{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T17:26:07Z","timestamp":1782235567082,"version":"3.54.5"},"reference-count":43,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T00:00:00Z","timestamp":1674000000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"ICRISAT"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Advances in biocontrol potentials and fungicide resistance are highly desirable for <jats:italic>Trichoderma<\/jats:italic>. Thus, it is profitable to use mutagenic agents to develop superior strains with enhanced biocontrol properties and fungicide tolerance in <jats:italic>Trichoderma<\/jats:italic>. This study investigates the N-methyl-n-nitro-N-nitrosoguanidine (NTG) (100 mg\/L) induced mutants of <jats:italic>Trichoderma asperellum<\/jats:italic>. Six NTG (3 each from 1<jats:sup>st<\/jats:sup> &amp; 2<jats:sup>nd<\/jats:sup> round) induced mutants were developed and evaluated their biocontrol activities and carbendazim tolerance. Among the mutant N2-3, N2-1, N1 and N2-2 gave the best antagonistic and volatile metabolite activities on inhibition of chickpea <jats:italic>F<\/jats:italic>. <jats:italic>oxysporum<\/jats:italic> f. sp. <jats:italic>ciceri<\/jats:italic>, <jats:italic>B<\/jats:italic>. <jats:italic>cinerea<\/jats:italic> and <jats:italic>R<\/jats:italic>. <jats:italic>bataticola<\/jats:italic> mycelium under in vitro condition. Mutant N2-2 (5626.40 \u03bcg\/ml) showed the highest EC<jats:sub>50<\/jats:sub> value against carbendazim followed by N2-3 (206.36 \u03bcg\/ml) and N2-1 (16.41 \u03bcg\/ml); and succeeded to sporulate even at 2000 \u03bcg\/ml of carbendazim. The biocontrol activity of N2-2 and N2 with half-dose of carbendazim was evaluated on chickpea dry root rot under controlled environment. Disease reduction and progress of the dry root rot was extremely low in T<jats:sub>7<\/jats:sub> (N2-2 + with half-dose of carbendazim) treatment. Further, carbendazim resistant mutants demonstrated mutation in <jats:italic>tub2<\/jats:italic> gene of \u03b2-tubulin family which was suggested through the 37 and 183 residue changes in the superimposed protein structures encoded by <jats:italic>tub2<\/jats:italic> gene in N2 and N2-2 with WT respectively. This study conclusively implies that the enhanced carbendazim tolerance in N2-2 mutant did not affect the mycoparasitism and plant growth activity of <jats:italic>Trichoderma<\/jats:italic>. These mutants were as good as the wild-type with respect to all inherent attributes.<\/jats:p>","DOI":"10.1371\/journal.pone.0280064","type":"journal-article","created":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T18:39:54Z","timestamp":1674067194000},"page":"e0280064","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":6,"title":["Genetic enhancement of Trichoderma asperellum biocontrol potentials and carbendazim tolerance for chickpea dry root rot disease management"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3967-178X","authenticated-orcid":true,"given":"Ramangouda","family":"G.","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M. K.","family":"Naik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rahul B.","family":"Nitnavare","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richa","family":"Yeshvekar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joorie","family":"Bhattacharya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pooja","family":"Bhatnagar-Mathur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5745-4693","authenticated-orcid":true,"given":"Mamta","family":"Sharma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2023,1,18]]},"reference":[{"key":"pone.0280064.ref001","doi-asserted-by":"crossref","first-page":"1910","DOI":"10.3389\/fmicb.2019.01910","article-title":"A novel seed-dressing formulation based on an improved mutant strain of Trichoderma virens, and its field evaluation","volume":"10","author":"PK Mukherjee","year":"2019","journal-title":"Front Microbiol"},{"key":"pone.0280064.ref002","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s10658-011-9782-6","article-title":"Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid\/ethylene and salicylic acid pathways","volume":"131","author":"MA Salas-Marina","year":"2011","journal-title":"Europ J Pl Pathol"},{"issue":"1","key":"pone.0280064.ref003","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s13225-020-00464-4","article-title":"In honor of John Bissett: authoritative guidelines on molecular identification of Trichoderma","volume":"107","author":"F Cai","year":"2021","journal-title":"Fungal Diversity"},{"issue":"1","key":"pone.0280064.ref004","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s11104-014-2069-x","article-title":"The 4-phosphopantetheinyl transferase of Trichoderma virens plays a role in plant protection against Botrytis cinerea through volatile organic compound emission","volume":"379","author":"HA Contreras-Cornejo","year":"2014","journal-title":"Plant and Soil"},{"issue":"1","key":"pone.0280064.ref005","doi-asserted-by":"crossref","first-page":"50","DOI":"10.5423\/PPJ.OA.09.2014.0087","article-title":"Characterization of Novel Trichoderma asperellum Isolates to Select Effective Biocontrol Agents Against Tomato Fusarium Wilt","volume":"31","author":"MH El-Komy","year":"2011","journal-title":"The Plant Pathol J"},{"key":"pone.0280064.ref006","first-page":"230","article-title":"Trichoderma in Plant Health Management","author":"NW Zaidi","year":"2014","journal-title":"Trichoderma: Biology and Applications"},{"issue":"3","key":"pone.0280064.ref007","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1007\/s002530000403","article-title":"Improvement of microbial strains and fermentation processes","volume":"54","author":"S Parekh","year":"2000","journal-title":"Appl Microbiol Biotechnol"},{"issue":"5","key":"pone.0280064.ref008","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1134\/S0003683813050086","article-title":"Novel mutations in \u03b2-tubulin gene in Trichoderma harzianum mutants resistant to methyl benzimidazole-2-YL carbamate","volume":"49","author":"M Li","year":"2013","journal-title":"Applied Biochem Microbiol"},{"issue":"03","key":"pone.0280064.ref009","first-page":"1649","article-title":"Mutagenesis of Trichoderma asperellum for Fungicide Tolerance","volume":"10","author":"AG Gathe","year":"2021","journal-title":"Inter J of Current Microb and Appl Sc"},{"issue":"4","key":"pone.0280064.ref010","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1007\/s10658-006-9031-6","article-title":"Biocontrol agents in combination with Moringa oleifera extract for integrated control of Sclerotium-caused cowpea damping-off and stem rot","volume":"115","author":"A Adandonon","year":"2006","journal-title":"Eur J Plant Pathol"},{"key":"pone.0280064.ref011","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1046\/j.1365-3059.2003.00861.x","article-title":"Studies on thiabendazole resistance of Penicillium expansum of pears: pathogenic fitness and genetic characterization","volume":"52","author":"E Baraldi","year":"2003","journal-title":"Plant Pathology"},{"issue":"2","key":"pone.0280064.ref012","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.pestbp.2010.04.007","article-title":"Effects of fungicides JS399-19, azoxystrobin, tebuconazloe, and carbendazim on the physiological and biochemical indices and grain yield of winter wheat","volume":"98","author":"YJ Zhang","year":"2010","journal-title":"Pesticide Biochemistry and Physiology"},{"key":"pone.0280064.ref013","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev.py.24.090186.000355","article-title":"Benzimidazole fungicides: mechanism of action and biological impact","volume":"24","author":"LC Davidse","year":"1986","journal-title":"Ann.Rev of Phytopathol"},{"key":"pone.0280064.ref014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fagro.2021.772170","article-title":"Tolerance and Biological Removal of Fungicides by Trichoderma Species Isolated From the Endosphere of Wild Rubiaceae Plants","volume":"3","author":"E Escudero-Leyva","year":"2022","journal-title":"Frontiers in Agronomy"},{"key":"pone.0280064.ref015","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/BF00276886","article-title":"Herrera-Estrella AA nucleotide substitution in one of the beta-tubulin genes of Trichoderma viride confers resistance to the antimitotic drug methyl benzimidazole-2-yl-carbamate","volume":"240","author":"GH Goldman","year":"1993","journal-title":"Mol Gen Gent"},{"key":"pone.0280064.ref016","unstructured":"Ramanagouda G. Genetic enhancement of biocontrol potential of Trichoderma spp. by induced mutation. PhD thesis, Univ. of Agri. Sci. Raichur, Karnataka, India. 2018, pp259."},{"key":"pone.0280064.ref017","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1007\/s42360-021-00325-3","article-title":"Compatibility studies of indigenous Trichoderma isolates with pesticides","volume":"74","author":"G Ramanagouda","year":"2021","journal-title":"Indian Phytopathol"},{"key":"pone.0280064.ref018","article-title":"Biocontrol potentials of novel indigenous Trichoderma isolates against Fusarium wilt of chickpea","author":"G Ramanagouda","year":"2021","journal-title":"Indian Phytopathol"},{"key":"pone.0280064.ref019","article-title":"Induction of stable benomyl-tolerant phenotypic mutants of Trichoderma pseudokoningii MTCC 3011 and their evaluation for antagonistic and biocontrol potential","volume":"37","author":"PK Mukherjee","year":"1997","journal-title":"Indian J of Exptl Biol"},{"key":"pone.0280064.ref020","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1094\/Phyto-61-42","article-title":"Fungitoxic spectrum of benzimidazole compounds","volume":"61","author":"LV Edington","year":"1971","journal-title":"Phytopathol"},{"issue":"2","key":"pone.0280064.ref021","first-page":"p04017097","article-title":"Active vibration control of composite pyramidal lattice truss core sandwich plates","volume":"31","author":"M Li","year":"2018","journal-title":"J Aerosp Eng"},{"key":"pone.0280064.ref022","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1007\/s42360-019-00151-8","article-title":"Carbendazim sensitivity of Fusarium solani soil isolates","volume":"72","author":"M Tarafder","year":"2019","journal-title":"Indian Phytopathol"},{"key":"pone.0280064.ref023","volume-title":"Introduction to plant disease epidemiology","author":"CL Campbell","year":"1990"},{"key":"pone.0280064.ref024","unstructured":"Vanderplank JE. Plant Diseases-Epidemics and Control Academic Press New York. 1963."},{"key":"pone.0280064.ref025","volume-title":"Statistical tables","author":"FJ Rohlf","year":"1995"},{"issue":"1","key":"pone.0280064.ref026","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1093\/nar\/gku316","article-title":"Deciphering key features in protein structures with the new END script server","volume":"42","author":"X Robert","year":"2014","journal-title":"Nucl Acids Res"},{"key":"pone.0280064.ref027","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.cropro.2017.09.014","article-title":"Improvement of the propamocarb-tolerance of Lecanicillium lecanii through UV-light radiation-based mutagenesis","volume":"103","author":"M Xie","year":"2018","journal-title":"Crop Protection"},{"issue":"4","key":"pone.0280064.ref028","doi-asserted-by":"crossref","first-page":"260","DOI":"10.15171\/ijb.1224","article-title":"Biocontrol activities of gamma induced mutants of Trichoderma harzianum against some soilborne fungal pathogens and their DNA fingerprinting","volume":"14","author":"S Abbasi","year":"2016","journal-title":"Iranian J Biotech"},{"key":"pone.0280064.ref029","volume-title":"Microbial genetics and breeding","author":"GJ Zhu","year":"2009"},{"issue":"4","key":"pone.0280064.ref030","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1111\/mpp.12189","article-title":"The toolbox of Trichoderma spp. in the biocontrol of Botrytis cinerea disease: Trichoderma biocontrol of Botrytis cinerea disease","volume":"16","author":"CMF Vos","year":"2015","journal-title":"Mol Plant Pathol"},{"issue":"2","key":"pone.0280064.ref031","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1111\/j.1365-2672.2004.02453.x","article-title":"Novel mutation method for increased cellulase production","volume":"98","author":"P Chand","year":"2005","journal-title":"J App Microbiol"},{"issue":"4","key":"pone.0280064.ref032","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1104\/pp.18.01092","article-title":"Trichoderma histone deacetylase HDA-2 modulates multiple responses in Arabidopsis","volume":"179","author":"M Estrada-Rivera","year":"2019","journal-title":"Plant Physiology"},{"issue":"10","key":"pone.0280064.ref033","first-page":"34","article-title":"Effect of volatile metabolites of Trichoderma species against seven fungal plant Pathogens in vitro","volume":"2","author":"A Faheem","year":"2010","journal-title":"J Phytol"},{"issue":"3","key":"pone.0280064.ref034","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1007\/s12298-017-0500-5","article-title":"A novel Trichoderma fusant for enhancing nutritional value and defence activity in chickpea","volume":"24","author":"A Mishra","year":"2018","journal-title":"Physiology and Molecular Biology of Plants"},{"key":"pone.0280064.ref035","unstructured":"Yardley J A. Understanding protoplast technology as a tool to enhance biocontrol, Lincoln University Digital Thesis. 2018;1\u2013160."},{"issue":"5","key":"pone.0280064.ref036","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1007\/BF03356122","article-title":"Development of UV-induced Carbendazim-resistant mutants of Trichoderma harzianum for integrated control of damping-off disease of cotton caused by Rhizoctonia solani","volume":"110","author":"J Jayaraj","year":"2003","journal-title":"J Pl Dis Protect"},{"key":"pone.0280064.ref037","doi-asserted-by":"crossref","first-page":"890551","DOI":"10.3389\/fpls.2022.890551","article-title":"Combined drought and heat stress influences the root water relation and determine the dry root rot disease development under field conditions: A study using contrasting chickpea genotypes","volume":"13","author":"AR Chilakala","year":"2022","journal-title":"Front. Plant Sci"},{"issue":"6","key":"pone.0280064.ref038","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1094\/PHYTO-07-10-0183","article-title":"Risk factors for crop health under global change and agricultural shifts: a framework of analyses using rice in tropical and subtropical Asia as a model","volume":"101","author":"S Savary","year":"2011","journal-title":"Phytopathol"},{"issue":"3","key":"pone.0280064.ref039","doi-asserted-by":"crossref","first-page":"584","DOI":"10.4236\/ajps.2013.43076","article-title":"Unravelling effects of temperature and soil moisture stress response on development of dry root rot [Rhizoctonia bataticola (Taub.)] Butler in Chickpea","volume":"4","author":"M Sharma","year":"2013","journal-title":"Am J Plant Sci"},{"issue":"1","key":"pone.0280064.ref040","first-page":"39","article-title":"Management of chickpea wilt through a combination of fungicides and bioagents","volume":"57","author":"RK Poddar","year":"2004","journal-title":"Indian Phytopath"},{"key":"pone.0280064.ref041","unstructured":"Mech S. UV-radiated mutant of Trichoderma harzianum Rifai and its carrier based formulation for the management of white mold of French bean. M.Sc. (Agri.) Thesis, Assam Agric. Univ., Jorhat, Assam. 2006."},{"issue":"4","key":"pone.0280064.ref042","first-page":"1023","article-title":"Induce mutations for Bavistin resistance in Trichoderma harzianum by UV-irradiation","volume":"54","author":"AM Al-araji","year":"2013","journal-title":"Iraqi J Sci"},{"issue":"1","key":"pone.0280064.ref043","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1007\/BF00712964","article-title":"Development of a homologous transformation system for Acremonium chrysogenum based on the \u03b2\u2212 tubulin gene","volume":"25","author":"C Nowak","year":"1994","journal-title":"Curr Genet"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0280064","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T18:40:54Z","timestamp":1674067254000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0280064"}},"subtitle":[],"editor":[{"given":"Abhay K.","family":"Pandey","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,1,18]]},"references-count":43,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,1,18]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0280064","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,18]]}}}