Skip to main content
Log in

Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions

  • Review
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

In the past decades our knowledge about fungal cell wall architecture increased tremendously and led to the identification of many enzymes involved in polysaccharide synthesis and remodeling, which are also of biotechnological interest. Fungal cell walls play an important role in conferring mechanic stability during cell division and polar growth. Additionally, in phytopathogenic fungi the cell wall is the first structure that gets into intimate contact with the host plant. A major constituent of fungal cell walls is chitin, a homopolymer of N-acetylglucosamine units. To ensure plasticity, polymeric chitin needs continuous remodeling which is maintained by chitinolytic enzymes, including lytic polysaccharide monooxygenases N-acetylglucosaminidases, and chitinases. Depending on the species and lifestyle of fungi, there is great variation in the number of encoded chitinases and their function. Chitinases can have housekeeping function in plasticizing the cell wall or can act more specifically during cell separation, nutritional chitin acquisition, or competitive interaction with other fungi. Although chitinase research made huge progress in the last decades, our knowledge about their role in phytopathogenic fungi is still scarce. Recent findings in the dimorphic basidiomycete Ustilago maydis show that chitinases play different physiological functions throughout the life cycle and raise questions about their role during plant-fungus interactions. In this work we summarize these functions, mechanisms of chitinase regulation and their putative role during pathogen/host interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams DJ (2004) Fungal cell wall chitinases and glucanases. Microbiology 150:2029–2035

    Article  CAS  PubMed  Google Scholar 

  • Akamatsu A, Wong Hann L, Fujiwara M, Okuda J, Nishide K, Uno K, Imai K, Umemura K, Kawasaki T, Kawano Y et al (2013) An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 13:465–476

    Article  CAS  PubMed  Google Scholar 

  • Baker LG, Specht CA, Lodge JK (2009) Chitinases are essential for sexual development but not vegetative growth in Cryptococcus neoformans. Eukaryot Cell 8:1692–1705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baladrón V, Ufano S, Duenas E, Martin-Cuadrado AB, del Rey F, Vazquez de Aldana CR (2002) Eng1p, an endo-1,3-β-glucanase localized at the daughter side of the septum, is involved in cell separation in Saccharomyces cerevisiae. Eukaryot Cell 1:774–786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beeson WT, Vu VV, Span EA, Phillips CM, Marletta MA (2015) Cellulose degradation by polysaccharide monooxygenases. Annu Rev Biochem 84:923–946

    Article  CAS  PubMed  Google Scholar 

  • Ben Khaled S, Postma J, Robatzek S (2015) A moving view: subcellular trafficking processes in pattern recognition receptor-triggered plant immunity. Annu Rev Phytopathol 53:379–402

    Article  CAS  PubMed  Google Scholar 

  • Bowen AR, Chen-Wu JL, Momany M, Young R, Szaniszlo PJ, Robbins PW (1992) Classification of fungal chitin synthases. Proc Natl Acad Sci USA 89:519–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. BioEssays 28:799–808

    Article  PubMed  Google Scholar 

  • Brace J, Hsu J, Weiss EL (2010) Mitotic exit control of the Saccharomyces cerevisiae Ndr/LATS kinase Cbk1 regulates daughter cell separation after cytokinesis. Mol Cell Biol 31:721–735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brunner K, Peterbauer CK, Mach RL, Lorito M, Zeilinger S, Kubicek CP (2003) The Nag1 N-acetylglucosaminidase of Trichoderma atroviride is essential for chitinase induction by chitin and of major relevance to biocontrol. Curr Genet 43:289–295

    Article  CAS  PubMed  Google Scholar 

  • Cabib E, Arroyo J (2013) How carbohydrates sculpt cells: chemical control of morphogenesis in the yeast cell wall. Nat Rev Microbiol 11:648–655

    Article  CAS  PubMed  Google Scholar 

  • Cabib E, Blanco N, Grau C, Rodriguez-Pena JM, Arroyo J (2007) Crh1p and Crh2p are required for the cross-linking of chitin to beta(1-6)glucan in the Saccharomyces cerevisiae cell wall. Mol Microbiol 63:921–935

    Article  CAS  PubMed  Google Scholar 

  • Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 3:e03766

    Article  PubMed Central  CAS  Google Scholar 

  • Carsolio C, Gutierrez A, Jimenez B, Van Montagu M, Herrera-Estrella A (1994) Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Proc Natl Acad Sci USA 91:10903–10907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carsolio C, Benhamou N, Haran S, Cortes C, Gutierrez A, Chet I, Herrera-Estrella A (1999) Role of the Trichoderma harzianum endochitinase gene, ech42, in mycoparasitism. Appl Environ Microbiol 65:929–935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaffin WL (2008) Candida albicans cell wall proteins. Microbiol Mol Biol Rev 72:495–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Chen X-Z, Qin L-N, Tao Y, Dong Z-Y (2015) Characterization and homologous overexpression of an N-acetylglucosaminidase Nag1 from Trichoderma reesei. Biochem Biophys Res Commun 459:184–188

    Article  CAS  PubMed  Google Scholar 

  • Colman-Lerner A, Chin TE, Brent R (2001) Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107:739–750

    Article  CAS  PubMed  Google Scholar 

  • Colussi PA, Specht CA, Taron CH (2005) Characterization of a nucleus-encoded chitinase from the yeast Kluyveromyces lactis. Appl Environ Microbiol 71:2862–2869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Z, Wang Y, Lei N, Wang K, Zhu T (2013) Botrytis cinerea chitin synthase BcChsVI is required for normal growth and pathogenicity. Curr Genet 59:119–128

    Article  CAS  PubMed  Google Scholar 

  • de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955

    Article  PubMed  CAS  Google Scholar 

  • de las Mercedes Dana M, Limón MC, Mejías R, Mach RL, Benítez T et al (2001) Regulation of chitinase 33 (chit33) gene expression in Trichoderma harzianum. Curr Genet 38:335–342

    Article  CAS  PubMed  Google Scholar 

  • Drouillard S, Armand S, Davies GJ, Vorgias CE, Henrissat B (1997) Serratia marcescens chitobiase is a retaining glycosidase utilizing substrate acetamido group participation. Biochem J 328(Pt 3):945–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dünkler A, Walther A, Specht CA, Wendland J (2005) Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae. Fungal Genet Biol 42:935–947

    Article  PubMed  CAS  Google Scholar 

  • Dünkler A, Jorde S, Wendland J (2008) An Ashbya gossypii cts2 mutant deficient in a sporulation-specific chitinase can be complemented by Candida albicans CHT4. Microbiol Res 163:701–710

    Article  PubMed  CAS  Google Scholar 

  • Durán A, Bowers B, Cabib E (1975) Chitin synthetase zymogen is attached to the yeast plasma membrane. Proc Natl Acad Sci USA 72:3952–3955

    Article  PubMed  PubMed Central  Google Scholar 

  • Egan MJ, McClintock MA, Reck-Peterson SL (2012) Microtubule-based transport in filamentous fungi. Curr Opin Microbiol 15:637–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eijsink VGH, Vaaje-Kolstad G, Vårum KM, Horn SJ (2008) Towards new enzymes for biofuels: lessons from chitinase research. Trends Biotechnol 26:228–235

    Article  CAS  PubMed  Google Scholar 

  • Feldbrügge M, Kämper J, Steinberg G, Kahmann R (2004) Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 7:666–672

    Article  PubMed  CAS  Google Scholar 

  • Frederiksen RF, Paspaliari DK, Larsen T, Storgaard BG, Larsen MH, Ingmer H, Palcic MM, Leisner JJ (2013) Bacterial chitinases and chitin-binding proteins as virulence factors. Microbiology 159:833–847

    Article  CAS  PubMed  Google Scholar 

  • García I, Jimenez D, Martin V, Duran A, Sanchez Y (2005) The alpha-glucanase Agn1p is required for cell separation in Schizosaccharomyces pombe. Biol Cell 97:569–576

    Article  PubMed  Google Scholar 

  • Gentzsch M, Tanner W (1997) Protein-O-glycosylation in yeast: protein-specific mannosyltransferases. Glycobiology 7:481–486

    Article  CAS  PubMed  Google Scholar 

  • Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B et al (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387–391

    Article  CAS  PubMed  Google Scholar 

  • Gruber S, Seidl-Seiboth V (2011) Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 158:26–34

    Article  PubMed  CAS  Google Scholar 

  • Gruber S, Kubicek CP, Seidl-Seiboth V (2011) Differential regulation of Orthologous chitinase genes in mycoparasitic Trichoderma species. Appl Environ Microbiol 77:7217–7226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartl L, Zach S, Seidl-Seiboth V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93:533–543

    Article  CAS  PubMed  Google Scholar 

  • Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K et al (2014) Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc Natl Acad Sci USA 111:E404–E413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heimel K, Scherer M, Schuler D, Kamper J (2010) The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell 22:2908–2922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henrissat B (1991) A classification of glycosyl hydrolases based on amino-acid-sequence similarities. Biochem J 280:309–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horn SJ, Sorbotten A, Synstad B, Sikorski P, Sorlie M, Varum KM, Eijsink VGH (2006) Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J 273:491–503

    Article  CAS  PubMed  Google Scholar 

  • Hours RA, Gortari MC (2013) Biotechnological processes for chitin recovery out of crustacean waste: a mini-review. Electron J Biotechnol 16:14

    Article  CAS  Google Scholar 

  • Ichinomiya M, Yamada E, Yamashita S, Ohta A, Horiuchi H (2005) Class I and class II chitin synthases are involved in septum formation in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 4:1125–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igarashi K, Uchihashi T, Koivula A, Wada M, Kimura S, Okamoto T, Penttila M, Ando T, Samejima M (2011) Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333:1279–1282

    Article  CAS  PubMed  Google Scholar 

  • Jashni MK, Dols IH, Iida Y, Boeren S, Beenen HG, Mehrabi R, Collemare J, de Wit PJ (2015) Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp. lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence. Mol Plant Microbe Interact 28:996–1008

    Article  CAS  PubMed  Google Scholar 

  • Jones CS, Kosman DJ (1980) Purification, properties, kinetics, and mechanism of beta-N-acetylglucosamidase from Aspergillus niger. J Biol Chem 255:11861–11869

    CAS  PubMed  Google Scholar 

  • Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci 103:11086–11091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kämper J, Kahmann R, Bölker M, Ma L-J, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101

    Article  PubMed  CAS  Google Scholar 

  • Karlsson M, Stenlid J (2008) Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evol Bioinform Online 4:47–60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JE, Lee HJ, Lee J, Kim KW, Yun SH, Shim WB, Lee YW (2009) Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Curr Genet 55:449–459

    Article  CAS  PubMed  Google Scholar 

  • Koepke J, Kaffarnik F, Haag C, Zarnack K, Luscombe NM, Konig J, Ule J, Kellner R, Begerow D, Feldbrugge M (2011) The RNA-binding protein Rrm4 is essential for efficient secretion of endochitinase Cts1. Mol Cell Proteomics 10:M111-011213

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kombrink A, Sanchez-Vallet A, Thomma BP (2011) The role of chitin detection in plant—pathogen interactions. Microbes Infect 13:1168–1176

    Article  CAS  PubMed  Google Scholar 

  • Kouzai Y, Nakajima K, Hayafune M, Ozawa K, Kaku H, Shibuya N, Minami E, Nishizawa Y (2013) CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol Biol 84:519–528

    Article  PubMed  CAS  Google Scholar 

  • Kuranda MJ, Robbins PW (1991) Chitinase is required for cell separation during growth of Saccharomyces cerevisiae. J Biol Chem 266:19758–19767

    CAS  PubMed  Google Scholar 

  • Lange J, Mohr U, Wiemken A, Boller T, Vogeli-Lange R (1996) Proteolytic processing of class IV chitinase in the compatible interaction of bean roots with Fusarium solani. Plant Physiol 111:1135–1144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langner T, Öztürk M, Hartmann S, Cord-Landwehr S, Moerschbacher B, Walton JD, Göhre V (2015) Chitinases are essential for cell separation in Ustilago maydis. Eukaryot Cell 14:846–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanver D, Berndt P, Tollot M, Naik V, Vranes M, Warmann T, Münch K, Rössel N, Kahmann R (2014) Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog 10:e1004272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Larsen T, Petersen BO, Storgaard BG, Duus JO, Palcic MM, Leisner JJ (2010) Characterization of a novel Salmonella Typhimurium chitinase which hydrolyzes chitin, chitooligosaccharides and an N-acetyllactosamine conjugate. Glycobiology 21:426–436

    Article  PubMed  CAS  Google Scholar 

  • Latgé J-P (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66:279–290

    Article  PubMed  CAS  Google Scholar 

  • Leake JR, Read DJ (1990) Chitin as a Nitrogen-source for mycorrhizal fungi. Mycol Res 94:993–995

    Article  CAS  Google Scholar 

  • Lenardon MD, Munro CA, Gow NA (2010) Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 13:416–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189:1145–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Liu Z, Song C, Hu Y, Han Z, She J, Fan F, Wang J, Jin C, Chang J et al (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–1164

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Grabherr HM, Willmann R, Kolb D, Brunner F, Bertsche U, Kuhner D, Franz-Wachtel M, Amin B, Felix G et al (2014) Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis. Elife 3:e01990

    PubMed Central  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495

    Article  CAS  PubMed  Google Scholar 

  • Lorito M, Mach RL, Sposato P, Strauss J, Peterbauer CK, Kubicek CP (1996) Mycoparasitic interaction relieves binding of the Cre1 carbon catabolite repressor protein to promoter sequences of the ech42 (endochitinase-encoding) gene in Trichoderma harzianum. Proc Natl Acad Sci USA 93:14868–14872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mach RL, Peterbauer CK, Payer K, Jaksits S, Woo SL, Zeilinger S, Kullnig CM, Lorito M, Kubicek CP (1999) Expression of two major chitinase genes of Trichoderma atroviride (T. harzianum P1) is triggered by different regulatory signals. Appl Environ Microbiol 65:1858–1863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maddi A, Bowman SM, Free SJ (2009) Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet Biol 46:768–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mamarabadi M, Jensen B, Lübeck M (2008) Three endochitinase-encoding genes identified in the biocontrol fungus Clonostachys rosea are differentially expressed. Curr Genet 54:57–70

    Article  CAS  PubMed  Google Scholar 

  • Mamarabadi M, Jensen DF, Lübeck M (2009) An N-acetyl-β-d-glucosaminidase gene, cr-nag1, from the biocontrol agent Clonostachys rosea is up-regulated in antagonistic interactions with Fusarium culmorum. Mycol Res 113:33–43

    Article  CAS  PubMed  Google Scholar 

  • Mancini Lombardi I, Palani S, Meitinger F, Darieva Z, Hofmann A, Sharrocks Andrew D, Pereira G (2013) Lre1 directly inhibits the NDR/lats kinase Cbk1 at the cell division site in a phosphorylation-dependent manner. Curr Biol 23:1736–1745

    Article  CAS  PubMed  Google Scholar 

  • Martin-Cuadrado AB (2003) The endo-beta-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe. J Cell Sci 116:1689–1698

    Article  CAS  PubMed  Google Scholar 

  • Mathé L, Van Dijck P (2013) Recent insights into Candida albicans biofilm resistance mechanisms. Curr Genet 59:251–264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BPHJ et al (2012) Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merzendorfer H (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206:4393–4412

    Article  CAS  PubMed  Google Scholar 

  • Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci 104:19613–19618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murata T, Amarume S, Hattori T, Tokuyama S, Tokuyasu K, Kawagishi H, Usui T (2005) Purification and characterization of a chitinase from Amycolatopsis orientalis with N-acetyllactosamine-repeating unit releasing activity. Biochem Biophys Res Commun 336:514–520

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa YS, Kudo M, Loose JSM, Ishikawa T, Totani K, Eijsink VGH, Vaaje-Kolstad G (2015) A small lytic polysaccharide monooxygenase from Streptomyces griseus targeting α- and β-chitin. FEBS J 282:1065–1079

    Article  CAS  PubMed  Google Scholar 

  • Naumann TA, Price NPJ (2012) Truncation of class IV chitinases from Arabidopsis by secreted fungal proteases. Mol Plant Pathol 13:1135–1139

    Article  CAS  PubMed  Google Scholar 

  • Naumann TA, Wicklow DT, Kendra DF (2009) Maize seed chitinase is modified by a protein secreted by Bipolaris zeicola. Physiol Mol Plant Pathol 74:134–141

    Article  CAS  Google Scholar 

  • Nelson B (2003) RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol Biol Cell 14:3782–3803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira-Garcia E, Valent B (2015) How eukaryotic filamentous pathogens evade plant recognition. Curr Opin Microbiol 26:92–101

    Article  CAS  PubMed  Google Scholar 

  • Patil RS, Ghormade VV, Deshpande MV (2000) Chitinolytic enzymes: an exploration. Enzyme Microb Technol 26:473–483

    Article  CAS  PubMed  Google Scholar 

  • Phillips CM, Beeson WT, Cate JH, Marletta MA (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6:1399–1406

    Article  CAS  PubMed  Google Scholar 

  • Roncero C (2002) The genetic complexity of chitin synthesis in fungi. Curr Genet 41:367–378

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Herrera J, Gonzalez-Prieto JM, Ruiz-Medrano R (2002) Evolution and phylogenetic relationships of chitin synthases from yeasts and fungi. FEMS Yeast Res 1:247–256

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Diaz A, Nkosi PJ, Murray S, Labib K (2012) The mitotic exit network and Cdc14 phosphatase initiate cytokinesis by counteracting CDK phosphorylations and blocking polarised growth. EMBO J 31:3620–3634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Vallet A, Saleem-Batcha R, Kombrink A, Hansen G, Valkenburg DJ, Thomma BP, Mesters JR (2013) Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2:e00790

    Article  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Vallet A, Mesters JR, Thomma BPHJ (2014) The battle for chitin recognition in plant-microbe interactions. FEMS Microbiol Rev 39:171–183

    Article  PubMed  Google Scholar 

  • Sarkari P, Reindl M, Stock J, Muller O, Kahmann R, Feldbrugge M, Schipper K (2014) Improved expression of single-chain antibodies in Ustilago maydis. J Biotechnol 191:165–175

    Article  CAS  PubMed  Google Scholar 

  • Schuster M, Treitschke S, Kilaru S, Molloy J, Harmer NJ, Steinberg G (2012) Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J 31:214–227

    Article  CAS  PubMed  Google Scholar 

  • Seidl V, Huemer B, Seiboth B, Kubicek CP (2005) A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J 272:5923–5939

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H et al (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin KS, Kwon NJ, Kim YH, Park HS, Kwon GS, Yu JH (2009) Differential roles of the ChiB chitinase in autolysis and cell death of Aspergillus nidulans. Eukaryot Cell 8:738–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinya T, Nakagawa T, Kaku H, Shibuya N (2015) Chitin-mediated plant–fungal interactions: catching, hiding and handshaking. Curr Opin Plant Biol 26:64–71

    Article  CAS  PubMed  Google Scholar 

  • Shoji J-Y, Kikuma T, Kitamoto K (2014) Vesicle trafficking, organelle functions, and unconventional secretion in fungal physiology and pathogenicity. Curr Opin Microbiol 20:1–9

    Article  CAS  PubMed  Google Scholar 

  • Sietsma JH, Beth Din A, Ziv V, Sjollema KA, Yarden O (1996) The localization of chitin synthase in membranous vesicles (chitosomes) in Neurospora crassa. Microbiology 142(Pt 7):1591–1596

    Article  CAS  PubMed  Google Scholar 

  • Silverman SJ, Sburlati A, Slater ML, Cabib E (1988) Chitin synthase 2 is essential for septum formation and cell division in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 85:4735–4739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starr TL, Pagant S, Wang CW, Schekman R (2012) Sorting signals that mediate traffic of chitin synthase III between the TGN/endosomes and to the plasma membrane in yeast. PLoS One 7:e46386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stegmeier F, Amon A (2004) Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu Rev Genet 38:203–232

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos I, de Wit PJGM (2009) Fungal effector proteins. Annu Rev Phytopathol 47:233–263

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos I, van den Burg HA, Okmen B, Beenen HG, van Liere S, Kema GHJ, de Wit PJGM (2010) Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proc Natl Acad Sci 107:7610–7615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steringer JP, Muller HM, Nickel W (2015) Unconventional secretion of fibroblast growth factor 2—a novel type of protein translocation across membranes? J Mol Biol 427:1202–1210

    Article  CAS  PubMed  Google Scholar 

  • Stock J, Sarkari P, Kreibich S, Brefort T, Feldbrugge M, Schipper K (2012) Applying unconventional secretion of the endochitinase Cts1 to export heterologous proteins in Ustilago maydis. J Biotechnol 161:80–91

    Article  CAS  PubMed  Google Scholar 

  • Su Y, Xu L, Wang S, Wang Z, Yang Y, Chen Y, Que Y (2015) Identification, phylogeny, and transcript of chitinase family genes in sugarcane. Sci Rep 5:10708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeshita N, Ohta A, Horiuchi H (2005) CsmA, a class V chitin synthase with a myosin motor-like domain, is localized through direct interaction with the actin cytoskeleton in Aspergillus nidulans. Mol Biol Cell 16:1961–1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka N, Fujita Y, Suzuki S, Morishita M, Giga-Hama Y, Shimoda C, Takegawa K (2005) Characterization of O-mannosyltransferase family in Schizosaccharomyces pombe. Biochem Biophys Res Commun 330:813–820

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Nguyen CT, Liang Y, Cao Y, Stacey G (2013) Role of LysM receptors in chitin-triggered plant innate immunity. Plant Signal Behav 8:e22598

    Article  PubMed  CAS  Google Scholar 

  • Teparić R, Mrša V (2013) Proteins involved in building, maintaining and remodeling of yeast cell walls. Curr Genet 59:171–185

    Article  PubMed  CAS  Google Scholar 

  • Teparić R, Stuparević I, Mrša V (2007) Binding assay for incorporation of alkali-extractable proteins in the Saccharomyces cerevisiae cell wall. Yeast 24:259–266

    Article  PubMed  CAS  Google Scholar 

  • Terwisscha van Scheltinga AC, Armand S, Kalk KH, Isogai A, Henrissat B, Dijkstra BW (1995) Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and X-ray structure of a complex with allosamidin evidence for substrate assisted catalysis. Biochemistry 34:15619–15623

    Article  CAS  PubMed  Google Scholar 

  • Tews I, Vincentelli R, Vorgias CE (1996) N-Acetylglucosaminidase (chitobiase) from Serratia marcescens: gene sequence, and protein production and purification in Escherichia coli. Gene 170:63–67

    Article  CAS  PubMed  Google Scholar 

  • Treitschke S, Doehlemann G, Schuster M, Steinberg G (2010) The myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell 22:2476–2494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzelepis GD, Melin P, Jensen DF, Stenlid J, Karlsson M (2012) Functional analysis of glycoside hydrolase family 18 and 20 genes in Neurospora crassa. Fungal Genet Biol 49:717–730

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G, Houston DR, Riemen AHK, Eijsink VGH, van Aalten DMF (2005) Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J Biol Chem 280:11313–11319

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sorlie M, Eijsink VG (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G, Bøhle LA, Gåseidnes S, Dalhus B, Bjørås M, Mathiesen G, Eijsink VGH (2012) Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol 416:239–254

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G, Horn SJ, Sørlie M, Eijsink VGH (2013) The chitinolytic machinery of Serratia marcescens—a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J 280:3028–3049

    Article  CAS  PubMed  Google Scholar 

  • Valdivia RH, Schekman R (2003) The yeasts Rho1p and Pkc1p regulate the transport of chitin synthase III (Chs3p) from internal stores to the plasma membrane. Proc Natl Acad Sci USA 100:10287–10292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Aalten DMF, Komander D, Synstad B, Gaseidnes S, Peter MG, Eijsink VGH (2001) Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc Natl Acad Sci 98:8979–8984

    Article  PubMed  PubMed Central  Google Scholar 

  • van den Burg HA, Harrison SJ, Joosten MH, Vervoort J, de Wit PJ (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19:1420–1430

    Article  PubMed  CAS  Google Scholar 

  • van Esse HP, Bolton MD, Stergiopoulos I, de Wit PJ, Thomma BP (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20:1092–1101

    Article  PubMed  CAS  Google Scholar 

  • Weber I, Assmann D, Thines E, Steinberg G (2006) Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 18:225–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams SJ, Mark BL, Vocadlo DJ, James MNG, Withers SG (2002) Aspartate 313 in the Streptomyces plicatus hexosaminidase plays a critical role in substrate-assisted catalysis by orienting the 2-acetamido group and stabilizing the transition state. J Biol Chem 277:40055–40065

    Article  CAS  PubMed  Google Scholar 

  • Wurzenberger C, Gerlich DW (2011) Phosphatases: providing safe passage through mitotic exit. Nat Rev Mol Cell Biol 12:469–482

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki H, Yamazaki D, Takaya N, Takagi M, Ohta A, Horiuchi H (2007) A chitinase gene, chiB, involved in the autolytic process of Aspergillus nidulans. Curr Genet 51:89–98

    Article  CAS  PubMed  Google Scholar 

  • Yamazaki H, Tanaka A, Kaneko J-I, Ohta A, Horiuchi H (2008) Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet Biol 45:963–972

    Article  CAS  PubMed  Google Scholar 

  • Zakariassen H, Aam BB, Horn SJ, Varum KM, Sorlie M, Eijsink VGH (2009) Aromatic residues in the catalytic center of chitinase A from Serratia marcescens affect processivity, enzyme activity, and biomass converting efficiency. J Biol Chem 284:10610–10617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zakariassen H, Hansen MC, Joranli M, Eijsink VG, Sorlie M (2011) Mutational effects on transglycosylating activity of family 18 chitinases and construction of a hypertransglycosylating mutant. Biochemistry 50:5693–5703

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Prof. Dr. Michael Feldbrügge and Dr. Kerstin Schipper for critical reading the manuscript and valuable discussion. Work of T.L. was supported by a doctoral fellowship of the DFG International Research Training Group 1525 iGRADplant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vera Göhre.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by M. Kupiec.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Langner, T., Göhre, V. Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions. Curr Genet 62, 243–254 (2016). https://doi.org/10.1007/s00294-015-0530-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-015-0530-x

Keywords

Navigation