Abstract
In the present study, 51 fungal endophytes (FEs) were isolated, purified and identified from the healthy leaf segments of ten grapevine varieties based on the spore and colony morphologies and ITS sequence information. The FEs belonged to the Ascomycota division comprising eight genera viz., Alternaria, Aspergillus, Bipolaris, Curvularia, Daldinia, Exserohilum, Fusarium and Nigrospora. The in vitro direct confrontation assay against Colletotrichum gloeosporioides revealed that six isolates viz., VR8 (70%), SB2 (83.15%), CS2 (88.42%), MN3 (88.42%), MS5 (78.94%) and MS15 (78.94%) inhibited the mycelial growth of test pathogen. The remaining 45 fungal isolates showed 20–59.9% growth inhibition of C. gloeosporioides. Indirect confrontation assay manifested that the isolates MN1 and MN4a showed 79.09% and 78.18% growth inhibition of C. gloeosporioides followed by MM4 (73.63%) and S5 (71.81%) isolates. Isolate S5 and MM4 were found to produce azulene and 1,3-Cyclopentanedione, 4,4-dimethyl as antimicrobial volatile organic compounds, respectively. The 38 FEs showed PCR amplification using internal transcribed spacer universal primers. The BLAST search revealed highest similarity with the existing sequences in the database. The phylogenetic analysis revealed the occurrence of seven distinct clusters each corresponding to single genus.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All the sequence data is available online and in the public domain (https://www.ncbi.nlm.nih.gov/).
References
Abdel-Motaal F, Kamel N, El-Zayat S, Abou-Ellail M (2020) Early blight suppression and plant growth promotion potential of the endophyte Aspergillus flavus in tomato plant. Ann Agric Sci 65:117–123. https://doi.org/10.1016/j.aoas.2020.07.001
Abou El-Soud NH, Deabes M, Abou El-Kassem L, Khalil M (2015) Chemical composition and antifungal activity of Ocimum basilicum L. essential oil. Maced J Med Sci 3:374. https://doi.org/10.3889/oamjms.2015.082
Alexopoulos CJ, Mims CW, Blackwell M (1996) Introductory mycology, 4th edn. Wiley
Ali HAM, Mohammed YH, Imad HH (2016) Determination of metabolites products by Cassia angustifolia and evaluate antimicrobial activity. J Pharmacognosy Phytother 8:25–48. https://doi.org/10.5897/JPP2015.0367
Arthur CL, Killam LM, Buchholz KD, Pawliszyn J, Berg JR (1992) Automation and optimization of solid-phase microextraction. Anal Chem 64:1960–1966. https://doi.org/10.1021/ac00041a034
Asghari G, Jalali M, Sadoughi E (2012) Antimicrobial activity and chemical composition of essential oil from the seeds of Artemisia aucheri Boiss. Jundishapur. J Nat Pharm Prod 7:11–15. https://doi.org/10.17795/jjnpp-3530
Bakshi S, Sztejnberg A, Yarden O (2001) Isolation and characterization of a cold-tolerant strain of Fusarium proliferatum, a biocontrol agent of grape downy mildew. Phytopathology 91:1062–1068. https://doi.org/10.1094/PHYTO.2001.91.11.1062
Bamisile BS, Dash CK, Akutse KS, Keppanan R, Wang L (2018) Fungal endophytes: beyond herbivore management. Front Microbiol 9:544. https://doi.org/10.3389/fmicb.2018.00544
Banani H, Roatti B, Ezzahi B, Giovannini O, Gessler G, Pertot I, Perazzolli M (2014) Characterization of resistance mechanisms activated by Trichoderma harzianum T39 and benzothiadiazole to downy mildew in different grapevine cultivars. Plant Pathol 63:334–343. https://doi.org/10.1111/ppa.12089
Burruano S, Alfonzo A, Lo Piccolo S, Conigliaro G, Mondello V, Torta L, Moretti M, Assante G (2008) Interaction between Acremonium byssoides and Plasmopara viticola in Vitis vinifera. Phytopathol Mediterr 47:122–131. https://doi.org/10.14601/Phytopathol_Mediterr-2615
Chaves FC, Gianfagna TJ, Aneja M, Posada F, Peterson SW, Vega FE (2012) Aspergillus oryzae NRRL 35191 from coffee, a non-toxigenic endophyte with the ability to synthesize kojic acid. Mycol Prog 11:263–267. https://doi.org/10.1007/s11557-011-0745-2
Cheong SL, Cheow YL, Ting ASY (2017) Characterizing antagonistic activities and host compatibility (via simple endophyte-calli test) of endophytes as biocontrol agents of Ganoderma boninense. Biol Control 105:86–92. https://doi.org/10.1016/j.biocontrol.2016.12.002
Chowdappa P, Reddy GS, Kumar A, Rao BM, Rawal RD (2009) Morphological and molecular characterisation of Colletotrichum spp. causing anthracnose disease of grapes. Asian Australas J Plant Sci Biotechnol 3:71–77
Ciccarese F, Longo O, Ambrico A, Schiavone D, Ziadi T (2008) Use of Aphanocladium album (isolate Mx-95) in the control of pre-and postharvest grape rot diseases. Atti Gior Fitopatolog 27–29 marzo, 2006:443–448. https://doi.org/10.3390/su14052693
Cole RJ, Schweikert MA, Jarvis BB (2003) Handbook of secondary fungal metabolites, vol 3. Gulf Professional Publishing
Cordero P, Principe A, Jofre E, Mori G, Fischer S (2014) Inhibition of the phytopathogenic fungus Fusarium proliferatum by volatile compounds produced by Pseudomonas. Arch Microbiol 196:803–809. https://doi.org/10.1007/s00203-014-1019-6
D’Alessandro MARCO, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J, Turlings TC (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 3:813–826. https://doi.org/10.1111/pce.12220
Dennis C, Webster J (1971) Antagonistic properties of species-groups of Trichoderma: II. Production of volatile antibiotics. Trans Br Mycol Soc 57:41–48. https://doi.org/10.1016/S0007-1536(71)80077-3
Elmer PAG, Reglinski T (2006) Biosuppression of Botrytis cinerea in grapes. Plant Pathol 55:155–177. https://doi.org/10.1111/j.1365-3059.2006.01348.x
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Firakova S, Sturdikova M, Mukkova M (2007) Bioactive secondary metabolites produced by microorganisms associated with plants. Biologia 62:251–257. https://doi.org/10.2478/s11756-007-0044-1
Gao FK, Dai CC, Liu XZ (2010) Mechanisms of fungal endophytes in plant protection against pathogens. Afr J Microbiol Res 4:1346–1351
Gao H, Li P, Xu X, Zeng Q, Guan W (2018) Research on volatile organic compounds from Bacillus subtilis CF-3: biocontrol effects on fruit fungal pathogens and dynamic changes during fermentation. Front Microbiol 9:456. https://doi.org/10.3389/fmicb.2018.00456
Ghosh S, Bhagwat T, Webster TJ (2021) Endophytic microbiomes and their plant growth-promoting attributes for plant health. In: Yadav AN, Singh J, Singh C, Yadav N (eds) Current trends in microbial biotechnology for sustainable agriculture. Springer, Singapore, pp 245–278
Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley, p 680
Gonzalez V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42. https://doi.org/10.1007/s13225-010-0073-x
Guarro J, Gene J, Stchigel AM (1999) Developments in fungal taxonomy. Clin Microbiol Rev 12(3):454–500. https://doi.org/10.1128/CMR.12.3.454
Guevara-Avendano E, Bejarano-Bolivar AA, Kiel-Martinez AL, Ramirez-Vazquez M, Mendez-Bravo A, von Wobeser EA, Sanchez-Rangel D, Guerrero-Analco JA, Eskalen A, Reverchon F (2019) Avocado rhizobacteria emit volatile organic compounds with antifungal activity against Fusarium solani, Fusarium sp. associated with Kuroshio shot hole borer, and Colletotrichum gloeosporioides. Microbiol Res 219:74–83. https://doi.org/10.1016/j.micres.2018.11.009
Hassan SRU, Strobel GA, Geary B, Sears J (2013) An endophytic Nodulisporium sp. from Central America producing volatile organic compounds with both biological and fuel potential. J Microbiol Biotechnol 23:29–35. https://doi.org/10.4014/jmb.1208.04062
Herrera JM, Pizzolitto RP, Zunino MP, Dambolena JS, Zygadlo JA (2015) Effect of fungal volatile organic compounds on a fungus and an insect that damage stored maize. J Stored Prod Res 62:74–80. https://doi.org/10.1016/j.jspr.2015.04.006
Huang R, Li GQ, Zhang J, Yang L, Che HJ, Jiang DH, Huang HC (2011) Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101:859–869. https://doi.org/10.1094/PHYTO-09-10-0255
Jayant KK, Vijayakumar BS (2021) In-vitro Anti-oxidant and anti-diabetic potential of endophytic fungi associated with Ficus religiosa. Ital J Mycol 50:10–20. https://doi.org/10.6092/issn.2531-7342/12104
Jia M, Chen L, Xin HL, Zheng CJ, Rahman K, Han T, Qin LP (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906. https://doi.org/10.3389/fmicb.2016.00906
Joshi D, Gupta J, Mishra A, Upadhyay M, Holkar SK, Singh P (2019) Distribution, composition and bioactivity of endophytic Trichoderma spp. associated with sugarcane. Proc Nat Acad Sci India B-Biol Sci 89:1189–1200. https://doi.org/10.1007/s40011-018-1036-3
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151. https://doi.org/10.3389/fpls.2015.00151
Karimi N, Salimikia I, Ramak P, Soheilikhah Z, Shamizadeh M, Gholivand MB (2016) Chemical composition, antioxidant and antimicrobial activities of essential oil from Leutea kurdistanica mozaff. Herb Med J 5:47–52. https://doi.org/10.22087/hmj.v1i1.564
Karthick P, Mohanraju R (2018) Antimicrobial potential of epiphytic bacteria associated with seaweeds of Little Andaman, India. Front Microbiol 9:611. https://doi.org/10.3389/fmicb.2018.00611
Khan IH, Javaid A (2020) In vitro biocontrol potential of Trichoderma pseudokoningii against Macrophomina phaseolina. Int J Agric Biol 24:730–736. https://doi.org/10.17957/IJAB/15.1494
Khan IH, Javaid A (2021) In vitro screening of Aspergillus spp. for their biocontrol potential against Macrophomina phaseolina. J Plant Pathol 103:1195–1205. https://doi.org/10.1007/s42161-021-00865-7
Khan IH, Javaid A (2022a) Biocontrol Aspergillus species together with plant biomass alter histochemical characteristics in diseased mungbean plants. Microsc Res Tech 85:2953–2964. https://doi.org/10.1002/jemt.24145
Khan IH, Javaid A (2022) Antagonistic activity of Aspergillus versicolor against Macrophomina phaseolina. Braz J Microbiol 53:1613–1621. https://doi.org/10.1007/s42770-022-00782-6
Khan IH, Javaid A (2022c) DNA cleavage of the fungal pathogen and production of antifungal compounds are the possible mechanisms of action of biocontrol agent Penicillium italicum against Macrophomina phaseolina. Mycologia 114:24–34. https://doi.org/10.1080/00275514.2021.1990627
Khan IH, Javaid A, Ahmed D (2021) Trichoderma viride controls Macrophomina phaseolina through its DNA disintegration and production of antifungal compounds. Int J Agric Biol 25:888–894. https://doi.org/10.17957/IJAB/15.1743
Khiralla A, Spina R, Saliba S, Laurain-Mattar D (2019) Diversity of natural products of the genera Curvularia and Bipolaris. Fungal Biol Rev 33:101–122. https://doi.org/10.1016/j.fbr.2018.09.002
Khruengsai S, Pripdeevech P, Tanapichatsakul C, Srisuwannapa C, D’Souza PE, Panuwet P (2021) Antifungal properties of volatile organic compounds produced by Daldinia eschscholtzii MFLUCC 19–0493 isolated from Barleria prionitis leaves against Colletotrichum acutatum and its post-harvest infections on strawberry fruits. Peer J 9:11242. https://doi.org/10.7717/peerj.11242
Kortekamp A (1997) Epicoccum nigrum LINK: a biological control agent of Plasmopara viticola (BERK. et CURT.). Vitis 36:215–216
Krishnaveni M, Kalaivani M, Banu CR, Kumari GK (2015) GC-MS/MS study of Parthenium hysterophorus L (N. Am) stem, antimicrobial activity. Res J Pharm Technol 8:517. https://doi.org/10.5958/0974-360X.2015.00086.4
Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71. https://doi.org/10.1016/j.biocontrol.2008.01.023
Kulisova M, Vrublevskaya M, Lovecka P, Vrchotova B, Stranska M, Kolarik M, Kolouchova I (2021) Fungal endophytes of Vitis vinifera-plant growth promotion factors. Agriculture 11:1250. https://doi.org/10.3390/agriculture11121250
Kumar S, Thind TS, Mohan C (1994) Occurrence of Gloeosporium ampelophagum and Colletotrichum gloeosporioides, the incitants of grape anthracnose, during different months in Punjab. Plant Dis Res 9:222–224
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Limsuwan S, Trip EN, Kouwen TR, Piersma S, Hiranrat A, Mahabusarakam W, Voravuthikunchai SP, van Dijl JM, Kayser O (2009) Rhodomyrtone: a new candidate as natural antibacterial drug from Rhodomyrtus tomentosa. Phytomedicine 16:645–651. https://doi.org/10.1016/j.phymed.2009.01.010
Liu Y, Nan L, Liu J, Yan H, Zhang D, Han X (2016) Isolation and identification of resveratrol-producing endophytes from wine grape Cabernet Sauvignon. SpringerPlus 5:1–13. https://doi.org/10.1186/s40064-016-2571-0
Liu Z, Zhao JY, Sun SF, Li Y, Qu J, Liu HT, Liu YB (2019) Sesquiterpenes from an endophytic Aspergillus flavus. J Nat Prod 82:1063–1071. https://doi.org/10.1021/acs.Jnatprod.8b01084
Ma YM, Ma CC, Li T, Wang J (2016) A new furan derivative from an endophytic Aspergillus flavus of Cephalotaxus fortunei. Nat Prod Res 30:79–84. https://doi.org/10.1080/14786419.2015.1038262
Magan N, Lacey J (1984) Effect of water activity, temperature and substrate on interactions between field and storage fungi. Trans Br Mycol Soc 82:83–93. https://doi.org/10.1016/S0007-1536(84)80214-4
Mao LJ, Chen JJ, Xia CY, Feng XX, Kong DD, Qi ZY, Liu F, Chen D, Lin FC, Zhang CL (2019) Identification and characterization of new Muscodor endophytes from gramineous plants in Xishuangbanna, China. Microbiology 8:e00666. https://doi.org/10.1002/mbo3.666
Mariappan VN, Pooja VS, Prabhu Dass Batvari B, Indirani R (2017) Grape cultivation and management approaches by geospatial tools-A review. J Adv Res GeoSci Rem Sens 4:17–28
Mehmood A, Hussain A, Irshad M, Hamayun M, Iqbal A, Khan N (2019) In vitro production of IAA by endophytic fungus Aspergillus awamori and its growth promoting activities in Zea mays. Symbiosis 77:225–235. https://doi.org/10.1007/s13199-018-0583-y
Mendez-Bravo A, Cortazar-Murillo EM, Guevara-Avendano E, Ceballos-Luna O, Rodriguez-Haas B, Kiel-Martinez AL (2018) Plant growth-promoting rhizobacteria associated with avocado display antagonistic activity against Phytophthora cinnamomi through volatile emissions. PLoS One 13:0194665. https://doi.org/10.1371/journal.pone.0194665
Mends MT, Yu E, Strobel GA, Hassan SRU, Booth E, Geary B (2012) An endophytic Nodulisporium sp. producing volatile organic compounds having bioactivity and fuel potential. J Pet Environ Biotechnol 8:349–353. https://doi.org/10.4172/2157-7463.1000117
Mercier J, Jimenez JI (2004) Control of fungal decay of apples and peaches by the biofumigant fungus Muscodor albus. Postharvest Biol Technol 31:1–8. https://doi.org/10.1016/j.postharvbio.2003.08.004
Mirica II (1998) Anthracnose. In: Pearson RC, Goheen AC (eds) Compendium of grape diseases. American Phytopathological Society, St. Paul, pp 18–19
Mishra Y, Singh A, Batra A, Sharma MM (2014) Understanding the biodiversity and biological applications of endophytic fungi: a review. J Microb Biochem Technol 8:4. https://doi.org/10.4172/1948-5948.S8-004
Mitchell AM, Strobel GA, Moore E, Robison R, Sears J (2009) Volatile antimicrobials from Muscodor crispans, a novel endophytic fungus. Microbiology 156:270–277. https://doi.org/10.1099/mic.0.032540-0
Mo EK, Sung CK (2007) Phenylethyl alcohol (PEA) application slows fungal growth and maintains aroma in strawberry. Postharvest Biol Technol 45:234–239. https://doi.org/10.1016/j.postharvbio.2007.02.005
Mookherjee A, Bera P, Mitra A, Maiti MK (2018) Characterization and synergistic effect of antifungal volatile organic compounds emitted by the Geotrichum candidum PF005, an endophytic fungus from the eggplant. Microb Ecol 75:647–661. https://doi.org/10.1007/s00248-017-1065-0
Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83. https://doi.org/10.1016/j.fbr.2012.07.001
Mukherjee K, Sen B (1998) Biological control of Fusarium wilt of muskmelon by formulations of Aspergillus niger. Israel J Plant Sci 46:67–72. https://doi.org/10.1080/07929978.1998.10676710
Musetti R, Vecchione A, Stringher L, Borselli S, Zulini L, Marzani C, D’Ambrosio M, Di Toppi LS, Pertot I (2006) Inhibition of sporulation and ultrastructural alterations of grapevine downy mildew by the endophytic fungus Alternaria alternata. Phytopathology 96:689–698. https://doi.org/10.1094/PHYTO-96-0689
NHB (2020–21) National Horticulture Board, Govt. of India, 1st advance estimates
Oldenburg KR, Vo KT, Ruhland B, Schatz PJ, Yuan Z (1996) A dual culture assay for detection of antimicrobial activity. J Biomol Screen 1:123–130. https://doi.org/10.1177/108705719600100305
Ortiz A, Orduz S (2001) In vitro evaluation of Trichoderma and Gliocladium antagonism against the symbiotic fungus of the leaf-cutting ant Atta cephalotes. Mycopathologia 150:53–60. https://doi.org/10.1023/A:1010843413085
Pandey A, Banerjee D (2014) Daldinia bambusicola Ch4/11 an endophytic fungus producing volatile organic compounds having antimicrobial and olio chemical potential. J Adv Microbiol 1:330–337
Parthasarathy R, Shanmuganathan R, Pugazhendhi A (2020) Vinblastine production by the endophytic fungus Curvularia verruculosa from the leaves of Catharanthus roseus and it’s in vitro cytotoxicity against HeLa cell line. Anal Biochem 593:113530. https://doi.org/10.1016/j.ab.2019.113530
Patil MP, Patil RH, Maheshwari VL (2015) Biological activities and identification of bioactive metabolite from endophytic Aspergillus flavus L7 isolated from Aegle marmelos. Curr Microbiol 71:39–48. https://doi.org/10.1007/s00284-015-0805-y
Ray P, Chowdhury S (2015) Popularizing grape cultivation and wine production in India–challenges and opportunities. Int J Soc Sci 4:9–28. https://doi.org/10.5958/2321-5771.2015.00002.2
Rodrigo S, Garcia-Latorre C, Santamaria O (2022) Metabolites produced by fungi against fungal phytopathogens: review, implementation and perspectives. Plants 11:81. https://doi.org/10.3390/plants11010081
Roy S, Banerjee D (2019) Volatile organic compounds from endophytic fungi. Recent advancement in white biotechnology through fungi. Springer, Cham, pp 149–175. https://doi.org/10.1007/978-3-030-14846-1_5
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sanchez-Ortiz BL, Sanchez-Fernandez RE, Duarte G, Lappe-Oliveras P, Macias-Rubalcava ML (2016) Antifungal, anti-oomycete and phytotoxic effects of volatile organic compounds from the endophytic fungus Xylaria sp. strain PB 3f3 isolated from Haematoxylon brasiletto. J Appl Microbiol 120:1313–1325. https://doi.org/10.1111/jam.13101
Sawant IS, Narkar SP, Shetty DS, Upadhyay A, Sawant SD (2012) Emergence of Colletotrichum gloeosporioides sensu lat o as the dominant pathogen of anthracnose disease of grapes in India as evidenced by cultural, morphological and molecular data. Australas Plant Pathol 41:493–504. https://doi.org/10.1007/s13313-012-0143-5
Sheron OP, Tonk DS, Kaushik LS, Hasija RC, Pannu RS (1998) Statistical software package for agricultural research workers. In: Hooda DS, Hasija RC (eds) recent advances in information theory, statistics and computer applications by department of mathematics statistics. CCS-HAU, Hisar, pp 139–143
Singh SK, Strobel GA, Knighton B, Geary B, Sears J, Ezra D (2011) An endophytic Phomopsis sp. possessing bioactivity and fuel potential with its volatile organic compounds. Microb Ecol 61:729–739. https://doi.org/10.1007/s00248-011-9818-7
Strobel G (2018) The emergence of endophytic microbes and their biological promise. J Fungi 4:57. https://doi.org/10.3390/jof4020057
Swindell SR, Plasterer TN (1997) Seqman. Sequence data analysis guidebook. Springer, Totowa, pp 75–89. https://doi.org/10.1385/0-89603-358-9:75
Szegedi E, Civerolo EL (2011) Bacterial diseases of grapevine. Int J Hortic Sci 17:45–49. https://doi.org/10.31421/IJHS/17/3/956
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Nat Acad Sci 101:11030–11035. https://doi.org/10.1073/pnas.0404206101
Thangaraj P, Subbiah KA, Uthandi S, Amirtham D (2021) Antifungal volatiles from macrobasidiomycetes inhibits Fusarium oxysporum f. sp. lycopersici. Madras Agric J 108:1. https://doi.org/10.29321/MAJ.10.000476
Thind TS, Arora JK, Mohan C, Raj P (2004) Epidemiology of powdery mildew, downy mildew and anthracnose diseases of grapevine. Dis Fruits and Veg I:621–638. https://doi.org/10.1007/1-4020-2606-414
Tripathi S, Kamal S, Sheramati I, Oelmuller R, Varma A (2008) Mycorrhizal fungi and other root endophytes as biocontrol agents against root pathogens. Mycorrhiza. Springer, Heidelberg, pp 281–306. https://doi.org/10.1007/978-3-540-78826-314
Vyas P, Bansal A (2018) Fungal endophytes: role in sustainable agriculture. Fungi and their role in sustainable development: current perspectives. Springer, Singapore, pp 107–120. https://doi.org/10.1007/978-981-13-0393-7_7
Wati L (2017) Role of endophytes in agriculture. Chem Sci Rev Lett 6:2397–2407
Wheatley R, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. inhibitory to wood decay fungi. Int Biodeterior Biodegradation 39:199–205. https://doi.org/10.1016/S0964-8305(97)00015-2
Wheeler KA, Hocking AD (1993) Interactions among xerophilic fungi associated with dried salted fish. J Appl Microbiol 74:164–169
White TJ, Bruns T, Lee SJWT, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications, vol 18. Academic Press, San Diego, pp 315–322
Wijekoon C, Quill Z (2021) Fungal endophyte diversity in table grapes. Can J Microbiol 67:29–36. https://doi.org/10.1139/cjm-2020-0293
Woo SL, Ruocco M, Vinale F, Nigro M, Lorito M (2014) Trichoderma-based products and their widespread use in agriculture. Open Mycol J 8:71–126. https://doi.org/10.2174/1874437001408010071
Wu YY, Zhang TY, Zhang MY, Cheng J, Zhang YX (2018) An endophytic fungi of Ginkgo biloba L. produces antimicrobial metabolites as potential inhibitors of FtsZ of Staphylococcus aureus. Fitoterapia 128:265–271. https://doi.org/10.1016/j.fitote.2018.05.033
Xie J, Wu YY, Zhang TY, Zhang MY, Peng F, Lin B, Zhang YX (2018) New antimicrobial compounds produced by endophytic Penicillium janthinellum isolated from Panax notoginseng as potential inhibitors of FtsZ. Fitoterapia 131:35–43. https://doi.org/10.1016/j.fitote.2018.10.006
Xing M, Zheng L, Deng Y, Xu D, Xi P, Li M, Kong G, Jiang Z (2018) Antifungal activity of natural volatile organic compounds against litchi downy blight pathogen Peronophythora litchii. Molecules 23:358. https://doi.org/10.3390/molecules23020358
Yan DH, Song X, Li H, Luo T, Dou G, Strobel G (2018) Antifungal activities of volatile secondary metabolites of four Diaporthe strains isolated from Catharanthus roseus. J Fungus 4:65. https://doi.org/10.3390/jof4020065
Yao YQ, Lan F, Qiao YM, Wei JG, Huang RS, Li LB (2017) Endophytic fungi harbored in the root of Sophora tonkinensis Gapnep: diversity and biocontrol potential against phytopathogens. Microbiol Open 6:00437. https://doi.org/10.1002/mbo3.437
Yeh CC, Wang CJ, Chen YJ, Tsai SH, Chung WH (2021) Potential of a volatile-producing endophytic fungus Nodulisporium sp. PDL-005 for the control of Penicillium digitatum. Biol Control 152:04459. https://doi.org/10.1016/j.biocontrol.2020.104459
Zahavi T, Cohen L, Weiss B, Schena L, Daus A, Kaplunov T, Zutkhi J, Ben-Arie R, Droby S (2000) Biological control of Botrytis, Aspergillus and Rhizopus rots on table and wine grapes in Israel. Postharvest Biol Technol 20:115–124. https://doi.org/10.1016/S0925-5214(00)00118-6
Zhang Q, Yang L, Zhang J, Wu M, Chen W, Jiang D, Li G (2015) Production of anti-fungal volatiles by non-pathogenic Fusarium oxysporum and its efficacy in suppression of Verticillium wilt of cotton. Plant Soil 392:101–114. https://doi.org/10.1007/s11104-015-2448-y
Zhang HY, Gao Y, Lai PX (2017) Chemical composition, antioxidant, antimicrobial and cytotoxic activities of essential oil from Premna microphylla Turczaninow. Molecules 22:381. https://doi.org/10.3390/molecules22030381
Acknowledgements
All the authors highly acknowledge the support provided by the Director, ICAR-National Research Centre, Pune to carry out the proposed research work.
Author information
Authors and Affiliations
Contributions
SKH: conceived idea and formulated the experiments, constructed phylogenetic tree, drafted and reviewed the manuscript, PSG: isolated, characterized, and evaluated the fungal endophytes in vitro, prepared figures and tables, analyzed sequence information VCB: purified and partially characterized the isolates, TL: generated ITS sequence information and reviewed the manuscript, SAS: maintained the pure culture isolates and isolated the genomic DNA of fungal endophytes, HM: formatting, statistical analysis, ASTP: identified VOCs from fungal endophytes and reviewed manuscript, SS: critically reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare that they have no conflict of interest in the publication.
Supplementary Information
Below is the link to the electronic supplementary material.
13205_2023_3675_MOESM1_ESM.docx
Supplementary file1 (DOCX 7686 KB) Microscopic observation of fungal endophytes isolated from leaf samples of ten grapevine genotypes cultivated at experimental fields of ICAR-National Research Centre for Grapes, Pune. All fungal endophyte species were observed under compound microscope at 100x resolution (Leica DM 750) stained with cotton blue. Shape of conidia and type of conidiophores were observed and recorded. CS: Cabernet Sauvignon, C: Crimson Seedless, MM: Manjari Medika, MN: Manjari Naveen, MS: Manjari Shyama, RG: Red Globe, SB: Sauvignon Blanc, S: Shiraz, T: Thompson Seedless, VR: Vitis rotundifolia
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Holkar, S.K., Ghotgalkar, P.S., Lodha, T.D. et al. Biocontrol potential of endophytic fungi originated from grapevine leaves for management of anthracnose disease caused by Colletotrichum gloeosporioides. 3 Biotech 13, 258 (2023). https://doi.org/10.1007/s13205-023-03675-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03675-z