Role of N-glycosylation sites and CXC motifs in trafficking of Medicago truncatula Nod factor perception protein to plasma membrane

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 10812-10823

  Lefebvre, Benoit ^a   Klaus Heisen, Doerte ^a   Pietraszewska Bogiel, Anna ^b   Hervé, Christine ^a   Camut, Sylvie ^a   Auriac, Marie Christine ^a   Gasciolli, Virginie ^a   Nurisso, Alessandra ^c   Gadella, Theodorus W J ^b   Cullimore, Julie ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; CONTROL MECHANISM; CYS RESIDUES; DISULFIDE BRIDGE; ENDOPLASMIC RETICULUM; EXTRACELLULAR REGION; GENETIC ANALYSIS; HIGHLY SENSITIVE; KINASE ACTIVITY; LEGUME-RHIZOBIA SYMBIOSIS; MEDICAGO TRUNCATULA; MUTANT ALLELES; N-GLYCOSYLATION; N-GLYCOSYLATION SITES; NOD FACTOR; RECEPTOR-LIKE KINASE; STRUCTURAL FEATURE;

BIOACTIVITY; CELL MEMBRANES; COVALENT BONDS; ENZYMES; NITROGEN FIXATION; PROTEINS;

FACTOR ANALYSIS;

CYSTEINE; LYSINE; NOD FACTOR PERCEPTION PROTEIN; PROTEIN KINASE; RECEPTOR LIKE KINASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ALLELE; AMINO TERMINAL SEQUENCE; ARTICLE; BARREL MEDIC; CELL MEMBRANE; CONTROLLED STUDY; CXC MOTIF; DISULFIDE BOND; ENDOPLASMIC RETICULUM; GENETIC COMPLEMENTATION; NODULATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

AMINO ACID MOTIFS; BINDING SITES; CELL MEMBRANE; CONSERVED SEQUENCE; ENDOPLASMIC RETICULUM; GLYCOSYLATION; LYSINE; MEDICAGO TRUNCATULA; MODELS, MOLECULAR; PLANT PROTEINS; PLANT ROOT NODULATION; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); MEDICAGO TRUNCATULA;

EID: 84859496064     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.281634     Document Type: Article

References (55)

1. Gough, C., and Cullimore, J. (2011) Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant Microbe Interact. 24, 867-878
2. Oldroyd, G. E., and Downie, J. A. (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546 (Pubitemid 351813041)
3. Arrighi, J. F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L. C., Mirabella, R., de Carvalho-Niebel, F., Journet, E. P., Ghérardi, M., Huguet, T., Geurts, R., Dénarié, J., Rougé, P., and Gough, C. (2006) The Medicago truncatula lysin [corrected] motif receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142, 265-279 (Pubitemid 44412246)
4. Madsen, E. B., Madsen, L. H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S., Sandal, N., and Stougaard, J. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637-640 (Pubitemid 37280149)
5. Radutoiu, S., Madsen, L. H., Madsen, E. B., Felle, H. H., Umehara, Y., Grønlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., and Stougaard, J. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592 (Pubitemid 37280137)
6. Smit, P., Limpens, E., Geurts, R., Fedorova, E., Dolgikh, E., Gough, C., and Bisseling, T. (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 145, 183-191 (Pubitemid 47416492)
7. Shiu, S. H., and Bleecker, A. B. (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. U.S.A. 98, 10763-10768
8. Madsen, E. B., Antolín-Llovera, M., Grossmann, C., Ye, J., Vieweg, S., Broghammer, A., Krusell, L., Radutoiu, S., Jensen, O. N., Stougaard, J., and Parniske, M. (2011) Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signaling in cooperation with Nod factor receptor 5. Plant J. 65, 404-417
9. Castells, E., and Casacuberta, J. M. (2007) Signaling through kinase-defective domains. The prevalence of atypical receptor-like kinases in plants. J. Exp. Bot. 58, 3503-3511 (Pubitemid 350233009)
10. Klaus-Heisen, D., Nurisso, A., Pietraszewska-Bogiel, A., Mbengue, M., Camut, S., Timmers, T., Pichereaux, C., Rossignol, M., Gadella, T. W., Imberty, A., Lefebvre, B., and Cullimore, J. V. (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
11. Fliegmann, J., Uhlenbroich, S., Shinya, T., Martinez, Y., Lefebvre, B., Shibuya, N., and Bono, J. J. (2011) Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. Plant Physiol. Biochem. 49, 709-720
12. Buist, G., Steen, A., Kok, J., and Kuipers, O. P. (2008) LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68, 838-847 (Pubitemid 351581067)
13. Bensmihen, S., de Billy, F., and 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
14. Radutoiu, S., Madsen, L. H., Madsen, E. B., Jurkiewicz, A., Fukai, E., Quistgaard, E. M., Albrektsen, A. S., James, E. K., Thirup, S., and Stougaard, J. (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26, 3923-3935 (Pubitemid 47367494)
15. Mulder, L., Lefebvre, B., Cullimore, J., and 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
16. Lerouge, P., Cabanes-Macheteau, M., Rayon, C., Fischette-Lainé, A. C., Gomord, V., and Faye, L. (1998) N-Glycoprotein biosynthesis in plants. Recent developments and future trends. Plant Mol. Biol. 38, 31-48 (Pubitemid 28403765)
17. Saijo, Y. (2010) ER quality control of immune receptors and regulators in plants. Cell Microbiol. 12, 716-724
18. Pattison, R. J., and Amtmann, A. (2009) N-glycan production in the endoplasmic reticulum of plants. Trends Plant Sci. 14, 92-99
19. Gomord, V., Fitchette, A. C., Menu-Bouaouiche, L., Saint-Jore-Dupas, C., Plasson, C., Michaud, D., and Faye, L. (2010) Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol. J. 8, 564-587
20. Vitale, A., and Boston, R. S. (2008) Endoplasmic reticulum quality control and the unfolded protein response. Insights from plants. Traffic 9, 1581-1588
21. Kremers, G. J., Goedhart, J., van Munster, E. B., and Gadella, T. W., Jr. (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochemistry 45, 6570-6580 (Pubitemid 43825357)
22. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E., and Tsien, R. Y. (2004) Improved monomeric red, orange, and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572 (Pubitemid 40039460)
23. +-ATPase to the plasma membrane is not by default and requires cytosolic structural determinants. Plant Cell 16, 1772-1789
24. Haseloff, J., Siemering, K. R., Prasher, D. C., and Hodge, S. (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. U.S.A. 94, 2122-2127 (Pubitemid 27136838)
25. Ivanchenko, M., Vejlupkova, Z., Quatrano, R. S., and Fowler, J. E. (2000) Maize ROP7 GTPase contains a unique, CaaX box-independent plasma membrane targeting signal. Plant J. 24, 79-90
26. Klarenbeek, J. B., Goedhart, J., Hink, M. A., Gadella, T. W., and Jalink, K. (2011) A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS One 6, e19170
27. Boisson-Dernier, A., Chabaud, M., Garcia, F., Bécard, G., Rosenberg, C., and Barker, D. G. (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 (Pubitemid 32464108)
28. van Bokhoven, H., Verver, J., Wellink, J., and van Kammen, A. (1993) Protoplasts transiently expressing the 200K coding sequence of cowpea mosaic virus B-RNA support replication of M-RNA. J. Gen. Virol. 74, 2233-2241 (Pubitemid 23299902)
29. Mbengue, M., Camut, S., de Carvalho-Niebel, F., Deslandes, L., Froidure, S., Klaus-Heisen, D., Moreau, S., Rivas, S., Timmers, T., Hervé, C., Cullimore, J., and Lefebvre, B. (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
30. Vitha, S., Baluska, F., Mews, M., and Volkmann, D. (1997) Immunofluorescence detection of F-actin on low melting point wax sections from plant tissues. J. Histochem. Cytochem. 45, 89-95 (Pubitemid 27045369)
31. Timmers, A. C., Auriac, M. C., and Truchet, G. (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126, 3617-3628 (Pubitemid 29419518)
32. Moreau, S., Verdenaud, M., Ott, T., Letort, S., de Billy, F., Niebel, A., Gouzy, J., de Carvalho-Niebel, F., and Gamas, P. (2011) Transcription reprogramming during root nodule development in Medicago truncatula. PLoS One 6, e16463
33. Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., and Cheatham, T. E. (1995) Comp. Phys. Commun. 91, 1-41
34. Powell, M. J. D. (1964) An efficient method for finding the minimum of a function of saved variables without calculating derivatives. Comput. J. 7, 55-162
35. Waldherr-Teschner, M., Goetze, T., Heiden, W., Knoblauch, M., Vollhardt, H., and Brickmann, J. (1992) Advances in Scientific Visualization, pp. 58-67, Springer, Heidelberg
36. Häweker, H., Rips, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., Robatzek, S., and von Schaewen, A. (2010) Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285, 4629-4636
37. Gómez-Gómez, L., Bauer, Z., and Boller, T. (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13, 1155-1163 (Pubitemid 32480648)
38. Navarro-Gochicoa, M. T., Camut, S., Timmers, A. C., Niebel, A., Herve, C., Boutet, E., Bono, J. J., Imberty, A., and Cullimore, J. V. (2003) Characterization of four lectin-like receptor kinases expressed in roots of Medicago truncatula. Structure, location, regulation of expression, and potential role in the symbiosis with Sinorhizobium meliloti. Plant Physiol. 133, 1893-1910 (Pubitemid 38047318)
39. Boudeau, J., Miranda-Saavedra, D., Barton, G. J., and Alessi, D. R. (2006) Emerging roles of pseudokinases. Trends Cell Biol. 16, 443-452 (Pubitemid 44293399)
40. Kannan, N., and Neuwald, A. F. (2005) Did protein kinase regulatory mechanisms evolve through elaboration of a simple structural component? J. Mol. Biol. 351, 956-972 (Pubitemid 41133444)
41. Li, J., Zhao-Hui, C., Batoux, M., Nekrasov, V., Roux, M., Chinchilla, D., Zipfel, C., and Jones, J. D. (2009) Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl. Acad. Sci. U.S.A. 106, 15973-15978
42. Lu, X., Tintor, N., Mentzel, T., Kombrink, E., Boller, T., Robatzek, S., Schulze-Lefert, P., and Saijo, Y. (2009) Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl. Acad. Sci. U.S.A. 106, 22522-22527
43. Nekrasov, V., Li, J., Batoux, M., Roux, M., Chu, Z. H., Lacombe, S., Rougon, A., Bittel, P., Kiss-Papp, M., Chinchilla, D., van Esse, H. P., Jorda, L., Schwessinger, B., Nicaise, V., Thomma, B. P., Molina, A., Jones, J. D., and Zipfel, C. (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28, 3428-3438
44. Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K., Häweker, H., Dong, X., Robatzek, S., and Schulze-Lefert, P. (2009) Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28, 3439-3449
45. van der Hoorn, R. A., Wulff, B. B., Rivas, S., Durrant, M. C., van der Ploeg, A., de Wit, P. J., and Jones, J. D. (2005) Structure-function analysis of cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17, 1000-1015 (Pubitemid 43138236)
46. Hong, Z., Jin, H., Tzfira, T., and Li, J. (2008) Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20, 3418-3429
47. Song, X., Guo, P., Li, C., and Liu, C. M. (2010) The cysteine pairs in CLV2 are not necessary for sensing the CLV3 peptide in shoot and root meristems. J. Integr. Plant Biol. 52, 774-781
48. José-Estanyol, M., Gomis-Rüth, F. X., and Puigdomènech, P. (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol. Biochem. 42, 355-365
49. Zhu, Q., Liang, S., Martin, L., Gasparini, S., Ménez, A., and Vita, C. (2002) Role of disulfide bonds in folding and activity of leiurotoxin I. Just two disulfides suffice. Biochemistry 41, 11488-11494
50. Joseph, P. R., Sarmiento, J. M., Mishra, A. K., Das, S. T., Garofalo, R. P., Navarro, J., and Rajarathnam, K. (2010) Probing the role of CXC motif in chemokine CXCL8 for high affinity binding and activation of CXCR1 and CXCR2 receptors. J. Biol. Chem. 285, 29262-29269
51. Derewenda, U., Boczek, T., Gorres, K. L., Yu, M., Hung, L. W., Cooper, D., Joachimiak, A., Raines, R. T., and Derewenda, Z. S. (2009) Structure and function of Bacillus subtilis YphP, a prokaryotic disulfide isomerase with a CXC catalytic motif. Biochemistry 48, 8664-8671
52. Woycechowsky, K. J., and Raines, R. T. (2003) The CXC motif. A functional mimic of protein-disulfide isomerase. Biochemistry 42, 5387-5394
53. Cacciapuoti, G., Peluso, I., Fuccio, F., and Porcelli, M. (2009) Purine nucleoside phosphorylases from hyperthermophilic Archaea require a CXC motif for stability and folding. FEBS J. 276, 5799-5805
54. Ohnuma, T., Onaga, S., Murata, K., Taira, T., and 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
55. Petutschnig, E. K., Jones, A. M., Serazetdinova, L., Lipka, U., and 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