The battle for chitin recognition in plant-microbe interactions

FEMS Microbiology Reviews

Volumn 39, Issue 2, 2015, Pages 171-183

  Sánchez Vallet, Andrea ^a,b   Mesters, Jeroen R ^c   Thomma, Bart P H J ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Effector; LysM; MAMP; Microbe associated molecular pattern; Mutualist; PAMP; Pathogen; Symbiont

Indexed keywords

CHITIN; ELONGATION FACTOR TU; FLAGELLIN; PATTERN RECOGNITION RECEPTOR; PEPTIDOGLYCAN;

BINDING AFFINITY; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; FUNGAL CELL WALL; LIPID HYDROLYSIS; NONHUMAN; PERCEPTION; PLANT FUNGUS INTERACTION; PLANT IMMUNITY; REVIEW; FUNGUS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PLANT;

CHITIN; FUNGI; HOST-PATHOGEN INTERACTIONS; PLANTS;

EID: 84928210945     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuu003     Document Type: Review

References (134)

1. Aboitiz N, Vila-Perelló M, Groves P, et al., NMR and modeling studies of protein-carbohydrate interactions: synthesis, three-dimensional structure, and recognition properties of a minimum hevein domain with binding affinity for chitooligosaccharides. Chembiochem 2004;5:1245-55.
2. Akamatsu A, Wong HL, Fujiwara M, et al., An OsCEBiP/OsCERK1-OsRacGEF1-OsRac1 module is an essential early component of chitin-induced rice immunity. Cell Host Microbe 2013;13:465-76.
3. Antolín-Llovera M, Ried MK, Binder A, et al., Receptor kinase signaling pathways in plant-microbe interactions. Annu Rev Phytopathol 2012;50:451-73.
4. Ao Y, Li Z, Feng D, et al., OsCERK1 and OsRLCK176 play important roles in peptidoglycan and chitin signaling in rice innate immunity. Plant J 2014, doi:10.1111/tpj.12710.
5. Balestrini R, Bonfante P. Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 2014;5:237.
6. Bateman A, Bycroft M. The structure of a LysM domain from E. coli membrane-bound lyticmurein transglycosylase D (MltD). J Mol Biol 2000;299:1113-9.
7. Baureithel K, Felix G, Boller T. Specific, high affinity binding of chitin fragments to tomato cells and membranes. J Biol Chem 1994;269:17931-8.
8. Beauvais A, Bozza S, Kniemeyer O, et al., Deletion of the a-(1,3)-glucan synthase genes induces a restructuring of the conidial cell wall responsible for the avirulence of Aspergillus fumigatus. PLoS Pathog 2013;9:e1003716.
9. Berman HM, Westbrook J, Feng Z, et al., The Protein Data Bank. Nucleic Acids Res 2000;28:235-42.
10. Bishop JG, Dean AM, Mitchell-Olds T. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. P Natl Acad Sci USA 1999;79:5322-7.
11. Blair DE, Hekmat O, Schüttelkopf AW, et al., Structure and mechanism of chitin deacetylase from the fungal pathogen Colletotrichum lindemuthianum. Biochemistry 2006;45:9416-26.
12. Blair DE, Schüttelkopf AW, MacRae JI, et al., Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. P Natl Acad Sci USA 2005;102:15429-34.
13. Bolton MD, van Esse HP, Vossen JH, et al., The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 2008;69:119-36.
14. Borgia PT, Iartchouk N, Riggle PJ, et al., The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. Fungal Genet Biol 1996;20:193-203.
15. Bracker CE, Ruiz-Herrera J, Bartnicki-Garcia S. Structure and transformation of chitin synthetase particles (chitosomes) during microfibril synthesis in vitro. P Natl Acad Sci USA 1976;73:4570-4.
16. Broghammer A, Krusell L, Blaise M, et al., Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. P Natl Acad Sci USA 2012;109:13859-64.
17. Brunke S, Seider K, Fischer D, et al., One small step for a yeastmicroevolution with macrophages renders Candida glabrata hypervirulent due to a single point mutation. PLoS Pathog 2014;10:e1004478.
18. Cabib E, Roh DH, Schmidt M, et al., Morphogenesis paradigms of cell growth and the yeast cell wall and septum. J Biol Chem 2001;276:19679-82.
19. Cao Y, Liang Y, Tanaka K, et al., The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitininduced complex with related lomase CERK1. eLife 2014;23:3.
20. Chen XL, Shi T, Yang J, et al., N-glycosylation of effector proteins by an a-1,3-mannosyltransferase is required for the rice blast fungus to evade host innate immunity. Plant Cell 2014;26:1360-76.
21. Chigira Y, Abe K, Gomi K, et al., chs Z, a gene for a novel class of chitin synthase from Aspergillus oryzae. Curr Genet 2002;41:261-7.
22. Choquer M, Boccara M, Goncalves IR, et al., Survey of the Botrytis cinerea chitin synthase multigenic family through the analysis of six euascomycetes genomes. Eur J Biochem 2004;271:2153-64.
23. Dénarié J, Debellé F, Promé JC. Rhizobium lipochitooligosaccharide nodulation factors: signalingmolecules mediating recognition and morphogenesis. Annu Rev Biochem 1996;65:503-35.
24. El Gueddari NE, Rauchhaus U, Moerschbacher BM, et al., Developmentally regulated conversion of surface-exposed chitin to chitosan in cell walls of plant pathogenic fungi. New Phytol 2002;156:103-12.
25. Faulkner C, Petutschnig E, Benitez-Alfonso Y, et al., LYM2-dependent chitin perception limits molecular flux via plasmodesmata. P Natl Acad Sci USA 2013;110:9166-70.
26. Felix G, Regenass M, Boller T. Specific perception of subnanomolar concentrations of chitin fragments by tomato cells: induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J 1993;4:307-16.
27. Free SJ. Fungal cellwall organization and biosynthesis. Adv Genet 2013;81:33-82.
28. Fujikawa T, Kuga Y, Yano S, et al., Dynamics of cell wall components of Magnaporthe grisea during infectious structure development. Mol Microbiol 2009;73:553-70.
29. Fujikawa T, Sakaguchi A, Nishizawa Y, et al., Surface a-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog 2012;8:e1002882.
30. Fukuda K, Yamada K, Deoka K, et al., Class III chitin synthase ChsB of Aspergillus nidulans localizes at the sites of polarized cell wall synthesis and is required for conidial development. Eukaryot Cell 2009;8:945-56.
31. Genre A, Chabaud M, Balzergue C, et al., Short-chain chitin oligomers fromarbuscularmycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 2013;198:190-202.
32. Gimenez-Ibanez S, Hann DR, Ntoukakis V, et al., AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 2009;19:423-9.
33. Gimenez-Ibanez S, Ntoukakis V, Rathjen JP. The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal Behav 2009;4:539-41.
34. Gómez-Gómez L, Bauer Z, Boller T. Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 2001;13:1155-63.
35. Gow NA, Hube B. Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 2012;15:406-12.
36. Güimil S, Chang HS, Zhu T, et al., Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. P Natl Acad Sci USA 2005;102:8066-70.
37. Hara M, Sugimoto H, Uemura M, et al., Involvement of Gln679, in addition to Trp687, in chitin-binding activity of the chitinbinding domain of chitinase A1 from Bacillus circulans WL-12. J Biochem 2013;154:185-93.
38. Hayafune M, Berisio R, Marchetti R, et al., Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. P Natl Acad Sci USA 2014;111:E404-13.
39. Ichinomiya M, Yamada E, Yamashita S, et al., Class I and class II chitin synthases are involved in septum formation in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 2005;4:1125-36.
40. Iizasa E, Mitsutomi M, Nagano Y. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem 2010;285:2996-3004.
41. Ikegami T, Okada T, Hashimoto M, et al., Solution structure of the chitin-binding domain of Bacillus circulans WL-12 chitinase A1. J Biol Chem 2000;275:13654-61.
42. Iriti M, Faoro F. Chitosan as a MAMP, searching for a PRR. Plant Signal Behav 2009;4:66-8.
43. Jacobs S, Zechmann B, Molitor A, et al., Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 2011;156:726-40.
44. de Jonge R, Bolton MD, Thomma BP. Howfilamentous pathogens co-opt plants: the ins and outs of fungal effectors. Curr Opin Plant Biol 2011;14:400-6.
45. de Jonge R, van Esse HP, Kombrink A, et al., Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010;329:953-5.
46. Kaku H, Nishizawa Y, Ishii-Minami N, et al., Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. P Natl Acad Sci USA 2006;103:11086-91.
47. Kemen E, Kemen A, Ehlers A, et al., A novel structural effector from rust fungi is capable of fibril formation. Plant J 2013;75:767-80.
48. Kloppholz S, Kuhn H, Requena N. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Opin 2011;21:1204-9.
49. Kollár R, Petráková E, Ashwell G, et al., Architecture of the yeast cell wall. The linkage between chitin and ß(1-3)-glucan. J Biol Chem 1995;270:1170-8.
50. Kombrink A, Sánchez-Vallet A, Thomma BP. The role of chitin detection in plant-pathogen interactions. Microbes Infect 2011;13:1168-76.
51. Kombrink A, Thomma BP. LysM effectors: secreted proteins supporting fungal life. PLoS Pathog 2013;9:e1003769.
52. Kong LA, Yang J, Li GT, et al., Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog 2012;8:e1002526.
53. Kouzai Y, Mochizuki S, Nakajima K, et al., Targeted gene disruption of OsCERK1 reveals its indispensable role in chitin perception and involvement in the peptidoglycan response and immunity in rice. Mol Plant Microbe In 2014a;27:975-82.
54. Kouzai Y, Nakajima K, Hayafune M, et al., CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol Biol 2014b;84:519-28.
55. Latgé JP. Tasting the fungal cell wall. Cell Microbiol 2010;12:863-72.
56. Latgé JP, Beauvais A. Functional duality of the cell wall. Curr Opin Microbiol 2014;20:111-7.
57. Le MH, Cao Y, Zhang XC, et al., LIK1, a CERK1-interacting kinase, regulates plant immune responses in Arabidopsis. PLoS One 2014;9:e102245.
58. Leal-Morales CA, Bracker CE, Bartnicki-Garcia S. Subcellular localization, abundance and stability of chitin synthetases 1 and 2 from Saccharomyces cerevisiae. Microbiology 1994;140:2207-16.
59. Lee WS, Rudd JJ, Hammond-Kosack KE, et al., Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Mol Plant Microbe In 2014;27:236-43.
60. Lenardon MD, Munro CA, Gow NAR. Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 2010;13:416-23.
61. Levasseur A, Drula E, Lombard V, et al., Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 2013;6:41.
62. Li H, Greene LH. Sequence and structural analysis of the chitinase insertion domain reveals two conserved motifs involved in chitin-binding. PLoS One 2010;5:e8654.
63. Liang Y, Cao Y, Tanaka K, et al., Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 2013;341:1384-7.
64. Limpens E, Franken C, Smit P, et al., LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 2003;302:630-3.
65. Liu B, Li JF, Ao Y, et al., Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 2012a;24:3406-19.
66. Liu T, Liu Z, Song C, et al., Chitin-induced dimerization activates a plant immune receptor. Science 2012b;336:1160-4.
67. Liu X, Grabherr HM, Willmann R, et al., Host-induced bacterial cell wall decomposition mediates pattern-triggered immunity in Arabidopsis. eLife 2014;3:e01990.
68. Lombard V, Golaconda Ramulu H, Drula E, et al., The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2014;42:D490-5.
69. Madrid MP, Di Pietro A, Roncero MI. Class V chitin synthase determines pathogenesis in the vascular wilt fungus Fusarium oxysporum and mediates resistance to plant defence compounds. Mol Microbiol 2003;47:257-66.
70. Madsen EB, Antolin-Llovera M, Grossmann C, et al., Autophosphorylation is essential for the in vivo function of the Lotus japonicas Nod factor receptor 1 and receptor-mediated signaling in cooperation with Nod factor receptor 5. Plant J 2011;65:404-17.
71. Madsen EB, Madsen LH, Radutoiu S, et al., A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 2003;425:637-40.
72. Maillet F, Poinsot V, André O, et al., Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011;469:58-63.
73. Marshall R, Kombrink A, Motteram J, et al., Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 2011;156:756-69.
74. Martin-Udiroz M, Madrid MP, Roncero MI. Role of chitin synthase genes in Fusarium oxysporum. Microbiol 2004;150:3175-87.
75. Martin-Urdiroz M, Roncero MI, Gonzalez-Reyes JA, et al., ChsVb, a class VII chitin synthase involved in septation, is critical for pathogenicity in Fusarium oxysporum. Eukaryot Cell 2008;7:112-21.
76. Matsuo Y, Tanaka K, Nakagawa T, et al., Genetic analysis of chs1+ and chs2+ encoding chitin synthases from Schizosaccharomyces pombe. Biosci Biotech Bioch 2004;68:1489-99.
77. Mentlak TA, Kombrink A, Shinya T, et al., Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012;24:322-35.
78. Mesnage S, Dellarole M, Baxter NJ, et al., Molecular basis for bacterial peptidoglycan recognition by LysM domains. Nat Commun 2014;5:4269.
79. Miya A, Albert P, Shinya T, et al., CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. P Natl Acad Sci USA 2007;104:19613-8.
80. Miyata K, Kozaki T, Kouzai Y, et al., Bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol 2014;55:1864-72.
81. Moebius N, Üzüm Z, Dijksterhuis J, et al., Active invasion of bacteria into living fungal cells. eLife 2014;3:e03007.
82. Morcx S, Kunz C, Choquer M, et al., Disruption of Bcchs4, Bcchs6 or Bcchs7 chitin synthase genes in Botrytis cinerea and the essential role of class VI chitin synthase (Bcchs6). Fungal Genet Biol 2013;52:1-8.
83. Mueller AN, Ziemann S, Treitschke S, et al., Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog 2013;9:e1003177.
84. Mulder L, Lefebvre B, Cullimore J, et al., LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors. Glycobiology. 2006;16:801-9.
85. Muszkieta L, Aimanianda V, Mellado E, et al., Deciphering the role of the chitin synthase families 1 and 2 in the in vivo and in vitro growth of Aspergillus fumigatus by multiple gene targeting deletion. Cell Microbiol 2014;16:1784-805.
86. Pareja-Jaime Y, Martín-Urdíroz M, Roncero MI, et al., Chitin synthase-deficient mutant of Fusarium oxysporum elicits tomato plant defence response and protects against wildtype infection. Mol Plant Pathol 2010;11:479-93.
87. Petutschnig EK, Jones AM, Serazetdinova L, et al., The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitinbinding protein in Arabidopsis thaliana and subject to chitininduced phosphorylation. J Biol Chem 2010;285:28902-11.
88. Petutschnig EK, Stolze M, Lipka U, et al., A novel Arabidopsis CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) mutant with enhanced pathogen-induced cell death and altered receptor processing. New Phytol. 2014;204:955-67.
89. Plett JM, Daguerre Y, Wittulsky S, et al., Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. P Natl Acad Sci USA 2014;111:8299-304.
90. Rabea EI, Badawy ME, Stevens CV, et al., Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 2003;4:1457-65.
91. Radutoiu S, Madsen LH, Madsen EB, et al., Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003;425:585-92.
92. Rappleye CA, Eissenberg LG, Goldman WE. Histoplasma capsulatum a-(1,3)-glucan blocks innate immune recognition by the ß-glucan receptor. P Natl Acad Sci USA 2007;104:1366-70.
93. Ride JP, Barber MS. Purification and characterization of multiple forms of endochitinase from wheat leaves. Plant Sci 1990;71:185-97.
94. Riquelme M, Bartnicki-García S, González-Prieto JM, et al., Spitzenkorper localization and intracellular traffic of green fluorescent protein-labeled CHS-3 and CHS-6 chitin synthases in living hyphae of Neurospora crassa. Eukaryot Cell 2007;6:1853-64.
95. Roncero C. The genetic complexity of chitin synthesis in fungi. Curr Genet 2002;41:367-78.
96. Rooney HC, Van't Klooster JW, van der Hoorn RA, et al., Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 2005;308:1783-6.
97. Rovenich H, Boshoven JC, Thomma BP. Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr Opin Plant Biol 2014;20:96-103.
98. Salzer P, Bonanomi A, Beyer K, et al., Differential expression of eight chitinase genes in Medicago truncatula roots during Mycorrhiza formation, nodulation and pathogen infection. Mol Plant Microbe In 2000;13:763-77.
99. Sánchez-León E, Verdín J, Freitag M, et al., Traffic of chitin synthase 1 (CHS-1) to the Spitzenkörper and developing septa in hyphae of Neurospora crassa: actin dependence and evidence of distinct microvesicle populations. Eukaryot Cell 2011;10:683-95.
100. Sánchez-Rangel D, Sánchez-Nieto S, Plasencia J. Fumonisin B1, a toxin produced by Fusarium verticillioides, modulates maize ß-1,3-glucanase activities involved in defense response. Planta 2012;235:965-78.
101. Sánchez-Vallet A, Saleem-Batcha R, Kombrink A, et al., Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. eLife 2013;2:e00790.
102. Shibuya N, Kaku H, Kuchitsu K, et al., Identification of a novel high-affinity binding site for N-acetylchitooligosaccharide elicitor in the membrane fraction from suspension-cultured rice cells. FEBS Lett 1993;329:75-8.
103. Shimizu T, Nakano T, Takamizawa D, et al., Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 2010;64:204-14.
104. Shinya T, Motoyama N, Ikeda A, et al., Functional characterization of CEBiP and CERK1 homologs in arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol 2012;53:1696-706.
105. Sietsma JH, Beth Din A, Ziv V, et al., The localization of chitin synthase in membranous vesicles (chitosomes) in Neurospora crassa. Microbiology 1996;142:1591-6.
106. Silverman SJ, Sburlati A, Slater ML, et al., Chitin synthase 2 is essential for septum formation and cell division in Saccharomyces cerevisiae. P Natl Acad Sci USA 1988;85:4735-9.
107. Sørensen KK, Simonsen JB, Maolanon NN, et al., Chemically synthesized 58-mer LysM domain binds lipochitin oligosaccharide. Chembiochem 2014;15:2097-105.
108. Soulie MC, Perino C, Piffeteau A, et al., Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell Microbiol 2006;8:1310-21.
109. Soulie MC, Piffeteau A, Choquer M, et al., Disruption of Botrytis cinerea class I chitin synthase gene Bcchs1 results in cell wall weakening and reduced virulence. Fungal Genet Biol 2003;40:38-46.
110. Stergiopoulos I, van den Burg HA, Okmen B, et al., Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. P Natl Acad Sci USA 2010;107:7610-5.
111. Suetake T, Tsuda S, Kawabata S, et al., Chitin-binding proteins in invertebrates and plants comprise a common chitin-binding structural motif. J Biol Chem 2000;275:17929-32.
112. Thomma BP, Nürnberger T, Joosten MH. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 2011;23:4-15.
113. Tisserant E, Malbreil M, Kuo A, et al., Genome of an arbuscularmycorrhizal fungus provides insight into the oldest plant symbiosis. P Natl Acad Sci USA 2013;110:20117-22.
114. Treitschke S, Doehlemann G, Schuster M, et al., The myosin motor domain of fungal chitin synthase V is dispensable for vesicle motility but required for virulence of the maize pathogen Ustilago maydis. Plant Cell 2010;22:2476-94.
115. Vaaje-Kolstad G, Horn SJ, van Aalten DM, et al., The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 2005;280:28492-7.
116. van den Burg HA, Harrison SJ, Joosten MH, et al., Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe In 2006;19:1420-30.
117. van der Linde K, Hemetsberger C, Kastner C, et al., A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell 2012;24:1285-300.
118. Vander P, V°arum KM, Domard A, et al., Comparison of the ability of partially N-acetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol 1998;118:1353-9.
119. van Esse HP, Bolton MD, Stergiopoulos I, et al., The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe In 2007;20:1092-101.
120. van Esse HP, Van't Klooster JW, Bolton MD, et al., The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 2008;20:1948-63.
121. Walker SA, Viprey V, Downie JA. Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by nod factors and chitin oligomers. P Natl Acad Sci USA 2000;97:13413-8.
122. Wan J, Tanaka K, Zhang XC, et al., LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 2012;160:396-406.
123. Wan J, Zhang XC, Neece D, et al., A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 2008;20:471-81.
124. Wang W, Xie ZP, Staehelin C. Functional analysis of chimeric lysin motif domain receptors mediating Nod factor-induced defense signaling in Arabidopsis thaliana and chitin-induced nodulation signaling in Lotus japonicus. Plant J 2014;78:56-69.
125. Weber I, Assmann D, Thines E, et al., Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 2006;18:225-42.
126. Werner S, Sugui JA, Steinberg G, et al., A chitin synthase with a myosin-like motor domain is essential for hyphal growth, appressorium differentiation, and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol Plant Microbe In 2007;20:1555-67.
127. Willmann R, Lajunen HM, Erbs G, et al., Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. P Natl Acad Sci USA 2011;108:19824-9.
128. Wilson D, Pethica R, Zhou Y, et al., Superfamily-comparative genomics, datamining and sophisticated visualisation. Nucleic Acids Res 2009;37:D380-6.
129. Wong HL, Pinontoan R, Hayashi K, et al., Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 2007;19:4022-34.
130. Wong JE, Alsarraf HM, Kaspersen JD, et al., Cooperative binding of LysM domains determines the carbohydrate affinity of a bacterial endopeptidase protein. FEBS J 2014;281:1196-208.
131. Yamaguchi K, Yamada K, Ishikawa K, et al., A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 2013;13:347-57.
132. Yarden O, Yanofsky C. Chitin synthase 1 plays a major role in cell wall biogenesis in Neurospora crassa. Gene Dev 1991;5:2420-30.
133. Zipfel C, Kunze G, Chinchilla D, et al., Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacteriummediated transformation. Cell 2006;125:749-60.
134. Zuccaro A, Lahrmann U, Guldener U, et al., Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 2011;7:e1002290.