Abstract
Sclerotinia stem rot caused by necrotrophic plant pathogenic fungus Sclerotinia sclerotiorum (Lib) de Bary is a highly pervasive disease affecting a wide range of agricultural and horticultural crops. In this study, fungal endophytes recovered from inflorescence tissues of Aloe vera L. were examined for their antagonist activity against S. sclerotiorum and the presence of plant growth-promoting traits. Fungal endophytes were characterized by microscopic and molecular (ITS rDNA sequencing) methods. Chaetomium globosum was the predominant endophytic species followed by Trichoderma harzanium in this study. Trichoderma harzanium tested positive for the presence of plant growth-promoting traits, i.e. siderophore, indole acetic acid, hydrogen cyanide production and phosphate solubilization. Chaetomium globosum strain 2 and T. harzanium survived stressful conditions (high temperature, cold stress and UV-B exposure). In antagonism assay, T. harzanium exhibited the highest growth inhibition per cent of 81.01 ± 0.63 against S. sclerotiorum and also restricted sclerotia formation. The hexane extract of T. harzanium (TH hex) obtained from solid fermentation depicted best antifungal activity against phytopathogen having an IC50 value of 3.987 mg/ml which is moderately comparable with positive control carbendazim (50%, WP). The GC–MS analysis of TH hex detected abundant presence (39.4%) of hexadecanoic acid, 2, 3-bis [(trimethylsilyl) oxy] propyl ester and other unsaturated fatty acids (palmitic and linoleic acid) having antifungal activity. The study demonstrates antifungal activity and plant growth-promoting potential of fungal endophytes residing in the inflorescence of A. vera.
Similar content being viewed by others
References
Bardin SD, Huang HC (2001) Research on biology and control of Sclerotinia diseases in Canada1. Can J Plant Pathol 23(1):88–98
Chowdhary K, Kumar A, Sharma S, Pathak R, Jangir M (2018) Ocimum sp.: source of biorational pesticides. Ind Crops Prod 122:686–701
Derbyshire MC, Denton-Giles M (2016) The control of sclerotinia stem rot on oilseed rape (Brassica napus): current practices and future opportunities. Plant Pathol 65(6):859–877
White JF, Torres MS, Johnson H, Irizarry I and Tadych M (2014) A functional view of plant microbiomes: endosymbiotic systems that enhance plant growth and survival. In: Advances in endophytic research, Springer, New Delhi, pp 425–439
Chowdhary K, Sharma S (2017) Potential of fungal endophytes in plant growth and disease management. In: Plant-microbe interactions in agro-ecological perspectives, Springer, Singapore, pp 275–290
Vassilev N, Eichler-Löbermann B, Flor-Peregrin E, Martos V, Reyes A, Vassileva M (2017) Production of a potential liquid plant bio-stimulant by immobilized Piriformospora indica in repeated-batch fermentation process. Amb Express 7(1):106
Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19(8):827–837
Passari AK, Mishra VK, Leo VV, Gupta VK, Singh BP (2016) Phytohormone production endowed with antagonistic potential and plant growth promoting abilities of culturable endophytic bacteria isolated from Clerodendrum colebrookianum Walp. Microbiol Res 193:57–73
Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS, Soltis DE, Stevens PF (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical J Linnean Soc 181(1):1–20
Maan AA, Nazir A, Khan MKI, Ahmad T, Zia R, Murid M, Abrar M (2018) The therapeutic properties and applications of aloe vera: a review. J Herb Med 12:1–10
Rosca-Casian O, Parvu M, Vlase L, Tamas M (2007) Antifungal activity of Aloe vera leaves. Fitoterapia 78(3):219–222
De Rodrıguez DJ, Hernández-Castillo D, Rodrıguez-Garcıa R, Angulo-Sánchez JL (2005) Antifungal activity in vitro of Aloe vera pulp and liquid fraction against plant pathogenic fungi. Ind Crops Prod 21(1):81–87
Bara R, Aly AH, Pretsch A, Wray V, Wang B, Proksch P, Debbab A (2013) Antibiotically active metabolites from Talaromyces wortmannii, an endophyte of Aloe vera. J Antibiotics 66(8):491
Yadav R, Singh AV, Joshi S, Kumar M (2015) Antifungal and enzyme activity of endophytic fungi isolated from Ocimum sanctum and Aloe vera. African J Microbiol Res 9(29):1783–1788
Chowdhary K, Kaushik N (2015) Fungal endophyte diversity and bioactivity in the Indian medicinal plant Ocimum sanctum Linn. PLoS ONE 10(11):141444
Zhang K, Yuan-Ying S, Cai L (2013) An optimized protocol of single spore isolation for fungi. Cryptogam Mycol 34(4):349–357
Kumar S, Kaushik N, Edrada-Ebel R, Ebel R, Proksch P (2011) Isolation, characterization, and bioactivity of endophytic fungi of Tylophora indica. World J Microbiol Biotechnol 27(3):571–577
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Kusari P, Kusari S, Spiteller M, Kayser O (2013) Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers 60(1):137–151
Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature's chemical diversity. Chem BioChem 3(7):619–627
Brustolin R, Reis EM, Pedron L (2016) Longevity of Sclerotinia sclerotiorumsclerotia on the soil surface under field conditions. Summa Phytopathol 42(2):172–174
Chowdhary K and Kaushik N (2017) Biodiversity and In vitro inhibition study of fungal endophytes of chlorophytum borivilianum against selected phytopathogens. In: Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, pp 1–9
Zhao SS, Zhang YY, Yan W, Cao LL, Xiao Y, Ye YH (2017) Chaetomium globosum CDW7, a potential biological control strain and its antifungal metabolites. Microbiol Lett 364(3):7
Potshangbam M, Devi SI, Sahoo D, Strobel GA (2017) Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Front Microbiol 8:325
Shaikh SS, Saraf MS (2017) Optimization of growth conditions For zinc solubilizing plant growth associated bacteria and fungi. J Adv Res Biotech 2(1):9
Kumar S, Kaushik N (2013) Endophytic fungi isolated from oil-seed crop Jatropha curcas produces oil and exhibit antifungal activity. PLoS ONE 8(2):e56202
Hirooka T, Ishii H (2013) Chemical control of plant diseases. J Gen Plant Pathol 79(6):390–401
Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, Ruan Y, Shen Q (2012) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49:435–446
Durán P, Acuña JJ, Jorquera MA, Azcón R, Paredes C, Rengel Z, de la Luz MM (2014) Endophytic bacteria from selenium-supplemented wheat plants could be useful for plant-growth promotion, biofortification and Gaeumannomyces graminis biocontrol in wheat production. Biol Fertil Soils 50(6):983–990
Rajeswari R, Umadevi M, Rahale CS, Pushpa R, Selvavenkadesh S, Kumar KS, Bhowmik D (2012) Aloe vera: the miracle plant its medicinal and traditional uses in India. J Pharmacogn Phytochem 1(4):118–124
He X, Han G, Lin Y, Tian X, Xiang C, Tian Q, He Z (2012) Diversity and decomposition potential of endophytes in leaves of a Cinnamomum camphora plantation in China. Ecological Res 27(2):273–284
Oh SY, Park MS, Cho HJ, Lim YW (2018) Diversity and effect of Trichoderma isolated from the roots of Pinus densiflora within the fairy ring of pine mushroom (Tricholoma matsutake). PLoS ONE 13(11):e0205900
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79(3):293–320
Pal KK, Gardener BM (2006) Biological control of plant pathogens. Plant Health Instr 2:1117–1142
Xiao Y, Li HX, Li C, Wang JX, Li J, Wang MH, Ye YH (2013) Antifungal screening of endophytic fungi from Ginkgo biloba for discovery of potent anti-phytopathogenic fungicides. FEMS Microbiol Lett 339(2):130–136
Chen JL, Sun SZ, Miao CP, Wu K, Chen YW, Xu LH, Zhao LX (2016) Endophytic Trichoderma gamsii YIM PH30019: a promising biocontrol agent with hyperosmolar, mycoparasitism, and antagonistic activities of induced volatile organic compounds on root-rot pathogenic fungi of Panax notoginseng. J Ginseng Res 40(4):315–324
Talapatra K, Das AR, Saha AK, Das P (2017) In vitro antagonistic activity of a root endophytic fungus towards plant pathogenic fungi. J Appl Biol Biotechnol 5(02):68–071
Mulaw TB, Druzhinina IS, Kubicek CP, Atanasova L (2013) Novel endophytic Trichoderma spp. isolated from healthy Coffea arabica roots are capable of controlling coffee tracheomycosis. Diversity 5(4):750–766
Metwaly AM, Kadry HA, Atef A, Mohammad AEI, Ma G, Cutler SJ, Ross SA (2014) Nigrosphaerin a a new isochromene derivative from the endophytic fungus Nigrospora sphaerica. Phytochem Lett 7:1–5
Smolińska U, Kowalska B (2018) Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum––a review. J Plant Pathol 100(1):1–12
Huang L, Li F, Liu R, Guo J, Yang Z, Bai L (2019) Antifungal activity of an endophytic strain of Phomopsis sp. on Sclerotinia sclerotiorum, the causal agent of Sclerotinia disease. J Plant Pathol 101(3):1–8
Kajula M, Tejesvi MV, Kolehmainen S, Mäkinen A, Hokkanen J, Mattila S, Pirttilä AM (2010) The siderophore ferricrocin produced by specific foliar endophytic fungi in vitro. Fungal Biol 114(2–3):248–254
Kremer RJ, Souissi T (2001) Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Current Microbiol 43(3):182–186
Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW (2013) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul 32(2):245–258
Liu FP, Liu HQ, Zhou HL, Dong ZG, Bai XH, Qiao JJ, (2014) Isolation and characterization of phosphate-solubilizing bacteria from betel nut (Areca catechu) and their effects on plant growth and phosphorus mobilization in tropical soils. Biol Fertil Soils 50(6):927–937
Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65(7):2926–2933
Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan GA, Kalluri UC (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ 36(5):909–919
Saber WI, Ghoneem KM, Rashad YM, Al-Askar AA (2017) Trichoderma harzianum WKY1: an indole acetic acid producer for growth improvement and anthracnose disease control in sorghum. Biocontrol Sci Tech 27(5):654–676
Khare E, Arora NK (2010) Effect of indole-3-acetic acid (IAA) produced by Pseudomonas aeruginosa in suppression of charcoal rot disease of chickpea. Curr Microbiol 61(1):64–68
Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17(9):10754–10773
Kuswinanti T, Syam’un E, Masniawati A, (2015) The potency of endophytic fungal isolates collected from local aromatic rice as indole acetic acid (IAA) producer. Proced Food Sci 3:96–103
El-Hasan A, Walker F, Schöne J, Buchenauer H (2009) Detection of viridiofungin A and other antifungal metabolites excreted by Trichoderma harzianum active against different plant pathogens. Eur J Plant Pathol 124(3):457–470
Vinale F, Ghisalberti EL, Sivasithamparam K, Marra R, Ritieni A, Ferracane R, Lorito M (2009) Factors affecting the production of Trichoderma harzianum secondary metabolites during the interaction with different plant pathogens. Lett Appl Microbiol 48(6):705–711
Choi NH, Jang JY, Choi GJ, Choi YH, Jang KS, Nguyen VT, Kim JC (2017) Antifungal activity of sterols and dipsacus saponins isolated from Dipsacus asper roots against phytopathogenic fungi. Pesticide Biochem Physiol 141:103–108
Ahluwalia V, Kumar J, Rana VS, Sati OP, Walia S (2015) Comparative evaluation of two Trichoderma harzianum strains for major secondary metabolite production and antifungal activity. Nat Prod Res 29(10):914–920
Altieri C, Bevilacqua A, Cardillo D, Sinigaglia M (2009) Antifungal activity of fatty acids and their monoglycerides against Fusarium spp. in a laboratory medium. Int J Food Sci Technol 44(2):242–245
Gołębiowski M, Urbanek A, Oleszczak A, Dawgul M, Kamysz W, Boguś MI, Stepnowski P (2014) The antifungal activity of fatty acids of all stages of Sarcophaga carnaria L. (Diptera: Sarcophagidae). Microbiol Res 169(4):279–286
Carvalho JM, Paixao LKOD, Dolabela MF, Marinho PSB, Marinho AMDR (2016) Phytosterols isolated from endophytic fungus Colletotrichum gloeosporioides (Melanconiaceae). Acta Amazon 46(1):69–72
Acknowledgements
One of the authors acknowledges funding from DST-NPDF Grant No. PDF/2016/000317 and infrastructural support provided by CRDT, IIT Delhi.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare non-existence of any conflict of interest to publish this manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Significance statement Endophytic Trichoderma harzanium tested positive for plant growth-promoting features. Further, it survived stressful conditions and in antagonism assay exhibited highest growth inhibition per cent of 81.01 ± 0.63 against Sclerotinia sclerotiorum.
Rights and permissions
About this article
Cite this article
Chowdhary, K., Sharma, S. Plant Growth Promotion and Biocontrol Potential of Fungal Endophytes in the Inflorescence of Aloe vera L.. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci. 90, 1045–1055 (2020). https://doi.org/10.1007/s40011-020-01173-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40011-020-01173-3