Bioinformatic characterisation of genes encoding cell wall degrading enzymes in the Phytophthora parasitica genome

BMC Genomics

Adrienne R Hardham²  Darren P Cullerne¹  Leila M Blackman² 

[1] Current address: CSIRO, Agriculture Flagship, Canberra ACT, 2601, Australia;Plant Science Division, Research School of Biology, College of Medicine, Biology and Environment, The Australian National University, Canberra ACT 0200, Australia

关键词: Phytophthora parasitica genome;    Polysaccharide lyase;    Glycoside hydrolase;    Cell wall degrading enzymes;    Carbohydrate esterase;    Carbohydrate binding module;    CAZymes;   

Others  :  1140557
DOI  :  10.1186/1471-2164-15-785

 received in 2014-03-27, accepted in 2014-09-03,  发布年份 2014

【 摘 要 】

Background

A critical aspect of plant infection by the majority of pathogens is penetration of the plant cell wall. This process requires the production and secretion of a broad spectrum of pathogen enzymes that target and degrade the many complex polysaccharides in the plant cell wall. As a necessary framework for a study of the expression of cell wall degrading enzymes (CWDEs) produced by the broad host range phytopathogen, Phytophthora parasitica, we have conducted an in-depth bioinformatics analysis of the entire complement of genes encoding CWDEs in this pathogen’s genome.

Results

Our bioinformatic analysis indicates that 431 (2%) of the 20,825 predicted proteins encoded by the P. parasitica genome, are carbohydrate-active enzymes (CAZymes) involved in the degradation of cell wall polysaccharides. Of the 431 proteins, 337 contain classical N-terminal secretion signals and 67 are predicted to be targeted to the non-classical secretion pathway. Identification of CAZyme catalytic activity based on primary protein sequence is difficult, nevertheless, detailed comparisons with previously characterized enzymes has allowed us to determine likely enzyme activities and targeted substrates for many of the P. parasitica CWDEs. Some proteins (12%) contain more than one CAZyme module but, in most cases, multiple modules are from the same CAZyme family. Only 12 P. parasitica CWDEs contain both catalytically-active (glycosyl hydrolase) and non-catalytic (carbohydrate binding) modules, a situation that contrasts with that in fungal phytopathogens. Other striking differences between the complements of CWDEs in P. parasitica and fungal phytopathogens are seen in the CAZyme families that target cellulose, pectins or β-1,3-glucans (e.g. callose). About 25% of P. parasitica CAZymes are solely directed towards pectin degradation, with the majority coming from pectin lyase or carbohydrate esterase families. Fungal phytopathogens typically contain less than half the numbers of these CAZymes. The P. parasitica genome, like that of other Oomycetes, is rich in CAZymes that target β-1,3-glucans.

Conclusions

This detailed analysis of the full complement of P. parasitica cell wall degrading enzymes provides a framework for an in-depth study of patterns of expression of these pathogen genes during plant infection and the induction or repression of expression by selected substrates.

【 授权许可】

   
2014 Blackman et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Liu H, Zhang S, Schell MA, Denny TP: Pyramiding unmarked deletions in Ralstonia solanacearum shows that secreted proteins in addition to plant cell-wall-degrading enzymes contribute to virulence. Mol Plant Microbe Interact 2005, 18:1296-1305.
• [2]Vorwerk S, Somerville S, Somerville C: The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 2004, 9:203-209.
• [3]Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A: Biochemistry of the cell wall molecules. In Plant Cell Walls from Chemistry to Biology. New York: Garland Science; 2011:68-118.
• [4]Caffall KH, Mohnen D: The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 2009, 344:1879-1900.
• [5]Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H: Toward a systems approach to understanding plant cell walls. Science 2004, 306:2206-2211.
• [6]Scheller HV, Ulvskov P: Hemicelluloses. Annu Rev Plant Biol 2010, 61:263-289.
• [7]Vincken J-P, Schols HA, Oomen RJFJ, McCann MC, Ulvskov P, Voragen AGJ, Visser RGF: If homogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiol 2003, 132:1781-1789.
• [8]Mohnen D: Pectin structure and biosynthesis. Curr Opin Plant Biol 2008, 11:266-277.
• [9]Ridley BL, O'Neill MA, Mohnen D: Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 2001, 57:929-967.
• [10]Pabst M, Fischl RM, Brecker L, Morelle W, Fauland A, Köfeler H, Altmann F, Léonard R: Rhamnogalacturonan II structure shows variation in the side chains monosaccharide composition and methylation status within and across different plant species. Plant J 2013, 76:61-72.
• [11]Wilson IB: Glycosylation of proteins in plants and invertebrates. Curr Opin Struct Biol 2002, 12:569-577.
• [12]Garbe J, Collin M: Bacterial hydrolysis of host glycoproteins - powerful protein modification and efficient nutrient acquisition. J Innate Immun 2012, 4:121-131.
• [13]Seifert GJ, Roberts K: The biology of arabinogalactan proteins. Annu Rev Plant Biol 2007, 58:137-161.
• [14]Williamson G, Kroon PA, Faulds CB: Hairy plant polysaccharides: a close shave with microbial esterases. Microbiology 1998, 144:2011-2023.
• [15]Hückelhoven R: Cell wall–associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 2007, 45:101-127.
• [16]Chen XY, Kim JY: Callose synthesis in higher plants. Plant Signal Behav 2009, 4:489-492.
• [17]Franková L, Fry SC: Biochemistry and physiological roles of enzymes that 'cut and paste' plant cell-wall polysaccharides. J Exp Bot 2013, 64:3519-3550.
• [18]van den Brink J, de Vries RP: Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol 2011, 91:1477-1492.
• [19]Henrissat B, Coutinho PM, Davies GJ: A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol Biol 2001, 47:55-72.
• [20]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:D233-D238.
• [21]Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B: Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 2013, 6:41.
• [22]Boraston AB, Bolam DN, Gilbert HJ, Davies GJ: Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 2004, 382:769-781.
• [23]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.
• [24]Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG: Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 2012, 5:45.
• [25]Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B: A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem J 2010, 432:437-444.
• [26]Henrissat B, Davies GJ: Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. Plant Physiol 2000, 124:1515-1519.
• [27]Hardham AR, Cahill DM: The role of oomycete effectors in plant–pathogen interactions. Funct Plant Biol 2010, 37:919-925.
• [28]Jiang RH, Tyler BM: Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol 2012, 50:295-318.
• [29]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.
• [30]Larroque M, Barriot R, Bottin A, Barre A, Rouge P, Dumas B, Gaulin E: The unique architecture and function of cellulose-interacting proteins in oomycetes revealed by genomic and structural analyses. BMC Genomics 2012, 13:605.
• [31]Zerillo MM, Adhikari BN, Hamilton JP, Buell CR, Lévesque CA, Tisserat N: Carbohydrate-active enzymes in Pythium and their role in plant cell wall and storage polysaccharide degradation. PLoS One 2013, 8:e72572.
• [32]Savory EA, Adhikari BN, Hamilton JP, Vaillancourt B, Buell CR, Day B: mRNA-seq analysis of the Pseudoperonospora cubensis transcriptome during cucumber (Cucumis sativus L.) infection. PLoS One 2012, 7:e35796.
• [33]Phytophthora parasitica INRA-310 Sequencing Project, Broad Institute of Harvard and MIT. http://www.broadinstitute.org/ webcite
• [34]Database for Carbohydrate-active enzyme ANnotation. http://csbl.bmb.uga.edu/dbCAN/index.php webcite
• [35]Yin Y, Mao X, Yang J, Chen X, Mao F, Ying X: dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucl Acids Res 2012, 40:W445-W451.
• [36]MyHits. http://myhits.isb-sib.ch webcite
• [37]Sigrist CJ, de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I: New and continuing developments at PROSITE. Nucleic Acids Res 2013, 41:D344-D347.
• [38]The PROSITE database. http://prosite.expasy.org/prosite.html webcite
• [39]National Center for Biotechnology Information. http://www.ncbi.nlm.nih.gov webcite
• [40]Pfam 27.0. http://pfam.sanger.ac.uk webcite
• [41]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD: The Pfam protein families database. Nucleic Acids Res 2012, 40:D290-D301.
• [42]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
• [43]The Carbohydrate-Active enZYmes Database. http://www.cazy.org webcite]
• [44]Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC: CAZymes Analysis Toolkit (CAT): Web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 2010, 20:1574-1584.
• [45]CAZYmes Analysis Toolkit. http://mothra.ornl.gov/cgi-bin/cat/cat.cgi webcite
• [46]INRA-310 Sequencing Project, Broad Institute of Harvard and MIT (V3). https://olive.broadinstitute.org/projects/phytophthora_parasitica webcite]
• [47]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
• [48]SignalP 4.1 Server. http://www.cbs.dtu.dk/services/SignalP/ webcite
• [49]Bendtsen JD, Jensen LJ, Blom N, von Heijne G, Brunak S: Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 2004, 17:349-356.
• [50]SecretomeP 1.0f. http://www.cbs.dtu.dk/services/SecretomeP/ webcite
• [51]Bendtsen JD, Nielsen H, von Heijne G, Brunak S: Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795.
• [52]Soanes DM, Richards TA, Talbot NJ: Insights from sequencing fungal and oomycete genomes: what can we learn about plant disease and the evolution of pathogenicity? Plant Cell 2007, 19:3318-3326.
• [53]A combined transmembrane topology and signal peptide predictor. http://phobius.sbc.su.se webcite
• [54]Krogh A, Larsson B, von Heijne G, Sonnhammer EL: Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305:567-580.
• [55]TMHMM Server v. 2.0. http://www.cbs.dtu.dk/services/TMHMM/ webcite
• [56]Pierleoni A, Martelli PL, Casadio R: PredGPI: a GPI-anchor predictor. BMC Bioinformatics 2008, 9:392.
• [57]PredGPI predictor. http://gpcr.biocomp.unibo.it/predgpi/pred.htm webcite
• [58]Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 11:4673-4680.
• [59]Network Protein Sequence Analysis: CLUSTALW. https://npsa-prabi.ibcp.fr/cgi-bin/npsa_automat.pl?page=npsa_clustalw.html webcite
• [60]Sander C, Schneider R: Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 1991, 9:56-68.
• [61]Lopez-Casado G, Urbanowicz BR, Damasceno CM, Rose JK: Plant glycosyl hydrolases and biofuels: a natural marriage. Curr Opin Plant Biol 2008, 11:329-337.
• [62]Hakkinen M, Arvas M, Oja M, Aro N, Penttila M, Saloheimo M, Pakula TM: Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb Cell Fact 2012, 11:134.
• [63]Davies GJ, Gloster TM, Henrissat B: Recent structural insights into the expanding world of carbohydrate-active enzymes. Curr Opin Struct Biol 2005, 15:637-645.
• [64]Minic Z: Physiological roles of plant glycoside hydrolases. Planta 2008, 227:723-740.
• [65]Mertz B, Gu X, Reilly PJ: Analysis of functional divergence within two structurally related glycoside hydrolase families. Biopolymers 2009, 91:478-495.
• [66]Ketudat Cairns JR, Esen A: β-Glucosidases. Cell Mol Life Sci 2010, 67:3389-3405.
• [67]Kuntothom T, Luang S, Harvey AJ, Fincher GB, Opassiri R, Hrmova M, Ketudat Cairns JR: Rice family GH1 glycoside hydrolases with β-D-glucosidase and β-D-mannosidase activities. Arch Biochem Biophys 2009, 491:85-95.
• [68]St John FJ, González JM, Pozharski E: Consolidation of glycosyl hydrolase family 30: A dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett 2010, 584:4435-4441.
• [69]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.
• [70]O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N, Altmuller J, Alvarado-Balderrama L, Bauser CA, Becker C, Birren BW, Chen Z, Choi J, Crouch JA, Duvick JP, Farman MA, Gan P, Heiman D, Henrissat B, Howard RJ, Kabbage M, Koch C, Kracher B, Kubo Y, Law AD, Lebrun MH, et al.: Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 2012, 44:1060-1065.
• [71]Zhao Z, Liu H, Wang C, Xu JR: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 2013, 14:274.
• [72]Minic Z, Jouanin L: Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 2006, 44:435-449.
• [73]Wymelenberg AV, Denman S, Dietrich D, Bassett J, Yu X, Atalla R, Predki P, Rudsander U, Teeri TT, Cullen D: Transcript analysis of genes encoding a family 61 endoglucanase and a putative membrane-anchored family 9 glycosyl hydrolase from Phanerochaete chrysosporium. Appl Environ Microbiol 2002, 68:5765-5768.
• [74]Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H: A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 1998, 17:5563-5576.
• [75]Brunner F, Wirtz W, Rose JK, Darvill AG, Govers F, Scheel D, Nürnberger T: A β-glucosidase/xylosidase from the phytopathogenic oomycete, Phytophthora infestans. Phytochemistry 2002, 59:689-696.
• [76]Costanzo S, Ospina-Giraldo MD, Deahl KL, Baker CJ, Jones RW: Alternate intron processing of family 5 endoglucanase transcripts from the genus Phytophthora. Curr Genet 2007, 52:115-123.
• [77]Mélida H, Sandoval-Sierra JV, Diéguez-Uribeondo J, Bulone V: Analyses of extracellular carbohydrates in Oomycetes unveil the existence of three different cell wall types. Eukaryot Cell 2013, 12:194-203.
• [78]Guillén D, Sánchez S, Rodríguez-Sanoja R: Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 2010, 85:1241-1249.
• [79]Li XL, Chen H, Ljungdahl LG: Two cellulases, CelA and CelC, from the polycentric anaerobic fungus Orpinomyces strain PC-2 contain N-terminal docking domains for a cellulase-hemicellulase complex. Appl Environ Microbiol 1997, 63:4721-4728.
• [80]Luo H, Yang J, Yang P, Li J, Huang H, Shi P, Bai Y, Wang Y, Fan Y, Yao B: Gene cloning and expression of a new acidic family 7 endo-β-1,3-1,4-glucanase from the acidophilic fungus Bispora sp. MEY-1. Appl Microbiol Biotechnol 2010, 85:1015-1023.
• [81]Goedegebuur F, Fowler T, Phillips J, van der Kley P, van Solingen P, Dankmeyer L, Power SD: Cloning and relational analysis of 15 novel fungal endoglucanases from family 12 glycosyl hydrolase. Curr Genet 2002, 41:89-98.
• [82]Master ER, Zheng Y, Storms R, Tsang A, Powlowski J: A xyloglucan-specific family 12 glycosyl hydrolase from Aspergillus niger: recombinant expression, purification and characterization. Biochem J 2008, 411:161-170.
• [83]Lafond M, Navarro D, Haon M, Couturier M, Berrin JG: Characterization of a broad-specificity β-glucanase acting on β-(1,3)-, β-(1,4)-, and β-(1,6)-glucans that defines a new glycoside hydrolase family. Appl Environ Microbiol 2012, 78:8540-8546.
• [84]Hemsworth GR, Taylor EJ, Kim RQ, Gregory RC, Lewis SJ, Turkenburg JP, Parkin A, Davies GJ, Walton PH: The copper active site of CBM33 polysaccharide oxygenases. J Am Chem Soc 2013, 135:6069-6077.
• [85]Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunaes AC, Stenstrom Y, MacKenzie A, Sorlie M, Horn SJ, Eijsink VG: Cleavage of cellulose by a CBM33 protein. Protein Sci 2011, 20:1479-1483.
• [86]Li X, Beeson WT, Phillips CM, Marletta MA, Cate JH: Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure 2012, 20:1051-1061.
• [87]Lee MH, Lai WL, Lin SF, Hsu CS, Liaw SH, Tsai YC: Structural characterization of glucooligosaccharide oxidase from Acremonium strictum. Appl Environ Microbiol 2005, 71:8881-8887.
• [88]Boraston AB, Tomme P, Amandoron EA, Kilburn DG: A novel mechanism of xylan binding by a lectin-like module from Streptomyces lividans xylanase 10A. Biochem J 2000, 350:933-941.
• [89]Georgelis N, Yennawar NH, Cosgrove DJ: Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin. Proc Natl Acad Sci U S A 2012, 109:14830-14835.
• [90]Mateos FV, Rickauer M, Esquerre-Tugaye MT: Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol Plant Microbe Interact 1997, 10:1045-1053.
• [91]Georgelis N, Nikolaidis N, Cosgrove DJ: Biochemical analysis of expansin-like proteins from microbes. Carbohydr Polym 2014, 100:17-23.
• [92]Hashimoto H: Recent structural studies of carbohydrate-binding modules. Cell Mol Life Sci 2006, 63:2954-2967.
• [93]Colletotrichum Sequencing Project, Broad Institute of Harvard and MIT. http://www.broadinstitute.org/annotation/genome/colletotrichum_group/MultiHome.html webcite
• [94]Gilbert HJ, Stalbrand H, Brumer H: How the walls come crumbling down: recent structural biochemistry of plant polysaccharide degradation. Curr Opin Plant Biol 2008, 11:338-348.
• [95]Kotake T, Hirata N, Degi Y, Ishiguro M, Kitazawa K, Takata R, Ichinose H, Kaneko S, Igarashi K, Samejima M, Tsumuraya Y: Endo-β-1,3-galactanase from winter mushroom Flammulina velutipes. J Biol Chem 2011, 286:27848-27854.
• [96]Steczkiewicz K, Knizewski L, Rychlewski L, Ginalski K: TOS1 is circularly permuted 1,3-β-glucanase. Cell Cycle 2010, 9:201-204.
• [97]Collins T, Gerday C, Feller G: Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 2005, 29:3-23.
• [98]Suzuki S, Fukuoka M, Ookuchi H, Sano M, Ozeki K, Nagayoshi E, Takii Y, Matsushita M, Tada S, Kusumoto K-I, Kashiwagi Y: Characterization of Aspergillus oryzae glycoside hydrolase family 43 β-xylosidase expressed in Escherichia coli. J Biosci Bioeng 2010, 109:115-117.
• [99]Ichinose H, Kotake T, Tsumuraya Y, Kaneko S: Characterization of an endo-β-1,6-galactanase from Streptomyces avermitilis NBRC14893. Appl Environ Microbiol 2008, 74:2283-2379.
• [100]Biely P: Microbial carbohydrate esterases deacetylating plant polysaccharides. Biotechnol Adv 2012, 30:1575-1588.
• [101]de Vries RP, VanKuyk PA, Kester HC, Visser J: The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds. Biochem J 2002, 363:377-386.
• [102]Dalrymple BP, Cybinski DH, Layton I, McSweeney CS, Xue GP, Swadling YJ, Lowry JB: Three Neocallimastix patriciarum esterases associated with the degradation of complex polysaccharides are members of a new family of hydrolases. Microbiology 1997, 143:2605-2614.
• [103]Randall TA, Dwyer RA, Huitema E, Beyer K, Cvitanich C, Kelkar H, Fong AMVA, Gates K, Roberts S, Yatzkan E, Gaffney T, Law M, Testa A, Torto-Alalibo T, Zhang M, Zheng L, Mueller E, Windass J, Binder A, Birch PRJ, Gisi U, Govers F, Gow NA, Mauch F, Van WP, Judelson HS: Large-scale gene discovery in the oomycete Phytophthora infestans reveals likely components of phytopathogenicity shared with true fungi. Mol Plant Microbe Interact 2005, 18:229-243.
• [104]Puchart V, Gariepy MC, Shareck F, Dupont C: Identification of catalytically important amino acid residues of Streptomyces lividans acetylxylan esterase A from carbohydrate esterase family 4. Biochim Biophys Acta 2006, 1764:263-274.
• [105]Blair DE, van Aalten DM: Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N-acetyl-glucosamine. FEBS Lett 2004, 570:13-19.
• [106]Shallom D, Shoham Y: Microbial hemicellulases. Curr Opin Microbiol 2003, 6:219-2128.
• [107]Pouvreau L, Jonathan MC, Kabel MA, Hinz SW, Gruppen H, Schols HA: Characterization and mode of action of two acetyl xylan esterases from Chrysosporium lucknowense C1 active towards acetylated xylans. Enzyme Microb Technol 2011, 49:312-320.
• [108]Soliday CL, Flurkey WH, Okita TW, Kolattukudy PE: Cloning and structure determination of cDNA for cutinase, an enzyme involved in fungal penetration of plants. Proc Natl Acad Sci U S A 1984, 81:3939-3943.
• [109]Belbahri L, Calmin G, Mauch F, Andersson JO: Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 2008, 408:1-8.
• [110]Pérez S, Rodríguez-Carvajal MA, Doco T: A complex plant cell wall polysaccharide: rhamnogalacturonan II, A structure in quest of a function. Biochimie 2003, 85:109-121.
• [111]Wu C-H, Yan H-Z, Liu L-F, Liou R-F: Functional characterization of a gene family encoding polygalacturonases in Phytophthora parasitica. Mol Plant Microbe Interact 2008, 21:480-489.
• [112]Yan HZ, Liou RF: Cloning and analysis of pppg1, an inducible endopolygalacturonase gene from the oomycete plant pathogen Phytophthora parasitica. Fungal Genet Biol 2005, 42:339-350.
• [113]Yadav V, Yadav PK, Yadav S, Yadav KDS: α-L-Rhamnosidase: A review. Process Biochem 2010, 45:1226-1235.
• [114]Itoh T, Ochiai A, Mikami B, Hashimoto W, Murata K: A novel glycoside hydrolase family 105: the structure of family 105 unsaturated rhamnogalacturonyl hydrolase complexed with a disaccharide in comparison with family 88 enzyme complexed with the disaccharide. J Mol Biol 2006, 360:573-585.
• [115]Ahn YO, Zheng M, Bevan DR, Esen A, Shiu SH, Benson J, Peng HP, Miller JT, Cheng CL, Poulton JE, Shih MC: Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry 2007, 68:1510-1520.
• [116]Vanholme B, Haegeman A, Jacob J, Cannoot B, Gheysen G: Arabinogalactan endo-1,4-β-galactosidase: a putative plant cell wall-degrading enzyme of plant-parasitic nematodes. Nematology 2009, 11:739-747.
• [117]Miyanaga A, Koseki T, Miwa Y, Mese Y, Nakamura S, Kuno A, Hirabayashi J, Matsuzawa H, Wakagi T, Shoun H, Fushinobu S: The family 42 carbohydrate-binding module of family 54 α-L-arabinofuranosidase specifically binds the arabinofuranose side chain of hemicellulose. Biochem J 2006, 399:503-511.
• [118]de Wet BJ, Matthew MK, Storbeck KH, van Zyl WH, Prior BA: Characterization of a family 54 α-L-arabinofuranosidase from Aureobasidium pullulans. Appl Microbiol Biotechnol 2008, 77:975-983.
• [119]Garron ML, Cygler M: Structural and mechanistic classification of uronic acid-containing polysaccharide lyases. Glycobiology 2010, 20:1547-1573.
• [120]Wang H, Fu L, Zhang X: Comparison of expression, purification and characterization of a new pectate lyase from Phytophthora capsici using two different methods. BMC Biotechnol 2011, 11:32.
• [121]Fu L, Wang HZ, Feng BZ, Zhang XG: Cloning, expression, purification and initial analysis of a novel pectate lyase Pcpel1 from Phytophthora capsici. J Phytopathol 2013, 161:230-238.
• [122]McDonough MA, Kadirvelraj R, Harris P, Poulsen JC, Larsen S: Rhamnogalacturonan lyase reveals a unique three-domain modular structure for polysaccharide lyase family 4. FEBS Lett 2004, 565:188-194.
• [123]de Vries RP, Visser J: Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol Mol Biol Rev 2001, 65:497-522.
• [124]Gou JY, Miller LM, Hou G, Yu XH, Chen XY, Liu CJ: Acetylesterase-mediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell 2012, 24:50-65.
• [125]Navarro-Fernández J, Martínez-Martínez I, Montoro-García S, García-Carmona F, Takami H, Sánchez-Ferrer A: Characterization of a new rhamnogalacturonan acetyl esterase from Bacillus halodurans C-125 with a new putative carbohydrate binding domain. J Bacteriol 2008, 190:1375-1382.
• [126]Abbott DW, Eirin-Lopez JM, Boraston AB: Insight into ligand diversity and novel biological roles for family 32 carbohydrate-binding modules. Mol Biol Evol 2008, 25:155-167.
• [127]Martin-Cuadrado AB, Fontaine T, Esteban PF, del Dedo JE, de Medina-Redondo M, del Rey F, Latge JP, de Aldana CR: Characterization of the endo-β-1,3-glucanase activity of S. cerevisiae Eng2 and other members of the GH81 family. Fungal Genet Biol 2008, 45:542-553.
• [128]Song JM, Nam K, Sun YU, Kang MH, Kim CG, Kwon ST, Lee J, Lee YH: Molecular and biochemical characterizations of a novel arthropod endo-β-1,3-glucanase from the Antarctic springtail, Cryptopygus antarcticus, horizontally acquired from bacteria. Comp Biochem Physiol B 2010, 155:403-412.
• [129]Enkerli K, Mims CW, Hahn MG: Immunogold localization of callose and other plant cell wall components in soybean roots infected with the oomycete Phytophthora sojae. Can J Bot 1997, 75:1509-1517.
• [130]Ragni E, Fontaine T, Gissi C, Latge JP, Popolo L: The Gas family of proteins of Saccharomyces cerevisiae: characterization and evolutionary analysis. Yeast 2007, 24:297-308.
• [131]Mouyna I, Fontaine T, Vai M, Monod M, Fonzi WA, Diaquin M, Popolo L, Hartland RP, Latge JP: Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 2000, 275:14882-14889.
• [132]Durand A, Hughes R, Roussel A, Flatman R, Henrissat B, Juge N: Emergence of a subfamily of xylanase inhibitors within glycoside hydrolase family 18. FEBS J 2005, 272:1745-1855.
• [133]Tzelepis GD, Melin P, Jensen DF, Stenlid J, Karlssona M: Functional analysis of glycoside hydrolase family 18 and 20 genes in Neurospora crassa. Fungal Genet Biol 2012, 49:717-730.
• [134]Lefebvre F, Joly DL, Labbé C, Teichmann B, Linning R, Belzile F, Bakkeren G, Bélanger RR: The transition from a phytopathogenic smut ancestor to an anamorphic biocontrol agent deciphered by comparative whole-genome analysis. Plant Cell 2013, 25:1946-1959.
• [135]Buist G, Steen A, Kok J, Kuipers OP: LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 2008, 68:838-847.
• [136]Gregg KJ, Zandberg WF, Hehemann JH, Whitworth GE, Deng L, Vocadlo DJ, Boraston AB: Analysis of a new family of widely distributed metal-independent α-mannosidases provides unique insight into the processing of N-linked glycans. J Biol Chem 2011, 286:15586-15596.
• [137]Miyazaki T, Matsumoto Y, Matsuda K, Kurakata Y, Matsuo I, Ito Y, Nishikawa A, Tonozuka T: Heterologous expression and characterization of processing α-glucosidase I from Aspergillus brasiliensis ATCC 9642. Glycoconj J 2011, 28:563-571.
• [138]Kato T, Fujita K, Takeuchi M, Kobayashi K, Natsuka S, Ikura K, Kumagai H, Yamamoto K: Identification of an endo-β-N-acetylglucosaminidase gene in Caenorhabditis elegans and its expression in Escherichia coli. Glycobiology 2002, 12:581-587.
• [139]Ficko-Blean E, Boraston AB: Structural analysis of a bacterial exo-α-D-N-acetylglucosaminidase in complex with an unusual disaccharide found in class III mucin. Glycobiology 2012, 22:590-595.
• [140]Cacas J-L, Buré C, Furt F, Maalouf J-P, Badoc A, Cluzet S, Schmitter J-M, Antajan E, Mongrand S: Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity. Phytochemistry 2013, 96:191-200.
• [141]Janeček Š, Svensson B, MacGregor EA: Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur J Biochem 2003, 270:635-645.
• [142]Christiansen C, Abou Hachem M, Janecek S, Viksø-Nielsen A, Blennow A, Svensson B: The carbohydrate-binding module family 20 - diversity, structure, and function. FEBS J 2009, 276:5006-5029.
• [143]Moreira LR, Filho EX: An overview of mannan structure and mannan-degrading enzyme systems. Appl Microbiol Biotechnol 2008, 79:165-178.
• [144]Larsbrink J, Izumi A, Ibatullin FM, Nakhai A, Gilbert HJ, Davies GJ, Brumer H: Structural and enzymatic characterization of a glycoside hydrolase family 31 α-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem J 2011, 436:567-580.
• [145]Springer WR, Cooper DN, Barondes SH: Discoidin I is implicated in cell-substratum attachment and ordered cell migration of Dictyostelium discoideum and resembles fibronectin. Cell 1984, 39:557-564.
• [146]Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W: Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 2009, 60:727-740.
• [147]Judelson HS, Tani S, Narayan RD: Metabolic adaptation of Phytophthora infestans during growth on leaves, tubers and artificial media. Mol Plant Pathol 2009, 10:843-855.
• [148]Phytophthora infestans: Sequencing Project, Broad Institute of Harvard and MIT. http://www.broadinstitute.org/ webcite
• [149]Adhikari BN, Hamilton JP, Zerillo MM, Tisserat N, Lévesque CA, Buell CR: Comparative genomics reveals insight into virulence strategies of plant pathogenic oomycetes. PLoS One 2013, 8:e75072.
• [150]Ospina-Giraldo MD, McWalters J, Seyer L: Structural and functional profile of the carbohydrate esterase gene complement in Phytophthora infestans. Curr Genet 2010, 56:495-506.
• [151]Wang G, Chen H, Xia Y, Cui J, Gu Z, Song Y, Chen YQ, Zhang H, Chen W: How are the non-classically secreted bacterial proteins released into the extracellular milieu? Curr Microbiol 2013, 67:688-695.
• [152]Prudovsky I, Tarantini F, Landriscina M, Neivandt D, Soldi R, Kirov A, Small D, Kathir KM, Rajalingam D, Kumar TK: Secretion without Golgi. J Cell Biochem 2008, 103:1327-1343.
• [153]Simon MC, Kusch J: Communicative functions of GPI-anchored surface proteins in unicellular eukaryotes. Crit Rev Microbiol 2013, 39:70-78.
• [154]Dorokhov YL, Skurat EV, Frolova OY, Gasanova TV, Ivanov PA, Ravin NV, Skryabin KG, Makinen KM, Klimyuk VI, Gleba YY, Atabekov JG: Role of the leader sequence in tobacco pectin methylesterase secretion. FEBS Lett 2006, 580:3329-3334.
• [155]De Groot PW, Ram AF, Klis FM: Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet Biol 2005, 42:657-675.
• [156]Deising H, Rauscher M, Haug M: Differentiation and cell wall degrading enzymes in the obligately biotrophic rust fungus Uromyces viciae-fabae. Can J Bot 1995, 73:S624-S631.
• [157]Brunner PC, Torriani SF, Croll D, Stukenbrock EH, McDonald BA: Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol Biol Evol 2013, 30:1337-1347.
• [158]Zhang XW, Jia LJ, Zhang Y, Jiang G, Li X, Zhang D, Tang WH: In planta stage-specific fungal gene profiling elucidates the molecular strategies of Fusarium graminearum growing inside wheat coleoptiles. Plant Cell 2012, 24:5159-5176.
• [159]Willats WG, McCartney L, Mackie W, Knox JP: Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 2001, 47:9-27.
• [160]Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP: An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 2009, 344:1858-1862.
• [161]Mingora C, Ewer J, Ospina-Giraldo M: Comparative structural and functional analysis of genes encoding pectin methylesterases in Phytophthora spp. Gene 2014, 538:74-83.
• [162]Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BPHJ, Chen Z, Henrissat B, Lee Y-H, Park J, Garcia-Pedrajas MD, Barbara DJ, Anchieta A, de Jonge R, Santhanam P, Maruthachalam K, Atallah Z, Amyotte SG, Paz Z, Inderbitzin P, Hayes RJ, Heiman DI, Young S, Zeng Q, Engels R, Galagan J, Cuomo CA, Dobinson KF, Ma L-J: Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 2011, 7:e1002137.
• [163]Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L, Lapalu N, Plummer KM, Pradier JM, Quevillon E, Sharon A, Simon A, ten Have A, Tudzynski B, Tudzynski P, Wincker P, Andrew M, Anthouard V, Beever RE, Beffa R, Benoit I, Bouzid O, et al.: Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 2011, 7:e1002230.
• [164]Cooper RM, Longman D, Campbell A, Henry M, Lees PE: Enzymic adaptation of cereal pathogens to the monocotyledonous primary wall. Physiol Mol Plant Pathol 1988, 32:33-47.
• [165]Luna E, Pastor V, Robert J, Victor Flors V, Mauch-Mani B, Ton J: Callose deposition: A multifaceted plant defense response. Mol Plant Microbe Interact 2011, 24:183-193.
• [166]Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somerville SC, Voigt CA: Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol 2013, 161:1433-1444.
• [167]Ham JH, Kim MG, Lee SY, Mackey D: Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv. phaseolicola. Plant J 2007, 51:604-616.