Contribution of NFP LysM domains to the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Bensmihen, Sandra ^a   de Billy, Françoise ^a   Gough, Clare ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE; NOD FACTOR; NOD FACTOR PERCEPTION; OLIGOSACCHARIDE; PROTEIN KINASE; SULFATE; UNCLASSIFIED DRUG; AMINO ACID; BACTERIAL PROTEIN; CELL SURFACE RECEPTOR; NITRIC OXIDE DIOXYGENASE; OXYGENASE; VEGETABLE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BARREL MEDIC; CONTROLLED STUDY; EXTRACELLULAR DOMAIN; GENE; HOST RANGE; LYSINE MOTIF DOMAIN; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEA; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RHIZOBIUM; SINORHIZOBIUM MELILOTI; SYM10 GENE; SYMBIOSIS; BACTERIAL INFECTION; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

MEDICAGO; MEDICAGO TRUNCATULA; PISUM SATIVUM; RHIZOBIUM; SINORHIZOBIUM MELILOTI;

AMINO ACIDS; BACTERIAL INFECTIONS; BACTERIAL PROTEINS; MEDICAGO TRUNCATULA; NITROGEN FIXATION; OXYGENASES; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

EID: 80555154254     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026114     Document Type: Article

References (43)

1. De Smet I, Voss U, Jurgens G, Beeckman T, (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11: 1166-1173.
2. Shiu S-H, Bleecker AB, (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proceedings of the National Academy of Sciences of the United States of America 98: 10763-10768.
3. Buist G, Steen A, Kok J, Kuipers OP, (2008) LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 68: 838-847.
4. Bateman A, Bycroft M, (2000) The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 299: 1113-1119.
5. Zhang XC, Wu X, Findley S, Wan J, Libault M, et al. (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144: 623-636.
6. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, et al. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci U S A 103: 11086-11091.
7. Ohnuma T, Onaga S, Murata K, Taira T, Katoh E, (2008) LysM domains from Pteris ryukyuensis chitinase-A: a stability study and characterization of the chitin-binding site. J Biol Chem 283: 5178-5187.
8. Lizasa Ei, Mitsutomi M, Nagano Y, (2010) Direct Binding of a Plant LysM Receptor-like Kinase, LysM RLK1/CERK1, to Chitin in Vitro. Journal of Biological Chemistry 285: 2996-3004.
9. Petutschnig EK, Jones AME, Serazetdinova L, Lipka U, Lipka V, (2010) The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 Is a Major Chitin-binding Protein in Arabidopsis thaliana and Subject to Chitin-induced Phosphorylation. Journal of Biological Chemistry 285: 28902-28911.
10. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640.
11. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, et al. (2006) The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
12. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, et al. (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. Embo J 26: 3923-3935.
13. Kinoshita T, Cano-Delgado AC, Seto H, Hiranuma S, Fujioka S, et al. (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433: 167-171.
14. Albert M, Jehle AK, Mueller K, Eisele C, Lipschis M, et al. (2010) Arabidopsis thaliana Pattern Recognition Receptors for Bacterial Elongation Factor Tu and Flagellin Can Be Combined to Form Functional Chimeric Receptors. Journal of Biological Chemistry 285: 19035-19042.
15. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585-592.
16. Dénarié J, Debellé F, Promé JC, (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535.
17. Roche P, Debellé F, Maillet F, Lerouge P, Faucher C, et al. (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67: 1131-1143.
18. Faucher C, Maillet F, Vasse J, Rosenberg C, van Brussel AA, et al. (1988) Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal. J Bacteriol 170: 5489-5499.
19. Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, et al. (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6: 1357-1374.
20. Ben Amor B, Shaw SL, Oldroyd GE, Maillet F, Penmetsa RV, et al. (2003) 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 34: 495-506.
21. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, et al. (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630-633.
22. Klaus-Heisen D, Nurisso A, Pietraszewska-Bogiel A, Mbengue M, Camut S, et al. (2011) Structure-function similarities between a plant receptor-like kinase and the human interleukin-1 receptor-associated kinase-4. J Biol Chem 286: 11202-11210.
23. Catoira R, Timmers AC, Maillet F, Galera C, Penmetsa RV, et al. (2001) The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling. Development 128: 1507-1518.
24. Mulder L, Lefebvre B, Cullimore J, Imberty A, (2006) LysM domains of Medicago truncatula NFP protein involved in Nod factor perception. Glycosylation state, molecular modeling and docking of chitooligosaccharides and Nod factors. Glycobiology 16: 801-809.
25. Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, et al. (2007) Medicago LYK3, an Entry Receptor in Rhizobial Nodulation Factor Signaling. Plant Physiol 145: 183-191.
26. Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, et al. (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125-130.
27. Cronk Q, Ojeda I, Pennington RT, (2006) Legume comparative genomics: progress in phylogenetics and phylogenomics. Curr Opin Plant Biol 9: 99-103.
28. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, et al. (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14: 737-748.
29. Charron D, Pingret JL, Chabaud M, Journet EP, Barker DG, (2004) Pharmacological evidence that multiple phospholipid signaling pathways link Rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression. Plant Physiol 136: 3582-3593.
30. Wais RJ, Keating DH, Long SR, (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129: 211-224.
31. Maillet F, Poinsot V, André O, Puech-Pages V, Haouy A, et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469: 58-63.
32. Staehelin C, Schultze M, Kondorosi Ãv, Mellor RB, Boiler T, et al. (1994) Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. The Plant Journal 5: 319-330.
33. Lohmann GV, Shimoda Y, Nielsen MW, Jorgensen FG, Grossmann C, et al. (2010) Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol Plant Microbe Interact 23: 510-521.
34. Bek AS, Sauer J, Thygesen MB, Duus JO, Petersen BO, et al. (2010) Improved characterization of nod factors and genetically based variation in LysM Receptor domains identify amino acids expendable for nod factor recognition in Lotus spp. Mol Plant Microbe Interact 23: 58-66.
35. Debellé F, Maillet F, Vasse J, Rosenberg C, de Billy F, et al. (1988) Interference between Rhizobium meliloti and Rhizobium trifolii nodulation genes: genetic basis of R. meliloti dominance. J Bacteriol 170: 5718-5727.
36. D'Haeze W, Holsters M, (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12: 79R-105R.
37. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953-955.
38. Cullimore J, Dénarié J, (2003) Plant sciences. How legumes select their sweet talking symbionts. Science 302: 575-578.
39. Oldroyd GE, Mitra RM, Wais RJ, Long SR, (2001) Evidence for structurally specific negative feedback in the Nod factor signal transduction pathway. Plant J 28: 191-199.
40. Boisson-Dernier A, Chabaud M, Garcia F, Becard G, Rosenberg C, et al. (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14: 695-700.
41. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, et al. (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
42. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, et al. (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12: 1647-1666.
43. Edwards K, Johnstone C, Thompson C, (1991) A simple and rapid method for preparation of plant genomic DNA for PCR analysis. Nucleic Acid Research 19: 1349.