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

Biology and Fertility of Soils

Volumn 48, Issue 5, 2012, Pages 519-529

  Khan, Abdul Latif ^a,b   Hamayun, Muhammad ^c   Waqas, Muhammad ^a   Kang, Sang Mo ^a   Kim, Yoon Ha ^a   Kim, Duk Hwan ^a   Lee, In Jung ^a  

^a Kyungpook National University   (South Korea)

^b KOHAT UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Pakistan)

^c ABDUL WALI KHAN UNIVERSITY   (Pakistan)

Author keywords

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

Indexed keywords

ELECTROKINESIS; ENDOPHYTE; FUNGUS; GROWTH RATE; HIGH TEMPERATURE; HOST PLANT; OXIDATION; PHYSIOLOGICAL RESPONSE; PHYTOMASS; TEMPERATURE TOLERANCE; VINE;

CUCUMIS SATIVUS; EMBRYOPHYTA; EXOPHIALA; TRACHEOPHYTA;

EID: 84862698759     PISSN: 01782762     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00374-011-0649-y     Document Type: Article

References (74)

1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105: 121-127.
2. Almeselmani M, Deshmukh PS, Sairam RK, Kushwaha SR, Singh TP (2006) Protective role of antioxidant enzymes under high temperature stress. Plant Sci 171: 382-388.
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: 891-896.
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 254-271.
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: 501-551.
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: 729-743.
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: 257-266.
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: 336-341.
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: 4114-4119.
10. Dakora FD, Phillips DA (1996) Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Mol Plant Physiol 49: 1-20.
11. Davey MW, Stals E, Panis B, Keulemans J, Swennen RL (2005) High-throughput determination of Malondialdehyde in plant tissues. Anal Biochem 347: 201-207.
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: 345-357.
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: 1595-1602.
14. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77.
15. 2-fixing cyanobacterium Anabaena variabilis. Plant Sci 99: 9-16.
16. Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipidperoxidation products: malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186: 407-421.
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: 17.
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 1-22.
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: 110-123.
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 207-212.
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: 560-570.
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: 2255-2264.
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: 1008-1015.
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: 989-995.
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: 98-112.
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: 893-904.
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: 45-53.
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: 369-373.
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: 264-269.
30. Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activites during rice leaf senescence. Plant Physiol 57: 315-319.
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: 329-343.
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: 440-447.
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: 852-862.
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: 451-458.
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: 245-252.
36. Kumazawa S, Hamasaka T, Nakayama T (2004) Antioxidant activity of propolis of various geographic origins. Food Chem 84: 329-339.
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: 587-601.
38. Liu TX, Zhang ZS, Wang JB, Li RQ (2009) Changes in abscisic acid immunolocalization in heat-stressed pepper seedlings. Pak J Bot 41: 1173-1178.
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: 513-515.
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: 373-377.
41. Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant-pathogen interactions. Cur Opin Plant Bio 8: 409-414.
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: 430-435.
43. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
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: 113-121.
45. Ohkawa H, Ohishi N, Yagi K (1979) Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem 95: 351-358.
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: 69-72.
47. Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14: 1-6.
48. Pietta P (2000) Flavonoids as antioxidants. J Nat Prod 63: 1035-104.
49. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10: 393-398.
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: 979-987.
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: 1581.
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.
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: 1285-1298.
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: 261-272.
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: 404-416.
56. Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exper Bot 69: 225-232.
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: 128-134.
58. Schulz B, Boyle C (2005) The endophytic continuum. Mycolog Res 109: 661-686.
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: 1575-1584.
60. Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London, pp 182-189.
61. Somerville C, Browse J (1991) Plant lipids, metabolism and membranes. Science 252: 80-87.
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: 261-273.
63. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Env Exp Bot 61: 199-223.
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: 13386-13391.
65. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond) 100: 681-697.
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: 297-306.
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: 877-889.
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: 274-285.
69. Yuan ZL, Dai CC, Chen LQ (2007) Regulation and accumulation of secondary metabolites in plant-fungus symbiotic system. Afr J Biotechnol 6: 1266-1271.
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: 5182-5192.
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: 1193-1199.
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: 109-113.
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: 768-777.
74. Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61: 1959-1968.