiwifruit during storage at different temperatures. Food Chem 110:891–896CrossRefGoogle Scholar
  4. Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Carson WF, Schnitzer SA (eds) Tropical Forest Community Ecology. John Wiley & Sons, Oxford, pp 254–271Google Scholar
  5. Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Gullner BBG, Janeczko A, Kogel K, Schäfer P, Schwarczinger P, Zuccaro A, Skoczowski A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180:501–551PubMedCrossRefGoogle Scholar
  6. Barret M, Morrissey JP, O’Gara F (2011) Functional genomics analysis of plant growth-promoting rhizobacterial traits involved in rhizosphere competence. Biol Fertil Soils 47:729–743CrossRefGoogle Scholar
  7. Catford JG, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266CrossRefGoogle Scholar
  8. Chandanie WA, Kubota M, Hyakumachi M (2010) Interactions between arbuscular mycorrhizal fungus Glomus mosseae and plant growth-promoting fungi and their significance for enhancing plant growth and suppressing damping-off of cucumber (Cucumis sativus L.). App Soil Eco 41:336–341CrossRefGoogle Scholar
  9. Creelman R, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Nat Acad Sci USA 92:4114–4119PubMedCrossRefGoogle Scholar
  10. Dakora FD, Phillips DA (1996) Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Mol Plant Physiol 49:1–20CrossRefGoogle Scholar
  11. Davey MW, Stals E, Panis B, Keulemans J, Swennen RL (2005) High-throughput determination of Malondialdehyde in plant tissues. Anal Biochem 347:201–207PubMedCrossRefGoogle Scholar
  12. Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357CrossRefGoogle Scholar
  13. Drozdov SN, Titov AF, Talanova VV, Kritenko SP, Sherudilo EG, Akimova TV (1984) The effect of temperature on cold and heat resistance of growing plants. J Exp Bot 35:1595–1602CrossRefGoogle Scholar
  14. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77PubMedCrossRefGoogle Scholar
  15. Esch H, Hundeshage B, Schneider-Poetsch HJ, Bothe H (1994) Demonstration of abscisic acid in spores and hyphae of the arbuscular– mycorrhizal fungus Glomus and in the N2-fixing cyanobacterium Anabaena variabilis. Plant Sci 99:9–16CrossRefGoogle Scholar
  16. Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipidperoxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407–421PubMedCrossRefGoogle Scholar
  17. Falcone DL, Ogas JP, Somerville CR (2004) Regulation of membrane fatty acid composition by temperature in mutants of Arabidopsis with alterations in membrane lipid composition. BMC Plant Biol 4:17PubMedCrossRefGoogle Scholar
  18. Gamalero E, Berta G, Glick BR (2009) The use of microorganisms to facilitate the growth of plants in saline soils. In: Khan MS, Zaidi A, Musarat J (eds) Microbial Strategies for Crop Improvement. Springer–Verlag, Berlin, pp 1–22CrossRefGoogle Scholar
  19. Garg N, Manchanda G (2009) Role of arbuscular mycorrhizae in the alleviation of ionic, osmotic and oxidative stresses induced by salinity in Cajanus cajan (L.) Millsp. (pigeonpea). J Agron Crop Sci 195:110–123CrossRefGoogle Scholar
  20. González L, González-Vilar M (2003) Determination of relative water content and electrolytic leakage. In: Roger MJR (ed) Handbook of Plant Ecophysiology Techniques. Springer, Dordrecht Netherlands, pp 207–212CrossRefGoogle Scholar
  21. Gough C, Galera C, Vasse J, Webster G, Cocking EC, Dénarié J (1997) Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571 10. Mol Plant Microb Interact 5:560–570CrossRefGoogle Scholar
  22. Guerzoni ME, Lanciotti R, Cocconcelli PS (2001) Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiol 147:2255–2264Google Scholar
  23. Gür A, Demirel U, Özden M, Kahraman A, Çopur O (2010) Diurnal gradual heat stress affects antioxidant enzymes, proline accumulation and some physiological components in cotton (Gossypium hirsutum L.). Af J Biotech 9:1008–1015Google Scholar
  24. Hamayun M, Khan SA, Khan AL, Rehman G, Kim YH, Iqbal I, Hussain J, Sohn WY, Lee IJ (2010) Gibberellin production and plant growth promoting from pure cultures of Cladosporiun sp. MH-6 isolated from cucumber (Cucumis sativus L.). Mycologia 102:989–995PubMedCrossRefGoogle Scholar
  25. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112PubMedCrossRefGoogle Scholar
  26. Im YJ, Ji M, Lee A, Killens R, Grunden AM, Boss WF (2009) Expression of Pyrococcus furiosus superoxide reductase in Arabidopsis enhances heat tolerance. Plant Physiol 151:893–904PubMedCrossRefGoogle Scholar
  27. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Eco 55:45–53CrossRefGoogle Scholar
  28. Janas KM, Cvikrová M, Agiewicz AP, Szafranska K, Posmyk MM (2002) Constitutive elevated accumulation of phenylpropanoids in soybean roots at low temperature. Plant Sci 163:369–373CrossRefGoogle Scholar
  29. Kang SM, Hamayun M, Joo GJ, Khan AL, Kim YH, Kim SK, Jeong HJ, Lee IJ (2010) Effect of Burkholderia sp. KCTC 11096BP on some physiochemical attributes of cucumber. Eur J Soil Biol 46:264–269CrossRefGoogle Scholar
  30. Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activites during rice leaf senescence. Plant Physiol 57:315–319PubMedCrossRefGoogle Scholar
  31. Khan AL, Hamayun M, Ahmad N, Waqas M, Kang SM, Kim YH, Lee IJ (2011a) Exophiala sp. LHL08 reprograms Cucumis sativus to higher growth under abiotic stresses. Physiol Plantarum 143:329–343CrossRefGoogle Scholar
  32. Khan AL, Hamayun M, Kim YH, Kang SM, Lee JH, Lee IJ (2011b) Gibberellins producing endophytic Aspergillus fumigatus sp. LH02 influenced endogenous phytohormonal levels, plant growth and isoflavone biosynthesis in soybean under salt stress. Process Biochem 46:440–447CrossRefGoogle Scholar
  33. Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011c) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–862PubMedCrossRefGoogle Scholar
  34. Kocsy G, Gabriella S, József S, Emil P, Gabor G (2004) Heat tolerance together with heat stress-induced changes in glutathione and hydroxymethylglutathione levels is affected by chromosome 5A of wheat. Plant Sci 166:451–458CrossRefGoogle Scholar
  35. Kohler J, Hernandez JA, Caravaca F, Roldan A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exper Bot 65:245–252CrossRefGoogle Scholar
  36. Kumazawa S, Hamasaka T, Nakayama T (2004) Antioxidant activity of propolis of various geographic origins. Food Chem 84:329–339CrossRefGoogle Scholar
  37. Lillo C, Lea US, Ruoff P (2008) Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 31:587–601PubMedCrossRefGoogle Scholar
  38. Liu TX, Zhang ZS, Wang JB, Li RQ (2009) Changes in abscisic acid immunolocalization in heat-stressed pepper seedlings. Pak J Bot 41:1173–1178Google Scholar
  39. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515PubMedCrossRefGoogle Scholar
  40. Matos T, de-Hoog GS, de Boer AG, de Crom I, Haase G (2002) High prevalence of the neurotrope Exophiala dermatitidis and related oligotrophic black yeasts in sauna facilities. Mycoses 45:373–377PubMedCrossRefGoogle Scholar
  41. Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Cur Opin Plant Bio 8:409–414CrossRefGoogle Scholar
  42. McCloud ES, Baldwin IT (1997) Herbivory and caterpillar regurgitants amplify the wound induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203:430–435CrossRefGoogle Scholar
  43. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410PubMedCrossRefGoogle Scholar
  44. Morrison MJ, Cober ER, Saleem MF, McLaughlin NB, Frégeau-Reid J, Ma BL, Woodrow L (2010) Seasonal changes in temperature and precipitation influence isoflavone concentration in short-season soybean. Field Crops Res 117:113–121CrossRefGoogle Scholar
  45. Ohkawa H, Ohishi N, Yagi K (1979) Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem 95:351–358PubMedCrossRefGoogle Scholar
  46. Oliveira LMN, Sobreira ACM, Monteiro FP, Melo DF (2010) Chill-induced changes in fatty acid composition of tonoplast vesicles from hypocotyls of Vigna unguiculata (L.) Walp. Braz J Plant Physiol 22:69–72CrossRefGoogle Scholar
  47. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:1–6CrossRefGoogle Scholar
  48. Pietta P (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–104PubMedCrossRefGoogle Scholar
  49. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398PubMedCrossRefGoogle Scholar
  50. Qi QG, Rose PA, Abrams GD, Taylor DC, Abrams SR, Cutler AJ (1998) Abscisic acid metabolism, 3-ketoacyl-coenzyme a synthase gene expression and very-long-chain monounsaturated fatty acid biosynthesis in Brassica napus embryos. Plant Physio 117:979–987CrossRefGoogle Scholar
  51. Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298:1581PubMedCrossRefGoogle Scholar
  52. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L et al (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6(7):e14823. doi: 10.1371/journal.pone.0014823 PubMedCrossRefGoogle Scholar
  53. Rijke ED, Aardenburg L, Dijk JV, Ariese F, Ernst WHO, Gooijer C, Brinkman UA (2005) Changed isoflavone levels in red clover (Trifolium pratense L.) leaves with disturbed root nodulation in response to waterlogging. J Chem Eco 31:1285–1298CrossRefGoogle Scholar
  54. Rodriguez RJ, Redman RS, Henson J (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9:261–272CrossRefGoogle Scholar
  55. Rodriguez RJ, Elizabeth JH, Marshal V, Leesa H, Beckwith LB, Kim Y, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416PubMedCrossRefGoogle Scholar
  56. Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exper Bot 69:225–232CrossRefGoogle Scholar
  57. Rydlová J, Püschel D, Sudová R, Gryndler M, Mikanová O, Vosátka M (2011) Interaction of arbuscular mycorrhizal fungi and rhizobia: effects on flax yield in spoil-bank clay J. Plant Nutr Soil Sci 174:128–134CrossRefGoogle Scholar
  58. Schulz B, Boyle C (2005) The endophytic continuum. Mycolog Res 109:661–686CrossRefGoogle Scholar
  59. Sharp ER, LeNoble ME, Else MA, Thorne ET, Gherardi F (2000) Endogenous ABA maintains shoot growth in tomato independtly of effects on plant water balance: evidence for an interaction with ethylene. J Exp Bot 51:1575–1584PubMedCrossRefGoogle Scholar
  60. Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London, pp 182–189Google Scholar
  61. Somerville C, Browse J (1991) Plant lipids, metabolism and membranes. Science 252:80–87PubMedCrossRefGoogle Scholar
  62. Subramanian S, Stacey G, Yu O (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J 48:261–273PubMedCrossRefGoogle Scholar
  63. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Env Exp Bot 61:199–223CrossRefGoogle Scholar
  64. Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, Von-Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformis indica reprograms barley to salt-stress tolerance, disease resistance and higher yield. Pro Nat Acad Sci 102:13386–13391CrossRefGoogle Scholar
  65. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond) 100:681–697CrossRefGoogle Scholar
  66. Wasternack C, Stenzel I, Hause B, Hause G, Kutter C, Maucher H, Neumerkel J, Feussner I, Miersch O (2006) The wound response in tomato-role of jasmonic acid. J Plant Physiol 163:297–306PubMedCrossRefGoogle Scholar
  67. Weber H, Chételat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to Malondialdehyde. Plant J 37:877–889PubMedCrossRefGoogle Scholar
  68. Xu S, Li J, Zhang X, Wei H, Cui L (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285CrossRefGoogle Scholar
  69. Yuan ZL, Dai CC, Chen LQ (2007) Regulation and accumulation of secondary metabolites in plant-fungus symbiotic system. Afr J Biotechnol 6:1266–1271Google Scholar
  70. Yuan Y, Liu Y, Luo Y, Huang L, Chen S, Yang Z, Qin S (2011) High temperature effects on flavones accumulation and antioxidant system in Scutellaria baicalensis Georgi cells. Af J Biotech 10:5182–5192Google Scholar
  71. Zahra P, Majid R, Amin B (2009) Seasonal changes of peroxidase, polyphenol oxidase enzyme activity and phenol content during and after rest in pistachio (Pistacia vera L.) flower buds. World App Sci J 6:1193–1199Google Scholar
  72. Zhang Z, Li R, Wang J (2001) Effects of oxalate treatment on the membrane permeability and calcium distribution in pepper leaves under heat stress. Acta Phytophysiol Sin 27:109–113Google Scholar
  73. Zhang JH, Liu YP, Pan QH, Zhan JC, Wang XQ, Huang WD (2006) Changes in membrane-associated H + -ATPase activities and amounts in young grape plants during the cross adaptation to temperature stresses. Plant Sci 170:768–777CrossRefGoogle Scholar
  74. Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Abdul Latif Khan
    • 1
    • 2
  • Muhammad Hamayun
    • 3
  • Muhammad Waqas
    • 1
  • Sang-Mo Kang
    • 1
  • Yoon-Ha Kim
    • 1
  • Duk-Hwan Kim
    • 1
  • In-Jung Lee
    • 1
  1. 1.School of Applied BiosciencesKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Department of Plant SciencesKohat University of Science & TechnologyKohatPakistan
  3. 3.Department of BotanyAbdul Wali Khan University MardanMardanPakistan

Personalised recommendations