Abstract
Fungi that interact with plants gain access to host tissues by actively passing the surface through the cuticle and/or cell wall. Cell walls provide plant tissue strength and structure, and form a barrier against microbial invasion. Plants invest substantial resources in constructing the cell wall and maintaining its integrity. On the other hand, carbon deposited in cell walls offers opportunities for fungi to utilise them as nutrients. This chapter discusses the opposite roles of plant cell walls, both as a barrier for penetration and a food source for fungi, with focus on pectin. We discuss the chemical structures of plant cell-wall polysaccharides, the cell-wall-associated mechanisms that confer resistance against pathogens, and the microbial enzymes involved in cell-wall decomposition. We then focus on plant cell-wall-degrading enzymes of pathogenic fungi, and illustrate with case studies how Botrytis cinerea decomposes pectin present in plant cell walls, and utilizes the breakdown products as nutrients.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681
Aguero CB, Uratsu SL, Greve C, Powell AL, Labavitch JM, Meredith CP, Dandekar AM (2005) Evaluation of tolerance to Pierce’s disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Mol Plant Pathol 6:43–51
Amselem J, Cuomo CA, van Kan JAL, 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, Brault B, Chen Z, Choquer M, Collemare J, Cotton P, Danchin EG, Da Silva C, Gautier A, Giraud C, Giraud T, Gonzalez C, Grossetete S, Guldener U, Henrissat B, Howlett BJ, Kodira C, Kretschmer M, Lappartient A, Leroch M, Levis C, Mauceli E, Neuveglise C, Oeser B, Pearson M, Poulain J, Poussereau N, Quesneville H, Rascle C, Schumacher J, Segurens B, Sexton A, Silva E, Sirven C, Soanes DM, Talbot NJ, Templeton M, Yandava C, Yarden O, Zeng Q, Rollins JA, Lebrun MH, Dickman M (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230
Aro N, Pakula T, Penttila M (2005) Transcriptional regulation of plant cell wall degradation by filamentous fungi. FEMS Microbiol Rev 29:719–739
Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W, Bittner-Eddy P, Boore JL, Chibucos MC, Coates M, Dehal P, Delehaunty K, Dong S, Downton P, Dumas B, Fabro G, Fronick C, Fuerstenberg SI, Fulton L, Gaulin E, Govers F, Hughes L, Humphray S, Jiang RH, Judelson H, Kamoun S, Kyung K, Meijer H, Minx P, Morris P, Nelson J, Phuntumart V, Qutob D, Rehmany A, Rougon-Cardoso A, Ryden P, Torto-Alalibo T, Studholme D, Wang Y, Win J, Wood J, Clifton SW, Rogers J, Van den Ackerveken G, Jones JD, McDowell JM, Beynon J, Tyler BM (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330:1549–1551
Billon-Grand G, Rascle C, Droux M, Rollins JA, Poussereau N (2012) pH modulation differs during sunflower cotyledon colonization by the two closely related necrotrophic fungi Botrytis cinerea and Sclerotinia sclerotiorum. Mol Plant Pathol 13:568–578
Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30
Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712
Brito N, Espino JJ, Gonzalez C (2006) The endo-beta-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol Plant Microbe Interact 19:25–32
Cabanne C, Doneche B (2002) Purification and characterization of two isozymes of polygalacturonase from Botrytis cinerea. Effect of calcium ions on polygalacturonase activity. Microbiol Res 157:183–189
Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238
Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277:1–10
Cosgrove DJ (2001) Plant cell walls: wall-associated kinases and cell expansion. Curr Biol 11:R558–R559
De Lorenzo G, D’Ovidio R, Cervone F (2001) The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu Rev Phytopathol 39:313–335
Dean R, van Kan JAL, Pretorius ZA, Hammond-Kosack KE, DI Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430
Duplessis S, Hacquard S, Delaruelle C, Tisserant E, Frey P, Martin F, Kohler A (2011) Melampsora larici-populina transcript profiling during germination and timecourse infection of poplar leaves reveals dynamic expression patterns associated with virulence and biotrophy. Mol Plant Microbe Interact 24:808–818
Espino JJ, Brito N, Noda J, Gonzalez C (2005) Botrytis cinerea endo-beta-1,4-glucanase Cel5A is expressed during infection but is not required for pathogenesis. Physiol Mol Plant Pathol 66:213–221
Espino JJ, Gutierrez-Sanchez G, Brito N, Shah P, Orlando R, Gonzalez C (2010) The Botrytis cinerea early secretome. Proteomics 10:3020–3034
Federici L, Di Matteo A, Fernandez-Recio J, Tsernoglou D, Cervone F (2006) Polygalacturonase inhibiting proteins: players in plant innate immunity? Trends Plant Sci 11:65–70
Fernandez-Acero FJ, Colby T, Harzen A, Carbu M, Wieneke U, Cantoral JM, Schmidt J (2010) 2-DE proteomic approach to the Botrytis cinerea secretome induced with different carbon sources and plant-based elicitors. Proteomics 10:2270–2280
Ferrari S, Vairo D, Ausubel FM, Cervone F, De Lorenzo G (2003) Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell 15:93–106
Ferrari S, Galletti R, Vairo D, Cervone F, De Lorenzo G (2006) Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Mol Plant Microbe Interact 19:931–936
Flors V, Ton J, van Doorn R, Jakab G, Garcia-Agustin P, Mauch-Mani B (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54:81–92
Garcia-Andrade J, Ramirez V, Flors V, Vera P (2011) Arabidopsis ocp3 mutant reveals a mechanism linking ABA and JA to pathogen-induced callose deposition. Plant J 67:783–794
Hückelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:101–127
Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H (2001) Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol Plant Microbe Interact 14:749–757
Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513
Janni M, Sella L, Favaron F, Blechl AE, De Lorenzo G, D’Ovidio R (2008) The expression of a bean PGIP in transgenic wheat confers increased resistance to the fungal pathogen Bipolaris sorokiniana. Mol Plant Microbe Interact 21:171–177
Jolie RP, Duvetter T, Van Loey AM, Hendrickx ME (2010) Pectin methylesterase and its proteinaceous inhibitor: a review. Carbohydr Res 345:2583–2595
Joubert DA, Kars I, Wagemakers L, Bergmann C, Kemp G, Vivier MA, van Kan JAL (2007) A polygalacturonase-inhibiting protein from grapevine reduces the symptoms of the endopolygalacturonase BcPG2 from Botrytis cinerea in Nicotiana benthamiana leaves without any evidence for in vitro interaction. Mol Plant Microbe Interact 20:392–402
Juge N (2006) Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci 11:359–367
Kämper J, Kahmann R, Bolker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HA, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrugge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho EC, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Hauser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schluter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Guldener U, Munsterkotter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97–101
Kars I, van Kan JAL (2004) Extracellular enzymes and metabolites involved in pathogenesis of Botrytis. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Kluwer, The Netherlands, pp 99–118
Kars I, McCalman M, Wagemakers L, VAN Kan JA (2005a) Functional analysis of Botrytis cinerea pectin methylesterase genes by PCR-based targeted mutagenesis: Bcpme1 and Bcpme2 are dispensable for virulence of strain B05.10. Mol Plant Pathol 6:641–652
Kars I, Krooshof GH, Wagemakers L, Joosten R, Benen JA, van Kan JAL (2005b) Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J 43:213–225
Koeck M, Hardham AR, Dodds PN (2011) The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cell Microbiol 13:1849–1857
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275
Manfredini C, Sicilia F, Ferrari S, Pontiggia D, Salvi G, Caprari C, Lorito M, De Lorenzo G (2005) Polygalacturonase-inhibiting protein 2 of Phaseolus vulgaris inhibits BcPG1, a polygalacturonase of Botrytis cinerea important for pathogenicity, and protects transgenic plants from infection. Physiol Mol Plant Pathol 67:108–115
Martens-Uzunova ES, Schaap PJ (2008) An evolutionary conserved d-galacturonic acid metabolic pathway operates across filamentous fungi capable of pectin degradation. Fungal Genet Biol 45:1449–1457
Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R, Porcel B, Rubini A, Amicucci A, Amselem J, Anthouard V, Arcioni S, Artiguenave F, Aury JM, Ballario P, Bolchi A, Brenna A, Brun A, Buee M, Cantarel B, Chevalier G, Couloux A, Da Silva C, Denoeud F, Duplessis S, Ghignone S, Hilselberger B, Iotti M, Marcais B, Mello A, Miranda M, Pacioni G, Quesneville H, Riccioni C, Ruotolo R, Splivallo R, Stocchi V, Tisserant E, Viscomi AR, Zambonelli A, Zampieri E, Henrissat B, Lebrun MH, Paolocci F, Bonfante P, Ottonello S, Wincker P (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038
Martin F, Cullen D, Hibbett D, Pisabarro A, Spatafora JW, Baker SE, Grigoriev IV (2011) Sequencing the fungal tree of life. New Phytol 190:818–821
Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277
Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972
Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Ibeta from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082
Noda J, Brito N, Gonzalez C (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10:38
Oeser B, Heidrich PM, Muller U, Tudzynski P, Tenberge KB (2002) Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol 36:176–186
Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA, Walton JD (2007) Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 7:3171–3183
Phalip V, Goubet F, Carapito R, Jeltsch JM (2009) Plant cell wall degradation with a powerful Fusarium graminearum enzymatic arsenal. J Microbiol Biotechnol 19:573–581
Powell AL, van Kan JAL, ten Have A, Visser J, Greve LC, Bennett AB, Labavitch JM (2000) Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol Plant Microbe Interact 13:942–950
Rha E, Park HJ, Kim MO, Chung YR, Lee CW, Kim JW(2001) Expression of exo-polygalacturonases in Botrytis cinerea. FEMS Microbiol Lett 201:105–109
Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289
Schols HA, Coenen GJ, Voragen AGJ (2009) Revealing pectin’s structure. In: Schols HA, Visser RGF, Voragen AGJ (eds) Pectins and pectinases. Wageningen Academic Publishers, The Netherlands, pp 19–34
Shah P, Gutierrez-Sanchez G, Orlando R, Bergmann C (2009a) A proteomic study of pectin-degrading enzymes secreted by Botrytis cinerea grown in liquid culture. Proteomics 9:3126–3135
Shah P, Atwood JA, Orlando R, El Mubarek H, Podila GK, Davis MR (2009b) Comparative proteomic analysis of Botrytis cinerea secretome. J Proteome Res 8:1123–1130
Shieh MT, Brown RL, Whitehead MP, Cary JW, Cotty PJ, Cleveland TE, Dean RA (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 63:3548–3552
Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stuber K, Loren V, van Themaat E, Brown JK, Butcher SA, Gurr SJ, Lebrun MH, Ridout CJ, Schulze-Lefert P, Talbot NJ, Ahmadinejad N, Ametz C, Barton GR, Benjdia M, Bidzinski P, Bindschedler LV, Both M, Brewer MT, Cadle-Davidson L, Cadle-Davidson MM, Collemare J, Cramer R, Frenkel O, Godfrey D, Harriman J, Hoede C, King BC, Klages S, Kleemann J, Knoll D, Koti PS, Kreplak J, Lopez-Ruiz FJ, Lu X, Maekawa T, Mahanil S, Micali C, Milgroom MG, Montana G, Noir S, O’Connell RJ, Oberhaensli S, Parlange F, Pedersen C, Quesneville H, Reinhardt R, Rott M, Sacristan S, Schmidt SM, Schon M, Skamnioti P, Sommer H, Stephens A, Takahara H, Thordal-Christensen H, Vigouroux M, Wessling R, Wicker T, Panstruga R (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546
ten Have A, Mulder W, Visser J, van Kan JAL (1998) The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant Microbe Interact 11:1009–1016
ten Have A, Breuil WO, Wubben JP, Visser J, van Kan JAL (2001) Botrytis cinerea endopolygalacturonase genes are differentially expressed in various plant tissues. Fungal Genet Biol 33:97–105
Valette-Collet O, Cimerman A, Reignault P, Levis C, Boccara M (2003) Disruption of Botrytis cinerea pectin methylesterase gene Bcpme1 reduces virulence on several host plants. Mol Plant Microbe Interact 16:360–367
van Kan JAL (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253
Verhoeff K, Leeman M, Vanpeer R, Posthuma L, Schot N, Vaneijk GW (1988) Changes in pH and the production of organic-acids during colonization of tomato petioles by Botrytis cinerea. J Phytopathol 122:327–336
Volpi C, Janni M, Lionetti V, Bellincampi D, Favaron F, D’Ovidio R (2011) The ectopic expression of a pectin methyl esterase inhibitor increases pectin methyl esterification and limits fungal diseases in wheat. Mol Plant Microbe Interact 24:1012–1019
Voragen AGJ, Schols HA, Pilnik W (1986) Determination of the degree of methylation and acetylation of pectins by h.p.l.c. Food Hydrocoll 1:65–70
Wang Y, Wu J, Park ZY, Kim SG, Rakwal R, Agrawal GK, Kim ST, Kang KY (2011) Comparative secretome investigation of Magnaporthe oryzae proteins responsive to nitrogen starvation. J Proteome Res 10:3136–3148
Williamson B, Tudzynski B, Tudzynski P, van Kan JAL (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580
Wubben JP, Mulder W, ten Have A, van Kan JAL, Visser J (1999) Cloning and partial characterization of endopolygalacturonase genes from Botrytis cinerea. Appl Environ Microbiol 65:1596–1602
Wubben JP, ten Have A, van Kan JAL, Visser J (2000) Regulation of endopolygalacturonase gene expression in Botrytis cinerea by galacturonic acid, ambient pH and carbon catabolite repression. Curr Genet 37:152–157
Yajima W, Kav NN (2006) The proteome of the phytopathogenic fungus Sclerotinia sclerotiorum. Proteomics 6:5995–6007
Yang F, Jensen JD, Svensson B, Jorgensen HJ, Collinge DB, Finnie C (2012) Secretomics identifies Fusarium graminearum proteins involved in the interaction with barley and wheat. Mol Plant Pathol 13:445–453
Zhang L, van Kan JAL (2013) Botrytis cinerea mutants deficient in D-galacturonic acid catabolism have a perturbed virulence on Nicotiana benthamiana and Arabidopsis, but not on tomato. Mol Plant Pathol 14:19–29
Zhang L, Thiewes H, van Kan JAL (2011) The D-galacturonic acid catabolic pathway in Botrytis cinerea. Fungal Genet Biol 48:990–997
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Zhang, L., van Kan, J.A.L. (2013). 14 Pectin as a Barrier and Nutrient Source for Fungal Plant Pathogens. In: Kempken, F. (eds) Agricultural Applications. The Mycota, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36821-9_14
Download citation
DOI: https://doi.org/10.1007/978-3-642-36821-9_14
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-36820-2
Online ISBN: 978-3-642-36821-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)