Killer toxin-like chitinases in filamentous fungi: Structure, regulation and potential roles in fungal biology

Fungal Biology Reviews - Tập 33 - Trang 123-132 - 2019
Georgios Tzelepis1, Magnus Karlsson2
1Department of Plant Biology, Uppsala BioCenter and Linnean Center for Plant Biology, Swedish University of Agricultural Sciences, Box 7080, S-75007 Uppsala, Sweden
2Department of Forest Mycology and Plant Pathology, Uppsala BioCenter, Swedish University of Agricultural Sciences, Box 7026, S-75007 Uppsala, Sweden

Tài liệu tham khảo

Baker, 2009, Chitinases are essential for sexual development but not vegetative growth in Cryptococcus neoformans, Eukaryot. Cell, 8, 1692, 10.1128/EC.00227-09 Bartnicki-Garcia, 1968, Cell wall chemistry, morphogenesis, and taxonomy of fungi, Annu. Rev. Microbiol., 22, 87, 10.1146/annurev.mi.22.100168.000511 Boldo, 2009, Endochitinase CHI2 of the biocontrol fungus Metarhizium anisopliae affects its virulence toward the cotton stainer bug Dysdercus peruvianus, Curr. Genet., 55, 551, 10.1007/s00294-009-0267-5 Boller, 2009, A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors, Annu. Rev. Plant Biol., 60, 379, 10.1146/annurev.arplant.57.032905.105346 Boraston, 2004, Carbohydrate-binding modules: fine-tuning polysaccharide recognition, Biochem. J., 382, 769, 10.1042/BJ20040892 Bowman, 2006, The structure and synthesis of the fungal cell wall, Bioessays, 28, 799, 10.1002/bies.20441 Buist, 2008, LysM, a widely distributed protein motif for binding to peptidoglycans, Mol. Microbiol., 68, 838, 10.1111/j.1365-2958.2008.06211.x Butler, 1991, Kluyveromyces lactis toxin has an essential chitinase activity, Eur. J. Biochem., 199, 483, 10.1111/j.1432-1033.1991.tb16147.x Chaudhary, 2013, Chitin synthase inhibitors as antifungal agents, Mini Rev. Med. Chem., 13, 222 de Jonge, 2009, Fungal LysM effectors: extinguishers of host immunity?, Trends Microbiol., 17, 151, 10.1016/j.tim.2009.01.002 de Jonge, 2010, Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants, Science, 329, 953, 10.1126/science.1190859 de Nobel, 2000, Cell wall maintenance in fungi, Trends Microbiol., 8, 344, 10.1016/S0966-842X(00)01805-9 Dunkler, 2005, Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae, Fungal Genet. Biol., 42, 935, 10.1016/j.fgb.2005.08.001 Gooday, 1990, Physiology of microbial degradation of chitin and chitosan, Biodegradation, 1, 177, 10.1007/BF00058835 Gortari, 2013, Biotechnological processes for chitin recovery out of crustacean waste: A mini review, Electron. J. Biotechnol., 16 Gruber, 2011, Analysis of subgroup C of fungal chitinases containing chitin-binding and LysM modules in the mycoparasite Trichoderma atroviride, Glycobiology, 21, 122, 10.1093/glycob/cwq142 Gruber, 2011, Differential regulation of orthologous chitinase genes in mycoparasitic Trichoderma species, Appl. Environ. Microbiol., 77, 7217, 10.1128/AEM.06027-11 Gruber, 2012, Self versus non-self: fungal cell wall degradation in Trichoderma, Microbiology-Sgm, 158, 26, 10.1099/mic.0.052613-0 Henrissat, 1991, A classification of glycosyl hydrolases based on amino acid sequence similarities, Biochem. J., 280, 309, 10.1042/bj2800309 Hill, 1991, Ascaris-Suum: stage-specific differences in lectin binding to the larval cuticle, Exp. Parasitol., 73, 376, 10.1016/0014-4894(91)90110-I Horn, 2006, Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens, FEBS J., 273, 491, 10.1111/j.1742-4658.2005.05079.x Ihrmark, 2010, Comparative molecular evolution of Trichoderma chitinases in response to mycoparasitic interactions, Evol. Bioinform., 6, 1, 10.4137/EBO.S4198 Kapaun, 1995, A chitin-like glycan in the cell wall of a Chlorella sp (Chlorococcales, Chlorophyceae), Planta, 197, 577, 10.1007/BF00191563 Karlsson, 2018, Necrotrophic mycoparasites and their genomes, 1005 Karlsson, 2016, Functional differentiation of chitinases in the white-rot fungus Phanerochaete chrysosporium, Fungal Ecol., 22, 52, 10.1016/j.funeco.2016.04.004 Karlsson, 2015, Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea, Genome Biol. Evol., 7, 465, 10.1093/gbe/evu292 Karlsson, 2009, Evolution of family 18 glycoside hydrolases: Diversity, domain-structures and phylogenetic relationships, J. Mol. Microbiol. Biotechnol., 16, 208, 10.1159/000151220 Karlsson, 2008, Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection, Evol. Bioinform., 4, 47, 10.4137/EBO.S604 Keegstra, 2010, Plant cell walls, Plant Physiol., 154, 483, 10.1104/pp.110.161240 Keyhani, 1999, Physiological aspects of chitin catabolism in marine bacteria, BBA Gen. Subj., 1473, 108, 10.1016/S0304-4165(99)00172-5 Klis, 2002, Dynamics of cell wall structure in Saccharomyces cerevisiae, FEMS Microbiol. Rev., 26, 239, 10.1111/j.1574-6976.2002.tb00613.x Kolbusz, 2014, Transcriptome and exoproteome analysis of utilization of plant-derived biomass by Myceliophthora thermophila, Fungal Genet. Biol., 72, 10, 10.1016/j.fgb.2014.05.006 Kubicek, 2011, Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma, Genome Biol., 12, R40, 10.1186/gb-2011-12-4-r40 Kuranda, 1991, Chitinase is required for cell separation during growth of Saccharomyces cerevisiae, J. Biol. Chem., 266, 19758, 10.1016/S0021-9258(18)55057-2 Kurita, 2006, Chitin and chitosan: Functional biopolymers from marine crustaceans, Mar. Biotechnol., 8, 203, 10.1007/s10126-005-0097-5 Latge, 2007, The cell wall: a carbohydrate armor for the fungal cell, Mol. Microbiol., 66, 279, 10.1111/j.1365-2958.2007.05872.x Lauge, 1997, The in planta-produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors, Mol. Plant Microbe Interact., 10, 725, 10.1094/MPMI.1997.10.6.725 Lombard, 2014, The carbohydrate-active enzymes database (CAZy) in 2013, Nucleic Acids Res., 42, D490, 10.1093/nar/gkt1178 Magliani, 1997, Yeast killer systems, Clin. Microbiol. Rev., 10, 369, 10.1128/CMR.10.3.369 Mamarabadi, 2008, Three endochitinase-encoding genes identified in the biocontrol fungus Clonostachys rosea are differentially expressed, Curr. Genet., 54, 57, 10.1007/s00294-008-0199-5 Merzendorfer, 2003, Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases, J. Exp. Biol., 206, 4393, 10.1242/jeb.00709 Mulisch, 1993, Chitin in protistan organisms; distribution, synthesis and deposition, Eur. J. Protistol., 29, 1, 10.1016/S0932-4739(11)80291-9 Newman, 2013, MAMP (microbe-associated molecular pattern) triggered immunity in plants, Front. Plant Sci., 4, 139, 10.3389/fpls.2013.00139 Nygren, 2018, The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey, Evol. Appl., 11, 931, 10.1111/eva.12609 Peters, 1972, Occurrence of chitin in mollusca, Comp. Biochem. Physiol., 41, 541 Quandt, 2016, Differential expression of genes involved in host recognition, attachment, and degradation in the mycoparasite Tolypocladium ophioglossoides, G3, 6, 731, 10.1534/g3.116.027045 Seidl, 2005, A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases, FEBS J., 272, 5923, 10.1111/j.1742-4658.2005.04994.x Seidl-Seiboth, 2014, Molecular evolution of Trichoderma chitinases, vol. 5, 67 Seidl-Seiboth, 2013, Spore germination of Trichoderma atroviride is inhibited by its LysM protein TAL6, FEBS J., 280, 1226, 10.1111/febs.12113 Shin, 2009, Differential roles of the ChiB chitinase in autolysis and cell death of Aspergillus nidulans, Eukaryot. Cell, 8, 738, 10.1128/EC.00368-08 Specht, 1996, The chsD and chsE genes of Aspergillus nidulans and their roles in chitin synthesis, Fungal Genet. Biol., 20, 153, 10.1006/fgbi.1996.0030 Spindler, 1990, Chitin metabolism; a target for drugs against parasites, Parasitol. Res., 76, 283, 10.1007/BF00928180 Stals, 2010, Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina, FEMS Microbiol. Lett., 303, 9, 10.1111/j.1574-6968.2009.01849.x Stark, 1986, The killer toxin of Kluyveromyces lactis; characterization of the toxin subunits and identification of the genes which encode them, EMBO J., 5, 1995, 10.1002/j.1460-2075.1986.tb04455.x Stark, 1990, The plasmid-encoded killer system of Kluyveromyces lactis: a review, Yeast, 6, 1, 10.1002/yea.320060102 Stergiopoulos, 2012, In silico characterization and molecular evolutionary analysis of a novel superfamily of fungal effector proteins, Mol. Biol. Evol., 29, 3371, 10.1093/molbev/mss143 Stergiopoulos, 2010, Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots, Proc. Natl. Acad. Sci. U.S.A., 107, 7610, 10.1073/pnas.1002910107 Tzelepis, 2017, Deglycosylating enzymes acting on N-glycans in fungi: Insights from a genome survey, BBA Gen. Subj., 1861, 2551, 10.1016/j.bbagen.2017.08.022 Tzelepis, 2015, Identifying glycoside hydrolase family 18 genes in the mycoparasitic fungal species Clonostachys rosea, Microbiology-Sgm, 161, 1407, 10.1099/mic.0.000096 Tzelepis, 2014, Endo-β-N-acetylglucosamidases (ENGases) in the fungus Trichoderma atroviride: Possible involvement of the filamentous fungi-specific cytosolic ENGase in the ERAD process, Biochem. Biophys. Res. Commun., 449, 256, 10.1016/j.bbrc.2014.05.017 Tzelepis, 2014, Functional analysis of the C-II subgroup killer toxin-like chitinases in the filamentous ascomycete Aspergillus nidulans, Fungal Genet. Biol., 64, 58, 10.1016/j.fgb.2013.12.009 Tzelepis, 2012, Functional analysis of glycoside hydrolase family 18 and 20 genes in Neurospora crassa, Fungal Genet. Biol., 49, 717, 10.1016/j.fgb.2012.06.013 van Aalten, 2001, Structural insights into the catalytic mechanism of a family 18 exo-chitinase, Proc. Natl. Acad. Sci. U.S.A., 98, 8979, 10.1073/pnas.151103798 Wouters, 2005, Evolution of distinct EGF domains with specific functions, Protein Sci., 14, 1091, 10.1110/ps.041207005 Zhang, 2009, Evolutionary genomics of LysM genes in land plants, BMC Evol. Biol., 9, 183, 10.1186/1471-2148-9-183