Abstract
Sclerotium rolfsii is a necrotrophic, soil-borne pathogenic fungus responsible for serious crop losses worldwide. It is one of the major phytopathogens infecting chilli and causes yield losses ranging from 16 to 80%. Among the various approaches to manage S. rolfsii, biological control is an environmentally acceptable alternative over other chemical methods. In this study, 120 endophytic fungal isolates obtained from a medicinal plant, Nothapodytes nimmoniana were evaluated for their in vitro and in vivo antagonism towards S. rolfsii. Among these, one isolate, Alternaria sp. exhibited 46.62% inhibition against S. rolfsii in dual culture assay on PDA. The inhibition was found to be mediated by the mycotoxin, tenuazonic acid, produced by the endophyte. Pre-germinated chilli seeds treated with mycelial suspension of Alternaria sp. reduced the seedling mortality due to S. rolfsii infection. Pretreatment with the endophyte also enhanced seedling growth and biomass compared to untreated seedlings under greenhouse conditions. These results suggest that the endophytic fungus, Alternaria sp. has potential implication for use as a biocontrol against S. rolfsii as well as for promoting growth of chilli.
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Aramsirirujiwet, Y., Gumlangmak, C., & Kitpreechavanich, V. (2016). Studies on antagonistic effect against plant pathogenic fungi from Endophytic fungi isolated from Hottuynia Cordata Thunb and screening for Siderophore and indole-3-acetic acid production. Asia-Pacific Journal of Science and Technology,21(1), 55–66.
Arx, J. V. (1981). The genera of fungi sporulating in pure culture. Lehre: J. Cramer.
Bardin, S. D., & Huang, H. C. (2001). Research on biology and control of Sclerotinia diseases in Canada 1. Canadian Journal of Plant Pathology,23(1), 88–98.
Bauer, A. W., Kirby, W. M., Sherries, J. C., & Turck, M. (1966). Antibiotics susceptibility testing by the standardized single disc method. American Journal of Clinical Pathology,45, 493–496.
Bilal, L., Asaf, S., Hamayun, M., Gul, H., Iqbal, A., Ullah, I., et al. (2018). Plant growth promoting endophytic fungi Asprgillus fumigatus TS1 and Fusarium proliferatum BRL1 produce gibberellins and regulates plant endogenous hormones. Symbiosis,76(2), 117–127.
Bitas, V., McCartney, N., Li, N., Demers, J., Kim, J. E., Kim, H. S., et al. (2015). Fusarium oxysporum volatiles enhance plant growth via affecting auxin transport and signalling. Frontiers in microbiology,6, 1248.
Dall’Asta, C., Cirlini, M., & Falavigna, C. (2014). Mycotoxins from Alternaria: toxicological implications. Advances in Molecular Toxicology,8, 107–121.
Daunde, A. T., Apet, K. T., Suryawanshi, A. P., & Khandare, V. S. (2018). Prevalence of collar rot of chilli caused by Sclerotium rolfsii Sacc. Under the agro-climatic zones of Marathwada region of Maharashtra. Journal of Pharmacognosy and Phytochemistry,7(4), 1905–1908.
Dhaliwal, M. S., Yadav, A., & Jindal, S. K. (2014). Molecular characterization and diversity analysis in chilli pepper using simple sequence repeats (SSR) markers. African Journal of Biotechnology,13, 31.
Dixit, R., Agrawal, L., Singh, S. P., Singh, P. C., Prasad, V., & Chauhan, P. S. (2018). Paenibacillus lentimorbus induces autophagy for protecting tomato from Sclerotium rolfsii infection. Microbiological Research,215, 164–174.
Ellis, M. B., & Ellis, J. P. (1985). Microfungi on land plants. In An identification handbook. London: Croom Helm Ltd.
Faruk, M. I. (2019). Management of barley seedling disease caused by Sclerotium rolfsii through soil amendment with tricho-compost. European Journal of Biophysics,7(1), 1–7.
Gao, Z., Zhang, B., Liu, H., Han, J., & Zhang, Y. (2017). Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biological Control,105, 27–39.
Gotthardt, M., Asam, S., Gunkel, K., Moghaddem, A. F., Baumann, E., Kietz, R., et al. (2019). Quantitation of six Alternaria toxins in infant foods applying stable isotope labeled standards. Frontiers in Microbiology,10, 109.
Hallmann, J., Quadt-Hallmann, A., Mahaffee, W. F., & Kloepper, J. W. (1997). Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology,43(10), 895–914.
Hirpara, D. G., Gajera, H. P., Hirpara, H. Z., & Golakiya, B. A. (2017). Molecular diversity and fingerprints of Trichoderma associated with antagonistic potentials against Sclerotium rolfsii Sacc. Journal of Plant Diseases and Protection,124(1), 31–40.
Isaias, C. O., Martins, I., Silva, J. B. T. D., Silva, J. P. D., & Mello, S. C. M. D. (2014). Antagonistic action and bioactive metabolites of Trichoderma spp. against the pathogens Sclerotium rolfsii and Verticillium dahliae. Summa Phytopathologica,40(1), 34–41.
Islam, M. M., Hossain, D. M., Nonaka, M., & Harada, N. (2017). Biological control of tomato collar rot induced by Sclerotium rolfsii using Trichoderma species isolated in Bangladesh. Archives of Phytopathology and Plant Protection,50(3–4), 109–116.
Karthikeyan, V., Sankaralingam, A., & Nakkeeran, S. (2006). Biological control of groundnut stem rot caused by Sclerotium rolfsii (Sacc.). Archives of Phytopathology and Plant Protection,39(3), 239–246.
Koivunen, E. E., Tully, K. L., & Swett, C. L. (2018). Co-managing soil and plant pathogens: effects of organic amendments on soil fertility and fungal pathogen survival. Plant and Soil,432(1–2), 171–189.
Kumar, R. (2018). Assessing fungicides for seedling protection of cucumber to collar rot disease caused by Sclerotium rolfsii. International Journal of Plant Protection,11(1), 10–17.
Kumar, S., Kaushik, N., & Proksch, P. (2013). Identification of antifungal principle in the solvent extract of an endophytic fungus Chaetomium globosum from Withania somnifera. Springer Plus,2(1), 37.
Lee, S. Y., Kim, B. Y., Ahn, J. H., Song, J., Seol, Y. J., Kim, W. G., et al. (2012). Draft genome sequence of the biocontrol bacterium Bacillus amyloliquefaciens strain M27. American Society of Microbiology. https://doi.org/10.1128/JB.01835-12.
Lehner, A., Meimoun, P., Errakhi, R., Madiona, K., Barakate, M., & Bouteau, F. (2008). Toxic and signalling effects of oxalic acid: Oxalic acid—Natural born killer or natural born protector? Plant Signaling and Behavior,3(9), 746–748.
Li, N., & Kang, S. (2018). Do volatile compounds produced by Fusarium oxysporum and Verticillium dahliae affect stress tolerance in plants? Mycology,9(3), 166–175.
Meronuck, R. A., Steele, J. A., Mirocha, C. J., & Christensen, C. M. (1972). Tenuazonic Acid, a Toxin Produced by Alternaria alternata. Applied and Environment Microbiology,23, 613–617.
Mukherjee, S., David, A., Yadav, S., Baluška, F., & Bhatla, S. C. (2014). Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiologia Plantarum,152(4), 714–728.
Nandi, S., Hembaram, S., Adhikari, A., Tiwari, B. K., & Dutta, S. (2017). Host Infection beyond the traditional range of Sclerotium (Athelia) rolfsii with Physalis minima. Bioinformation,13(10), 333.
Perva-Uzunalić, A., Škerget, M., Weinreich, B., & Knez, Ž. (2004). Extraction of chilli pepper with supercritical CO2: Effect of pressure and temperature on capsaicinoid and colour extraction efficiency. Food Chemistry,87(1), 51–58.
Rahman, M. A., Begum, M. F., & Alam, M. F. (2009). Screening of Trichoderma isolates as a biological control agent against Ceratocystis paradoxa causing pineapple disease of sugarcane. Mycobiology,37(4), 277–285.
Ramesha, B. T., Amna, T., Ravikanth, G., Gunaga, R. P., Vasudeva, R., Ganeshaiah, K. N., et al. (2008). Prospecting for camptothecines from Nothapodytes nimmoniana in the Western Ghats, South India: Identification of high-yielding sources of camptothecin and new families of camptothecines. Journal of Chromatographic Science,46(4), 362–368.
Ryan, R. P., Germaine, K., Franks, A., Ryan, D. J., & Dowling, D. N. (2008). Bacterial endophytes: Recent developments and applications. FEMS Microbiology Letters,278(1), 1–9.
Sangamesh, M. B., Jambagi, S., Vasanthakumari, M. M., Shetty, N. J., Kolte, H., Ravikanth, G., et al. (2018). Thermotolerance of fungal endophytes isolated from plants adapted to the Thar Desert, India. Symbiosis,75(2), 135–147.
Saravanakumar, P., Karthikeyan, V., Patharajan, S., & Kannabiran, B. (2011). Antifungal activity of Plumbago species against anthracnose fungus Colletotrichum gloeosporidodes (Penz.) of chilli. Archives of Phytopathology and Plant Protection,44(3), 287–297.
Schulz, B., Wanke, U., Draeger, S., & Aust, H. J. (1993). Endophytes from herbaceous plants and shrubs: Effectiveness of surface sterilization methods. Mycological Research,97(12), 1447–1450.
Shweta, S., Zuehlke, S., Ramesha, B. T., Priti, V., Kumar, P. M., Ravikanth, G., et al. (2010). Endophytic fungal strains of Fusarium solani, from Apodytes dimidiata E. Mey. ex Arn (Icacinaceae) produce camptothecin, 10-hydroxycamptothecin and 9-methoxycamptothecin. Phytochemistry,71(1), 117–122.
Simmons, E.G., 2007. Alternaria: An identification manual. CBS.
Suryanarayanan, T. S. (1992). Light-incubation: A neglected procedure in mycology. Mycologist,6(3), 144.
Sutton, B. C. (1980) The Coelomycetes: Fungi imperfecti with pycnidia acervuli and stromata, (p. 696). Commonwealth mycological Institute.
Toghueo, R. M. K., Eke, P., Zabalgogeazcoa, Í., de Aldana, B. R. V., Nana, L. W., & Boyom, F. F. (2016). Biocontrol and growth enhancement potential of two endophytic Trichoderma spp. from Terminalia catappa against the causative agent of Common Bean Root Rot (Fusarium solani). Biological Control,96, 8–20.
Vainio, E. J., Korhonen, K., & Hantula, J. (1998). Genetic variation in Phlebiopsis gigsntea as detected with random amplified microsatellite (RAMS) markers. Mycological Research,102, 187–192.
Verma, V. C., Gond, S. K., Mishra, A., Kuma, R. A., & Kharwar, R. N. (2008). Selection of natural strains of fungal endophytes from Azadirachta indica A. Juss, with anti- microbial activity against dermatophytes. Current Bioactive Compounds.,4(1), 36–40.
Volpiano, C. G., Lisboa, B. B., São José, J. F. B., de Oliveira, A. M. R., Beneduzi, A., Passaglia, L. M. P., et al. (2018). Rhizobium strains in the biological control of the phytopathogenic fungi Sclerotium (Athelia) rolfsii on the common bean. Plant and Soil,432(1–2), 229–243.
Whipps, J. M. (1987). Effect of media on growth and interactions between a range of soil-borne glasshouse pathogens and antagonistic fungi. New Phytologist,107(1), 127–142.
White, T. J., Bruns, T., Lee, S. J., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols,18, 315–322.
Yun, C. S., Motoyama, T., & Osada, H. (2015). Biosynthesis of the mycotoxin tenuazonic acid by a fungal NRPS–PKS hybrid enzyme. Nature Communications,6, 8758.
Zhang, F., Yang, X., Ran, W., & Shen, Q. (2014). Fusarium oxysporum induces the production of proteins and volatile organic compounds by Trichoderma harzianum T-E5. FEMS Microbiology Letters,359(1), 116–123.
Acknowledgements
The authors acknowledge the support received from the Department of Biotechnology, Government of India, New Delhi (Chemical Ecology of the North East Region (NER) of India: A collaborative programme Linking NER and Bangalore Researchers; DBT-NER/Agri/24/2013 for carrying out this work. The authors thank the Kerala Forest Department for permission granted to collect the samples of the tree species Nothapodytes nimmoniana. R. Uma Shaanker was partially supported by grants from the ICAR Emeritus Scientist program (ICAR F.NO. 9(16)/2018-ES-HRD).
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Rajani, P., Aiswarya, H., Vasanthakumari, M.M. et al. Inhibition of the collar rot fungus, Sclerotium rolfsii Sacc. by an endophytic fungus Alternaria sp.: implications for biocontrol. Plant Physiol. Rep. 24, 521–532 (2019). https://doi.org/10.1007/s40502-019-00484-6
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DOI: https://doi.org/10.1007/s40502-019-00484-6