Plant LysM proteins: Modules mediating symbiosis and immunity

Trends in Plant Science

Volumn 17, Issue 8, 2012, Pages 495-502

  Gust, Andrea A ^a   Willmann, Roland ^a   Desaki, Yoshitake ^a   Grabherr, Heini M ^a   Nürnberger, Thorsten ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; CERK1 PROTEIN, ARABIDOPSIS; LIGAND; N ACETYLGLUCOSAMINE; POLYSACCHARIDE; PROTEIN SERINE THREONINE KINASE;

ARABIDOPSIS; EVOLUTION; FUNGUS; GROWTH, DEVELOPMENT AND AGING; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; PLANT IMMUNITY; PROTEIN MOTIF; REVIEW; RHIZOBIACEAE; SYMBIOSIS;

ACETYLGLUCOSAMINE; AMINO ACID MOTIFS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL EVOLUTION; FUNGI; IMMUNE EVASION; LIGANDS; PLANT DISEASES; PLANT IMMUNITY; POLYSACCHARIDES; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RHIZOBIACEAE; SYMBIOSIS;

BACTERIA (MICROORGANISMS);

EID: 84864385295     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2012.04.003     Document Type: Review

References (94)

1. Mendes R., et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 2011, 332:1097-1100.
2. Oldroyd G.E., Robatzek S. The broad spectrum of plant associations with other organisms. Curr. Opin. Plant Biol. 2011, 14:347-350.
3. Spoel S.H., Dong X. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 2012, 12:89-100.
4. Chisholm S.T., et al. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
5. Dangl J.L., Jones J.D. Plant pathogens and integrated defence responses to infection. Nature 2001, 411:826-833.
6. Gough C., Cullimore J. Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant Microbe Interact. 2011, 24:867-878.
7. Zipfel C. Pattern-recognition receptors in plant innate immunity. Curr. Opin. Immunol. 2008, 20:10-16.
8. Boller T., Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009, 60:379-406.
9. Kaku H., et al. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11086-11091.
10. Kishimoto K., et al. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J. 2010, 64:343-354.
11. Miya A., et al. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:19613-19618.
12. Shimizu T., et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 2010, 64:204-214.
13. Wan J., et al. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 2008, 20:471-481.
14. Willmann R., et al. Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:19824-19829.
15. Limpens E., et al. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 2003, 302:630-633.
16. Madsen E.B., et al. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 2003, 425:637-640.
17. Op den Camp R., et al. LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 2011, 331:909-912.
18. Radutoiu S., et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003, 425:585-592.
19. Bateman A., Bycroft M. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 2000, 299:1113-1119.
20. Zhang X.C., et al. Evolutionary genomics of LysM genes in land plants. BMC Evol. Biol. 2009, 9:183.
21. Buist G., et al. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 2008, 68:838-847.
22. Bielnicki J., et al. B-subtilis ykuD protein at 2.0 A resolution: insights into the structure and function of a novel, ubiquitous family of bacterial enzymes. Proteins 2006, 62:144-151.
23. Mulder L., 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, 16:801-809.
24. Buist G., et al. Molecular cloning and nucleotide sequence of the gene encoding the major peptidoglycan hydrolase of Lactococcus lactis, a muramidase needed for cell separation. J. Bacteriol. 1995, 177:1554-1563.
25. Ohnuma T., et al. LysM domains from Pteris ryukyuensis chitinase-A: a stability study and characterization of the chitin-binding site. J. Biol. Chem. 2008, 283:5178-5187.
26. Glauner B., et al. The composition of the murein of Escherichia coli. J. Biol. Chem. 1988, 263:10088-10095.
27. Schleifer K.H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 1972, 36:407-477.
28. Ponting C.P., et al. Eukaryotic signalling domain homologues in archaea and bacteria. Ancient ancestry and horizontal gene transfer. J. Mol. Biol. 1999, 289:729-745.
29. Erbs G., et al. Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem. Biol. 2008, 15:438-448.
30. Gust A.A., et al. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 2007, 282:32338-32348.
31. Hamel L.P., Beaudoin N. Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant-microbe interactions. Planta 2010, 232:787-806.
32. Kombrink A., et al. The role of chitin detection in plant-pathogen interactions. Microbes Infect. 2011, 13:1168-1176.
33. Shibuya N., Minami E. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant P 2001, 59:223-233.
34. Geurts R., et al. Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 2005, 8:346-352.
35. Arrighi J.F., et al. The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 2006, 142:265-279.
36. Fliegmann J., et al. Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. Plant Physiol. Biochem. 2011, 49:709-720.
37. Lohmann G.V., et al. Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant Microbe Interact. 2010, 23:510-521.
38. Shiu S.H., et al. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004, 16:1220-1234.
39. Medzhitov R., Janeway C.A. Innate immunity: the virtues of a nonclonal system of recognition. Cell 1997, 91:295-298.
40. Nürnberger T., et al. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 2004, 198:249-266.
41. Iriti M., Faoro F. Chitosan as a MAMP, searching for a PRR. Plant Signal. Behav. 2009, 4:66-68.
42. Felix G., et al. 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, 4:307-316.
43. Ren Y.Y., West C.A. Elicitation of diterpene biosynthesis in rice (Oryza sativa L.) by chitin. Plant Physiol. 1992, 99:1169-1178.
44. Baureithel K., et al. Specific, high affinity binding of chitin fragments to tomato cells and membranes. Competitive inhibition of binding by derivatives of chitooligosaccharides and a Nod factor of Rhizobium. J. Biol. Chem. 1994, 269:17931-17938.
45. Day R.B., et al. Binding site for chitin oligosaccharides in the soybean plasma membrane. Plant Physiol. 2001, 126:1162-1173.
46. Shibuya N., et al. Localization and binding characteristics of a high-affinity binding site for N-acetylchitooligosaccharide elicitor in the plasma membrane from suspension-cultured rice cells suggest a role as a receptor for the elicitor signal at the cell surface. Plant Cell Physiol. 1996, 37:894-898.
47. Shibuya N., 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, 329:75-78.
48. Petutschnig E.K., et al. The lysin motif receptor-like kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 2010, 285:28902-28911.
49. Iizasa E., et al. Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J. Biol. Chem. 2010, 285:2996-3004.
50. Felix G., Boller T. Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 2003, 278:6201-6208.
51. Millet Y.A., et al. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 2010, 22:973-990.
52. Nguyen H.P., et al. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol. Plant Microbe Interact. 2010, 23:991-999.
53. Conrath U., et al. Priming: getting ready for battle. Mol. Plant Microbe Interact. 2006, 19:1062-1071.
54. Gimenez-Ibanez S., et al. AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 2009, 19:423-429.
55. Bonfante P., Genre A. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 2010, 1:48.
56. Ferguson B.J., et al. Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 2010, 52:61-76.
57. Oldroyd G.E., Downie J.A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 2008, 59:519-546.
58. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 2008, 6:763-775.
59. Smith S.E., Smith F.A. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 2011, 62:227-250.
60. Day D.A., et al. Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules. Cell. Mol. Life Sci. 2001, 58:61-71.
61. D'Haeze W., Holsters M. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 2002, 12:79R-105R.
62. Long S.R. Rhizobium symbiosis: nod factors in perspective. Plant Cell 1996, 8:1885-1898.
63. Perret X., et al. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 2000, 64:180-201.
64. Goedhart J., et al. Identical accumulation and immobilization of sulfated and nonsulfated Nod factors in host and nonhost root hair cell walls. Mol. Plant Microbe Interact. 2003, 16:884-892.
65. Parniske M., Downie J.A. Plant biology: locks, keys and symbioses. Nature 2003, 425:569-570.
66. Bensmihen S., et al. Contribution of NFP LysM domains to the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS ONE 2011, 6:e26114.
67. Radutoiu S., et al. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 2007, 26:3923-3935.
68. Madsen E.B., et al. Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 2011, 65:404-417.
69. Amor B.B., et al. The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J. 2003, 34:495-506.
70. Smit P., et al. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 2007, 145:183-191.
71. Zhukov V., et al. The pea Sym37 receptor kinase gene controls infection-thread initiation and nodule development. Mol. Plant Microbe Interact. 2008, 21:1600-1608.
72. Maillet F., et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469:58-63.
73. Ercolin F., Reinhardt D. Successful joint ventures of plants: arbuscular mycorrhiza and beyond. Trends Plant Sci. 2011, 16:356-362.
74. Streng A., et al. Evolutionary origin of rhizobium Nod factor signaling. Plant Signal. Behav. 2011, 6:1510-1514.
75. Gomez S.K., et al. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. 2009, 9:10.
76. Jones J.D., Dangl J.L. The plant immune system. Nature 2006, 444:323-329.
77. Segonzac C., Zipfel C. Activation of plant pattern-recognition receptors by bacteria. Curr. Opin. Microbiol. 2011, 14:54-61.
78. Block A., Alfano J.R. Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys?. Curr. Opin. Microbiol. 2011, 14:39-46.
79. Stergiopoulos I., de Wit P.J. Fungal effector proteins. Annu. Rev. Phytopathol. 2009, 47:233-263.
80. Tyler B.M. Entering and breaking: virulence effector proteins of oomycete plant pathogens. Cell. Microbiol. 2009, 11:13-20.
81. Göhre V., et al. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 2008, 18:1824-1832.
82. Bolton M.D., et al. The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 2008, 69:119-136.
83. de Jonge R., Thomma B.P. Fungal LysM effectors: extinguishers of host immunity?. Trends Microbiol. 2009, 17:151-157.
84. de Jonge R., et al. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 2010, 329:953-955.
85. Marshall R., 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, 156:756-769.
86. Mentlak T.A., et al. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 2012, 24:322-335.
87. Cárdenas L., et al. Fast, transient and specific intracellular ROS changes in living root hair cells responding to Nod factors (NFs). Plant J. 2008, 56:802-813.
88. Ramu S.K., et al. Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Mol. Plant Microbe Interact. 2002, 15:522-528.
89. Felle H.H., et al. How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. Plant Physiol. 2000, 124:1373-1380.
90. Nakagawa T., et al. From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant J. 2011, 65:169-180.
91. Zhang B., et al. Characterization of early, chitin-induced gene expression in Arabidopsis. Mol. Plant Microbe Interact. 2002, 15:963-970.
92. Stacey G., Shibuya N. Chitin recognition in rice and legumes. Plant Soil 1997, 194:161-169.
93. Zhu H., et al. Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. Genetics 2006, 172:2491-2499.
94. Zhang X.C., et al. Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol. 2007, 144:623-636.