Lotus japonicus cytokinin receptors work partially redundantly to mediate nodule formation

Plant Cell

Volumn 26, Issue 2, 2014, Pages 678-694

  Held, Mark ^a,b,e   Hou, Hongwei ^a   Miri, Mandana ^a,b   Huynh, Christian ^a   Ross, Loretta ^a   Hossain, Md Shakhawat ^a   Sato, Shusei ^c,f   Tabata, Satoshi ^c   Perry, Jillian ^d   Wang, Trevor L ^d   Szczyglowski, Krzysztof ^a,b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^d JOHN INNES CENTRE   (United Kingdom)

^e UNIVERSITY OF MINNESOTA   (United States)

^f TOHOKU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CYTOKININ; MESSENGER RNA; VEGETABLE PROTEIN;

ALLELE; ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECT; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LOTUS; MESORHIZOBIUM; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; MUTATION; NODULATION; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PHYLOGENY; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

ALLELES; ARABIDOPSIS; CYTOKININS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, PLANT; LOTUS; MESORHIZOBIUM; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; ORGANOGENESIS; PHYLOGENY; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; RNA, MESSENGER; ROOT NODULES, PLANT; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84897084235     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.119362     Document Type: Article

References (81)

1. Ariel, F., et al. (2012). Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell 24: 3838-3852.
2. Bauer, P., Ratet, P., Crespi, M.D., Schultze, M., and Kondorosi, A. (1996). Nod factors and cytokinins induce similar cortical cell division, amyloplast deposition and MsEnod12A expression patterns in alfalfa roots. Plant J. 10: 91-105.
3. Bek, A.S., Sauer, J., Thygesen, M.B., Duus, J.O., Petersen, B.O., Thirup, S., James, E., Jensen, K.J., Stougaard, J., and Radutoiu, S. (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.
4. Broughton, W.J., and Dilworth, M.J. (1971). Control of leghaemoglobin synthesis in snake beans. Biochem. J. 125: 1075-1080.
5. Combier, J.P., de Billy, F., Gamas, P., Niebel, A., and Rivas, S. (2008). Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. Genes Dev. 22: 1549-1559.
6. Combier, J.P., Frugier, F., de Billy, F., Boualem, A., El-Yahyaoui, F., Moreau, S., Vernié, T., Ott, T., Gamas, P., Crespi, M., and Niebel, A. (2006). MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev. 20: 3084-3088.
7. Cooper, J.B., and Long, S.R. (1994). Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6: 215-225.
8. Desbrosses, G.J., and Stougaard, J. (2011). Root nodulation: A paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 10: 348-358.
9. Doyle, J.J. (2011). Phylogenetic perspectives on the origins of nodulation. Mol. Plant Microbe Interact. 24: 1289-1295.
10. Duc, G., Trouvelot, A., Gianinazzi-Pearson, V., and Gianinazzi, S. (1989). First report of non-mycorrhizal plant mutants (Myc2) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci. 60: 215-222.
11. Ferreira, F.J., and Kieber, J.J. (2005). Cytokinin signaling. Curr. Opin. Plant Biol. 8: 518-525.
12. Frugier, F., Kosuta, S., Murray, J.D., Crespi, M., and Szczyglowski, K. (2008). Cytokinin: Secret agent of symbiosis. Trends Plant Sci. 13: 115-120.
13. Gleason, C., Chaudhuri, S., Yang, T., Muñoz, 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.
14. Gonzalez-Rizzo, S., Crespi, M., and Frugier, F. (2006). The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18: 2680-2693.
15. 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.
16. Grunewald, W., van Noorden, G., Van Isterdael, G., Beeckman, T., Gheysen, G., and Mathesius, U. (2009). Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. Plant Cell 21: 2553-2562.
17. Hayashi, T., Banba, M., Shimoda, Y., Kouchi, H., Hayashi, M., and Imaizumi-Anraku, H. (2010). A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J. 63: 141-154.
18. 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.
19. Heckmann, A.B., Sandal, N., Bek, A.S., Madsen, L.H., Jurkiewicz, A., Nielsen, M.W., Tirichine, L., and Stougaard, J. (2011). Cytokinin induction of root nodule primordia in Lotus japonicus is regulated by a mechanism operating in the root cortex. Mol. Plant Microbe Interact. 24: 1385-1395.
20. Held, M., Hossain, M.S., Yokota, K., Bonfante, P., Stougaard, J., and Szczyglowski, K. (2010). Common and not so common symbiotic entry. Trends Plant Sci. 15: 540-545.
21. Heyl, A., Riefler, M., Romanov, G.A., and Schmülling, T. (2012). Properties, functions and evolution of cytokinin receptors. Eur. J. Cell Biol. 91: 246-256.
22. Heyl, A., Wulfetange, K., Pils, B., Nielsen, N., Romanov, G.A., and Schmülling, T. (2007). Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain. BMC Evol. Biol. 7: 62-69.
23. Hirsch, A.M., Bhuvaneswari, T.V., Torrey, J.G., and Bisseling, T. (1989). Early nodulin genes are induced in alfalfa root outgrowths elicited by auxin transport inhibitors. Proc. Natl. Acad. Sci. USA 86: 1244-1248.
24. Hoagland, D.R., and Arnon, D.I. (1950). The water-culture method for growing plants without soil. Calif. Agric. Exper. Stat. Circ. 347: 1-32.
25. Horst, I., Welham, T., Kelly, S., Kaneko, T., Sato, S., Tabata, S., Parniske, M., and Wang, T.L. (2007). TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol. 144: 806-820.
26. Hossain, M.S., Liao, J., James, E.K., Sato, S., Tabata, S., Jurkiewicz, A., Madsen, L.H., Stougaard, J., Ross, L., and Szczyglowski, K. (2012). Lotus japonicus ARPC1 is required for rhizobial infection. Plant Physiol. 160: 917-928.
27. Hwang, I., Sheen, J., and Müller, B. (2012). Cytokinin signaling networks. Annu. Rev. Plant Biol. 63: 353-380.
28. Inoue, T., Higuchi, M., Hashimoto, Y., Seki, M., Kobayashi, M., Kato, T., Tabata, S., Shinozaki, K., and Kakimoto, T. (2001). Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063.
29. Kaló, P., et al. (2005). Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786-1789.
30. Karas, B., Murray, J., Gorzelak, M., Smith, A., Sato, S., Tabata, S., and Szczyglowski, K. (2005). Invasion of Lotus japonicus root hairless 1 by Mesorhizobium loti involves the nodulation factordependent induction of root hairs. Plant Physiol. 137: 1331-1344.
31. 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.
32. Kosuta, S., Held, M., Hossain, M.S., Morieri, G., Macgillivary, A., Johansen, C., Antolín-Llovera, M., Parniske, M., Oldroyd, G.E., Downie, A.J., Karas, B., and Szczyglowski, K. (2011). Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J. 67: 929-940.
33. Laloum, T., De Mita, S., Gamas, P., Baudin, M., and Niebel, A. (2013). CCAAT-box binding transcription factors in plants: Y so many? Trends Plant Sci. 18: 157-166.
34. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.C., and Dénarié, J. (1990). Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781-784.
35. Le Signor, C., Savois, V., Aubert, G., Verdier, J., Nicolas, M., Pagny, G., Moussy, F., Sanchez, M., Baker, D., Clarke, J., and Thompson, R. (2009). Optimizing TILLING populations for reverse genetics in Medicago truncatula. Plant Biotechnol. J. 7: 430-441.
36. Lévy, J., et al. (2004). A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
37. Liao, J., Singh, S., Hossain, M.S., Andersen, S.U., Ross, L., Bonetta, D., Zhou, Y., Sato, S., Tabata, S., Stougaard, J., Szczyglowski, K., and Parniske, M. (2012). Negative regulation of CCaMK is essential for symbiotic infection. Plant J. 72: 572-584.
38. Lohar, D.P., Schaff, J.E., Laskey, J.G., Kieber, J.J., Bilyeu, K.D., and Bird, D.M. (2004). Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J. 38: 203-214.
39. Lombari, P., Ercolano, E., El Alaouri, E., and Chiurazzi, M. (2005). Agrobacterium-mediated in vitro transformation. In Lotus japonicus Handbook, A.J. Marquez, ed (Dordrecht, The Netherlands: Springer), pp. 87-95.
40. 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.
41. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A. B., Bek, A.S., Ronson, C.W., James, E.K., and Stougaard, J. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1: 10.
42. Maeda, T., Wurgler-Murphy, S.M., and Saito, H. (1994). A twocomponent system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245.
43. 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 rhizobialindependent nodule organogenesis induced by autoactive calcium/ calmodulin-dependent protein kinase. Plant Physiol. 144: 324-335.
44. Mathesius, U., Charon, C., Rolfe, B.G., Kondorosi, A., and Crespi, M. (2000). Temporal and spatial order of events during the induction of cortical cell divisions in white clover by Rhizobium leguminosarum bv. trifolii inoculation or localized cytokinin addition. Mol. Plant Microbe Interact. 13: 617-628.
45. 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.
46. Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E., and Long, S.R. (2004). A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. USA 101: 4701-4705.
47. Müller, B., and Sheen, J. (2008). Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094-1097.
48. Mumberg, D., Müller, R., and Funk, M. (1995). Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119-122.
49. 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.
50. Murray, J., et al. (2006). Genetic suppressors of the Lotus japonicus har1-1 hypernodulation phenotype. Mol. Plant Microbe Interact. 19: 1082-1091.
51. Murray, J.D., Karas, B.J., Sato, S., Tabata, S., Amyot, L., and Szczyglowski, K. (2007). A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315: 101-104.
52. Nishimura, C., Ohashi, Y., Sato, S., Kato, T., Tabata, S., and Ueguchi, C. (2004). Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16: 1365-1377.
53. Op den Camp, R., Streng, A., De Mita, S., Cao, Q., Polone, E., Liu, W., Ammiraju, J.S., Kudrna, D., Wing, R., Untergasser, A., Bisseling, T., and Geurts, R. (2011). LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331: 909-912.
54. Petit, A., Stougaard, J., Kühle, A., Marcker, K.A., and Tempé, J. (1987). Transformation and regeneration of the legume Lotus corniculatus: A system for molecular studies of nitrogen fixation. Mol. Gen. Genet. 207: 245-250.
55. Plet, J., Wasson, A., Ariel, F., Le Signor, C., Baker, D., Mathesius, U., Crespi, M., and Frugier, F. (2011). MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J. 65: 622-633.
56. 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.
57. Santi, C., Bogusz, D., and Franche, C. (2013). Biological nitrogen fixation in non-legume plants. Ann. Bot. (Lond.) 111: 743-767.
58. Sayano, T., Kouchi, H., Hirota, A., and Hayashi, M. (2013). Nodule inception directly targets NF-Y subunit genes to regulate essential processes of root nodule development in Lotus japonicus. PLoS Genet. 9: e1003352.
59. Schauser, L., Roussis, A., Stiller, J., and Stougaard, J. (1999). A plant regulator controlling development of symbiotic root nodules. Nature 402: 191-195.
60. Sieberer, B.J., Chabaud, M., Fournier, J., Timmers, A.C., and Barker, D.G. (2012). A switch in Ca2+ spiking signature is concomitant with endosymbiotic microbe entry into cortical root cells of Medicago truncatula. Plant J. 69: 822-830.
61. Singh, S., and Parniske, M. (2012). Activation of calcium-and calmodulindependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr. Opin. Plant Biol. 15: 444-453.
62. Smit, P., Raedts, J., Portyanko, V., Debellé, 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.
63. Sprent, J.I., and James, E.K. (2007). Legume evolution: Where do nodules and mycorrhizas fit in? Plant Physiol. 144: 575-581.
64. Suzaki, T., Yano, K., Ito, M., Umehara, Y., Suganuma, N., and Kawaguchi, M. (2012). Positive and negative regulation of cortical cell division during root nodule development in Lotus japonicus is accompanied by auxin response. Development 139: 3997-4006.
65. Szczyglowski, K., and Amyot, L. (2003). Symbiosis, inventiveness by recruitment? Plant Physiol. 131: 935-940.
66. Szczyglowski, K., Shaw, S.R., Wopereis, J., Hamburger, D., Copeland, S., Dazzo, F.B., and de Bruijn, F.J. (1998). Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant Microbe Interact. 11: 684-697.
67. Thimann, K.V. (1936). On the physiology of the formation of nodules on legume roots. Proc. Natl. Acad. Sci. USA 22: 511-514.
68. Tirichine, L., et al. (2006a). Deregulation of a Ca2+/calmodulindependent kinase leads to spontaneous nodule development. Nature 441: 1153-1156.
69. Tirichine, L., James, E.K., Sandal, N., and Stougaard, J. (2006b). Spontaneous root-nodule formation in the model legume Lotus japonicus: A novel class of mutants nodulates in the absence of rhizobia. Mol. Plant Microbe Interact. 19: 373-382.
70. Tirichine, L., Sandal, N., Madsen, L.H., Radutoiu, S., Albrektsen, A. S., Sato, S., Asamizu, E., Tabata, S., and Stougaard, J. (2007). A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315: 104-107.
71. Truchet, G., Barker, D.G., Camut, S., de Billy, V.J., and Huguet, T. (1989). Alfalfa nodulation in the absence of Rhizobium. Mol. Gen. Genet. 219: 65-68.
72. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, J.-C., and Dénarié, J. (1991). Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670-673.
73. Ueguchi, C., Koizumi, H., Suzuki, T., and Mizuno, T. (2001). Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 42: 231-235.
74. van Spronsen, P.C., Grønlund, M., Pacios Bras, C., Spaink, H.P., and Kijne, J.W. (2001). Cell biological changes of outer cortical root cells in early determinate nodulation. Mol. Plant Microbe Interact. 14: 839-847.
75. Verdier, J., Torres-Jerez, I., Wang, M., Andriankaja, A., Allen, S.N., He, J., Tang, Y., Murray, J.D., and Udvardi, M.K. (2013). Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation. Plant J. 74: 351-362.
76. Wais, R.J., Galera, C., Oldroyd, G., Catoira, R., Penmetsa, R.V., Cook, D., Gough, C., Denarié, 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.
77. Walker, S.A., and Downie, J.A. (2000). Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal Nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Mol. Plant Microbe Interact. 13: 754-762.
78. Wopereis, J., Pajuelo, E., Dazzo, F.B., Jiang, Q., Gresshoff, P.M., De Bruijn, F.J., Stougaard, J., and Szczyglowski, K. (2000). Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J. 23: 97-114.
79. Wulfetange, K., Lomin, S.N., Romanov, G.A., Stolz, A., Heyl, A., and Schmülling, T. (2011). The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 156: 1808-1818.
80. Yamada, H., Suzuki, T., Terada, K., Takei, K., Ishikawa, K., Miwa, K., Yamashino, T., and Mizuno, T. (2001). The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42: 1017-1023.
81. Yokota, K., et al. (2009). Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21: 267-284.