{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T22:00:28Z","timestamp":1791583228830,"version":"4.3.4"},"reference-count":134,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,2,17]],"date-time":"2026-02-17T00:00:00Z","timestamp":1771286400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Fungal Biol."],"abstract":"<jats:p>\n                    <jats:italic>Metarhizium anisopliae<\/jats:italic>\n                    is an entomopathogenic fungus that is widely used in the biological control of agricultural pests. During host infection,\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    secretes an arsenal of hydrolytic enzymes such as proteases and chitinases that allow for cuticle penetration and host colonization. The degradation of chitin into N-acetylglucosamine (GlcNAc) monomers is carried out by chitinases and \u03b2-N-acetylglucosaminidases (NAGases). Chitin-degrading enzymes of\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    have been the subject of extensive research; however, these studies have not been consolidated into a comprehensive review. This review highlights our current knowledge of the chitinolytic enzymes from\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    , emphasizing the classification of these enzymes based on their mode of action and domain architecture.\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    possesses a set of 21 chitinases that are classified into four glycoside hydrolase family 18 (GH18) subgroups: A, B, C, and D. In addition,\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    produces two GH20 and two GH3 NAGases. The domain architectures of chitinases and NAGases from\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    are highly similar to those found in\n                    <jats:italic>Trichoderma<\/jats:italic>\n                    spp. but exhibit some evolutionary distinctions. Moreover, this review integrates insights from other entomopathogenic fungi to identify molecular mechanisms underlying the expression of chitinase and NAGase genes in\n                    <jats:italic>M. anisopliae<\/jats:italic>\n                    . The regulatory mechanisms underlying gene expression of chitinolytic enzymes are complex and involve several regulators and metabolic pathways. Finally, chitinases have the potential to be used as biopesticides against fungal pathogens and pest infestations.\n                  <\/jats:p>","DOI":"10.3389\/ffunb.2026.1732437","type":"journal-article","created":{"date-parts":[[2026,2,17]],"date-time":"2026-02-17T10:18:03Z","timestamp":1771323483000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["The chitinolytic enzymes from the entomopathogenic fungus Metarhizium anisopliae: GH family distribution, domain architecture, and protein regulation"],"prefix":"10.3389","volume":"7","author":[{"given":"Qusai","family":"Al Abdallah","sequence":"first","affiliation":[{"name":"Department of Agricultural Biotechnology and Genetic Engineering, Faculty of Agricultural Technology, Al-Ahliyya Amman University","place":["Amman, Jordan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kholoud M.","family":"Alananbeh","sequence":"additional","affiliation":[{"name":"Department of Plant Protection, School of Agriculture, The University of Jordan","place":["Amman, Jordan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nehaya","family":"Al-Karablieh","sequence":"additional","affiliation":[{"name":"Department of Plant Protection, School of Agriculture, The University of Jordan","place":["Amman, Jordan"]},{"name":"Hamdi Mango Center for Scientific Research, The University of Jordan","place":["Amman, Jordan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Salah-Eddin","family":"Araj","sequence":"additional","affiliation":[{"name":"Department of Plant Protection, School of Agriculture, The University of Jordan","place":["Amman, Jordan"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,2,17]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"6799","DOI":"10.1080\/03067319.2024.2429792","article-title":"Nanoarchitectonics of biohybrid polymer nanocomposite of carboxylated chitosan-phthalate\/SnO2 nanoparticles for dye wastewater treatment: characterisation, isotherm, kinetic, and adsorption optimisation","volume":"105","author":"Abdulhameed","year":"2025","journal-title":"Int. J. Environ. Anal. Chem."},{"key":"B2","doi-asserted-by":"publisher","first-page":"339","DOI":"10.4155\/tde-2023-0136","article-title":"Preparation, characterization and in vitro evaluation of 5-fluorouracil loaded into chitosan\u2013acacia gum nanoparticles","volume":"15","author":"Al-Nasrawi","year":"2024","journal-title":"Ther. Deliv."},{"key":"B3","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1016\/B978-0-12-374144-8.00103-X","article-title":"Chapter 94 - exoskeleton","volume-title":"Encyclopedia of insects","author":"Andersen","year":"2009"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1098\/rsos.190412","article-title":"Chitinase genes from Metarhizium anisopliae for the control of whitefly in cotton","volume":"6","author":"Anwar","year":"2019","journal-title":"R. Soc Open Sci."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1471","DOI":"10.1016\/j.chembiol.2012.09.016","article-title":"Active site plasticity within the glycoside hydrolase nagZ underlies a dynamic mechanism of substrate distortion","volume":"19","author":"Bacik","year":"2012","journal-title":"Chem. Biol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1007\/s00284-006-0078-6","article-title":"Isolation, Characterization, and Transcriptional Analysis of the Chitinase chi2 Gene (DQ011663) from the Biocontrol Fungus Metarhizium anisopliae var. anisopliae","volume":"53","author":"Baratto","year":"2006","journal-title":"Curr. Microbiol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1139\/w03-085","article-title":"Expression and characterization of the 42 kDa chitinase of the biocontrol fungus Metarhizium anisopliae in Escherichia coli","volume":"49","author":"Baratto","year":"2003","journal-title":"Can. J. Microbiol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1007\/s00284-003-4063-z","article-title":"Distribution of chitinases in the entomopathogen metarhizium anisopliae and effect of N-acetylglucosamine in protein secretion","volume":"48","author":"Barreto","year":"2004","journal-title":"Curr. Microbiol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"2282","DOI":"10.1021\/pr401204y","article-title":"Secretome of the Biocontrol Agent Metarhizium anisopliae Induced by the Cuticle of the Cotton Pest Dysdercus Peruvianus Reveals New Insights into Infection","volume":"13","author":"Beys-da-Silva","year":"2014","journal-title":"J. Proteome Res."},{"key":"B10","doi-asserted-by":"publisher","first-page":"628","DOI":"10.1002\/jobm.201100274","article-title":"Expression of chitinase genes of Metarhizium anisopliae isolates in lepidopteran pests and on synthetic media","volume":"52","author":"Bhanu Prakash","year":"2012","journal-title":"J. Basic Microbiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1198","DOI":"10.1139\/b98-115","article-title":"Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats","volume":"76","author":"Bidochka","year":"1998","journal-title":"Can. J. Bot."},{"key":"B12","doi-asserted-by":"publisher","first-page":"512","DOI":"10.3852\/07-202","article-title":"A multilocus phylogeny of the Metarhizium anisopliae lineage","volume":"101","author":"Bischoff","year":"2009","journal-title":"Mycologia"},{"key":"B13","doi-asserted-by":"publisher","first-page":"426","DOI":"10.3732\/ajb.1000298","article-title":"The Fungi: 1, 2, 3 \u2026 5.1 million species","volume":"98","author":"Blackwell","year":"2011","journal-title":"Am. J. Bot."},{"key":"B14","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1007\/s002849900368","article-title":"A Chitinase Encoding Gene (chit1 Gene) from the Entomopathogen Metarhizium anisopliae: Isolation and Characterization of Genomic and Full-Length cDNA","volume":"37","author":"Bogo","year":"1998","journal-title":"Curr. Microbiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.gene.2010.04.005","article-title":"Evidence of alternative splicing of the chi2 chitinase gene from Metarhizium anisopliae","volume":"462","author":"Boldo","year":"2010","journal-title":"Gene"},{"key":"B16","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1007\/s00294-009-0267-5","article-title":"Endochitinase CHI2 of the biocontrol fungus Metarhizium anisopliae affects its virulence toward the cotton stainer bug Dysdercus Peruvianus","volume":"55","author":"Boldo","year":"2009","journal-title":"Curr. Genet."},{"key":"B17","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1186\/s12864-015-1601-6","article-title":"Classification of fungal and bacterial lytic polysaccharide monooxygenases","volume":"16","author":"Busk","year":"2015","journal-title":"BMC Genomics"},{"key":"B18","article-title":"Chapter nine - entomopathogenic fungi: new insights into host\u2013pathogen interaction","volume-title":"Advances in genetics","author":"Butt","year":"2016"},{"key":"B19","doi-asserted-by":"publisher","first-page":"1593","DOI":"10.3390\/v17121593","article-title":"Mycoviruses in entomopathogenic fungi","volume":"17","author":"Camargo","year":"2025","journal-title":"Viruses"},{"key":"B20","doi-asserted-by":"publisher","first-page":"1151","DOI":"10.1128\/ec.2.6.1151-1161.2003","article-title":"Whole-genome analysis of two-component signal transduction genes in fungal pathogens","volume":"2","author":"Catlett","year":"2003","journal-title":"Eukaryot. Cell"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1016\/j.bioteChadv.2020.107553","article-title":"Glycoside hydrolase family 18 chitinases: The known and the unknown","volume":"43","author":"Chen","year":"2020","journal-title":"Biotechnol. Adv."},{"key":"B22","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1016\/j.actbio.2007.12.010","article-title":"Structure and mechanical properties of crab exoskeletons","volume":"4","author":"Chen","year":"2008","journal-title":"Acta Biomater."},{"key":"B23","doi-asserted-by":"publisher","first-page":"1048","DOI":"10.1111\/1462-2920.13198","article-title":"MAPK cascade-mediated regulation of pathogenicity, conidiation and tolerance to abiotic stresses in the entomopathogenic fungus Metarhizium robertsii","volume":"18","author":"Chen","year":"2016","journal-title":"Environ. Microbiol."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens10060746","article-title":"Diversity and function of appressoria","volume":"10","author":"Chethana","year":"2021","journal-title":"Pathog. Basel Switz."},{"key":"B25","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1016\/j.resmic.2004.10.013","article-title":"Cuticle-induced endo\/exoacting chitinase CHIT30 from Metarhizium anisopliae is encoded by an ortholog of the chi3 gene","volume":"156","author":"da Silva","year":"2005","journal-title":"Res. Microbiol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1007\/s00284-002-3678-9","article-title":"Characterization of mycoviruses and analyses of chitinase secretion in the biocontrol fungus metarhizium anisopliae","volume":"45","author":"de la Paz Gim\u00e9nez-Pecci","year":"2002","journal-title":"Curr. Microbiol."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.3389\/ffunb.2024.1456964","article-title":"General aspects, host interaction, and application of Metarhizium sp. in arthropod pest and vector control","volume":"5","author":"de Miranda","year":"2024","journal-title":"Front. Fungal Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1016\/j.tplants.2012.06.004","article-title":"Unconventional protein secretion","volume":"17","author":"Ding","year":"2012","journal-title":"Trends Plant Sci."},{"key":"B29","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1007\/978-3-319-40740-1_10","article-title":"Targeting cuticular components for pest management","volume-title":"Extracellular composite matrices in arthropods","author":"Doucet","year":"2016"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.71.1.363-370.2005","article-title":"Cloning of beauveria bassiana chitinase gene bbchit1 and its application to improve fungal strain virulence","volume":"71","author":"Fang","year":"2005","journal-title":"Appl. Environ. Microbiol"},{"key":"B31","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1128\/ec.00245-10","article-title":"Fungal skn7 stress responses and their relationship to virulence","volume":"10","author":"Fassler","year":"2011","journal-title":"Eukaryot. Cell"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1016\/j.napere.2023.100020","article-title":"Entomopathogenic fungi hydrolytic enzymes: A new approach to biocontrol","volume":"3","author":"Ferreira","year":"2023","journal-title":"J. Nat. Pestic. Res."},{"key":"B33","doi-asserted-by":"publisher","first-page":"e1001264","DOI":"10.1371\/journal.pgen.1001264","article-title":"Genome Sequencing and Comparative Transcriptomics of the Model Entomopathogenic Fungi Metarhizium anisopliae and M. acridum","volume":"7","author":"Gao","year":"2011","journal-title":"PloS Genet."},{"key":"B34","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1186\/s13104-022-06004-4","article-title":"Extracellular enzyme activity of entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae and their pathogenicity potential as a bio-control agent against whitefly pests, Bemisia tabaci and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae)","volume":"15","author":"Gebremariam","year":"2022","journal-title":"BMC Res. Notes"},{"key":"B35","doi-asserted-by":"publisher","first-page":"1658","DOI":"10.1194\/jlr.RA120000975","article-title":"Sterol regulatory element-binding protein Sre1 regulates carotenogenesis in the red yeast Xanthophyllomyces dendrorhous","volume":"61","author":"G\u00f3mez","year":"2020","journal-title":"J. Lipid Res."},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2180-12-213","article-title":"High abundance of Serine\/Threonine-rich regions predicted to be hyper-O-glycosylated in the secretory proteins coded by eight fungal genomes","volume":"12","author":"Gonz\u00e1lez","year":"2012","journal-title":"BMC Microbiol."},{"key":"B37","first-page":"9","article-title":"Insect cuticle: structure and properties of the material","volume-title":"Attachment devices of insect cuticle","author":"Gorb","year":"2001"},{"key":"B38","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1007\/s11557-008-0571-3","article-title":"Fungal chitinases and their biological role in the antagonism onto nematode eggs. A review","volume":"7","author":"Gortari","year":"2008","journal-title":"Mycol. Prog."},{"key":"B39","doi-asserted-by":"publisher","first-page":"7217","DOI":"10.1128\/AEM.06027-11","article-title":"Differential regulation of orthologous chitinase genes in mycoparasitic Trichoderma species","volume":"77","author":"Gruber","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1099\/mic.0.052613-0","article-title":"Self versus non-self: fungal cell wall degradation in Trichoderma","volume":"158","author":"Gruber","year":"2012","journal-title":"Microbiology"},{"key":"B41","doi-asserted-by":"publisher","first-page":"e2320572121","DOI":"10.1073\/pnas.2320572121","article-title":"Transfection of entomopathogenic Metarhizium species with a mycovirus confers hypervirulence against two lepidopteran pests","volume":"121","author":"Guo","year":"2024","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1186\/1475-2859-11-134","article-title":"Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates","volume":"11","author":"H\u00e4kkinen","year":"2012","journal-title":"Microb. Cell Factories"},{"key":"B43","doi-asserted-by":"publisher","first-page":"21","DOI":"10.4103\/0975-7406.106559","article-title":"Chitinases: an update","volume":"5","author":"Hamid","year":"2013","journal-title":"J. Pharm. Bioallied Sci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1111\/jeu.12246","article-title":"Characterization of the first fungal glycosyl hydrolase family 19 chitinase (NbchiA) from nosema bombycis (Nb)","volume":"63","author":"Han","year":"2016","journal-title":"J. Eukaryot. Microbiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1007\/s00253-011-3723-3","article-title":"Fungal chitinases: diversity, mechanistic properties and biotechnological potential","volume":"93","author":"Hartl","year":"2012","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1016\/S0959-440X(97)80072-3","article-title":"Structural and sequence-based classification of glycoside hydrolases","volume":"7","author":"Henrissat","year":"1997","journal-title":"Curr. Opin. Struct. Biol."},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.3390\/v15051202","article-title":"Fungal viruses unveiled: A comprehensive review of mycoviruses","volume":"15","author":"Hough","year":"2023","journal-title":"Viruses"},{"key":"B48","doi-asserted-by":"publisher","first-page":"994","DOI":"10.1111\/1462-2920.12451","article-title":"MrpacC regulates sporulation, insect cuticle penetration and immune evasion in Metarhizium robertsii","volume":"17","author":"Huang","year":"2015","journal-title":"Environ. Microbiol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1093\/glycob\/cwr092","article-title":"The GH18 family of chitinases: their domain architectures, functions and evolutions","volume":"22","author":"Huang","year":"2012","journal-title":"Glycobiology"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-8-214","article-title":"Phylogenetic analyses suggest multiple changes of substrate specificity within the Glycosyl hydrolase 20 family","volume":"8","author":"Intra","year":"2008","journal-title":"BMC Evol. Biol."},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.1093\/g3journal\/jkab416","article-title":"Genomic signatures and insights into host niche adaptation of the entomopathogenic fungus Metarhizium humberi","volume":"12","author":"Iwanicki","year":"2022","journal-title":"G3 GenesGenomesGenetics"},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.3389\/fmats.2025.1537067","article-title":"Chitin: a comparison between its main sources","volume":"12","author":"Izadi","year":"2025","journal-title":"Front. Mater."},{"key":"B53","doi-asserted-by":"publisher","first-page":"308","DOI":"10.1007\/s11274-025-04524-2","article-title":"Characterization of a \u03b2-N-acetylhexosaminidase CgNagase20 from Chaetomium globosum with antifungal activity against Fusarium sporotrichioides","volume":"41","author":"Jiang","year":"2025","journal-title":"World J. Microbiol. Biotechnol."},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.3390\/md18010064","article-title":"Crab vs. Mushroom: A review of crustacean and fungal chitin in wound treatment","volume":"18","author":"Jones","year":"2020","journal-title":"Mar. Drugs"},{"key":"B55","doi-asserted-by":"publisher","first-page":"e107864","DOI":"10.1371\/journal.pone.0107864","article-title":"Genomic analyses and transcriptional profiles of the glycoside hydrolase family 18 genes of the entomopathogenic fungus metarhizium anisopliae","volume":"9","author":"Junges","year":"2014","journal-title":"PloS One"},{"key":"B56","doi-asserted-by":"publisher","first-page":"640","DOI":"10.1111\/mmi.13256","article-title":"The N-acetylglucosamine catabolic gene cluster in Trichoderma reesei is controlled by the Ndt80-like transcription factor RON1","volume":"99","author":"Kappel","year":"2016","journal-title":"Mol. Microbiol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1933","DOI":"10.1007\/s12010-009-8701-1","article-title":"Expression of a Chitinase Gene from Metarhizium anisopliae in Tobacco Plants Confers Resistance against Rhizoctonia solani","volume":"160","author":"Kern","year":"2010","journal-title":"Appl. Biochem. Biotechnol."},{"key":"B58","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/978-3-540-79307-6_3","article-title":"Entomopathogenic fungi: biochemistry and molecular biology","volume-title":"Human and animal relationships","author":"Khachatourians","year":"2008"},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.1186\/s43008-024-00154-9","article-title":"Integrative taxonomy of Metarhizium anisopliae species complex, based on phylogenomics combined with morphometrics, metabolomics, and virulence data","volume":"15","author":"Kobmoo","year":"2024","journal-title":"IMA Fungus"},{"key":"B60","doi-asserted-by":"publisher","first-page":"0205","DOI":"10.1007\/s00284-002-3863-x","article-title":"Regulation of Extracellular Chitinases and proteases in the entomopathogen and acaricide metarhizium anisopliae","volume":"46","author":"Krieger de Moraes","year":"2003","journal-title":"Curr. Microbiol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"R40","DOI":"10.1186\/gb-2011-12-4-r40","article-title":"Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma","volume":"12","author":"Kubicek","year":"2011","journal-title":"Genome Biol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1016\/j.jip.2018.10.008","article-title":"Microbial biopesticides for insect pest management in India: Current status and future prospects","volume":"165","author":"Kumar","year":"2019","journal-title":"J. Invertebr. Pathol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"1875","DOI":"10.3390\/polym3041875","article-title":"Biomedical activity of chitin\/chitosan based materials\u2014Influence of physicochemical properties apart from molecular weight and degree of N-acetylation","volume":"3","author":"Kumirska","year":"2011","journal-title":"Polymers"},{"key":"B64","doi-asserted-by":"publisher","first-page":"243","DOI":"10.1007\/s00294-015-0530-x","article-title":"Fungal chitinases: function, regulation, and potential roles in plant\/pathogen interactions","volume":"62","author":"Langner","year":"2016","journal-title":"Curr. Genet."},{"key":"B65","doi-asserted-by":"publisher","first-page":"1723","DOI":"10.1111\/febs.15808","article-title":"Function of pH-dependent transcription factor PacC in regulating development, pathogenicity, and mycotoxin biosynthesis of phytopathogenic fungi","volume":"289","author":"Li","year":"2022","journal-title":"FEBS J."},{"key":"B66","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1080\/03601234.2012.668455","article-title":"Construction of transgenic Trichoderma koningi with chit42 of Metarhizium anisopliae and analysis of its activity against the Asian corn borer","volume":"47","author":"Li","year":"2012","journal-title":"J. Environ. Sci. Health Part B"},{"key":"B67","doi-asserted-by":"publisher","DOI":"10.3390\/jof8060602","article-title":"Host\u2013pathogen interactions between metarhizium spp. and locusts","volume":"8","author":"Li","year":"2022","journal-title":"J. Fungi"},{"key":"B68","doi-asserted-by":"publisher","DOI":"10.1080\/19490976.2022.2143221","article-title":"Nucleotide binding as an allosteric regulatory mechanism for Akkermansia muciniphila \u03b2-N-acetylhexosaminidase Am2136","volume":"14","author":"Li","year":"2022","journal-title":"Gut Microbes"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1016\/j.fgb.2021.103612","article-title":"Regulation of conidiation, polarity growth, and pathogenicity by MrSte12 transcription factor in entomopathogenic fungus, Metarhizium rileyi","volume":"155","author":"Lin","year":"2021","journal-title":"Fungal Genet. Biol."},{"key":"B70","doi-asserted-by":"publisher","first-page":"512","DOI":"10.2174\/138945012799499730","article-title":"Comparative biochemistry of GH3, GH20 and GH84 \u03b2-N-acetyl-Dhexosaminidases and recent progress in selective inhibitor discovery","volume":"13","author":"Liu","year":"2012","journal-title":"Curr. Drug Targets"},{"key":"B71","doi-asserted-by":"publisher","first-page":"5137","DOI":"10.1111\/j.1742-4658.2009.07211.x","article-title":"The \u03b2-N-acetylglucosaminidases NAG1 and NAG2 are essential for growth of Trichoderma atroviride on chitin","volume":"276","author":"L\u00f3pez-Mond\u00e9jar","year":"2009","journal-title":"FEBS J."},{"key":"B72","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.funk-0001-2016","article-title":"The insect pathogens","volume":"5","author":"Lovett","year":"2017","journal-title":"Microbiol. Spectr."},{"key":"B73","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2023.1329843","article-title":"A life-and-death struggle: interaction of insects with entomopathogenic fungi across various infection stages","volume":"14","author":"Ma","year":"2024","journal-title":"Front. Immunol."},{"key":"B74","doi-asserted-by":"publisher","first-page":"4887","DOI":"10.1074\/jbc.M114.621110","article-title":"N-acetylglucosaminidases from CAZy family GH3 are really glycoside phosphorylases, thereby explaining their use of histidine as an acid\/base catalyst in place of glutamic acid*","volume":"290","author":"Macdonald","year":"2015","journal-title":"J. Biol. Chem."},{"key":"B75","doi-asserted-by":"publisher","DOI":"10.3390\/biomimetics9050297","article-title":"Update on chitin and chitosan from insects: sources, production, characterization, and biomedical applications","volume":"9","author":"Mei","year":"2024","journal-title":"Biomimetics"},{"key":"B76","doi-asserted-by":"publisher","first-page":"10.1128\/msystems.00499","DOI":"10.1128\/msystems.00499-21","article-title":"A novel nitrogen and carbon metabolism regulatory cascade is implicated in entomopathogenicity of the fungus metarhizium robertsii","volume":"6","author":"Meng","year":"2021","journal-title":"mSystems"},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.3389\/ffunb.2023.1276287","article-title":"Utilization of Metarhizium as an insect biocontrol agent and a plant bioinoculant with special reference to Brazil","volume":"4","author":"Mesquita","year":"2023","journal-title":"Front. Fungal Biol."},{"key":"B78","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1016\/B978-0-08-088504-9.00235-X","article-title":"Biological control","volume-title":"Comprehensive biotechnology","author":"Moazami","year":"2011"},{"key":"B79","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1016\/j.funeco.2019.06.004","article-title":"Generalist and specialist Metarhizium insect pathogens retain ancestral ability to colonize plant roots","volume":"41","author":"Moonjely","year":"2019","journal-title":"Fungal Ecol."},{"key":"B80","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1146\/annurev-phyto-082712-102353","article-title":"Trichoderma research in the genome era","volume":"51","author":"Mukherjee","year":"2013","journal-title":"Annu. Rev. Phytopathol."},{"key":"B81","doi-asserted-by":"publisher","DOI":"10.3390\/catal10040365","article-title":"\u03b2-N-acetylhexosaminidases for carbohydrate synthesis via trans-glycosylation","volume":"10","author":"Muschiol","year":"2020","journal-title":"Catalysts"},{"key":"B82","doi-asserted-by":"publisher","first-page":"235","DOI":"10.47371\/mycosci.2024.07.001","article-title":"Phylogenetic classification and physiological and ecological traits of Metarhizium spp","volume":"65","author":"Nishi","year":"2024","journal-title":"Mycoscience"},{"key":"B83","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1590\/1678-4685-GMB-2017-0363","article-title":"Molecular evolution and transcriptional profile of GH3 and GH20 \u03b2-N-acetylglucosaminidases in the entomopathogenic fungus Metarhizium anisopliae","volume":"41","author":"Oliveira","year":"2018","journal-title":"Genet. Mol. Biol."},{"key":"B84","doi-asserted-by":"publisher","first-page":"357","DOI":"10.3390\/insects4030357","article-title":"Action on the surface: entomopathogenic fungi versus the insect cuticle","volume":"4","author":"Ortiz-Urquiza","year":"2013","journal-title":"Insects"},{"key":"B85","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/bs.adgen.2015.11.003","article-title":"Molecular genetics of beauveria bassiana infection of insects","volume":"94","author":"Ortiz-Urquiza","year":"2016","journal-title":"Adv. Genet."},{"key":"B86","doi-asserted-by":"publisher","first-page":"BSR2018032300","DOI":"10.1042\/BSR20180323","article-title":"Chitinase: diversity, limitations, and trends in engineering for suitab le applications","volume":"38","author":"Oyeleye","year":"2018","journal-title":"Biosci. Rep."},{"key":"B87","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1111\/j.1365-2672.2007.03567.x","article-title":"Effect of chitosan on hyphal growth and spore germination of plant pathogenic and biocontrol fungi","volume":"104","author":"Palma-Guerrero","year":"2008","journal-title":"J. Appl. Microbiol."},{"key":"B88","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-660","article-title":"The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species","volume":"15","author":"Pattemore","year":"2014","journal-title":"BMC Genomics"},{"key":"B89","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1139\/cjm-2019-0129","article-title":"Identification and characterization of the glycoside hydrolase family 18 genes from the entomopathogenic fungus Isaria cicadae genome","volume":"66","author":"Peng","year":"2020","journal-title":"Can. J. Microbiol."},{"key":"B90","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.vetpar.2014.02.011","article-title":"Enzymatic activities and effects of mycovirus infection on the virulence of Metarhizium anisopliae in Rhipicephalus microplus","volume":"203","author":"Perinotto","year":"2014","journal-title":"Vet. Parasitol."},{"key":"B91","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1139\/m97-045","article-title":"Purification and characterization of an extracellular chitinase from the entomopathogen Metarhizium anisopliae","volume":"43","author":"Pinto","year":"1997","journal-title":"Can. J. Microbiol."},{"key":"B92","doi-asserted-by":"publisher","DOI":"10.1016\/j.micres.2024.127922","article-title":"Sterol regulatory element-binding proteins mediate intrinsic fungicide tolerance and antagonism in the fungal biocontrol agent Clonostachys rosea IK726","volume":"289","author":"Piombo","year":"2024","journal-title":"Microbiol. Res."},{"key":"B93","doi-asserted-by":"publisher","DOI":"10.3390\/biology10121319","article-title":"Current perspectives on chitinolytic enzymes and their agro-industrial applications","volume":"10","author":"Poria","year":"2021","journal-title":"Biology"},{"key":"B94","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1016\/j.ijbiomac.2022.03.037","article-title":"The transcription factor Ron1 is required for chitin metabolism, asexual development and pathogenicity in Beauveria bassiana, an entomopathogenic fungus","volume":"206","author":"Qiu","year":"2022","journal-title":"Int. J. Biol. Macromol."},{"key":"B95","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.fbr.2022.04.001","article-title":"Myco-chitinases as versatile biocatalysts for translation of coastal residual resources to eco-competent chito-bioactives","volume":"41","author":"Rajput","year":"2022","journal-title":"Fungal Biol. Rev."},{"key":"B96","doi-asserted-by":"publisher","first-page":"220","DOI":"10.1007\/s00284-015-0943-2","article-title":"Secretome Analysis of Metarhizium anisopliae Under Submerged Conditions Using Bombyx mori Chrysalis to Induce Expression of Virulence-Related Proteins","volume":"72","author":"Rustiguel","year":"2016","journal-title":"Curr. Microbiol."},{"key":"B97","doi-asserted-by":"publisher","first-page":"874","DOI":"10.1016\/j.toxicon.2009.12.012","article-title":"Conidial surface proteins of Metarhizium anisopliae: Source of activities related with toxic effects, host penetration and pathogenesis","volume":"55","author":"Santi","year":"2010","journal-title":"Toxicon"},{"key":"B98","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1016\/j.funbio.2010.01.006","article-title":"Metarhizium anisopliae host\u2013pathogen interaction: differential immunoproteomics reveals proteins involved in the infection process of arthropods","volume":"114","author":"Santi","year":"2010","journal-title":"Fungal Biol."},{"key":"B99","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/978-981-16-3989-0_2","article-title":"Entomopathogenic fungi: current status and prospects","volume-title":"New and future development in biopesticide research: biotechnological exploration","author":"Santos","year":"2022"},{"key":"B100","doi-asserted-by":"publisher","DOI":"10.1093\/femsle\/fnab066","article-title":"The deletion of chiMaD1, a horizontally acquired chitinase of Metarhizium anisopliae, led to higher virulence towards the cattle tick (Rhipicephalus microplus)","volume":"368","author":"Sbaraini","year":"2021","journal-title":"FEMS Microbiol. Lett."},{"key":"B101","doi-asserted-by":"publisher","first-page":"R320","DOI":"10.1016\/j.cub.2011.02.045","article-title":"Two-component systems and their co-option for eukaryotic signal transduction","volume":"21","author":"Schaller","year":"2011","journal-title":"Curr. Biol."},{"key":"B102","doi-asserted-by":"publisher","first-page":"1267","DOI":"10.1016\/j.toxicon.2010.03.008","article-title":"Metarhizium anisopliae enzymes and toxins","volume":"56","author":"Schrank","year":"2010","journal-title":"Toxicon"},{"key":"B103","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1006\/jipa.2001.5067","article-title":"Transformants of Metarhizium anisopliae sf. anisopliae overexpressing chitinase from Metarhizium anisopliae sf. acridum show early induction of native chitinase but are not altered in pathogenicity to Manduca sexta","volume":"78","author":"Screen","year":"2001","journal-title":"J. Invertebr. Pathol."},{"key":"B104","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.fbr.2008.03.002","article-title":"Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions","volume":"22","author":"Seidl","year":"2008","journal-title":"Fungal Biol. Rev."},{"key":"B105","doi-asserted-by":"publisher","first-page":"5923","DOI":"10.1111\/j.1742-4658.2005.04994.x","article-title":"A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases","volume":"272","author":"Seidl","year":"2005","journal-title":"FEBS J."},{"key":"B106","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/B978-0-444-59576-8.00005-9","article-title":"Molecular evolution of Trichoderma chitinases","volume-title":"Biotechnology and biology of trichoderma","author":"Seidl-Seiboth","year":"2014"},{"key":"B107","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1128\/ec.00266-14","article-title":"MrSkn7 controls sporulation, cell wall integrity, autolysis, and virulence in metarhizium robertsii","volume":"14","author":"Shang","year":"2015","journal-title":"Eukaryot. Cell"},{"key":"B108","doi-asserted-by":"publisher","DOI":"10.3390\/jof11030223","article-title":"Transcription factors in biocontrol fungi","volume":"11","author":"Song","year":"2025","journal-title":"J. Fungi"},{"key":"B109","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1007\/s11274-015-1801-x","article-title":"Role of two Nomuraea rileyi transmembrane sensors Sho1p and Sln1p in adaptation to stress due to changing culture conditions during microsclerotia development","volume":"31","author":"Song","year":"2015","journal-title":"World J. Microbiol. Biotechnol."},{"key":"B110","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.01946","article-title":"The maCreA gene regulates normal conidiation and microcycle conidiation in metarhizium acridum","volume":"10","author":"Song","year":"2019","journal-title":"Front. Microbiol."},{"key":"B111","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-14-411","article-title":"Comparative transcriptome analysis of microsclerotia development in Nomuraea rileyi","volume":"14","author":"Song","year":"2013","journal-title":"BMC Genomics"},{"key":"B112","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-822","article-title":"Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins","volume":"15","author":"Staats","year":"2014","journal-title":"BMC Genomics"},{"key":"B113","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.funbio.2012.12.006","article-title":"Metarhizium anisopliae chitinase CHIT30 is involved in heat-shock stress and contributes to virulence against Dysdercus Peruvianus","volume":"117","author":"Staats","year":"2013","journal-title":"Fungal Biol."},{"key":"B114","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1016\/0022-2011(91)90188-V","article-title":"Characterization of chitinase and chitobiase produced by the entomopathogenic fungus Metarhizium anisopliae","volume":"58","author":"St. Leger","year":"1991","journal-title":"J. Invertebr. Pathol."},{"key":"B115","doi-asserted-by":"publisher","first-page":"907","DOI":"10.1128\/aem.62.3.907-912.1996","article-title":"Characterization and Ultrastructural Localization of Chitinases from Metarhizium anisopliae, M. flavoviride, and Beauveria bassiana during Fungal Invasion of Host (Manduca sexta) Cuticle","volume":"62","author":"St. Leger","year":"1996","journal-title":"Appl. Environ. Microbiol."},{"key":"B116","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.200307","article-title":"Metarhizium: jack of all trades, master of many","volume":"10","author":"St. Leger","year":"2020","journal-title":"Open Biol."},{"key":"B117","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1271\/bbb.62.60","article-title":"Cloning and characterization of a chitinase-encoding gene (chiA) from Aspergillus nidulans, disruption of which decreases germination frequency and hyphal growth","volume":"62","author":"Takaya","year":"1998","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"B118","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1186\/s13068-016-0538-6","article-title":"Natural diversity of cellulases, xylanases, and chitinases in bacteria","volume":"9","author":"Talamantes","year":"2016","journal-title":"Biotechnol. Biofuels"},{"key":"B119","doi-asserted-by":"publisher","DOI":"10.3389\/ffunb.2022.911366","article-title":"New downstream signaling branches of the mitogen-activated protein kinase cascades identified in the insect pathogenic and plant symbiotic fungus metarhizium robertsii","volume":"3","author":"Tang","year":"2022","journal-title":"Front. Fungal Biol."},{"key":"B120","doi-asserted-by":"publisher","first-page":"e23","DOI":"10.1002\/npp2.23","article-title":"Metarhizium fungi as plant symbionts","volume":"2","author":"Tang","year":"2025","journal-title":"New Plant Prot."},{"key":"B121","doi-asserted-by":"publisher","DOI":"10.1186\/1756-0500-5-581","article-title":"Bacterial and fungal chitinase chiJ orthologs evolve under different selective constraints following horizontal gene transfer","volume":"5","author":"Ubhayasekera","year":"2012","journal-title":"BMC Res. Notes"},{"key":"B122","doi-asserted-by":"publisher","first-page":"3072","DOI":"10.1111\/febs.70015","article-title":"N-acetylglucosamine sensing in the filamentous soil fungus Trichoderma reesei","volume":"292","author":"Ullah","year":"2025","journal-title":"FEBS J."},{"key":"B123","doi-asserted-by":"publisher","first-page":"e0128075","DOI":"10.1371\/journal.pone.0128075","article-title":"Structural-functional analysis reveals a specific domain organization in family GH20 hexosaminidases","volume":"10","author":"Val-Cid","year":"2015","journal-title":"PloS One"},{"key":"B124","doi-asserted-by":"crossref","first-page":"1924","DOI":"10.1016\/B0-08-043152-6\/00350-8","article-title":"Cuticle","volume-title":"Encyclopedia of materials: science and technology","author":"Vincent","year":"2001"},{"key":"B125","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1111\/j.1574-6968.2001.tb10710.x","article-title":"Antifungal activity of a novel endochitinase gene (chit36) from Trichoderma harzianum Rifai TM","volume":"200","author":"Viterbo","year":"2001","journal-title":"FEMS Microbiol. Lett."},{"key":"B126","doi-asserted-by":"publisher","first-page":"20230075","DOI":"10.1098\/rsfs.2023.0075","article-title":"Structural diversity of crustacean exoskeletons and its implications for biomimetics","volume":"14","author":"Vittori","year":"2024","journal-title":"Interface Focus"},{"key":"B127","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1146\/annurev-ento-031616-035509","article-title":"Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements","volume":"62","author":"Wang","year":"2017","journal-title":"Annu. Rev. Entomol."},{"key":"B128","doi-asserted-by":"publisher","first-page":"e1011397","DOI":"10.1371\/journal.ppat.1011397","article-title":"A novel partitivirus orchestrates conidiation, stress response, pathogenicity, and secondary metabolism of the entomopathogenic fungus Metarhizium majus","volume":"19","author":"Wang","year":"2023","journal-title":"PloS Pathog."},{"key":"B129","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1134\/S002689331805014X","article-title":"Transgenic Expression of chit42 gene from Metarhizium anisopliae in Trichoderma harzianum Enhances Antagonistic Activity against Botrytis cinerea","volume":"52","author":"Xia","year":"2018","journal-title":"Mol. Biol."},{"key":"B130","doi-asserted-by":"publisher","DOI":"10.1038\/srep00483","article-title":"Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana","volume":"2","author":"Xiao","year":"2012","journal-title":"Sci. Rep."},{"key":"B131","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1016\/j.fgb.2008.02.008","article-title":"Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites","volume":"45","author":"Yamazaki","year":"2008","journal-title":"Fungal Genet. Biol."},{"key":"B132","doi-asserted-by":"publisher","first-page":"5181","DOI":"10.1021\/jf500912b","article-title":"Biochemical characterization of the first fungal glycoside hydrolyase family 3 \u03b2-N-acetylglucosaminidase from rhizomucor miehei","volume":"62","author":"Yang","year":"2014","journal-title":"J. Agric. Food Chem."},{"key":"B133","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1186\/s12985-023-02217-6","article-title":"Hypovirulence-associated mycovirus epidemics cause pathogenicity degeneration of Beauveria bassiana in the field","volume":"20","author":"Zhang","year":"2023","journal-title":"Virol. J."},{"key":"B134","doi-asserted-by":"publisher","first-page":"e3001360","DOI":"10.1371\/journal.pbio.3001360","article-title":"A novel cascade allows Metarhizium robertsii to distinguish cuticle and hemocoel microenvironments during infection of insects","volume":"19","author":"Zhang","year":"2021","journal-title":"PloS Biol."}],"container-title":["Frontiers in Fungal Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/ffunb.2026.1732437\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,17]],"date-time":"2026-02-17T10:18:06Z","timestamp":1771323486000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/ffunb.2026.1732437\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,17]]},"references-count":134,"alternative-id":["10.3389\/ffunb.2026.1732437"],"URL":"https:\/\/doi.org\/10.3389\/ffunb.2026.1732437","relation":{},"ISSN":["2673-6128"],"issn-type":[{"value":"2673-6128","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,17]]},"article-number":"1732437"}}