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Induction of systemic resistance in grapevines against powdery mildew by Trichoderma asperelloides strains

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Abstract

Thirty four Trichoderma isolates were systematically screened for induction of systemic resistance in grapevines against powdery mildew disease. Trichoderma 5R, NAIMCC-F-01769, NAIMCC-F-01812 and NAIMCC-F-01951 were selected for field trials based on initial screening on potted plants. All the four isolates tested positive for production of plant growth promoting bio-chemicals, indole acetic acid, siderophore, ammonia, hydrogen cyanide and phosphate solubilization and produced chitinase, β-1,3-glucanase, cellulase, amylase and protease. These four isolates were compatible with each other and were tested singly or as mixtures. In the three grapevine field trials conducted during the fruiting growth phase 2015–16 and 2016–17 and the vegetative growth phase 2016, the maximum reduction in powdery mildew severity was found in vines treated with 5R + NAIMCC-F-01812, followed by vines treated with 5R alone showing that the efficacy of 5R was slightly enhanced when used along with NAIMCC-F-01812. Total phenol contents, and chitinase and β-1, 3-glucanase activities were highest in leaves of vines treated with 5R + F-01812 corroborating the field observations. The peroxidase and polyphenol oxidase activities were also high in leaves of vines under this treatment. Multilocus analysis using partial nucleotide sequences of act, rpb2 and tef1 genes showed phylogenetic affiliations of all four isolates to T. asperelloides.

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References

  • Altomare C, Norvell WA, Bjorkman 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 65:2926–2933

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aziz A, Verhagen B, Magnin-Robert M, Couderchet M, Clément C, Jeandet P, Trotel-Aziz P (2016) Effectiveness of beneficial bacteria to promote systemic resistance of grapevine to gray mold as related to phytoalexin production in vineyards. Plant Soil 405:141–153

    CAS  Google Scholar 

  • Bennett FG, Westcott B (1982) Field assessment of resistance to powdery mildew in mature wheat plants. Plant Pathol 31:261–268

    Google Scholar 

  • Brotman Y, Lisec J, Meret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiol 158:139–146

    CAS  Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

    CAS  Google Scholar 

  • Cutler HG, Himmelsbach DS, Arrendale RF, Cox RH (1989) Koninginin a: a novel plant growth regulator from Trichoderma koningii. Agric Biol Chem 53:2605–2611

    CAS  Google Scholar 

  • Cutler HG, Jacyno JM, Phillips RS, Vontersch RL, Cole PD, Montemurro N (1991) Cyclonerodiol from a novel source, Trichoderma koningii: plant growth regulatory activity. Agric Biol Chem 55:243–244

    CAS  Google Scholar 

  • Darlu P, Lecointre G (2002) When does the incongruence length difference test fail? Mol Biol Evol 19:432–437

    CAS  PubMed  Google Scholar 

  • Dixit R, Singh RB, Singh HB (2015) Screening of antagonistic potential and plant growth promotion activities of Trichoderma spp. and fluorescent Pseudomonas spp. isolates against Sclerotinia sclerotiorum causing stem rot of French bean. Legume Res 38:375–381

    Google Scholar 

  • Elad Y (2000) Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot 19:709–714

    Google Scholar 

  • Fuchs JG, Moënne-Loccoz Y, Défago G (1997) Nonpathogenic Fusarium oxysporum strain Fo47 induces resistance to Fusarium wilt in tomato. Plant Dis 81:492–496

    PubMed  Google Scholar 

  • Gupta P, Ravi I, Sharma V (2013) Induction of β-1, 3-glucanase and chitinase activity in the defense response of Eruca sativa plants against the fungal pathogen Alternaria brassicicola. J Plant Interact 8:155–161

    CAS  Google Scholar 

  • Hanson LE, Howell CR (2004) Elicitors of plant defense responses from biocontrol strains of Trichoderma virens. Phytopathol 94:171–176

    CAS  Google Scholar 

  • Horsfall JG, Heuberger JW (1942) Measuring magnitude of a defoliation disease in tomatoes. Phytopathol 32:226–232

    Google Scholar 

  • Howell CR, Hanson LE, Stipanovic RD, Puckhaber LS (2000) Induction of terpenoid synthesis in cotton roots and control of Rhizoctonia solani by seed treatment with Trichoderma virens. Phytopathol 90:248–252

    CAS  Google Scholar 

  • Hoyos-Carvajal L, Orduz S, Bissett J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51:409–416

    Google Scholar 

  • Jangid PK, Mathur PN, Mathur K (2004) Role of chitinase and β-1,3 glucanase elicitation in the Trichoderma harzianum induced systemic resistance in capsicum. Indian Phytopathol 57:217–221

    CAS  Google Scholar 

  • Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Control 24:285–291

    Google Scholar 

  • Jogaiah S, Abdelrahman A, Tran LSP, Shin-ichi I (2013) Characterization of rhizosphere fungi that mediate resistance in tomato against bacterial wilt disease. J Exp Bot 64:3829–3842. https://doi.org/10.1093/jxb/ert212

    Article  CAS  PubMed  Google Scholar 

  • Joosten MH, De-Wit PJ (1989) Identification of several pathogenesis-related proteins in tomato leaves inoculated with Cladosporium fulvum (syn. Fulvia fulva) as 1,3-β-glucanases and chitinases. Plant Physiol 89:945–951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khan J, Ooka JJ, Miller SA, Madden LV, Hoitink HAJ (2004) Systemic resistance induced by Trichoderma hamatum 382 in cucumber against Phytophthora crown rot and leaf blight. Plant Dis 88:280–286

    CAS  PubMed  Google Scholar 

  • Koike N, Hyakumachi M, Kageyama K, Tsuyumu S, Doke N (2001) Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. Eur J Plant Pathol 107:523–533. https://doi.org/10.1023/A:1011203826805

    Article  CAS  Google Scholar 

  • Konappa N, Krishnamurthy S, Siddaiah CN, Ramachandrappa NS, Chowdappa S (2018) Evaluation of biological efficacy of Trichoderma asperellum against tomato bacterial wilt caused by Ralstonia solanacearum. Egypt J Biol Pest Con 28:63

    Google Scholar 

  • Legler SE, Pintye A, Caffi T, Gulyas S, Bohár G, Rossi V, Kiss L (2016) Sporulation rate in culture and mycoparasitic activity, but not mycohost specificity, are the key factors for selecting Ampelomyces strains for biocontrol of grapevine powdery mildew (Erysiphe necator). Eur J Plant Pathol 144:723–736

    Google Scholar 

  • Li Y, Gu Y, Li J, Xu M, Wei Q, Wang Y (2015) Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Front Microbiol 6:883. https://doi.org/10.3389/fmicb.2015.00883

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16:1799–1808

    CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrough NJ, Fair AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Marques APGC, Pires C, Moreira H, Rangel AOSS, Castro PML (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235

    CAS  Google Scholar 

  • Meyer GD, Bigirimana J, Elad Y, Hofte M (1998) Induced systemic resistance in Trichoderma harzianum T39 biocontrol of Botrytis cinerea. Eur J Plant Pathol 104:279–286

    Google Scholar 

  • Perazzolli M, Dagostin S, Ferrari A, Elad Y, Pertot I (2008) Induction of systemic resistance against Plasmopara viticola in grapevine by Trichoderma harzianum T39 and benzothiadiazole. Biol Control 47:228–234

    CAS  Google Scholar 

  • Perez-Miranda S, Cabirol N, George-Tellez R, Zamudio-Rivera LS, Fernandez FJ (2007) O-CAS, a fast and universal method for siderophore production. J Microbiol Methods 70:127–131

    CAS  PubMed  Google Scholar 

  • Purwantisari S, Priyatmojo A, Sancayaningsih RP, Kasiamdari RS, Budihardjo K (2018) Systemic inducing resistance against late blight by applying antagonist Trichoderma viride. In journal of physics: conference series, IOP publishing, 1025-p. 012053

  • Sadasivam S, Manickam A (1996) Biochemical methods for agricultural sciences. New age international (P) ltd., New Delhi, India

  • Samuels GJ, Dodd SL, Lu B-S, Petrini O, Schroers H-J, Druzhinina IS (2006) The Trichoderma koningii aggregate species. Stud Mycol 56:67–133

    PubMed  PubMed Central  Google Scholar 

  • Samuels GJ, Ismaiel A, Bon MC, De Respinis S, Petrini O (2010) Trichoderma asperellum sensu lato consists of two cryptic species. Mycologia 102:944–966

    CAS  PubMed  Google Scholar 

  • Sawant IS, Sawant SD (2011) Integration of Trichoderma harzianum 5R with low dose of Sulphur dioxide generator sheet for control of postharvest decay of Tas-A-Ganesh (Vitis vinifera L.) during and after long duration low temperature storage. J Eco-friendly Agric 6:180–186

    Google Scholar 

  • Sawant IS, Rajguru YR, Salunkhe VP, Wadkar PN (2012) Evaluation and selection of efficient isolates of Trichoderma species from diverse locations in India for biological control of anthracnose disease of grapes. J Biol Control 26:144–154

  • Sawant SD, Sawant IS, Shetty D, Shinde M, Jade S, Waghmare M (2011) Control of powdery mildew in vineyards by Milastin K, a commercial formulation of Bacillus subtilis (KTBS). J Biol Control 25:26–32

    Google Scholar 

  • Sawant IS, Wadkar PN, Ghule SB, Rajguru YR, Salunkhe VP, Sawant SD (2017) Enhanced biological control of powdery mildew in vineyards by integrating a strain of Trichoderma afroharzianum with Sulphur. Biol Control 114:133–143

    CAS  Google Scholar 

  • Schuster A, Schmoll M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol 87:787–799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    CAS  PubMed  Google Scholar 

  • Sharma P, Sain SK (2004) Induction of systemic resistance in tomato and cauliflower by Trichoderma spp. against stalk rot pathogen, Sclerotinia sclerotiorum (lib) de Bary. J Biol Control 18:21–28

    Google Scholar 

  • Simko I, Piepho HP (2012) The area under the disease progress stairs: calculation, advantage, and application. Phytopathol 102:381–389

    Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetery of total phenolics with phosphomolybdic-phosphotungstic acid reagent. Am J Enol Vitic 19:144–158

    Google Scholar 

  • Sumayo M, Ghim SY (2013) Plant growth-promoting rhizobacteria for plant immunity. In: Maheshwari D, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin, Heidelberg

    Google Scholar 

  • Vinale F, Nigro M, Sivasithamparam K, Flematti G, Ghisalberti EL, Ruocco M, Varlese R, Marra R, Lanzuise S, Eid A, Woo SL, Lorito M (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347:123–129. https://doi.org/10.1111/1574-6968.12231

    Article  CAS  PubMed  Google Scholar 

  • Viterbo A, Horwitz B (2010) In: Borkovich K, Ebbole D (eds) Mycoparasitism. ASM Press, Cellular and Molecular Biology of Filamentous Fungi, pp 676–693

    Google Scholar 

  • Viterbo A, Landau U, Kim S, Chernin L, Chet I (2010) Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS Microbiol Lett 305:42–48

    CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications eds. Innis MA, Gelfand DH, Sninsky JJ, White TJ (Academic Press, Inc, California), 315–322

  • Woo SL, Scala F, Ruocco M, Lorito M (2006) The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathol 96:181–185

    CAS  Google Scholar 

  • Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yedidia I, Benhamou N, Kapulnik Y, Chet I (2000) Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol Biochem 38:863–873

    CAS  Google Scholar 

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Acknowledgements

The authors are thankful to the Indian Council of Agricultural Research (ICAR), New Delhi for funding the research under the AMAAS Project and Dr. A. K. Upadhyay for soil analysis.

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Correspondence to Indu S. Sawant.

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Sawant, I.S., Wadkar, P.N., Ghule, S.B. et al. Induction of systemic resistance in grapevines against powdery mildew by Trichoderma asperelloides strains. Australasian Plant Pathol. 49, 107–117 (2020). https://doi.org/10.1007/s13313-020-00679-8

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