Lotus japonicus E3 ligase SEVEN IN ABSENTIA4 destabilizes the symbiosis receptor-like Kinase SYMRK and negatively regulates rhizobial infection

Plant Cell

Volumn 24, Issue 4, 2012, Pages 1691-1707

  den Herder, Griet ^a,c   Yoshida, Satoko ^a,b,d   Antolín Llovera, Meritxell ^a   Ried, Martina K ^a   Parniskea, Martin ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b SAINSBURY LABORATORY   (United Kingdom)

^c Bayer Cropscience Belgium   (Belgium)

^d RIKEN Plant Science Center   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LOTUS CORNICULATUS VAR. JAPONICUS; NICOTIANA BENTHAMIANA;

EID: 84861675060     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.082248     Document Type: Article

References (97)

1. Albert, M., Jehle, A.K., Lipschis, M., Mueller, K., Zeng, Y., and Felix, G. (2010). Regulation of cell behaviour by plant receptor kinases: Pattern recognition receptors as prototypical models. Eur. J. Cell Biol. 89: 200-207.
2. Arrighi, J.F., et al. (2006). The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new noduleexpressed genes. Plant Physiol. 142: 265-279.
3. Bachmair, A., Novatchkova, M., Potuschak, T., and Eisenhaber, F. (2001). Ubiquitylation in plants: A post-genomic look at a posttranslational modification. Trends Plant Sci. 6: 463-470.
4. Bayle, V., Nussaume, L., and Bhat, R.A. (2008). Combination of novel green fluorescent protein mutant TSapphire and DsRed variant mOrange to set up a versatile in planta FRET-FLIM assay. Plant Physiol. 148: 51-60.
5. Bersoult, A., Camut, S., Perhald, A., Kereszt, A., Kiss, G.B., and Cullimore, J.V. (2005). Expression of the Medicago truncatula DM12 gene suggests roles of the symbiotic nodulation receptor kinase in nodules and during early nodule development. Mol. Plant Microbe Interact. 18: 869-876.
6. Bonfante, P., and Genre, A. (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1: 48.
7. Brewin, N.J. (2004). Plant cell wall remodelling in the rhizobiumlegume symbiosis. Crit. Rev. Plant Sci. 23: 293-316.
8. Broughton, W.J., and Dilworth, M.J. (1971). Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125: 1075-1080.
9. Capoen, W., Goormachtig, S., De Rycke, R., Schroeyers, K., and Holsters, M. (2005). SrSymRK, a plant receptor essential for symbiosome formation. Proc. Natl. Acad. Sci. USA 102: 10369-10374.
10. Carthew, R.W., and Rubin, G.M. (1990). seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 63: 561-577.
11. Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E., and Parniske, M. (2008). Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20: 3467-3479.
12. Ciechanover, A. (1998). The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 17: 7151-7160.
13. Cooper, S.E., Murawsky, C.M., Lowe, N., and Travers, A.A. (2008). Two modes of degradation of the tramtrack transcription factors by Siah homologues. J. Biol. Chem. 283: 1076-1083.
14. Cormack, B. (1997). Directed mutagenesis using the polymerase chain reaction. Curr. Protoc. Mol. Biol. 37: 8.5.1-8.5.10.
15. Della, N.G., Senior, P.V., and Bowtell, D.D. (1993). Isolation and characterisation of murine homologues of the Drosophila seven in absentia gene (sina). Development 117: 1333-1343.
16. Demchenko, K., Winzer, T., Stougaard, J., Parniske, M., and Pawlowski, K. (2004). Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol. 163: 381-392.
17. Den Herder, G., De Keyser, A., De Rycke, R., Rombauts, S., Van de Velde, W., Clemente, M.R., Verplancke, C., Mergaert, P., Kondorosi, E., Holsters, M., and Goormachtig, S. (2008). Seven in absentia proteins affect plant growth and nodulation in Medicago truncatula. Plant Physiol. 148: 369-382.
18. Den Herder, G., Van Isterdael, G., Beeckman, T., and De Smet, I. (2010). The roots of a new green revolution. Trends Plant Sci. 15: 600-607.
19. Depaux, A., Regnier-Ricard, F., Germani, A., and Varin-Blank, N. (2006). Dimerization of hSiah proteins regulates their stability. Biochem. Biophys. Res. Commun. 348: 857-863.
20. De Smet, I., Voss, U., Jürgens, G., and Beeckman, T. (2009). Receptor- like kinases shape the plant. Nat. Cell Biol. 11: 1166-1173.
21. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., and Kiss G.B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966.
22. Fox, J.D., and Waugh, D.S. (2003). Maltose-binding protein as a solubility enhancer. Methods Mol. Biol. 205: 99-117.
23. Franck, T., Krueger, R., Woitalla, D., Müller, T., Engelender, S., and Riess, O. (2006). Mutation analysis of the seven in absentia homolog 1 (SIAH1) gene in Parkinson's disease. J. Neural Transm. 113: 1903-1908.
24. Geldner, N., Hyman, D.L., Wang, X., Schumacher, K., and Chory, J. (2007). Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21: 1598-1602.
25. Gherbi, H., Markmann, K., Svistoonoff, S., Estevan, J., Autran, D., Giczey, G., Auguy, F., Péret, B., Laplaze, L., Franche, C., Parniske, M., and Bogusz, D. (2008). SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc. Natl. Acad. Sci. USA 105: 4928-4932.
26. Gibson, K.E., Kobayashi, H., and Walker, G.C. (2008). Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42: 413-441.
27. Gimenez-Ibanez, S., Hann, D.R., Ntoukakis, V., Petutschnig, E., Lipka, V., and Rathjen, J.P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol. 19: 423-429.
28. Goff, K.E., and Ramonell, K.M. (2007). The role and regulation of receptor-like kinases in plant defense. Gene Regul. Syst. Bio. 1: 167-175.
29. Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., de Torres, M., Mansfield, J.W., and Robatzek, S. (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18: 1824-1832.
30. Groothuis, T.A., Dantuma, N.P., Neefjes, J., and Salomons, F.A. (2006). Ubiquitin crosstalk connecting cellular processes. Cell Div. 1: 21.
31. Groth, M., Takeda, N., Perry, J., Uchida, H., Dräxl, S., Brachmann, A., Sato, S., Tabata, S., Kawaguchi, M., Wang, T.L., and Parniske, M. (2010). NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22: 2509-2526.
32. Hall, T. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
33. Hare, P.D., Seo, H.S., Yang, J.Y., and Chua, N.H. (2003). Modulation of sensitivity and selectivity in plant signaling by proteasomal destabilization. Curr. Opin. Plant Biol. 6: 453-462.
34. Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67: 425-479.
35. House, C.M., Möller, A., and Bowtell, D.D. (2009). Siah proteins: Novel drug targets in the Ras and hypoxia pathways. Cancer Res. 69: 8835-8838.
36. Hu, G., and Fearon, E.R. (1999). Siah-1 N-terminal RING domain is required for proteolysis function, and C-terminal sequences regulate oligomerization and binding to target proteins. Mol. Cell. Biol. 19: 724-732.
37. Ichimura, T., Yamamura, H., Sasamoto, K., Tominaga, Y., Taoka, M., Kakiuchi, K., Shinkawa, T., Takahashi, N., Shimada, S., and Isobe, T. (2005). 14-3-3 proteins modulate the expression of epithelial Na+ channels by phosphorylation-dependent interaction with Nedd4-2 ubiquitin ligase. J. Biol. Chem. 280: 13187-13194.
38. Javot, H., Pumplin, N., and Harrison, M.J. (2007). Phosphate in the arbuscular mycorrhizal symbiosis: Transport properties and regulatory roles. Plant Cell Environ. 30: 310-322.
39. Joazeiro, C.A., and Weissman, A.M. (2000). RING finger proteins: Mediators of ubiquitin ligase activity. Cell 102: 549-552.
40. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
41. Kato, T., Goto, Y., Ono, K., Hayashi, M., and Murooka, Y. (2005). Expression of a major house dust mite allergen gene from Dermatophagoides farinae in Lotus japonicus accession Miyakojima MG- 20. J. Biosci. Bioeng. 99: 165-168.
42. Kawaguchi, M., Motomura, T., Imaizumi-Anraku, H., Akao, S., and Kawasaki, S. (2001). Providing the basis for genomics in Lotus japonicus: The accessions Miyakojima and Gifu are appropriate crossing partners for genetic analyses. Mol. Genet. Genomics 266: 157-166.
43. Kerppola, T.K. (2008). Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu. Rev. Biophys. 37: 465-487.
44. Kevei, Z., et al. (2007). 3-Hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19: 3974-3989.
45. Khurana, A., Nakayama, K., Williams, S., Davis, R.J., Mustelin, T., and Ronai, Z. (2006). Regulation of the ring finger E3 ligase Siah2 by p38 MAPK. J. Biol. Chem. 281: 35316-35326.
46. Kim, H., Jeong, W., Ahn, K., Ahn, C., and Kang, S. (2004). Siah-1 interacts with the intracellular region of polycystin-1 and affects its stability via the ubiquitin-proteasome pathway. J. Am. Soc. Nephrol. 15: 2042-2049.
47. Kiss, E., Oláh, B., Kaló, P., Morales, M., Heckmann, A.B., Borbola, A., Lózsa, A., Kontár, K., Middleton, P., Downie, J.A., Oldroyd G.E., and Endre, G. (2009). LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes. Plant Physiol. 151: 1239-1249.
48. Kistner, C., Winzer, T., Pitzschke, A., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Webb, K.J., Szczyglowski, K., and Parniske, M. (2005). Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17: 2217-2229.
49. Kuppusamy, K.T., Endre, G., Prabhu, R., Penmetsa, R.V., Veereshlingam, H., Cook, D.R., Dickstein, R., and Vandenbosch, K.A. (2004). LIN, a Medicago truncatula gene required for nodule differentiation and persistence of rhizobial infections. Plant Physiol. 136: 3682-3691.
50. Kwak, S.H., and Schiefelbein, J. (2008). A feedback mechanism controlling SCRAMBLED receptor accumulation and cell-type pattern in Arabidopsis. Curr. Biol. 18: 1949-1954.
51. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
52. Lefebvre, B., et al. (2010). A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc. Natl. Acad. Sci. USA 107: 2343-2348.
53. Le Roy, C., and Wrana, J.L. (2005). Clathrin- and non-clathrinmediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 6: 112-126.
54. Li, W., Tu, D., Brunger, A.T., and Ye, Y. (2007). A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446: 333-337.
55. Limpens, E., Mirabella, R., Fedorova, E., Franken, C., Franssen, H., Bisseling, T., and Geurts, R. (2005). Formation of organelle-like N2- fixing symbiosomes in legume root nodules is controlled by DMI2. Proc. Natl. Acad. Sci. USA 102: 10375-10380.
56. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-D D C(T)) Method. Methods 25: 402-408.
57. Lovly, C.M., Yan, L., Ryan, C.E., Takada, S., and Piwnica-Worms, H. (2008). Regulation of Chk2 ubiquitination and signaling through autophosphorylation of serine 379. Mol. Cell. Biol. 28: 5874-5885.
58. Lu, D., Lin, W., Gao, X., Wu, S., Cheng, C., Avila, J., Heese, A., Devarenne, T.P., He, P., and Shan, L. (2011). Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332: 1439-1442.
59. 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.
60. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S., Ronson, C.W., Janes, E.K., and Stougaard, J. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Comm. 1: 10.
61. Maekawa, T., Kusakabe, M., Shimoda, Y., Sato, S., Tabata, S., Murooka, Y., and Hayashi, M. (2008). Polyubiquitin promoterbased binary vectors for overexpression and gene silencing in Lotus japonicus. Mol. Plant Microbe Interact. 21: 375-382.
62. Markmann, K., Giczey, G., and Parniske, M. (2008). Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol. 6: e68.
63. 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.
64. Moon, J., Parry, G., and Estelle, M. (2004). The ubiquitin-proteasome pathway and plant development. Plant Cell 16: 3181-3195.
65. 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.
66. Oldroyd, G.E., and Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59: 519-546.
67. Parniske, M. (2008). Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 6: 763-775.
68. Passmore, L.A., and Barford, D. (2004). Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochem. J. 379: 513-525.
69. Pickart, C.M. (2001). Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70: 503-533.
70. Poulsen, C., and Pødenphant, L. (2002). Expressed sequence tags from roots and nodule primordia of Lotus japonicus infected with Mesorhizobium loti. Mol. Plant Microbe Interact. 15: 376-379.
71. 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.
72. 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.
73. Raffaele, S., et al. (2009). Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21: 1541-1555.
74. Ramakers, C., Ruijter, J.M., Deprez, R.H., and Moorman, A.F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339: 62-66.
75. Robatzek, S., Chinchilla, D., and Boller, T. (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20: 537-542.
76. Samuel, M.A., Mudgil, Y., Salt, J.N., Delmas, F., Ramachandran, S., Chilelli, A., and Goring, D.R. (2008). Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol. 147: 2084-2095.
77. Santelli, E., Leone, M., Li, C., Fukushima, T., Preece, N.E., Olson, A.J., Ely, K.R., Reed, J.C., Pellecchia, M., Liddington, R.C., and Matsuzawa, S. (2005). Structural analysis of Siah1-Siah-interacting protein interactions and insights into the assembly of an E3 ligase multiprotein complex. J. Biol. Chem. 280: 34278-34287.
78. Sato, S., Nakamura, Y., Asamizu, E., Isobe, S., and Tabata, S. (2007). Genome sequencing and genome resources in model legumes. Plant Physiol. 144: 588-593.
79. Schauser, L., Roussis, A., Stiller, J., and Stougaard, J. (1999). A plant regulator controlling development of symbiotic root nodules. Nature 402: 191-195.
80. Shimomura, K., Nomura, M., Tajima, S., and Kouchi, H. (2006). LjnsRING, a novel RING finger protein, is required for symbiotic interactions between Mesorhizobium loti and Lotus japonicus. Plant Cell Physiol. 47: 1572-1581.
81. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55: 555-590.
82. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K., and Parniske, M. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962.
83. Sullivan, J.T., et al. (2002). Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 184: 3086-3095.
84. Tansengco, M.L., Hayashi, M., Kawaguchi, M., Imaizumi-Anraku, H., and Murooka, Y. (2003). crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair, trichome, and seed development in Lotus japonicus. Plant Physiol. 131: 1054-1063.
85. Timmers, A.C. (2008). The role of the plant cytoskeleton in the interaction between legumes and rhizobia. J. Microsc. 231: 247-256.
86. 2+/calmodulindependent kinase leads to spontaneous nodule development. Nature 441: 1153-1156.
87. Vinardell, J.M., Fedorova, E., Cebolla, A., Kevei, Z., Horvath, G., Kelemen, Z., Tarayre, S., Roudier, F., Mergaert, P., Kondorosi, A., and Kondorosi, E. (2003). Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15: 2093-2105.
88. Walter, M., Chaban, C., Schütze, K., Batistic, O., Weckermann, K., Näke, C., Blazevic, D., Grefen, C., Schumacher, K., Oecking, C., Harter, K., and Kudla, J. (2004). Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40: 428-438.
89. Wang, M., Jin, Y., Fu, J., Zhu, Y., Zheng, J., Hu, J., and Wang, G. (2008). Genome-wide analysis of SINA family in plants and their phylogenetic relationships. DNA Seq. 19: 206-216.
90. Wang, Y.S., Pi, L.Y., Chen, X., Chakrabarty, P.K., Jiang, J., De Leon, A.L., Liu, G.Z., Li, L., Benny, U., Oard, J., Ronald, P.C., and Song, W.Y. (2006). Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18: 3635-3646.
91. Welsch, R., Maass, D., Voegel, T., Dellapenna, D., and Beyer, P. (2007). Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol. 145: 1073-1085.
92. Xie, Q., Frugis, G., Colgan, D., and Chua, N.-H. (2000). Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14: 3024-3036.
93. Xie, Q., Guo, H.-S., Dallman, G., Fang, S., Weissman, A.M., and Chua, N.-H. (2002). SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419: 167-170.
94. Yano, K., et al. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. USA 105: 20540-20545.
95. Yoshida, S., and Parniske, M. (2005). Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J. Biol. Chem. 280: 9203-9209.
96. Zeng, L.R., Vega-Sánchez, M.E., Zhu, T., and Wang, G.L. (2006). Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions. Cell Res. 16: 413-426.
97. Zhu, H., Chen, T., Zhu, M., Fang, Q., Kang, H., Hong, Z., and Zhang, Z. (2008). A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus. Plant Physiol. 148: 337-347.