Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 34, 2012, Pages 13859-13864

  Broghammer, Angelique ^a   Krusell, Lene ^a   Blaise, Mickaël ^a   Sauer, Jørgen ^a,b   Sullivan, John T ^a,c   Maolanon, Nicolai ^a,b   Vinther, Maria ^a   Lorentzen, Andrea ^d   Madsen, Esben B ^a   Jensen, Knud J ^a,b   Roepstorff, Peter ^d   Thirup, Søren ^a   Ronson, Clive W ^a,c   Thygesen, Mikkel B ^a,b   Stougaard, Jens ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Lysin motif proteins; Lysin motif receptor like kinase; Non self recognition; Plant microbe interactions; Symbiotic signalling

Indexed keywords

GLYCAN; NOD FACTOR RECEPTOR 1; NOD FACTOR RECEPTOR 5; OLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; IN VITRO STUDY; LOTUS JAPONICUS; MASS SPECTROMETRY; NICOTIANA BENTHAMIANA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; BINDING SITES; FABACEAE; KINETICS; LIGANDS; MASS SPECTROMETRY; MODELS, BIOLOGICAL; MUCOPROTEINS; OLIGOSACCHARIDES; PHOSPHORYLATION; PLANT PROTEINS; PLANTS; POLYSACCHARIDES; PROTEIN BINDING; RHIZOBIUM; SYMBIOSIS;

EID: 84865287241     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1205171109     Document Type: Article

References (42)

1. Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885-1898.
2. Ehrhardt DW, Atkinson EM, Long SR (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256:998-1000.
3. Truchet G, et al. (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670-673.
4. Radutoiu S, et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585-592.
5. Madsen EB, et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637-640.
6. Zhukov V, et al. (2008) The pea Sym37 receptor kinase gene controls infection-thread initiation and nodule development. Mol Plant Microbe Interact 21:1600-1608.
7. Arrighi JF, et al. (2006) The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265-279.
8. Limpens E, et al. (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630-633.
9. Amor BB, 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.
10. Indrasumunar A, et al. (2011) Nodulation factor receptor kinase 1α controls nodule organ number in soybean (Glycine max L. Merr). Plant J 65:39-50.
11. Indrasumunar A, et al. (2010) Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol 51:201-214.
12. Smit P, et al. (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145:183-191.
13. Felle HH, Kondorosi E, Kondorosi A, Schultze M (2000) How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. Plant Physiol 124:1373-1380.
14. 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.
15. Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19:914-923.
16. Walker SA, Viprey V, Downie JA (2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by nod factors and chitin oligomers. Proc Natl Acad Sci USA 97:13413-13418.
17. Madsen EB, et al. (2011) 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 65:404-417.
18. Klaus-Heisen D, 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.
19. Haney CH, et al. (2011) Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell 23:2774-2787.
20. Lefebvre B, et al. (2010) A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc Natl Acad Sci USA 107:2343-2348.
21. Madsen LH, et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:10-22.
22. Radutoiu S, et al. (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923-3935.
23. Bensmihen S, de Billy F, Gough C (2011) Contribution of NFP LysM domains to the recognition of Nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS ONE 6:e26114.
24. Li R, et al. (2011) Natural variation in host-specific nodulation of pea is associated with a haplotype of the SYM37 LysM-type receptor-like kinase. Mol Plant Microbe Interact 24:1396-1403.
25. Rothbauer U, et al. (2008) A versatile nanotrap for biochemical and functional studies with fluorescent fusion proteins. Mol Cell Proteomics 7:282-289.
26. Thygesen MB, Sauer J, Jensen KJ (2009) Chemoselective capture of glycans for analysis on gold nanoparticles: Carbohydrate oxime tautomers provide functional recognition by proteins. Chemistry 15:1649-1660.
27. Thygesen MB, et al. (2010) Nucleophilic catalysis of carbohydrate oxime formation by anilines. J Org Chem 75:1752-1755.
28. Lienemann M, et al. (2009) Characterization of the wheat germ agglutinin binding to self-assembled monolayers of neoglycoconjugates by AFM and SPR. Glycobiology 19:633-643.
29. Wienken CJ, Baaske P, Rothbauer U, Braun D, Duhr S (2010) Protein-binding assays in biological liquids using microscale thermophoresis. Nat Commun 1:100-107.
30. Hadian K, et al. (2011) NF-κB essential modulator (NEMO) interaction with linear and lys-63 ubiquitin chains contributes to NF-κB activation. J Biol Chem 286:26107-26117.
31. Wang X, et al. (2011) Peptide surfactants for cell-free production of functional G protein-coupled receptors. Proc Natl Acad Sci USA 108:9049-9054.
32. Mbengue M, et al. (2010) The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22:3474-3488.
33. Liu T, et al. (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336:1160-1164.
34. Lefebvre B, et al. (2012) Role of N-glycosylation sites and CXC motifs in trafficking of Medicago trunculata Nod factor perception protein to the plasma membrane. J Biol Chem 287:10812-10823.
35. Lerouge P, et al. (1998) N-glycoprotein biosynthesis in plants: Recent developments and future trends. Plant Mol Biol 38:31-48.
36. Gomord V, et al. (2010) Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 8:564-587.
37. Hammond C, Braakman I, Helenius A (1994) Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Natl Acad Sci USA 91:913-917.
38. 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.
39. López-Lara IM, et al. (1995) Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol Microbiol 15:627-638.
40. Bek AS, 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.
41. Iizasa EI, Mitsutomi M, Nagano Y (2010) Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem 285:2996-3004.
42. Petutschnig EK, Jones AM, 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. J Biol Chem 285:28902-28911.