Skip to main content
Log in

Mutualistic association of Paecilomyces formosus LHL10 offers thermotolerance to Cucumis sativus

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

We investigated in this study the influence of an endophytic fungus, Paecilomyces formosus LHL10, on the thermotolerance of cucumber (Cucumis sativus) upon exposure to high (38°C) and low (8°C) temperature stresses. The results showed that endophyte-inoculated plants had significantly higher plant growth attributes under high-temperature stress. However, they were either low or insignificant in non-inoculated control and inoculated plants with 8°C treatments. Lower stress-promulgated water deficit and cellular membrane damage were observed in endophyte-treated plants after 38°C treatment than in control plants under 8°C stress. Total polyphenol, reduced glutathione, and lipid peroxidation activities were reduced in endophyte-associated plants after exposure to 38°C as compared with control and 8°C-treated plants. The concentration of saturated fatty acids (palmitic-C16:0; stearic-C18:0) was lower in endophyte-treated plants with or without low-temperature stress, but after 8°C treatment increased compared with controls. Unsaturated fatty acids (oleic-C18:1; linoleic-C18:2; linolenic-C18:3 acids) were similar at normal conditions; however, at 38°C, C18:2 and C18:3 were decreased, and C18:1 was increased in endophyte-treated plants compared with controls, while the inverse relationship was found at 8°C. Low levels of abscisic acid in P. formosus-associated plants after 38°C treatments revealed stress tolerance compared with control and 8°C-treated plants. In contrast, salicylic acid was pronounced in endophyte-treated plants after low-temperature stress as compared to other treatments. The results provide evidence that the response to P. formosus association was beneficial at normal growth temperature and had varying effects in response to temperature stress.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Alonso-Ramirez A, Rodriguez D, Reyes D, Jimenez JA, Nicolas G, Lopez-Climent M et al (2009) Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol 150:1335–1344

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Carson WF, Schnitzer SA (eds) Tropical forest community ecology. Wiley, Oxford, pp 254–271

    Google Scholar 

  • Auge′ RM (2004) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Google Scholar 

  • Bouton JH, Gates RN, Belesky DP, Owsley M (1993) Yield and persistence of tall fescue in the southeastern coastal plain after removal of its endophyte. Agron J 85:52–55

    Article  Google Scholar 

  • Chandanie WA, Kubota M, Hyakumachi M (2009) 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.). Appl Soil Ecol 41:336–341

    Article  Google Scholar 

  • Cheruiyot E, Mumera KLM, Netich WK, Hassanali A, Wachira F (2007) Polyphenols as potential indicators for drought tolerance in tea (Camellia sinensis L.). Biosci Biotechnol Biochem 71:2190–2197

    Article  PubMed  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  PubMed  CAS  Google Scholar 

  • 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 99:9–16

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Farooq S, Azam F (2006) The use of cell membrane stability (CMS) technique to screen for salt tolerant wheat varieties. J Plant Physiol 163:629–637

    Article  PubMed  CAS  Google Scholar 

  • Gadallah MAA (2000) Effects of indole-3-acetic acid and zinc on the growth, osmotic potential and soluble carbon and nitrogen components of soybean plants growing under water deficit. J Arid Environ 44:451–467

    Article  Google Scholar 

  • 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, Berlin, pp 1–22

    Chapter  Google Scholar 

  • González L, González-Vilar M (2003) Determination of relative water content and electrolytic leakage. In: Roger MJR (ed) Handbook of plant ecophysiology techniques. Springer, Netherlands, pp 207–212

    Chapter  Google Scholar 

  • Grover A, Agarwal M, Katiyar-Argarwal S, Sahi C, Argarwal S (2000) Production of high temperature tolerant transgenic plants through manipulation of membrane lipids. Curr Sci 79:5

    Google Scholar 

  • 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. Microbiology 147:2255–2264

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hashizume Y, Fakuda K, Sahashi N (2010) Effect of summer temperature on fungal endophyte assemblage in Japanses beech leaves in pure beech stand. Botany 88:266–274

    Article  CAS  Google Scholar 

  • 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 Ecol 55:45–53

    Article  PubMed  Google Scholar 

  • Khan AL, Hamayun M, Kim YH, Kang SM, Lee JH, Lee IJ (2011a) 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

    Article  CAS  Google Scholar 

  • Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011b) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of glycine max L. Plant Physiol Biochem 49:852–861

    Google Scholar 

  • Koch JR, Creelman RA, Eshita SM, Seskar M, Mullet J, Davis KR (2000) Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid: the role of programmed cell death in lesion formation. Plant Physiol 123:487–496

    Article  PubMed  CAS  Google Scholar 

  • Kocsy G, Gabriella S, J′ozsef 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

    Article  CAS  Google Scholar 

  • 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 Exp Bot 65:245–252

    Article  CAS  Google Scholar 

  • Kumazawa S, Hamasaka T, Nakayama T (2004) Antioxidant activity of propolis of various geographic origins. Food Chem 84:329–339

    Article  CAS  Google Scholar 

  • Liu TX, Zhang ZS, Wang JB, Li RQ (2009) Changes in abscisic acid immunolocalization in heat-stressed pepper seedlings. Pak J Bot 41(3):1173–1178

    CAS  Google Scholar 

  • Maestri E, Klueva N, Perrotta C, Gulli M, Nguyen HT, Marmiroli N (2002) Molecular genetics of heat tolerance and heat shock proteins in cereals. Plant Mol Biol 48:667–681

    Article  PubMed  CAS  Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Curr Opin Plant Biol 8:409–414

    Article  PubMed  CAS  Google Scholar 

  • Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K (2000) Trienoic fatty acids and plant tolerance of high temperature. Science 287:476

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay of lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  PubMed  CAS  Google Scholar 

  • 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(1):69–72

    Article  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:1–6

    Article  Google Scholar 

  • Pieckova′ E, Samson RA (2000) Heat resistance of Paecilomyces variotii in sauce and juice. J Ind Microbiol Biotechnol 24:227–230

    Article  Google Scholar 

  • Pietikainen J, Pettersson M, Baath E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiol Ecol 52:49–58

    Article  PubMed  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • 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 Physiol 117:979–987

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Richardson AE, Barea J, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330

    Article  PubMed  CAS  Google Scholar 

  • Ruelland E, Zachowski A (2010) How plant sense temperature. Environ Exp Bot 69:225–232

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Samson RA, Houbraken J, Varga J, Frisvad JC (2009) Polyphasic taxonomy of the heat resistant ascomycete genus Byssochlamys and its Paecilomyces anamorphs. Persoonia 22:14–27

    Article  PubMed  CAS  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Smith S, Read D (2008) Mycorrhizal symbiosis. Academic Press, Newyork, pp 182–189

    Google Scholar 

  • Somerville C, Browse J (1991) Plant lipids, metabolism and membranes. Science 252:80–87

    Article  PubMed  CAS  Google Scholar 

  • Sullivan CY (1971) The techniques for measuring plant drought stress. In: Larson KL, Epstain JD (eds) Drought Injury and resistance in crops. Crop Science Society of America, Madison, pp 1–18

    Google Scholar 

  • Talanova VV, Titov AF (1994) Endogenous abscisic acid content in cucumber leaves under the influence of unfavourable temperatures and salinity. J Exp Bot 45(7):1031–1033

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • 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. Proc Natl Acad Sci USA 102:13386–13391

    Article  PubMed  CAS  Google Scholar 

  • Wang Li-Jun, Li Shao-Hua (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2 + homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694

    Article  CAS  Google Scholar 

  • Wang Y, Mopper S, Hasenstein KH (2001) Effects of salinity on endogenous ABA, IAA, JA, and SA in Iris hexagon. J Chem Ecol 27:327–342

    Article  PubMed  CAS  Google Scholar 

  • Weber H, Chetelat A, Reymond P, Farmer EE (2004) Selective and powerful stressgeneexpression in Arabidopsis inresponse to malondialdehyde. Plant J 37:877–888

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Yuan ZL, Dai CC, Chen LQ (2007) Regulation and accumulation of secondary metabolites in plant-fungus symbiotic system. Afr J Biotechnol 6:1266–1271

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research study was funded by the Eco-Innovation Project, Korean Government’s R & D program on Environmental Technology and Development and Brain Korea 21 Project, Republic of Korea.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to In-Jung Lee.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khan, A.L., Hamayun, M., Radhakrishnan, R. et al. Mutualistic association of Paecilomyces formosus LHL10 offers thermotolerance to Cucumis sativus . Antonie van Leeuwenhoek 101, 267–279 (2012). https://doi.org/10.1007/s10482-011-9630-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-011-9630-x

Keywords

Navigation