1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Phytopathology
  4. Volume 52, 2014
  5. Article

Annual Review of Phytopathology

Volume 52, 2014

Plant Cell Wall–Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi

Abstract

Approximately a tenth of all described fungal species can cause diseases in plants. A common feature of this process is the necessity to pass through the plant cell wall, an important barrier against pathogen attack. To this end, fungi possess a diverse array of secreted enzymes to depolymerize the main structural polysaccharide components of the plant cell wall, i.e., cellulose, hemicellulose, and pectin. Recent advances in genomic and systems-level studies have begun to unravel this diversity and have pinpointed cell wall–degrading enzyme (CWDE) families that are specifically present or enhanced in plant-pathogenic fungi. In this review, we discuss differences between the CWDE arsenal of plant-pathogenic and non-plant-pathogenic fungi, highlight the importance of individual enzyme families for pathogenesis, illustrate the secretory pathway that transports CWDEs out of the fungal cell, and report the transcriptional regulation of expression of CWDE genes in both saprophytic and phytopathogenic fungi.

Keyword(s): cellulases, enzyme secretion, hemicellulases, pectin, plant cell wall, plant pathogens, transcriptional regulation
Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-102313-045831
2014-08-04
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/phyto/52/1/annurev-phyto-102313-045831.html?itemId=/content/journals/10.1146/annurev-phyto-102313-045831&mimeType=html&fmt=ahah

Literature Cited

  1. Aalto MK, Ronne H, Keranen S. 1.  1993. Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J. 12:4095–104 [Google Scholar]
  2. Amselem J, Cuomo CA, van Kan JA, Viaud M, Benito EP. 2.  et al. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7:e1002230 [Google Scholar]
  3. Annis SL, Goodwin PH. 3.  1997. Recent advances in the molecular genetics of plant cell wall–degrading enzymes produced by plant pathogenic fungi. Eur. J. Plant Pathol. 103:1–14 [Google Scholar]
  4. Beeson WT, Phillips CM, Cate JH, Marletta MA. 4.  2012. Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J. Am. Chem. Soc. 134:890–92 [Google Scholar]
  5. Benatti MR, Penning BW, Carpita NC, McCann MC. 5.  2012. We are good to grow: dynamic integration of cell wall architecture with the machinery of growth. Front. Plant Sci. 3:187 [Google Scholar]
  6. Benz JP, Chau BH, Zheng D, Bauer S, Glass NL, Somerville CR. 6.  2013. A comparative systems analysis of polysaccharide-elicited responses in Neurospora crassa reveals carbon source–specific cellular adaptations. Mol. Microbiol. 91:275–99 [Google Scholar]
  7. Biely P, Vrsanska M, Tenkanen M, Kluepfel D. 7.  1997. Endo-β-1,4-xylanase families: differences in catalytic properties. J. Biotechnol. 57:151–66 [Google Scholar]
  8. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ. 8.  2004. Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem. J. 382:769–81 [Google Scholar]
  9. Braakman I, Hebert DN. 9.  2013. Protein folding in the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 5:a013201 [Google Scholar]
  10. Brito N, Espino JJ, Gonzalez C. 10.  2006. The endo-β-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol. Plant-Microbe Interact. 19:25–32 [Google Scholar]
  11. Brodsky JL. 11.  1999. The requirement for molecular chaperones during endoplasmic reticulum–associated protein degradation demonstrates that protein export and import are mechanistically distinct. J. Biol. Chem. 274:3453–60 [Google Scholar]
  12. Brodsky JL, Goeckeler J, Schekman R. 12.  1995. BiP and Sec63p are required for both co- and posttranslational protein translocation into the yeast endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92:9643–46 [Google Scholar]
  13. Brunner K, Lichtenauer AM, Kratochwill K, Delic M, Mach RL. 13.  2007. Xyr1 regulates xylanase but not cellulase formation in the head blight fungus Fusarium graminearum. Curr. Genet. 52:213–20 [Google Scholar]
  14. Calero-Nieto F, Di Pietro A, Roncero MI, Hera C. 14.  2007. Role of the transcriptional activator xlnR of Fusarium oxysporum in regulation of xylanase genes and virulence. Mol. Plant-Microbe Interact. 20:977–85 [Google Scholar]
  15. Caracuel Z, Roncero MI, Espeso EA, Gonzalez-Verdejo CI, Garcia-Maceira FI, Di Pietro A. 15.  2003. The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol. Microbiol. 48:765–79 [Google Scholar]
  16. Cervone F, De Lorenzo G, Pressey R, Darvill AG, Albersheim P. 16.  1990. Can Phaseolus PGIP inhibit pectic enzymes from microbes and plants?. Phytochemistry 29:447–49 [Google Scholar]
  17. Cervone F, Hahn MG, De Lorenzo G, Darvill A, Albersheim P. 17.  1989. Host-pathogen interactions: XXXIII. A plant protein converts a fungal pathogenesis factor into an elicitor of plant defense responses. Plant Physiol. 90:542–48 [Google Scholar]
  18. Cho Y, Kim KH, La Rota M, Scott D, Santopietro G. 18.  et al. 2009. Identification of novel virulence factors associated with signal transduction pathways in Alternaria brassicicola. Mol. Microbiol. 72:1316–33 [Google Scholar]
  19. Conesa A, Punt PJ, van Luijk N, van den Hondel CA. 19.  2001. The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet. Biol. 33:155–71 [Google Scholar]
  20. Coradetti ST, Craig JP, Xiong Y, Shock T, Tian C, Glass NL. 20.  2012. Conserved and essential transcription factors for cellulase gene expression in ascomycete fungi. Proc. Natl. Acad. Sci. USA 109:7397–402 [Google Scholar]
  21. Cosgrove DJ. 21.  2005. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 6:850–61 [Google Scholar]
  22. Cox JS, Chapman RE, Walter P. 22.  1997. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8:1805–14 [Google Scholar]
  23. Cross BC, Sinning I, Luirink J, High S. 23.  2009. Delivering proteins for export from the cytosol. Nat. Rev. Mol. Cell Biol. 10:255–64 [Google Scholar]
  24. Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG. 24.  et al. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–2 [Google Scholar]
  25. Dean RA, Timberlake WE. 25.  1989. Production of cell wall–degrading enzymes by Aspergillus nidulans: a model system for fungal pathogenesis of plants. Plant Cell 1:265–73 [Google Scholar]
  26. De Lorenzo G, D'Ovidio R, Cervone F. 26.  2001. The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu. Rev. Phytopathol. 39:313–35 [Google Scholar]
  27. De Lorenzo G, Ferrari S. 27.  2002. Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr. Opin. Plant Biol. 5:295–99 [Google Scholar]
  28. Deshpande N, Wilkins MR, Packer N, Nevalainen H. 28.  2008. Protein glycosylation pathways in filamentous fungi. Glycobiology 18:626–37 [Google Scholar]
  29. de Vries RP, Visser J. 29.  2001. Aspergillus enzymes involved in degradation of plant cell wall polysaccharides. Microbiol. Mol. Biol. Rev. 65:497–522 [Google Scholar]
  30. Dowzer CE, Kelly JM. 30.  1991. Analysis of the creA gene, a regulator of carbon catabolite repression in Aspergillus nidulans. Mol. Cell. Biol. 11:5701–9 [Google Scholar]
  31. Espino JJ, Brito N, Noda J, Gonzalez C. 31.  2005. Botrytis cinerea endo-β-1,4-glucanase Cel5A is expressed during infection but is not required for pathogenesis. Physiol. Mol. Plant Pathol. 66:213–21 [Google Scholar]
  32. Fajardo-Somera RA, Bowman B, Riquelme M. 32.  2013. The plasma membrane proton pump PMA-1 is incorporated into distal parts of the hyphae independently of the Spitzenkörper in Neurospora crassa. Eukaryot. Cell 12:1097–105 [Google Scholar]
  33. Felenbok B, Flipphi M, Nikolaev I. 33.  2001. Ethanol catabolism in Aspergillus nidulans: a model system for studying gene regulation. Prog. Nucleic Acid Res. Mol. Biol. 69:149–204 [Google Scholar]
  34. Fernandez J, Wright JD, Hartline D, Quispe CF, Madayiputhiya N, Wilson RA. 34.  2012. Principles of carbon catabolite repression in the rice blast fungus: Tps1, Nmr1-3, and a MATE-family pump regulate glucose metabolism during infection. PLoS Genet. 8:e1002673 [Google Scholar]
  35. Fernandez-Acero FJ, Colby T, Harzen A, Carbu M, Wieneke U. 35.  et al. 2010. 2-DE proteomic approach to the Botrytis cinerea secretome induced with different carbon sources and plant-based elicitors. Proteomics 10:2270–80 [Google Scholar]
  36. Fernandez-Alvarez A, Elias-Villalobos A, Ibeas JI. 36.  2010. Protein glycosylation in the phytopathogen Ustilago maydis: from core oligosaccharide synthesis to the ER glycoprotein quality control system, a genomic analysis. Fungal Genet. Biol. 47:727–35 [Google Scholar]
  37. Fernandez-Alvarez A, Marin-Menguiano M, Lanver D, Jimenez-Martin A, Elias-Villalobos A. 37.  et al. 2012. Identification of O-mannosylated virulence factors in Ustilago maydis. PLoS Pathog. 8:e1002563 [Google Scholar]
  38. Gibson DM, King BC, Hayes ML, Bergstrom GC. 38.  2011. Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Curr. Opin. Microbiol. 14:264–70 [Google Scholar]
  39. Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M. 39.  et al. 2013. Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat. Commun. 4:1996 [Google Scholar]
  40. Glass NL, Schmoll M, Cate JH, Coradetti S. 40.  2013. Plant cell wall deconstruction by ascomycete fungi. Annu. Rev. Microbiol. 67:477–98 [Google Scholar]
  41. Gonzalez M, Brito N, Frias M, Gonzalez C. 41.  2013. Botrytis cinerea protein O-mannosyltransferases play critical roles in morphogenesis, growth, and virulence. PLoS ONE 8:e65924 [Google Scholar]
  42. Goto M. 42.  2007. Protein O-glycosylation in fungi: diverse structures and multiple functions. Biosci. Biotechnol. Biochem. 71:1415–27 [Google Scholar]
  43. Guillemette T, van Peij N, Goosen T, Lanthaler K, Robson GD. 43.  et al. 2007. Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger. BMC Genomics 8:158 [Google Scholar]
  44. Hayakawa Y, Ishikawa E, Shoji JY, Nakano H, Kitamoto K. 44.  2011. Septum-directed secretion in the filamentous fungus Aspergillus oryzae. Mol. Microbiol. 81:40–55 [Google Scholar]
  45. He B, Guo W. 45.  2009. The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 21:537–42 [Google Scholar]
  46. Hematy K, Cherk C, Somerville S. 46.  2009. Host-pathogen warfare at the plant cell wall. Curr. Opin. Plant Biol. 12:406–13 [Google Scholar]
  47. Henrissat B, Bairoch A. 47.  1993. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293:781–88 [Google Scholar]
  48. Herrmann MC, Vrsanska M, Jurickova M, Hirsch J, Biely P, Kubicek CP. 48.  1997. The β-d-xylosidase of Trichoderma reesei is a multifunctional β-d-xylan xylohydrolase. Biochem. J. 321:375–81 [Google Scholar]
  49. Horbach R, Navarro-Quesada AR, Knogge W, Deising HB. 49.  2011. When and how to kill a plant cell: infection strategies of plant pathogenic fungi. J. Plant Physiol. 168:51–62 [Google Scholar]
  50. Hutagalung AH, Novick PJ. 50.  2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91:119–49 [Google Scholar]
  51. Islam MS, Haque MS, Islam MM, Emdad EM, Halim A. 51.  et al. 2012. Tools to kill: genome of one of the most destructive plant pathogenic fungi Macrophomina phaseolina. BMC Genomics 13:493 [Google Scholar]
  52. Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H. 52.  2001. Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol. Plant-Microbe Interact. 14:749–57 [Google Scholar]
  53. Jonkers W, Rep M. 53.  2009. Mutation of CRE1 in Fusarium oxysporum reverts the pathogenicity defects of the FRP1 deletion mutant. Mol. Microbiol. 74:1100–13 [Google Scholar]
  54. Joubert A, Simoneau P, Campion C, Bataille-Simoneau N, Iacomi-Vasilescu B. 54.  et al. 2011. Impact of the unfolded protein response on the pathogenicity of the necrotrophic fungus Alternaria brassicicola. Mol. Microbiol. 79:1305–24 [Google Scholar]
  55. Juge N. 55.  2006. Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci. 11:359–67 [Google Scholar]
  56. Kabani M, Kelley SS, Morrow MW, Montgomery DL, Sivendran R. 56.  et al. 2003. Dependence of endoplasmic reticulum–associated degradation on the peptide binding domain and concentration of BiP. Mol. Biol. Cell 14:3437–48 [Google Scholar]
  57. Katoh H, Ohtani K, Yamamoto H, Akimitsu K. 57.  2007. Overexpression of a gene encoding a catabolite repression element in Alternaria citri causes severe symptoms of black rot in citrus fruit. Phytopathology 97:557–63 [Google Scholar]
  58. Kema GH, van der Lee TA, Mendes O, Verstappen EC, Lankhorst RK. 58.  et al. 2008. Large-scale gene discovery in the Septoria tritici blotch fungus Mycosphaerella graminicola with a focus on in planta expression. Mol. Plant-Microbe Interact. 21:1249–60 [Google Scholar]
  59. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY. 59.  et al. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388–403 [Google Scholar]
  60. Kienle N, Kloepper TH, Fasshauer D. 60.  2009. Phylogeny of the SNARE vesicle fusion machinery yields insights into the conservation of the secretory pathway in fungi. BMC Evol. Biol. 9:19 [Google Scholar]
  61. King BC, Waxman KD, Nenni NV, Walker LP, Bergstrom GC, Gibson DM. 61.  2011. Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol. Biofuels 4:4 [Google Scholar]
  62. Kriangkripipat T, Momany M. 62.  2009. Aspergillus nidulans protein O-mannosyltransferases play roles in cell wall integrity and developmental patterning. Eukaryot. Cell 8:1475–85 [Google Scholar]
  63. Kubicek CP. 63.  2012. Fungi and Lignocellulose Biomass New York: Wiley and Sons
  64. Kurasin M, Valjamae P. 64.  2011. Processivity of cellobiohydrolases is limited by the substrate. J. Biol. Chem. 286:169–77 [Google Scholar]
  65. Kuratsu M, Taura A, Shoji JY, Kikuchi S, Arioka M, Kitamoto K. 65.  2007. Systematic analysis of SNARE localization in the filamentous fungus Aspergillus oryzae. Fungal Genet. Biol. 44:1310–23 [Google Scholar]
  66. Lara-Márquez A, Zavala-Páramo MG, López-Romero E, Camacho HC. 66.  2011. Biotechnological potential of pectinolytic complexes of fungi. Biotechnol. Lett. 33:859–68 [Google Scholar]
  67. Lehle L, Strahl S, Tanner W. 67.  2006. Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. 45:6802–18 [Google Scholar]
  68. Lombard V, Bernard T, Rancurel C, Brumer H, Coutinho PM, Henrissat B. 68.  2010. A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem. J. 432:437–44 [Google Scholar]
  69. Lommel M, Strahl S. 69.  2009. Protein O-mannosylation: conserved from bacteria to humans. Glycobiology 19:816–28 [Google Scholar]
  70. Louw C, Young PR, van Rensburg P, Divol B. 70.  2010. Regulation of endo-polygalacturonase activity in Saccharomyces cerevisiae. FEMS Yeast Res. 10:44–57 [Google Scholar]
  71. Malsam J, Kreye S, Sollner TH. 71.  2008. Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65:2814–32 [Google Scholar]
  72. Martinez-Soto D, Robledo-Briones AM, Estrada-Luna AA, Ruiz-Herrera J. 72.  2013. Transcriptomic analysis of Ustilago maydis infecting Arabidopsis reveals important aspects of the fungus pathogenic mechanisms. Plant Signal Behav. 8:pii:e25059 [Google Scholar]
  73. Mathioni SM, Belo A, Rizzo CJ, Dean RA, Donofrio NM. 73.  2011. Transcriptome profiling of the rice blast fungus during invasive plant infection and in vitro stresses. BMC Genomics 12:49 [Google Scholar]
  74. Miyara I, Shafran H, Kramer Haimovich H, Rollins J, Sherman A, Prusky D. 74.  2008. Multi-factor regulation of pectate lyase secretion by Colletotrichum gloeosporioides pathogenic on avocado fruits. Mol. Plant Pathol. 9:281–91 [Google Scholar]
  75. Molinari M, Galli C, Vanoni O, Arnold SM, Kaufman RJ. 75.  2005. Persistent glycoprotein misfolding activates the glucosidase II/UGT1-driven calnexin cycle to delay aggregation and loss of folding competence. Mol. Cell 20:503–12 [Google Scholar]
  76. Moreira LR, Filho EX. 76.  2008. An overview of mannan structure and mannan-degrading enzyme systems. Appl. Microbiol. Biotechnol. 79:165–78 [Google Scholar]
  77. Morrow MW, Janke MR, Lund K, Morrison EP, Paulson BA. 77.  2011. The Candida albicans Kar2 protein is essential and functions during the translocation of proteins into the endoplasmic reticulum. Curr. Genet. 57:25–37 [Google Scholar]
  78. Mouyna I, Kniemeyer O, Jank T, Loussert C, Mellado E. 78.  et al. 2010. Members of protein O-mannosyltransferase family in Aspergillus fumigatus differentially affect growth, morphogenesis and viability. Mol. Microbiol. 76:1205–21 [Google Scholar]
  79. Murphy C, Powlowski J, Wu M, Butler G, Tsang A. 79.  2011. Curation of characterized glycoside hydrolases of fungal origin. Database 2011:bar020 [Google Scholar]
  80. Nguyen QB, Itoh K, Van Vu B, Tosa Y, Nakayashiki H. 80.  2011. Simultaneous silencing of endo-β-1,4 xylanase genes reveals their roles in the virulence of Magnaporthe oryzae. Mol. Microbiol. 81:1008–19 [Google Scholar]
  81. Noda J, Brito N, Gonzalez C. 81.  2010. The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol. 10:38 [Google Scholar]
  82. Nykanen M, Saarelainen R, Raudaskoski M, Nevalainen K, Mikkonen A. 82.  1997. Expression and secretion of barley cysteine endopeptidase B and cellobiohydrolase I in Trichoderma reesei. Appl. Environ. Microbiol. 63:4929–37 [Google Scholar]
  83. Oeser B, Heidrich PM, Muller U, Tudzynski P, Tenberge KB. 83.  2002. Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet. Biol. 36:176–86 [Google Scholar]
  84. Oka M, Maruyama J-I, Arioka M, Nakajima H, Kitamoto K. 84.  2004. Molecular cloning and functional characterization of avaB, a gene encoding Vam6p/Vps39p-like protein in Aspergillus nidulans. FEMS Microbiol. Lett. 232:113–21 [Google Scholar]
  85. Oka OB, Bulleid NJ. 85.  2013. Forming disulfides in the endoplasmic reticulum. Biochim. Biophys. Acta 1833:2425–29 [Google Scholar]
  86. Ostling J, Ronne H. 86.  1998. Negative control of the Mig1p repressor by Snf1p-dependent phosphorylation in the absence of glucose. Eur. J. Biochem. 252:162–68 [Google Scholar]
  87. Patil C, Walter P. 87.  2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349–55 [Google Scholar]
  88. Penalva MA, Arst HN Jr. 88.  2004. Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu. Rev. Microbiol. 58:425–51 [Google Scholar]
  89. Penalva MA, Tilburn J, Bignell E, Arst HN Jr. 89.  2008. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 16:291–300 [Google Scholar]
  90. Portnoy T, Margeot A, Linke R, Atanasova L, Fekete E. 90.  et al. 2011. The CRE1 carbon catabolite repressor of the fungus Trichoderma reesei: a master regulator of carbon assimilation. BMC Genomics 12:269 [Google Scholar]
  91. Prusky D, Yakoby N. 91.  2003. Pathogenic fungi: leading or led by ambient pH?. Mol. Plant Pathol. 4:509–16 [Google Scholar]
  92. Punt PJ, Seiboth B, Weenink XO, van Zeijl C, Lenders M. 92.  et al. 2001. Identification and characterization of a family of secretion-related small GTPase-encoding genes from the filamentous fungus Aspergillus niger: a putative SEC4 homologue is not essential for growth. Mol. Microbiol. 41:513–25 [Google Scholar]
  93. Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen JC. 93.  et al. 2011. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc. Natl. Acad. Sci. USA 108:15079–84 [Google Scholar]
  94. Read ND. 94.  2011. Exocytosis and growth do not occur only at hyphal tips. Mol. Microbiol. 81:4–7 [Google Scholar]
  95. Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller KK. 95.  et al. 2009. A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog. 5:e1000258 [Google Scholar]
  96. Ridley BL, O'Neill MA, Mohnen D. 96.  2001. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–67 [Google Scholar]
  97. Riquelme M, Yarden O, Bartnicki-Garcia S, Bowman B, Castro-Longoria E. 97.  et al. 2011. Architecture and development of the Neurospora crassa hypha: a model cell for polarized growth. Fungal Biol. 115:446–74 [Google Scholar]
  98. Rose JK, Saladie M, Catala C. 98.  2004. The plot thickens: new perspectives of primary cell wall modification. Curr. Opin. Plant Biol. 7:296–301 [Google Scholar]
  99. Sallese M, Giannotta M, Luini A. 99.  2009. Coordination of the secretory compartments via inter-organelle signalling. Semin. Cell Dev. Biol. 20:801–9 [Google Scholar]
  100. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B. 100.  et al. 2002. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur. J. Biochem. 269:4202–11 [Google Scholar]
  101. Saloheimo M, Valkonen M, Penttila M. 101.  2003. Activation mechanisms of the HAC1-mediated unfolded protein response in filamentous fungi. Mol. Microbiol. 47:1149–61 [Google Scholar]
  102. Sarkar P, Bosneaga E, Auer M. 102.  2009. Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J. Exp. Bot. 60:3615–35 [Google Scholar]
  103. Schekman R. 103.  2010. Charting the secretory pathway in a simple eukaryote. Mol. Biol. Cell 21:3781–84 [Google Scholar]
  104. Schwarz F, Aebi M. 104.  2011. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol. 21:576–82 [Google Scholar]
  105. Seiboth B, Herold S, Kubicek CP. 105.  2012. Metabolic engineering of inducer formation for cellulase and hemicellulase gene expression in Trichoderma reesei. Subcell. Biochem. 64:367–90 [Google Scholar]
  106. Sevier CS. 106.  2012. Erv2 and quiescin sulfhydryl oxidases: Erv-domain enzymes associated with the secretory pathway. Antioxid. Redox Signal. 16:800–8 [Google Scholar]
  107. Shieh MT, Brown RL, Whitehead MP, Cary JW, Cotty PJ. 107.  et al. 1997. Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Appl. Environ. Microbiol. 63:3548–52 [Google Scholar]
  108. Shoji JY, Arioka M, Kitamoto K. 108.  2008. Dissecting cellular components of the secretory pathway in filamentous fungi: insights into their application for protein production. Biotechnol. Lett. 30:7–14 [Google Scholar]
  109. Siriputthaiwan P, Jauneau A, Herbert C, Garcin D, Dumas B. 109.  2005. Functional analysis of CLPT1, a Rab/GTPase required for protein secretion and pathogenesis in the plant fungal pathogen Colletotrichum lindemuthianum. J. Cell Sci. 118:323–29 [Google Scholar]
  110. Spang A. 110.  2008. The life cycle of a transport vesicle. Cell. Mol. Life Sci. 65:2781–89 [Google Scholar]
  111. Srivastava A, Ohm RA, Oxiles L, Brooks F, Lawrence CB. 111.  et al. 2012. A zinc-finger-family transcription factor, AbVf19, is required for the induction of a gene subset important for virulence in Alternaria brassicicola. Mol. Plant-Microbe Interact. 25:443–52 [Google Scholar]
  112. Steel GJ, Fullerton DM, Tyson JR, Stirling CJ. 112.  2004. Coordinated activation of Hsp70 chaperones. Science 303:98–101 [Google Scholar]
  113. Struck C. 113.  2006. Infection strategies of plant parasitic fungi. The Epidemiology of Plant Diseases BM Cooke, D Gareth Jones, B Kaye 117–37 Dordrecht, The Neth.: Springer [Google Scholar]
  114. Su G, Suh SO, Schneider RW, Russin JS. 114.  2001. Host specialization in the charcoal rot fungus, Macrophomina phaseolina. Phytopathology 91:120–26 [Google Scholar]
  115. Sun J, Glass NL. 115.  2011. Identification of the CRE-1 cellulolytic regulon in Neurospora crassa. PLoS ONE 6:e25654 [Google Scholar]
  116. Sun J, Tian C, Diamond S, Glass NL. 116.  2012. Deciphering transcriptional regulatory mechanisms associated with hemicellulose degradation in Neurospora crassa. Eukaryot. Cell 11:482–93 [Google Scholar]
  117. Taheri-Talesh N, Horio T, Araujo-Bazan L, Dou X, Espeso EA. 117.  et al. 2008. The tip growth apparatus of Aspergillus nidulans. Mol. Biol. Cell 19:1439–49 [Google Scholar]
  118. Teeri TT. 118.  1997. Crystalline cellulose degradation: new insight into the function of cellobiohydrolases. Trends Biotechol. 15:160–67 [Google Scholar]
  119. ten Have A, Mulder W, Visser J, van Kan JA. 119.  1998. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol. Plant-Microbe Interact. 11:1009–16 [Google Scholar]
  120. Tenkanen M, Vrsanska M, Siika-aho M, Wong DW, Puchart V. 120.  et al. 2013. Xylanase XYN IV from Trichoderma reesei showing exo- and endo-xylanase activity. FEBS J. 280:285–301 [Google Scholar]
  121. Tonukari NJ. 121.  2003. Enzymes and fungal virulence. J. Appl. Sci. Environ. Manag. 7:5–8 [Google Scholar]
  122. Tonukari NJ, Scott-Craig JS, Walton JD. 122.  2000. The Cochliobolus carbonum SNF1 gene is required for cell wall–degrading enzyme expression and virulence on maize. Plant Cell 12:237–48 [Google Scholar]
  123. Underwood W. 123.  2012. The plant cell wall: a dynamic barrier against pathogen invasion. Front. Plant Sci. 3:85 [Google Scholar]
  124. Valkonen M, Kalkman ER, Saloheimo M, Penttila M, Read ND, Duncan RR. 124.  2007. Spatially segregated SNARE protein interactions in living fungal cells. J. Biol. Chem. 282:22775–85 [Google Scholar]
  125. van den Brink J, de Vries RP. 125.  2011. Fungal enzyme sets for plant polysaccharide degradation. Appl. Microbiol. Biotechnol. 91:1477–92 [Google Scholar]
  126. van der Does HC, Rep M. 126.  2007. Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Mol. Plant-Microbe Interact. 20:1175–82 [Google Scholar]
  127. Van Vu B, Itoh K, Nguyen QB, Tosa Y, Nakayashiki H. 127.  2012. Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol. Plant-Microbe Interact. 25:1135–41 [Google Scholar]
  128. Wong Sak Hoi J, Dumas B. 128.  2010. Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryot. Cell 9:480–85 [Google Scholar]
  129. Yazawa T, Kawahigashi H, Matsumoto T, Mizuno H. 129.  2013. Simultaneous transcriptome analysis of sorghum and Bipolaris sorghicola by using RNA-seq in combination with de novo transcriptome assembly. PLoS ONE 8:e62460 [Google Scholar]
  130. Yi M, Chi MH, Khang CH, Park SY, Kang S. 130.  et al. 2009. The ER chaperone LHS1 is involved in asexual development and rice infection by the blast fungus Magnaporthe oryzae. Plant Cell 21:681–95 [Google Scholar]
  131. Yi M, Park JH, Ahn JH, Lee YH. 131.  2008. MoSNF1 regulates sporulation and pathogenicity in the rice blast fungus Magnaporthe oryzae. Fungal Genet. Biol. 45:1172–81 [Google Scholar]
  132. Zhao Z, Liu H, Wang C, Xu JR. 132.  2013. Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14:274 [Google Scholar]
  133. Zimmermann R, Eyrisch S, Ahmad M, Helms V. 133.  2011. Protein translocation across the ER membrane. Biochim. Biophys. Acta 1808:912–24 [Google Scholar]
  134. Znameroski EA, Glass NL. 134.  2013. Using a model filamentous fungus to unravel mechanisms of lignocellulose deconstruction. Biotechnol. Biofuels 6:6 [Google Scholar]
/content/journals/10.1146/annurev-phyto-102313-045831
Loading
Plant Cell Wall–Degrading Enzymes and Their Secretion in Plant-Pathogenic Fungi
Annual Review of Phytopathology 52, 427 (2014); https://doi.org/10.1146/annurev-phyto-102313-045831
/content/journals/10.1146/annurev-phyto-102313-045831
/content/journals/10.1146/annurev-phyto-102313-045831
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error