Abstract
Understanding how endophytic fungi mitigate abiotic stresses in plants will be important in a changing global climate. A few endophytes can produce phytohormones, but their ability to induce physiological changes in host plants during extreme environmental conditions are largely unexplored. In the present study, we investigated the ability of Penicillium resedanum LK6 to produce gibberellins and its role in improving the growth of Capsicum annuum L. under salinity, drought, and heat stresses. These effects were compared with exogenous application of gibberellic acid (GA3). Endophyte treatment significantly increased shoot length, biomass, chlorophyll content, and the photosynthesis rate compared with the uninfected control during abiotic stresses. The endophyte and combined endophyte + GA3 treatments significantly ameliorated the negative effects of stresses compared with the control. Stress-responsive endogenous abscisic acid and its encoding genes, such as zeaxanthin epoxidase, 9-cis-epoxycarotenoid dioxygenase 3, and ABA aldehyde oxidase 3, were significantly reduced in endophyte-treated plants under stress. Conversely, salicylic acid and biosynthesis-related gene (isochorismate synthase) had constitutive expressions while pathogenesis related (PR1 and PR5) genes showed attenuated responses during endophyte treatment under abiotic stresses. The present findings suggest that endophytes have effects comparable to those of exogenous GA3; both can significantly increase plant growth and yield under changing environmental conditions by reprogramming the host plant’s physiological responses.
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Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, Climent ML, Gómez-Cadenas A, Nicolás C (2009) Cross-talk between gibberellins and salicylic acid in early stress responses in Arabidopsis thaliana seeds. Plant Sig Beh 4:750–751
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
Barrero JM, Rodríguez PL, Quesada V, Piqueras P, Ponce MR, Micol JL (2006) Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress. Plant Cell Environ 29:2000–2008
Bomke C, Rojas MC, Gong F, Hedden P, Tudzynski B (2008) Isolation and characterization of the gibberellin biosynthetic gene cluster in Sphaceloma manihoticola. Appl Environ Microbiol 74:5325–5339
Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030
Cao MJ, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M, Xiang CB (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163
Ghelis T, Dellis O, Jeannette E, Dardat F, Cornel D, Miginiac E, Rona JP, Sotta B (2000) Abscisic acid specific expression of RAB18 involves activation of anion channels in Arabidopsis thaliana suspension cells. FEBS Lett 474(1):43–47
Hamayun M, Khan SA, Iqbal I, Ahmad B, Lee IJ (2010a) Isolation of a gibberellin-producing fungus (Penicillium sp. MH7) and growth promotion of crown daisy (Chrysanthemum coronarium). J Microbiol Biotechnol 20:202–207
Hamayun M, Khan SA, Khan AL, Shin JH, Lee IJ (2010b) Exogenous gibberellic acid reprograms soybean to higher growth and salt stress tolerance. J Agric Food Chem 58:7226–7232
Hamilton CE, Bauerle TL (2012) A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers 54:39–49
Harrower J, Wildermuth MC (2011) Exogenous salicylic acid treatment of Arabidopsis thaliana Col-0. NCBI Gene Expression Omnibus Accession No. GSE33402
Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110
Hossain MM, Sultana F, Kubota M, Hyakumachi M (2008) Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP16-2 and its cell free filtrate. Plant Soil 304:227–239
Iqbal M, Ashraf M (2010) Gibberellic acid mediated induction of salt tolerance in wheat plants: growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environ Exper Botany. doi:10.1016/j.envexpbot.2010.06.002
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
Jakab G, Ton J, Flors V, Zimmedi L, Metraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis Salt and Drought Stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274
Khan SA, Hamayun M, Kim YH, Kim HY, Suh SJ, Hwang SK, Kim JM, Lee IJ, Choo YS, Yoon UH, Kong WS, Lee BM, Kim JG (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:231
Khan AL, Hamayun M, Kim YH, Kang SM, Lee IJ (2011) Ameliorative symbiosis of endophyte (Penicillium funiculosum LHL06) under salt stress elevated plant growth of Glycine max L. Plant Physiol Biochem 49:852–862
Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2013a) Endophytic fungi: a source of gibberellins and crop resistance to abiotic stress. Crit Rev Biotech. doi:10.3109/07388551.2013.800018
Khan AL, Kang SM, Dakal HK, Hussain J, Adnan M, Kim JG, Lee IJ (2013b) Flavonoid and amino acid regulation in Capsicum annuum L. by endophytic fungi under different heat stress regimes. Sci Hort 155:1–7
Khan AL, Waqas M, Hamayun M, Al-Harrasi A, Al-Rawahi A, Lee IJ (2013c) Co-synergism of endophyte Penicillium resedanum LK6 with salicylic acid helped Capsicum annuum in biomass recovery and osmotic stress mitigation. BMC Microbial 13:1–13
Kusari S, Hertweck C, Spiteller M (2012) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19(7):792–798
Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60
Lee IJ, Foster K, Morgan PW (1998) Photoperiod control of gibberellin levels and flowering in sorghum. Plant Physiol 116:1003–1011
Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Curr Opin Plant Biol 8:409–414
Miransari M, Abrishamchi A, Khoshbakht K, Niknam V (2012) Plant hormones as signals in arbuscular mycorrhizal symbiosis. Crit Rev Biotechnol. doi:10.3109/07388551.2012.731684
Nicolas R, Jean-Pierre J (2008) Getting sick may help plants overcome abiotic stress. New Phytol 180:738–741
Pal M, Kovács V, Szalai G, Soós V, Ma X, Liu H, Mei H, Janda T (2014) Salicylic acid and abiotic stress responses in rice. J Agron Crop Sci 200:1–11
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Cur Opin Plant Biol 14:290–295
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:e14823. doi:10.1371/journal.pone.0014823
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
Schafer P, Pfiffi S, Voll LM, Zajic D, Chandler PM et al (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J 59:461–474
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686
Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483
Seo PJ, Lee AK, Xiang F, Park CM (2008) Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49:334–344
Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392
Shinozaki YK, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Ann Rev Plant Biol 57:781–803
Troncoso C, Gonzalez X, Bomke C, Tudzynski B, Gong F, Hedden P, Rojas MC (2010) Gibberellin biosynthesis and gibberellin oxidase activities in Fusarium sacchari, Fusarium konzum and Fusarium subglutinans strains. Phytochemistry 71:1322–1331
Tuna LA, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exper Bot 62:1–9
Tuteja N, Sopory SK (2008) Chemical signalling under abiotic stress environment in plants. Plant Signal Behav 3:525–536
Vicente MR, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and Development. J Exper Bot 62:3321–3338
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 Nat Acad Sci USA 102:13386–13391
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565
Xiong L, Zhu JK (2003) Regulation of abscisic acid biosynthesis. Plant Physiol 133:29–36
Acknowledgments
The authors are thankful to Eduardo Blumwald, University of California—Davis, for his suggestions during manuscript preparation. This work was financially supported by the Eco-Innovation Project of the Korean Government’s R & D program on Environmental Technology and Development and National Research Foundation Korea (Project # 2011-0022027).
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Khan, A.L., Waqas, M. & Lee, IJ. Resilience of Penicillium resedanum LK6 and exogenous gibberellin in improving Capsicum annuum growth under abiotic stresses. J Plant Res 128, 259–268 (2015). https://doi.org/10.1007/s10265-014-0688-1
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DOI: https://doi.org/10.1007/s10265-014-0688-1