Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi

Springer Science and Business Media LLC - Tập 14 Số 1 - 2013
Zhongtao Zhao1, Huiquan Liu1, Chenfang Wang1, Jin‐Rong Xu2
1NWAFU-PU Joint Research Center and State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant Protection, Northwest A&F University, Yangling, Shaanxi, 712100, China
2Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA

Tóm tắt

Abstract EDITOR'S NOTE Readers are alerted that there is currently a discussion regarding the use of some of the unpublished genomic data presented in this manuscript. Appropriate editorial action will be taken once this matter is resolved. Background Fungi produce a variety of carbohydrate activity enzymes (CAZymes) for the degradation of plant polysaccharide materials to facilitate infection and/or gain nutrition. Identifying and comparing CAZymes from fungi with different nutritional modes or infection mechanisms may provide information for better understanding of their life styles and infection models. To date, over hundreds of fungal genomes are publicly available. However, a systematic comparative analysis of fungal CAZymes across the entire fungal kingdom has not been reported. Results In this study, we systemically identified glycoside hydrolases (GHs), polysaccharide lyases (PLs), carbohydrate esterases (CEs), and glycosyltransferases (GTs) as well as carbohydrate-binding modules (CBMs) in the predicted proteomes of 103 representative fungi from Ascomycota, Basidiomycota, Chytridiomycota, and Zygomycota. Comparative analysis of these CAZymes that play major roles in plant polysaccharide degradation revealed that fungi exhibit tremendous diversity in the number and variety of CAZymes. Among them, some families of GHs and CEs are the most prevalent CAZymes that are distributed in all of the fungi analyzed. Importantly, cellulases of some GH families are present in fungi that are not known to have cellulose-degrading ability. In addition, our results also showed that in general, plant pathogenic fungi have the highest number of CAZymes. Biotrophic fungi tend to have fewer CAZymes than necrotrophic and hemibiotrophic fungi. Pathogens of dicots often contain more pectinases than fungi infecting monocots. Interestingly, besides yeasts, many saprophytic fungi that are highly active in degrading plant biomass contain fewer CAZymes than plant pathogenic fungi. Furthermore, analysis of the gene expression profile of the wheat scab fungus Fusarium graminearum revealed that most of the CAZyme genes related to cell wall degradation were up-regulated during plant infection. Phylogenetic analysis also revealed a complex history of lineage-specific expansions and attritions for the PL1 family. Conclusions Our study provides insights into the variety and expansion of fungal CAZyme classes and revealed the relationship of CAZyme size and diversity with their nutritional strategy and host specificity.

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Tài liệu tham khảo

Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B: The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009, 37 (Database issue): D233-D238.

Ospina-Giraldo MD, Griffith JG, Laird EW, Mingora C: The CAZyome of Phytophthora spp: a comprehensive analysis of the gene complement coding for carbohydrate-active enzymes in species of the genus Phytophthora. BMC Genomics. 2010, 11: 525-10.1186/1471-2164-11-525.

Murphy C, Powlowski J, Wu M, Butler G, Tsang A: Curation of characterized glycoside hydrolases of fungal origin. Database (Oxford). 2011, 2011: doi:10.1093/database/bar020

Couturier M, Navarro D, Olive C, Chevret D, Haon M, Favel A, Lesage-Meessen L, Henrissat B, Coutinho PM, Berrin JG: Post-genomic analyses of fungal lignocellulosic biomass degradation reveal the unexpected potential of the plant pathogen Ustilago maydis. BMC Genomics. 2012, 13: 57-10.1186/1471-2164-13-57.

King BC, Waxman KD, Nenni NV, Walker LP, Bergstrom GC, Gibson DM: Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol Biofuels. 2011, 4: 4-10.1186/1754-6834-4-4.

Lu X, Sun J, Nimtz M, Wissing J, Zeng A-P, Rinas U: The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate. Microb Cell Fact. 2010, 9 (1): 23-10.1186/1475-2859-9-23.

Yuan X-L, Kaaij RM, Hondel CAMJJ, Punt PJ, Maarel MJEC, Dijkhuizen L, Ram AFJ: Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles. Mol Genet Genomics. 2008, 279 (6): 545-561. 10.1007/s00438-008-0332-7.

Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA, Walton JD: Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics. 2007, 7 (17): 3171-3183. 10.1002/pmic.200700184.

Mastronunzio JE, Tisa LS, Normand P, Benson DR: Comparative secretome analysis suggests low plant cell wall degrading capacity in Frankia symbionts. BMC Genomics. 2008, 9 (1): 47-10.1186/1471-2164-9-47.

Brown NA, Antoniw J, Hammond-Kosack KE: The predicted secretome of the plant pathogenic fungus Fusarium graminearum: a refined comparative analysis. PLoS One. 2012, 7 (4): e33731-10.1371/journal.pone.0033731.

Battaglia E, Benoit I, van den Brink J, Wiebenga A, Coutinho PM, Henrissat B, de Vries RP: Carbohydrate-active enzymes from the zygomycete fungus Rhizopus oryzae: a highly specialized approach to carbohydrate degradation depicted at genome level. BMC Genomics. 2011, 12: 38-10.1186/1471-2164-12-38.

Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, Cate JHD, Glass NL: Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci. 2009, 106 (52): 22157-22162. 10.1073/pnas.0906810106.

Dashtban M, Schraft H, Syed TA, Qin W: Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Biol. 2010, 1 (1): 36-50.

Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS, et al: The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science. 2012, 336 (6089): 1715-1719. 10.1126/science.1221748.

Douaiher MN, Nowak E, Durand R, Halama P, Reignault P: Correlative analysis of Mycosphaerella graminicola pathogenicity and cell wall‒degrading enzymes produced in vitro: the importance of xylanase and polygalacturonase. Plant pathology. 2007, 56 (1): 79-86.

Ferrari S, Galletti R, Pontiggia D, Manfredini C, Lionetti V, Bellincampi D, Cervone F, De Lorenzo G: Transgenic Expression of a Fungal endo-Polygalacturonase Increases Plant Resistance to Pathogens and Reduces Auxin Sensitivity. Plant Physiol. 2007, 146 (2): 669-681. 10.1104/pp.107.109686.

Kikot GE, Hours RA, Alconada TM: Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: a review. J Basic Microbiol. 2009, 49 (3): 231-241. 10.1002/jobm.200800231.

Skamnioti P, Furlong RF, Gurrl SJ: The fate of gene duplicates in the genomes of fungal pathogens. Communicative & Integrative Biology. 2008, 1 (2): 196-198. 10.4161/cib.1.2.7144.

Vogel J: Unique aspects of the grass cell wall. Curr Opin Plant Biol. 2008, 11 (3): 301-307. 10.1016/j.pbi.2008.03.002.

Lagaert S, Belien T, Volckaert G: Plant cell walls: Protecting the barrier from degradation by microbial enzymes. Semin Cell Dev Biol. 2009, 20 (9): 1064-1073. 10.1016/j.semcdb.2009.05.008.

Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y: dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2012, 40 (Web Server issue): W445-451.

Tyler L, Bragg JN, Wu J, Yang X, Tuskan GA, Vogel JP: Annotation and comparative analysis of the glycoside hydrolase genes in Brachypodium distachyon. BMC Genomics. 2010, 11: 600-10.1186/1471-2164-11-600.

Yip VL, Withers SG: Breakdown of oligosaccharides by the process of elimination. Curr Opin Chem Biol. 2006, 10 (2): 147-155. 10.1016/j.cbpa.2006.02.005.

Biely P: Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol Adv. 2012, 30 (6): 1575-1588. 10.1016/j.biotechadv.2012.04.010.

Boraston AB, Bolam DN, Gilbert HJ, Davies GJ: Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J. 2004, 382 (Pt 3): 769-781.

Daviesa KA, Loronoa ID, Fosterb SJ, Lia D, Johnstonea K, Ashby AM: Evidence for a role of cutinase in pathogenicity of Pyrenopeziza brassicae on brassicas. Physiological and Molecular Plant Pathology. 2000, 57 (2): 63-75. 10.1006/pmpp.2000.0282.

Alghisi P, Favaron F: Pectin-degrading enzymes and plant-parasite interactions. Eur J Plant Pathol. 1995, 101: 365-375. 10.1007/BF01874850.

Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, et al: Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature. 2010, 464 (7291): 1033-1038. 10.1038/nature08867.

Bubner P, Dohr J, Plank H, Mayrhofer C, Nidetzky B: Cellulases dig deep: in situ observation of the mesoscopic structural dynamics of enzymatic cellulose degradation. J Biol Chem. 2011, 287 (4): 2759-2765.

Aro N, Pakula T, Penttila M: Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev. 2005, 29 (4): 719-739. 10.1016/j.femsre.2004.11.006.

Li DC, Li AN, Papageorgiou AC: Cellulases from thermophilic fungi: recent insights and biotechnological potential. Enzyme Res. 2011, 2011: 308730-

Shallom D, Leon M, Bravman T, Ben-David A, Zaide G, Belakhov V, Shoham G, Schomburg D, Baasov T, Shoham Y: Biochemical characterization and identification of the catalytic residues of a family 43 beta-D-xylosidase from Geobacillus stearothermophilus T-6. Biochemistry. 2005, 44 (1): 387-397. 10.1021/bi048059w.

Medie FM, Davies GJ, Drancourt M, Henrissat B: Genome analyses highlight the different biological roles of cellulases. Nat Rev Microbiol. 2012, 10 (3): 227-234. 10.1038/nrmicro2729.

Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E, Sweeney MD: Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol. 2011, 77 (19): 7007-7015. 10.1128/AEM.05815-11.

Harvey AJ, Hrmova M, De Gori R, Varghese JN, Fincher GB: Comparative modeling of the three-dimensional structures of family 3 glycoside hydrolases. Proteins. 2000, 41 (2): 257-269. 10.1002/1097-0134(20001101)41:2<257::AID-PROT100>3.0.CO;2-C.

Aspeborg H, Coutinho PM, Wang Y, Brumer H, Henrissat B: Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol. 2012, 12: 186-10.1186/1471-2148-12-186.

Dias FM, Vincent F, Pell G, Prates JA, Centeno MS, Tailford LE, Ferreira LM, Fontes CM, Davies GJ, Gilbert HJ: Insights into the molecular determinants of substrate specificity in glycoside hydrolase family 5 revealed by the crystal structure and kinetics of Cellvibrio mixtus mannosidase 5A. J Biol Chem. 2004, 279 (24): 25517-25526. 10.1074/jbc.M401647200.

van den Brink J, de Vries RP: Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol. 2011, 91 (6): 1477-1492. 10.1007/s00253-011-3473-2.

Ducros V, Charnock SJ, Derewenda U, Derewenda ZS, Dauter Z, Dupont C, Shareck F, Morosoli R, Kluepfel D, Davies GJ: Substrate specificity in glycoside hydrolase family 10. Structural and kinetic analysis of the Streptomyces lividans xylanase 10A. J Biol Chem. 2000, 275 (30): 23020-23026. 10.1074/jbc.275.30.23020.

Paes G, Skov LK, O’Donohue MJ, Remond C, Kastrup JS, Gajhede M, Mirza O: The structure of the complex between a branched pentasaccharide and Thermobacillus xylanilyticus GH-51 arabinofuranosidase reveals xylan-binding determinants and induced fit. Biochemistry. 2008, 47 (28): 7441-7451. 10.1021/bi800424e.

Ishida T, Fushinobu S, Kawai R, Kitaoka M, Igarashi K, Samejima M: Crystal structure of glycoside hydrolase family 55 β-1,3-glucanase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem. 2009, 284 (15): 10100-10109. 10.1074/jbc.M808122200.

Skamnioti P, Gurr SJ: Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. The Plant Cell Online. 2007, 19 (8): 2674-2689. 10.1105/tpc.107.051219.

Skamnioti P, Gurr SJ: Cutinase and hydrophobin interplay: A herald for pathogenesis?. Plant Signal Behav. 2008, 3 (4): 248-250. 10.4161/psb.3.4.5181.

Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, et al: The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 2012, 40 (Database issue): D26-32.

Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, et al: The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008, 452 (7183): 88-92. 10.1038/nature06556.

Liu Z, Ellwood SR, Oliver RP, Friesen TL: Pyrenophora teres: profile of an increasingly damaging barley pathogen. Mol Plant Pathol. 2011, 12 (1): 1-19. 10.1111/j.1364-3703.2010.00649.x.

Dawson TL: Malassezia globosa and restricta: Breakthrough Understanding of the Etiology and Treatment of Dandruff and Seborrheic Dermatitis through Whole-Genome Analysis. J Investig Dermatol Symp Proc. 2007, 12 (2): 15-19. 10.1038/sj.jidsymp.5650049.

Symonds EP, Trott DJ, Bird PS, Mills P: Growth characteristics and enzyme activity in Batrachochytrium dendrobatidis isolates. Mycopathologia. 2008, 166 (3): 143-147. 10.1007/s11046-008-9135-y.

Wong HC, Fear AL, Calhoon RD, Eichinger GH, Mayer R, Amikam D, Benziman M, Gelfand DH, Meade JH, Emerick AW, et al: Genetic organization of the cellulose synthase operon in Acetobacter xylinum. Proc Natl Acad Sci USA. 1990, 87 (20): 8130-8134. 10.1073/pnas.87.20.8130.

Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Hofte H: A plasma membrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 1998, 17 (19): 5563-5576. 10.1093/emboj/17.19.5563.

Battke F, Symons S, Nieselt K: Mayday–integrative analytics for expression data. BMC Bioinformatics. 2010, 11: 121-10.1186/1471-2105-11-121.

Grigorieva IV, Cullenb D, Goodwinc SB, Hibbettd D, Jeffriesb TW, Kubiceke CP, Kuskef C, Magnusong JK, Martinh F, Spataforai JW, et al: Fueling the future with fungal genomics. Mycology. 2011, 2 (3): 192-209.

Eddy SR: A new generation of homology search tools based on probabilistic inference. Genome Inform. 2009, 23 (1): 205-211.

Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C: T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 2011, 39 (Web Server issue): W13-17.

Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 2005, 21 (9): 2104-2105. 10.1093/bioinformatics/bti263.

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