GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatulaw

Plant Cell

Volumn 21, Issue 2, 2009, Pages 545-557

  Hirsch, Sibylle ^a   Kim, Jiyoung ^a   Muñoz, Alfonso ^a,b   Heckmann, Anne B ^a,c   Downie, J Allan ^a   Oldroyd, Giles E D ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

MEDICAGO; MEDICAGO TRUNCATULA; RHIZOBIACEAE;

EID: 64749101372     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.064501     Document Type: Article

References (46)

1. Andriankaja, A., Boisson-Dernier, A., Frances, L., Sauviac, L., Jauneau, A., Barker, D.G., and de Carvalho-Niebel, F. (2007). AP2-ERF transcription factors mediate nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19: 2866-2885.
2. Ane, J.M., et al. (2004). Medicago truncatula DM11 required for bacterial and fungal symbioses in legumes. Science 303: 1364-1367.
3. Boisson-Dernier, A., Andriankaja, A., Chabaud, M., Niebel, A., Journet, E.P., Barker, D.G., and de Carvalho-Niebel, F. (2005). MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. Mol. Plant Microbe Interact. 18: 1269-1276.
4. Boisson-Dernier, A., Chabaud, M., Garcia, F., Becard, G., Rosenberg, C., and Barker, D.G. (2001). Agrobacterium rhizogenestransformed roots of Medicago truncatula for the study of nitrogenfixing and endomycorrhizal symbiotic associations. Mol. Plant Microbe Interact. 14: 695-700.
5. Bolle, C. (2004). The role of GRAS proteins in plant signal transduction and development. Planta 218: 683-692.
6. Catoira, R., Galera, C., de Billy, F., Penmetsa, R.V., Journet, E.P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., and Denarie, J. (2000). Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12: 1647-1665.
7. 2+ spiking and specific ENOD gene expression. Plant Physiol. 136: 3582-3593.
8. Cui, H., Levesque, M.P., Vernoux, T., Jung, J.W., Paquette, A.J., Gallagher, K.L., Wang, J.Y., Blilou, I., Scheres, B., and Benfey, P.N. (2007). An evolutionarly conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316: 421-425.
9. Delaney, K.J., Xu, R., Zhang, J., Li, Q.Q., Yun, K.Y., Falcone, D.L., and Hunt, A.G. (2006). Calmodulin interacts with and regulates the RNA-binding activity of an Arabidopsis polyadenylation factor subunit. Plant Physiol. 140: 1507-1521.
10. de Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M.A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
11. Denarie, J., Debelle, F., and Prome, J.C. (1996). Rhizobium lipochitooligosaccharide nodulation factors: Signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65: 503-535.
12. Downie, J.A., and Walker, S.A. (1999). Plant responses to nodulation factors. Curr. Opin. Plant Biol. 2: 483-489.
13. Ehrhardt, D.W., Wais, R., Long, S.R. (1996). Calcium spiking in plant root hairs responding to rhizobium nodulation signals. Cell. 85: 673-681.
14. Feng, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479.
15. Gietz, R.D., and Woods, R.A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350: 87-96.
16. Gleason, C., Chaudhuri, S., Yang, T.B., Munoz, A., Poovaiah, B.W., and Oldroyd, G.E.D. (2006). Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441: 1149-1152.
17. Heckmann, A.B., Lombardo, F., Miwa, H., Perry, J.A., Bunnewell, S., Parniske, M., Wang, T.L., and Downie, J.A. (2006). Lotus japonicus nodulation requires two GRAS-domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol. 142: 1739-1750.
18. Imaizumi-Anraku, H., et al. (2005). Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433: 527-531.
19. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
20. Journet, E.P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., Arnould, C., Morandi, D., Barker, D.G., and Gianinazzi- Pearson, V. (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.
21. Kalo, P., et al. (2005). Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786-1789.
22. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl. Acad. Sci. USA 103: 359-364.
23. Kim, J., and Kim, H.Y. (2006). Functional analysis of a calcium-binding transcription factor involved in plant salt stress signaling. FEBS Lett. 580: 5251-5256.
24. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
25. Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., and Geurts, R. (2003). LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630-633.
26. 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.
27. Marsh, J.F., Rakocevic, A., Mitra, R.M., Brocard, L., Sun, J., Eschstruth, A., Long, S.R., Schultze, M., Ratet, P., and Oldroyd, G.E. (2007). Medicago truncatula NIN is essential for rhizobiumindependent nodule organogenesis induced by autoactive CCaMK. Plant Physiol. 144: 324-335.
28. Middleton, P.H., et al. (2007). An ERF transcription factor in Medicago truncatula that is essential for nod factor signal transduction. Plant Cell 19: 1221-1234.
29. 2+/ calmodulindependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. USA 101: 4701-4705.
30. Miwa, H., Sun, J., Oldroyd, G.E., and Downie, J.A. (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.
31. Morohashi, K., Minami, M., Takase, H., Hotta, Y., and Hiratsuka, K. (2003). Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J. Biol. Chem. 278: 20865-20873.
32. Murakami, Y., Miwa, H., Imaizumi-Anraku, H., Kouchi, H., Downie, J.A., Kawaguchi, M., and Kawasaki, S. (2006). Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation. DNA Res. 13: 255-265.
33. Oldroyd, G.E., and Downie, J.A. (2006). Nuclear calcium changes at the core of symbiosis signalling. Curr. Opin. Plant Biol. 9: 351-357.
34. Oldroyd, G.E.D., and Downie, J.A. (2004). Calcium, kinases and nodulation signalling in legumes. Nat. Rev. Mol. Cell Biol. 5: 566-576.
35. Oldroyd, G.E.D., and Long, S.R. (2003). Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiol. 131: 1027-1032.
36. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, 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.
37. Riely, B.K., Lougnon, G., Ane, J.M., and Cook, D.R. (2007). The symbiotic ion channel homolog DM11 is localized in the nuclear membrane of Medicago truncatula roots. Plant J. 49: 208-216.
38. Saito, K., et al. (2007). NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19: 610-624.
39. Schauser, L., Roussis, A., Stiller, J., and Stougaard, J. (1999). A plant regulator controlling development of symbiotic root nodules. Nature 402: 191-195.
40. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T., and Geurts, R. (2005). NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791.
41. 2+3p/calmodulindependent kinase leads to spontaneous nodule development. Nature 441: 1153-1156.
42. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
43. Wais, R.J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R.V., Cook, D., Gough, C, Denarie, J., and Long, S.R. (2000). Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc. Natl. Acad. Sci. USA 97: 13407-13412.
44. Walker, S.A., Viprey, V., and Downie, J.A. (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.
45. Wilson, D., Sheng, G., Lecuit, T., Dostatni, N., and Desplan, C. (1993). Cooperative dimerization of paired class homeo domains on DNA. Genes Dev. 7: 2120-2134.
46. Witte, C.P., Noel, L.D., Gielbert, J., Parker, J.E., and Romeis, T. (2004). Rapid one-step protein purification from plant material using the eight-amino acid Strepll epitope. Plant Mol. Biol. 55: 135-147.