Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Long-Distance Control of Nodulation: Molecules and Models

  • Magori, Shimpei (Department of Biological Sciences, Graduate School of Science, The University of Tokyo) ;
  • Kawaguchi, Masayoshi (Department of Biological Sciences, Graduate School of Science, The University of Tokyo)
  • Received : 2008.12.21
  • Accepted : 2008.12.25
  • Published : 2009.02.28
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Abstract

Legume plants develop root nodules to recruit nitrogen-fixing bacteria called rhizobia. This symbiotic relationship allows the host plants to grow even under nitrogen limiting environment. Since nodule development is an energetically expensive process, the number of nodules should be tightly controlled by the host plants. For this purpose, legume plants utilize a long-distance signaling known as autoregulation of nodulation (AON). AON signaling in legumes has been extensively studied over decades but the underlying molecular mechanism had been largely unclear until recently. With the advent of the model legumes, L. japonicus and M. truncatula, we have been seeing a great progress including isolation of the AON-associated receptor kinase. Here, we summarize recent studies on AON and discuss an updated view of the long-distance control of nodulation.

Keywords

Acknowledgement

Supported by : Ministry of Education, Culture, Sports, Science and Technology

References

  1. Combier, J.P., Kuster, H., Journet, E.P., Hohnjec, N., Gamas, P., and Niebel, A. (2008). Evidence for the involvement in nodulation of the two small putative regulatory peptide-encoding genes MtRALFL1 and MtDVL1. Mol. Plant Microbe. Interact. 21, 1118-1127 https://doi.org/10.1094/MPMI-21-8-1118
  2. Delves, A.C., Mathews, A., Day, D.A., Carter, A.S., Carroll, B.J., and Gresshoff, P.M. (1986). Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiol. 82, 588-590 https://doi.org/10.1104/pp.82.2.588
  3. D'Haeze, W., and Holsters, M. (2002). Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12, 79-105 https://doi.org/10.1093/glycob/12.6.79R
  4. Dievart, A., Dalal, M., Tax, F.E., Lacey, A.D., Huttly, A., Li, J., and Clark, S.E. (2003). CLAVATA 1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell 15, 1198-1211 https://doi.org/10.1105/tpc.010504
  5. Geurts, R., Fedorova, E., and Bisseling, T. (2005). Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 8, 346-352 https://doi.org/10.1016/j.pbi.2005.05.013
  6. Gleason, C., Chaudhuri, S., Yang, T., Munoz, A., Poovaiah, B.W., and Oldroyd, G.E. (2006). Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441, 1149-1152 https://doi.org/10.1038/nature04812
  7. 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 https://doi.org/10.1104/pp.106.089508
  8. Kalo, P., Gleason, C., Edwards, A., Marsh, J., Mitra, R.M., Hirsch, S., Jakab, J., Sims, S., Long, S.R., Rogers, J., et al. (2005). Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786-1789 https://doi.org/10.1126/science.1110951
  9. Kawaguchi, M., Imaizumi-Anraku, H., Koiwa, H., Niwa, S., Ikuta, A., Syono, K., and Akao, S. (2002). Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant-Microbe Interact. 15, 17-26 https://doi.org/10.1094/MPMI.2002.15.1.17
  10. Kinkema, M., and Gresshoff, P.M. (2008). Investigation of downstream signals of the soybean autoregulation of nodulation receptor kinase GmNARK. Mol. Plant-Microbe Interact. 21, 1337-1348 https://doi.org/10.1094/MPMI-21-10-1337
  11. Kosslak, R.M., and Bohlool, B.B. (1984). Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiol. 75, 125-130 https://doi.org/10.1104/pp.75.1.125
  12. Krusell, L., Madsen, L.H., Sato, S., Aubert, G., Genua, A., Szczy-glowski, K., Duc, G., Kaneko, T., Tabata, S., de Bruijn, F., et al. (2002). Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420, 422-426 https://doi.org/10.1038/nature01207
  13. Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.P., Ane, J.M., Lauber, E., Bisseling, T., et al. (2004). A putative Ca$^{2}^{+}$ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361-1364 https://doi.org/10.1126/science.1093038
  14. Lough, T.J., and Lucas, W.J. (2006). Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu. Rev. Plant Biol. 57, 203-232 https://doi.org/10.1146/annurev.arplant.56.032604.144145
  15. Madsen, E.B., Madsen, L.H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S., Sandal, N., et al. (2003). A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637-640 https://doi.org/10.1038/nature02045
  16. Magori, S., Oka-Kira, E., Shibata, S., Umehara, Y., Kouchi, H., Hase, Y., Tanaka, A., Sato, S., Tabata, S., and Kawaguchi, M. (2009). TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Mol. Plant-Microbe Interact. (in press) https://doi.org/10.1094/MPMI-22-3-0259
  17. Malik, N.S., and Bauer, W.D. (1988). When does the self-regulatory response elicited in soybean root after Inoculation occur? Plant Physiol. 88, 537-539 https://doi.org/10.1104/pp.88.3.537
  18. Mitra, R.M., Gleason, C.A., Edwards, A., Hadfield, J., Downie, J.A., Oldroyd, G.E., and Long, S.R. (2004). A $Ca^{2+}$/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc. Natl. Acad. Sci. USA 101, 4701-4705 https://doi.org/10.1073/pnas.0400595101
  19. Miwa, H., Betsuyaku, S., Iwamoto, K., Kinoshita, A., Fukuda, H., and Sawa, S. (2008). The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 49, 1752-1757 https://doi.org/10.1093/pcp/pcn148
  20. Miyahara, A., Hirani, T.A., Oakes, M., Kereszt, A., Kobe, B., Djordjevic, M.A., and Gresshoff, P.M. (2008). Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. J. Biol. Chem. 283, 25381-25391 https://doi.org/10.1074/jbc.M800400200
  21. Muller, R., Bleckmann, A., and Simon, R. (2008). The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20, 934-946 https://doi.org/10.1105/tpc.107.057547
  22. 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 https://doi.org/10.1093/dnares/dsl017
  23. Nakagawa, T., and Kawaguchi, M. (2006). Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol. 47, 176-180 https://doi.org/10.1093/pcp/pci222
  24. Nishimura, R., Hayashi, M., Wu, G.J., Kouchi, H., Imaizumi-Anraku, H., Murakami, Y., Kawasaki, S., Akao, S., Ohmori, M., Naga-sawa, M., et al. (2002). HAR1 mediates systemic regulation of symbiotic organ development. Nature 420, 426-429 https://doi.org/10.1038/nature01231
  25. Nontachaiyapoom, S., Scott, P.T., Men, A.E., Kinkema, M., Schenk, P.M., and Gresshoff, P.M. (2007). Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Mol. Plant-Microbe Interact. 20, 769-780 https://doi.org/10.1094/MPMI-20-7-0769
  26. Nutman, P.S. (1952). Studies on the physiology of nodule formation. III. Experiments on the excision of root-tips and nodules. Ann. Bot. 16, 79-101 https://doi.org/10.1093/oxfordjournals.aob.a083304
  27. Ogawa, M., Shinohara, H., Sakagami, Y., and Matsubayashi, Y. (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodo-main. Science 319, 294 https://doi.org/10.1126/science.1150083
  28. Oka-Kira, E., Tateno, K., Miura, K., Haga, T., Hayashi, M., Harada, K., Sato, S., Tabata, S., Shikazono, N., Tanaka, A., et al. (2005). klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J. 44, 505-515 https://doi.org/10.1111/j.1365-313X.2005.02543.x
  29. Okamoto, S., Ohnishi, E., Sato, S., Takahashi, H., Nakazono, M., Tabata, S., and Kawaguchi, M. (2009). Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 50, 67-77 https://doi.org/10.1093/pcp/pcn194
  30. Oldroyd, G.E., and Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546 https://doi.org/10.1146/annurev.arplant.59.032607.092839
  31. Pacios-Bras, C., Schlaman, H.R., Boot, K., Admiraal, P., Langerak, J.M., Stougaard, J., and Spaink, H.P. (2003) Auxin distribution in Lotus japonicus during root nodule development. Plant Mol. Biol. 52, 1169-1180 https://doi.org/10.1023/B:PLAN.0000004308.78057.f5
  32. Penmetsa, R.V., and Cook, D.R. (1997). A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527-530 https://doi.org/10.1126/science.275.5299.527
  33. Penmetsa, R.V., Frugoli, J.A., Smith, L.S., Long, S.R., and Cook, D.R. (2003). Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol. 131, 998-1008 https://doi.org/10.1104/pp.015677
  34. Pierce, M., and Bauer, W.D. (1983). A rapid regulatory response governing nodulation in soybean. Plant Physiol. 73, 286-290 https://doi.org/10.1104/pp.73.2.286
  35. Postma, J.G., Jacobsen, E., and Feenstra, W. (1988). Three pea mutants with an altered nodulation studied by genetic analysis and grafting. J. Plant Physiol. 132, 424-430 https://doi.org/10.1016/S0176-1617(88)80056-7
  36. Prayitno, J., Rolfe, B.G., and Mathesius, U. (2006). The Ethylene-insensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation. Plant Physiol. 142, 168-180 https://doi.org/10.1104/pp.106.080093
  37. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., et al. (2003). Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592 https://doi.org/10.1038/nature02039
  38. Sagan, M., and Duc, G. (1996). Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L). Symbiosis 20, 229-245
  39. Schnabel, E., Journet, E.P., de Carvalho-Niebel, F., Duc, G., and Frugoli, J. (2005). The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol. Biol. 58, 809-822 https://doi.org/10.1007/s11103-005-8102-y
  40. Searle, I.R., Men, A.E., Laniya, T.S., Buzas, D.M., Iturbe-Ormaetxe, I., Carroll, B.J., and Gresshoff, P.M. (2003). Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299, 109-112 https://doi.org/10.1126/science.1077937

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