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Plant hormonal regulation of nitrogen-fixing nodule organogenesis

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Molecules and Cells

Abstract

Legumes have evolved symbiotic interactions with rhizobial bacteria to efficiently utilize nitrogen. Recent progress in symbiosis has revealed several key components of host plants required for nitrogen-fixing nodule organogenesis, in which complicated metabolic and signaling pathways in the host plant are reprogrammed to generate nodules in the cortex upon perception of the rhizobial Nod factor. Following the recognition of Nod factors, plant hormones are likely to be essential throughout nodule organogenesis for integration of developmental and environmental signaling cues into nodule development. Here, we review the molecular events involved in plant hormonal regulation and signaling cross-talk for nitrogen-fixing nodule development, and discuss how these signaling networks are integrated into Nod factor-mediated signaling during plantmicrobe interactions.

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References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ane, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E., Ayax, C., Levy, J., Debelle, F., Baek, J.M., Kalo, P., et al. (2004). Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364–1367.

    Article  PubMed  CAS  Google Scholar 

  • Arrighi, J.F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L.C., Mirabella, R., de Carvalho-Niebel, F., Journet, E.P., Gherardi, M., Huguet, T., et al. (2006). The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142, 265–279.

    Article  PubMed  CAS  Google Scholar 

  • Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M., and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983.

    Article  PubMed  CAS  Google Scholar 

  • Bao, F., Shen, J., Brady, S.R., Muday, G.K., Asami, T., and Yang, Z. (2004) Brassinosteroids interact with auxin to promote lateral root development in Arabidopsis. Plant Physiol. 134, 1624–1631.

    Article  PubMed  CAS  Google Scholar 

  • Barnett, M.J., and Fisher, R.F. (2006). Global gene expression in the rhizobial-legume symbiosis. Symbiosis 42, 1–24.

    CAS  Google Scholar 

  • Ben Amor, B., Shaw, S.L., Oldroyd, G.E.D., Maillet, F., Penmetsa, R.V., Cook, D., Long, S.R., Denarie, J., and Gough, C. (2003). The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J. 34, 495–506.

    Article  CAS  Google Scholar 

  • Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602.

    Article  PubMed  CAS  Google Scholar 

  • Biswas, B., Chan, P.K., and Gresshoff, P.M. (2009) A novel ABA insensitive mutant of Lotus japonicus with a wilty phenotype displays unaltered nodulation regulation. Mol. Plant 2, 487–499.

    Article  PubMed  CAS  Google Scholar 

  • Borisov, A.Y., Madsen, L.H., Tsyganov, V.E., Umehara, Y., Voroshilova, V.A., Batagov, A.O., Sandal, N., Mortensen, A., Schauser, L., Ellis, N., et al. (2003). The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol. 131, 1009–1017.

    Article  PubMed  CAS  Google Scholar 

  • Cardinale, F., Meskiene, I., Ouaked, F., and Hirt, H. (2002). Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell 14, 703–711.

    PubMed  CAS  Google Scholar 

  • 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, 1647–1666.

    PubMed  CAS  Google Scholar 

  • Chen, T., Zhu, H., Ke, D., Cai, K., Wang, C., Gou, H., Hong, Z., and Zhang, Z. (2012). A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24, 823–838.

    Article  PubMed  CAS  Google Scholar 

  • Cooper, J.B., and Long, S.R. (1994). Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6, 215–225.

    PubMed  CAS  Google Scholar 

  • Den Herder, G., and Parniske, M. (2009). The unbearable naivety of legumes in symbiosis. Curr. Opin. Plant Biol. 12, 491–499.

    Article  CAS  Google Scholar 

  • Ding, Y., Kalo, P., Yendrek, C., Sun, J., Liang, Y., Marsh, J.F., Harris, J.M., and Oldroyd, G.E. (2008). Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell 20, 2681–2695.

    Article  PubMed  CAS  Google Scholar 

  • Duzan, H.M., Zhou, X., Souleimanov, A., and Smith, D.L. (2004). Perception of Bradyrhizobium japonicum Nod factor by soybean [Glycine max (L.) Merr.] root hairs under abiotic stress conditions. J. Exp. Bot. 55, 2641–2646.

    Article  PubMed  CAS  Google Scholar 

  • Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kalo, P., and Kiss, G.B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962–966.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson, B.J., and Beveridge, C.A. (2009). Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol. 149, 1929–1944.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson, B.J., Ross, J.J., and Reid, J.B. (2005). Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol. 138, 2396–2405.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.-H., Lin, Y.-H., and Reid, D.E. (2010). Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61–76.

    Article  PubMed  CAS  Google Scholar 

  • Foo, E., and Davies, N.W. (2011). Strigolactones promote nodulation in pea. Planta 234, 1073–1081.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pages, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455, 189–194.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, A., Bhuvaneswari, T., Torrey, J., 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.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, S., Kim, J., Munoz, A., Heckmann, A.B., Downie, J.A., and Oldroyd, G.E. (2009). GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21, 545–557.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kawaguchi, M., and Minamisawa, K. (2010). Plant-microbe communications for symbiosis. Plant Cell Physiol. 51, 1377–1380.

    Article  PubMed  CAS  Google Scholar 

  • Kevei, Z., Lougnon, G., Mergaert, P., Horvath, G.V., Kereszt, A., Jayaraman, D., Zaman, N., Marcel, F., Regulski, K., Kiss, G.B., et al. (2007). 3-hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19, 3974–3989.

    Article  PubMed  CAS  Google Scholar 

  • Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A., and Ecker, J.R. (1993). CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427–441.

    Article  PubMed  CAS  Google Scholar 

  • Kiegerl, S., Cardinale, F., Siligan, C., Gross, A., Baudouin, E., Liwosz, A., Eklof, S., Till, S., Bogre, L., Hirt, H., et al. (2000). SIMKK, a mitogen-activated protein kinase (MAPK) kinase, is a specific activator of the salt stress-induced MAPK, SIMK. Plant Cell 12, 2247–2258.

    PubMed  CAS  Google Scholar 

  • Kim, C.Y., Liu, Y., Thorne, E.T., Yang, H., Fukushige, H., Gassmann, W., Hildebrand, D., Sharp, R.E., and Zhang, S. (2003). Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15, 2707–2718.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kouchi, H., Imaizumi-Anraku, H., Hayashi, M., Hakoyama, T., Nakagawa, T., Umehara, Y., Suganuma, N., and Kawaguchi, M. (2010). How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol. 51, 1381–1397.

    Article  PubMed  CAS  Google Scholar 

  • Krusell, L., Madsen, L.H., Sato, S., Aubert, G., Genua, A., Szczyglowski, 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303, 1361–1364.

    Article  PubMed  CAS  Google Scholar 

  • Lievens, S., Goormachtig, S., Den Herder, J., Capoen, W., Mathis, R., Hedden, P., and Holsters, M. (2005). Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol. 139, 1366–1379.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., and Zhang, S. (2004). Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386–3399.

    Article  PubMed  CAS  Google Scholar 

  • Lohar, D., Schaff, J., Laskey, J., Kieber, J., Bilyeu, K., and Bird, D. (2004). Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. Plant J. 38, 203–214.

    Article  PubMed  CAS  Google Scholar 

  • Lohar, D.P., Sharopova, N., Endre, G., Penuela, S., Samac, D., Town, C., Silverstein, K.A., and VandenBosch, K.A. (2006). Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol. 140, 221–234.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Gomez, M., Sandal, N., Stougaard, J., and Boller, T. (2011). Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J. Exp. Bot. 63, 393–401.

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo, O., Piqueras, R., Sanchez-Serrano, J.J., and Solano, R. (2003). ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165–178.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Maekawa, T., Maekawa-Yoshikawa, M., Takeda, N., Imaizumi-Anraku, H., Murooka, Y., and Hayashi, M. (2009). Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J. 58, 183–194.

    Article  PubMed  CAS  Google Scholar 

  • 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 Int. 22, 259–268.

    Article  CAS  Google Scholar 

  • Markmann, K., and Parniske, M. (2009). Evolution of root endosymbiosis with bacteria: How novel are nodules? Trends Plant Sci. 14, 77–86.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Mathesius, U., Schlaman, H.R., Spaink, H.P., Of Sautter, C., Rolfe, B.G., and Djordjevic, M.A. (1998). Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J. 14, 23–34.

    Article  PubMed  CAS  Google Scholar 

  • Mellor, R.B., and Collinge, D.B. (1995). A simple-model based on known plant defense reactions is sufficient to explain most aspects of nodulation. J. Exp. Bot. 46, 1–18.

    Article  CAS  Google Scholar 

  • Middleton, P.H., Jakab, J., Penmetsa, R.V., Starker, C.G., Doll, J., Kalo, P., Prabhu, R., Marsh, J.F., Mitra, R.M., Kereszt, A., et al. (2007). An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19, 1221–1234.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Mortier, V., Den Herder, G., Whitford, R., Van de Velde, W., Rombauts, S., D’Haeseleer, K., Holsters, M., and Goormachtig, S. (2010). CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 153, 222–237.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa, T., and Kawaguchi, M. (2006). Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol. 47, 176–180.

    Article  PubMed  CAS  Google Scholar 

  • Nakamura, A., Goda, H., Shimada, Y., and Yoshida, S. (2004). Brassinosteroid selectively regulates PIN gene expression in Arabidopsis. Biosci. Biotechnol. Biochem. 68, 952–954.

    Article  PubMed  CAS  Google Scholar 

  • Nishimura, R., Hayashi, M., Wu, G.J., Kouchi, H., Imaizumi-Anraku, H., Murakami, Y., Kawasaki, S., Akao, S., Ohmori, M., Nagasawa, M., et al. (2002). HAR1 mediates systemic regulation of symbiotic organ development. Nature 420, 426–429.

    Article  PubMed  CAS  Google Scholar 

  • 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 Int. 20, 769–780.

    Article  CAS  Google Scholar 

  • Nutman, P.S. (1952). Host-factors influencing infection and nodule development in leguminous plants. Proc. R Soc. Lond. B Biol. Sci. 139, 176–185; discussion 202–177.

    Article  PubMed  CAS  Google Scholar 

  • Oka-Kira, E., and Kawaguchi, M. (2006). Long-distance signaling to control root nodule number. Curr. Opin. Plant Biol. 9, 496–502.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd, G.E., and Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519–546.

    Article  PubMed  CAS  Google Scholar 

  • Oldroyd, G.E., Engstrom, E.M., and Long, S.R. (2001). Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13, 1835–1849.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–775.

    Article  PubMed  CAS  Google Scholar 

  • Peer, W.A., Bandyopadhyay, A., Blakeslee, J.J., Makam, S.N., Chen, R.J., Masson, P.H., and Murphy, A.S. (2004). Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16, 1898–1911.

    Article  PubMed  CAS  Google Scholar 

  • Penmetsa, R.V., and Cook, D.R. (1997). A legume ethylene-Insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527–530.

    Article  PubMed  CAS  Google Scholar 

  • Penmetsa, R.V., Uribe, P., Anderson, J., Lichtenzveig, J., Gish, J.C., Nam, Y.W., Engstrom, E., Xu, K., Sckisel, G., Pereira, M., et al. (2008). The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations. Plant J. 55, 580–595.

    Article  PubMed  CAS  Google Scholar 

  • Perret, X., Staehelin, C., and Broughton, W.J. (2000). Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180–201.

    Article  PubMed  CAS  Google Scholar 

  • Pii, Y., Crimi, M., Cremonese, G., Spena, A., and Pandolfini, T. (2007). Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol. 7, 21–31.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ronald, P.C., and Beutler, B. (2010). Plant and animal sensors of conserved microbial signatures. Science 330, 1061–1064.

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Medrano, R., Xoconostle-Cazares, B., and Lucas, W.J. (2001). The phloem as a conduit for inter-organ communication. Curr. Opin. Plant Biol. 4, 202–209.

    Article  PubMed  CAS  Google Scholar 

  • Sandal, N., Krusell, L., Radutoiu, S., Olbryt, M., Pedrosa, A., Stracke, S., Sato, S., Kato, T., Tabata, S., Parniske, M., et al. (2002). A genetic linkage map of the model legume Lotus japonicus and strategies for fast mapping of new loci. Genetics 161, 1673–1683.

    PubMed  CAS  Google Scholar 

  • Santos, R., Herouart, D., Sigaud, S., Touati, D., and Puppo, A. (2001). Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant Microbe Int. 14, 86–89.

    Article  CAS  Google Scholar 

  • Schauser, L., Roussis, A., Stiller, J., and Stougaard, J. (1999). A plant regulator controlling development of symbiotic root nodules. Nature 402, 191–195.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sinha, A.K., Jaggi, M., Raghuram, B., and Tuteja, N. (2011). Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav. 6, 196–203.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Soto, M.J., Fernandez-Aparicio, M., Castellanos-Morales, V., Garcia-Garrido, J.M., Ocampo, J.A., Delgado, M.J., and Vierheilig, H. (2010). First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol. Biochem. 42, 383–385.

    Article  CAS  Google Scholar 

  • Stacey, G., McAlvin, C.B., Kim, S.Y., Olivares, J., and Soto, M.J. (2006). Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol. 141, 1473–1481.

    Article  PubMed  CAS  Google Scholar 

  • Stahl, Y., and Simon, R. (2010). Plant primary meristems: shared functions and regulatory mechanisms. Curr. Opin. Plant Biol. 13, 53–58.

    Article  PubMed  CAS  Google Scholar 

  • Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K., et al. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962.

    Article  PubMed  CAS  Google Scholar 

  • Subramanian, S., Stacey, G., and Yu, O. (2006). Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J. 48, 261–273.

    Article  PubMed  CAS  Google Scholar 

  • Sun, J., Cardoza, V., Mitchell, D.M., Bright, L., Oldroyd, G., and Harris, J.M. (2006). Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J. 46, 961–970.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, A., Akune, M., Kogiso, M., Imagama, Y., Osuki, K., Uchiumi, T., Higashi, S., Han, S.Y., Yoshida, S., Asami, T., et al. (2004). Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol. 45, 914–922.

    Article  PubMed  CAS  Google Scholar 

  • Symons, G.M., and Reid, J.B. (2004). Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels. Plant Physiol. 135, 2196–2206.

    CAS  Google Scholar 

  • Taylor, L.P., and Grotewold, E. (2005). Flavonoids as developmental regulators. Curr. Opin. Plant Biol. 8, 317–323.

    Article  PubMed  CAS  Google Scholar 

  • Terakado, J., Yoneyama, T., and Fujihara, S. (2006). Shoot-applied polyamines suppress nodule formation in soybean (Glycine max). J. Plant Physiol. 163, 497–505.

    Article  PubMed  CAS  Google Scholar 

  • Tirichine, L., Imaizumi-Anraku, H., Yoshida, S., Murakami, Y., Madsen, L.H., Miwa, H., Nakagawa, T., Sandal, N., Albrektsen, A.S., Kawaguchi, M., et al. (2006). Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441, 1153–1156.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., et al. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195–200.

    Article  PubMed  CAS  Google Scholar 

  • van Noorden, G.E., Ross, J.J., Reid, J.B., Rolfe, B.G., and Mathesius, U. (2006). Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant. Plant Physiol. 140, 1494–1506.

    Article  PubMed  CAS  Google Scholar 

  • van Noorden, G.E., Kerim, T., Goffard, N., Wiblin, R., Pellerone, F. I., Rolfe, B.G., and Mathesius, U. (2007). Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol. 144, 1115–1131.

    Article  PubMed  CAS  Google Scholar 

  • Vernie, T., Moreau, S., de Billy, F., Plet, J., Combier, J.P., Rogers, C., Oldroyd, G., Frugier, F., Niebel, A., and Gamas, P. (2008). EFD Is an ERF transcription factor involved in the control of nodule number and differentiation in Medicago truncatula. Plant Cell 20, 2696–2713.

    Article  PubMed  CAS  Google Scholar 

  • Wasson, A.P., Pellerone, F.I., and Mathesius, U. (2006). Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18, 1617–1629.

    Article  PubMed  CAS  Google Scholar 

  • Xie, X.N., Yoneyama, K., and Yoneyama, K. (2010). The strigolactone story. Ann. Rev. Phytopathol. 48, 93–117.

    Article  CAS  Google Scholar 

  • Yano, K., Yoshida, S., Muller, J., Singh, S., Banba, M., Vickers, K., Markmann, K., White, C., Schuller, B., Sato, S., et al. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. USA 105, 20540–20545.

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama, K., Xie, X., Sekimoto, H., Takeuchi, Y., Ogasawara, S., Akiyama, K., Hayashi, H., and Yoneyama, K. (2008). Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol. 179, 484–494.

    Article  PubMed  CAS  Google Scholar 

  • Yoo, S.D., Cho, Y.H., Tena, G., Xiong, Y., and Sheen, J. (2008). Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451, 789–795.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, S., and Klessig, D.F. (2001). MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520–527.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Ildoo Hwang.

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Ryu, H., Cho, H., Choi, D. et al. Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Mol Cells 34, 117–126 (2012). https://doi.org/10.1007/s10059-012-0131-1

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