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Total crude protein extract of Trichoderma spp. induces systemic resistance in pearl millet against the downy mildew pathogen

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Abstract

Several proteins and peptides of microbial origin are reported for their elicitor properties, which play a vital role in the development of local and systemic resistances in plants. In this study, the efficacy of total crude proteins (TCP) extracted from six different Trichoderma spp. (T. asperellum, T. harzianum, T. atroviride, T. virens, T. longibrachiatum, and T. brevicompactum) was evaluated for their ability to elicit defense responses in pearl millet against downy mildew disease. Priming of pearl millet seeds (with or without mannitol) with different concentrations of TCP from Trichoderma spp. does not affect the seed germination and seedling vigor significantly. Under greenhouse conditions, a varied level of disease protection was recorded with TCP of different Trichoderma spp., and furthermore, its efficacy was found increased when treated with mannitol. Total crude protein extracts of T. atroviride (75 µg/ml) with mannitol recorded significantly higher disease protection of 53.6% in comparison with respective controls. Furthermore, this observation was supported by elevated levels of peroxidase (7.7 U @ 36 h after inoculation) and lipoxygenase (29.5 U @ 48 h after inoculation) and hypersensitive necrotic spots (56% @ 24 h after inoculation). The present study illustrated the capability of TCP extracted from different Trichoderma spp. to elicit the disease resistance mechanism in pearl millet seedlings against Sclerospora graminicola.

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References

  • Abdul Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria. Crop Sci 13:630–633

    Article  Google Scholar 

  • Afzal I, Ashraf S, Qasim M, Basra SMA, Shahid M, Hussain B (2011) Mannitol priming induces biochemical changes and enhances germination capacity and seedling vigor in marigold (Tagetes spp.). Acta Hortic 898:25–29

    Article  CAS  Google Scholar 

  • Agrios GN (2004) Plant pathology, 5th edn. Academic Press, San Diego

    Google Scholar 

  • Aliyu B, Hati SS, Dimari GA, Donli PO (2011) Comparative assessment of metalaxyl enhanced protection of pearl millet varieties in the control of downy mildew. J Cereals Oilseeds 2:26–31

    CAS  Google Scholar 

  • Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60(2):377–390

    Article  CAS  Google Scholar 

  • 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  Google Scholar 

  • Anup CP, Melvin M, Shilpa N, Gandhi MN, Jadhav M, Ali H, Kini KR (2015) Proteomic analysis of elicitation of downy mildew disease resistance in pearl millet by seed priming with β-aminobutyric acid and Pseudomonas fluorescens. J Proteomics 120:58–74

    Article  CAS  Google Scholar 

  • Axelrod B, Cheesbrough TM, Laakso S (1981) Lipoxygenase from soybeans. Methods Enzymol 71:441–451

    Article  CAS  Google Scholar 

  • Baillieul F, Genetet I, Kopp M, Saindrenan P, Fritig B, Kauffmann S (1995) A new elicitor of the hypersensitive response in tobacco: a fungal glycoprotein elicits cell death, expression of defense genes, production of salicylic acid, and induction of systemic acquired resistance. Plant J 8:551–560

    Article  CAS  Google Scholar 

  • Borthakur AB, Bhat G, Ramadoss CS (1987) The positional specifications of the oxygenation of linolenic acid catalyzed by two forms of lipoxygenase isolated from Bengal gram (Cicer arietinum). J Biosci 11:257–263

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Carvajal LH, Orduz S, Bissett J (2009) Growth stimulation in bean (Phaseolus vulgaris L.) by Trichoderma. Biol Control 51(3):409–416

    Article  Google Scholar 

  • Chandrashekhara, Niranjanraj S, Deepak SA, Amruthesh KN, Shetty NP, Shetty HS (2007) Endophytic bacteria from different plant origin enhance growth and induce downy mildew resistance in pearl millet. Asian J Plant Pathol 1:1–11

    Article  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    Article  CAS  Google Scholar 

  • Djonovic S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM (2006) Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microb Interact 19:838–853

    Article  CAS  Google Scholar 

  • Hammerschmidt R, Nuckles EM, Kuc J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. Physiol Mol Plant Pathol 20:73–82

    Article  CAS  Google Scholar 

  • Hammond-Kosack KE, Silverman P, Raskin I, Jones JDG (1996) Race-specific elicitors of Cladosporium fulvum induce changes in cell morphology and the synthesis of ethylene and salicylic acid in tomato plants carrying the corresponding Cf disease resistance gene. Plant Physiol 110:1381–1394

    Article  CAS  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species-opportunistic a virulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  CAS  Google Scholar 

  • Hückelhoven R, Fodor J, Preis C, Kogel KH (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol 119:1251–1260

    Article  Google Scholar 

  • Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 8:802–806

    Article  Google Scholar 

  • International Crops Research Institute for the Semi-Arid Tropics (ICRISAT) (2014) Proceedings of the consultants’ group meetings on downy mildew and ergot of pearl millet. In: Williams RJ (ed) Patancheru 502 324, Andhra Pradesh, India: International Crops Research Institute for the Semi-Arid Tropics

  • ISTA (2005) International Seed Testing Association. Proceedings of the International Seed Testing Association. International Rules of Seed Testing. Seed Sci Technol 15:1–9

  • Jogaiah S, Kurjogi M, Govind SR, Shetty HS, Basappa VA, Tran LSP (2016) Isolation and evaluation of proteolytic actinomycete isolates as novel inducers of pearl millet downy mildew disease protection. Sci Rep 6:1–13

    Article  Google Scholar 

  • Katiyar D, Hemantaranjan A, Singh B (2015) Chitosan as a promising natural compound to enhance potential physiological responses in plant: a review. Ind J Plant Physiol 20:1–9

    Article  CAS  Google Scholar 

  • Lavanya SN, Amruthesh KN (2016) 3, 5-Dichloroanthranilic acid (DCA)—an elicitor induces systemic resistance against downy mildew in pearl millet. Int J Life Sci 4:97–106

    Google Scholar 

  • Mukherjee PK, Buensanteai N, Moran-Diez ME, Druzhinina IS, Kenerley CM (2012) Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in induced systemic resistance response in maize. Microbiology 158:155–165

    Article  CAS  Google Scholar 

  • Myers JP, Antoniou MN, Blumberg B, Carroll L, Colborn T, Everett LG, Hansen M, Landrigan PJ, Lanphear BP, Mesnage R, Vandenberg LN, Saal FSV, Welshons WV, Benbrook CM (2016) Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ Health 15:19

    Article  Google Scholar 

  • Nandini B, Hariprasad P, Niranjana SR, Shetty HS, Geetha NP (2013) Elicitaion of resistance in pearl millet by oligosaccharides of Trichoderma spp. against downy mildew disease. J Plant Inter 8:45–55

    CAS  Google Scholar 

  • Niranjan Raj S, Chaluvaraju G, Amruthesh KN, Shetty HS, Reddy MS, Kloepper JW (2003a) Induction of growth promotion and resistance against downy mildew on pearl millet (Pennisetum glaucum) by rhizobacteria. Plant Dis 87:340–345

    Google Scholar 

  • Niranjan Raj S, Chaluvaraju G, Amruthesh KN, Shetty HS (2003b) Induction of growth promotion and resistance against downy mildew on pearl millet (Pennisetum glaucum) by rhizobacteria. Plant Dis 87:380–384

    Article  Google Scholar 

  • Niranjan Raj S, Lavanya SN, Amruthesh KN, Shetty HS (2011) Comparative evaluation of Pseudomonas fluorescens and their lipopolysaccharides as implicated in induction of resistance against pearl millet downy mildew. Arch Phytopath Plant Protect 44(13):1285–1299

    Article  CAS  Google Scholar 

  • Olson P, Varner J (1993) Hydrogen peroxide and lignification. Plant J 4:887–892

    Article  CAS  Google Scholar 

  • Peever TL, Higgins VJ (1989) Electrolyte leakage, lipoxygenase and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum. Plant Physiol 90:867–875

    Article  CAS  Google Scholar 

  • Pel MJC, Pieterse CMJ (2013) Microbial recognition and evasion of host immunity. J Expt Bot 64:1237–1248

    Article  CAS  Google Scholar 

  • Porta H, Rocha-Sosa M (2002) Plant lipoxygenases: physiological and molecular features. Plant Physiol 130:15–21

    Article  CAS  Google Scholar 

  • Reithner B, Ibarra-Laclette E, Mach RL, Herrera-Estrella A (2011) Identification of mycoparasitism-related genes in Trichoderma atroviride. Appl Environ Microbiol 77:4361–4370

    Article  CAS  Google Scholar 

  • Rustérucci C, Montillet JL, Agnel JP, Battesti C, Alonso B, Knoll A, Bessoule JJ, Etienne P, Suty L, Blein JP, Triantaphylidès C (1999) Involvement of lipoxygenase-dependent production of fatty acid hydroperoxides in the development of the hypersensitive cell death induced by cryptogein of tobacco leaves. J Biol Chem 274:36446–36455

    Article  Google Scholar 

  • Safeeulla KM (1976) Biology and control of the downy mildew of pearl millet, sorghum and finger millet. Wesley Press, Mysore

    Google Scholar 

  • Salas-Marina MA, Isordia-Jasso M, Islas-Osuna MA, Delgado-Sánchez P, Jiménez-Bremont JF, Rodríguez-Kessler M, Rosales-Saavedra MT, Herrera-Estrella A, Casas-Flores S (2015) The Epl1and Sm1proteins from Trichoderma atroviride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum. Front Plant Sci 6:77

    Article  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  CAS  Google Scholar 

  • Shailasree S, Melvin P (2015) β-amino butyric acid–resistance inducing agent in pearl millet. J Plant BiochemPhysiol 2:144

    Google Scholar 

  • Sharathchandra RG, Niranjan Raj S, Shetty NP, Amruthesh KN, Shetty HS (2004) A chitosan formulation Elexa induces downy mildew disease resistance and growth promotion in pearl millet. Crop Prot 23:881–888

    Article  CAS  Google Scholar 

  • Shcherbakova LA, Odintsova TI, Stakheev AA, Fravel DR, Zavriev SK (2016) Identification of a novel small cysteine-rich protein in the fraction from the biocontrol Fusarium oxysporum strain CS-20 that mitigates Fusarium wilt symptoms and triggers defense responses in tomato. Front Plant Sci 6:1–15

    Article  Google Scholar 

  • Sherwood RT, Vance CP (1976) Histochemsitry of papillae formed in reed canary grass leaves in response to infecting pathogenic fungi. Phytopathol 66:503–510

    Article  Google Scholar 

  • Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plantresponses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    Article  CAS  Google Scholar 

  • Singh SD, Gopinath R (1985) A seedling inoculation technique for detecting downy mildew resistance in pearl millet. Plant Dis 72:425–428

    Article  Google Scholar 

  • Taiz L, Zeiger E (2006) Plant physiology. Sinauer Associates Inc. Publishers, Massachusetts

    Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 accumulation in papillae and hypersensitive response during the barley powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Upadhyaya HD, Reddy KN, Irshad Ahmed M, Ramachandran S, Vinod Kumar, Singh S (2016) Characterization and genetic potential of African pearl millet named landraces conserved at the ICRISAT genebank. Plant Genet Res 1:1–15

    Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Barbetti MJ, Li H, Woo SL, Lorito M (2008) A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol Mol Plant Pathol 72:80–86

    Article  CAS  Google Scholar 

  • Waghunde RR, Shelake RM, Sabalpara AN (2016) Trichoderma: a significant fungus for agriculture and environment. Afr J Agric Res 11:1952–1965

    Google Scholar 

  • Wiesel L, Newton AC, Elliott I, Booty D, Gilroy EM, Birch PRJ, Hein I (2014) Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front Plant Sci 5:1–13

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Studies in Biotechnology, University of Mysore, Manasagangotri, Mysuru, Karnataka, 570 006, India

    Boregowda Nandini, Harischandra Sripathy Prakash & Nagaraja Geetha

  2. Centre for Rural Development and Technology, Indian Institute of Technology, Hauz Khas, New Delhi, 110016, India

    Puttaswamy Hariprasad

  3. Vijnana Bhavan, Institution of Excellence, University of Mysore, Manasagangotri, Mysuru, Karnataka, 570 006, India

    Harohalli Nanjegowda Shankara

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  1. Boregowda Nandini
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  2. Puttaswamy Hariprasad
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  3. Harohalli Nanjegowda Shankara
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  4. Harischandra Sripathy Prakash
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  5. Nagaraja Geetha
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Correspondence to Nagaraja Geetha.

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Nandini, B., Hariprasad, P., Shankara, H.N. et al. Total crude protein extract of Trichoderma spp. induces systemic resistance in pearl millet against the downy mildew pathogen. 3 Biotech 7, 183 (2017). https://doi.org/10.1007/s13205-017-0816-4

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