Plant hormonal regulation of nitrogen-fixing nodule organogenesis

Molecules and Cells

Volumn 34, Issue 2, 2012, Pages 117-126

  Ryu, Hojin ^a   Cho, Hyunwoo ^a   Choi, Daeseok ^a   Hwang, Ildoo ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Cross talk; Hormone; Legume; Nitrogen fixing; Symbiosis

Indexed keywords

ABSCISIC ACID; AUXIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CYTOKININ; ETHYLENE; GIBBERELLIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; JASMONIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; NITROGEN; NODULIN; PHYTOHORMONE; SALICYLIC ACID; TRANSCRIPTOME;

ALFALFA; ARABIDOPSIS; AUTOREGULATION; AUXIN TRANSPORT; BEAN; CELL DIFFERENTIATION; CELL MIGRATION; COWPEA; GENE EXPRESSION; HORMONAL REGULATION; LEGUME; LOSS OF FUNCTION MUTATION; MOLECULAR INTERACTION; NODULATION; NONHUMAN; ORGANOGENESIS; PLANT DEVELOPMENT; PROTEIN BINDING; PROTEIN DOMAIN; REVIEW; RHIZOBIUM; RHIZOBIUM RADIOBACTER; SIGNAL TRANSDUCTION; SYMBIOSIS;

FABACEAE; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; NITROGEN FIXATION; PLANT GROWTH REGULATORS; PLANT PHYSIOLOGICAL PHENOMENA; PLANT PROTEINS; PLANTS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION;

EID: 84865336929     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-012-0131-1     Document Type: Review

References (108)

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. (Pubitemid 350046234)
2. 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. (Pubitemid 38269428)
3. 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. (Pubitemid 44412246)
4. 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. (Pubitemid 34193435)
5. 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. (Pubitemid 38527370)
6. Barnett, M.J., and Fisher, R.F. (2006). Global gene expression in the rhizobial-legume symbiosis. Symbiosis 42, 1-24. (Pubitemid 46150747)
7. 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. (Pubitemid 36631880)
8. 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. (Pubitemid 37506047)
9. 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.
10. 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. (Pubitemid 36405304)
11. 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. (Pubitemid 34299673)
12. 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.
13. 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.
14. Cooper, J.B., and Long, S.R. (1994). Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6, 215-225.
15. Den Herder, G., and Parniske, M. (2009). The unbearable naivety of legumes in symbiosis. Curr. Opin. Plant Biol. 12, 491-499.
16. 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. (Pubitemid 352844584)
17. 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. (Pubitemid 40025079)
18. 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. (Pubitemid 34716874)
19. Ferguson, B.J., and Beveridge, C.A. (2009). Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol. 149, 1929-1944.
20. 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. (Pubitemid 43733580)
21. 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.
22. Foo, E., and Davies, N.W. (2011). Strigolactones promote nodulation in pea. Planta 234, 1073-1081.
23. 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. (Pubitemid 43990735)
24. 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.
25. 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. (Pubitemid 44749897)
26. 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. (Pubitemid 44956948)
27. 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.
28. 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.
29. 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. (Pubitemid 40848006)
30. Kawaguchi, M., and Minamisawa, K. (2010). Plant-microbe communications for symbiosis. Plant Cell Physiol. 51, 1377-1380.
31. 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. (Pubitemid 351253114)
32. 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. (Pubitemid 23059412)
33. 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. (Pubitemid 32053407)
34. 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. (Pubitemid 37470670)
35. 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.
36. 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.
37. 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. (Pubitemid 35415653)
38. 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. (Pubitemid 38269427)
39. 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. (Pubitemid 43786837)
40. 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. (Pubitemid 37310916)
41. 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. (Pubitemid 41096013)
42. 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. (Pubitemid 38503723)
43. 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. (Pubitemid 43956317)
44. 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.
45. 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. (Pubitemid 36137669)
46. 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. (Pubitemid 44061024)
47. 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. (Pubitemid 37280149)
48. 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.
49. 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.
50. Markmann, K., and Parniske, M. (2009). Evolution of root endosymbiosis with bacteria: How novel are nodules? Trends Plant Sci. 14, 77-86.
51. 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. (Pubitemid 46941636)
52. 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. (Pubitemid 28181337)
53. 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.
54. 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. (Pubitemid 46941650)
55. 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. (Pubitemid 38437474)
56. 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.
57. 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. (Pubitemid 46391482)
58. 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. (Pubitemid 46196989)
59. Nakagawa, T., and Kawaguchi, M. (2006). Shoot-Applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol. 47, 176-180. (Pubitemid 43278257)
60. Nakamura, A., Goda, H., Shimada, Y., and Yoshida, S. (2004). Brassinosteroid selectively regulates PIN gene expression in Arabidopsis. Biosci. Biotechnol. Biochem. 68, 952-954. (Pubitemid 39251473)
61. 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. (Pubitemid 35415654)
62. 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. (Pubitemid 46944971)
63. 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.
64. Oka-Kira, E., and Kawaguchi, M. (2006). Long-distance signaling to control root nodule number. Curr. Opin. Plant Biol. 9, 496-502. (Pubitemid 44292058)
65. 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.
66. 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.
67. Oldroyd, G.E., and Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546. (Pubitemid 351813041)
68. 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. (Pubitemid 32781994)
69. 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. (Pubitemid 37514737)
70. Parniske, M. (2008). Arbuscular mycorrhiza: The mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775.
71. 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. (Pubitemid 38908783)
72. Penmetsa, R.V., and Cook, D.R. (1997). A legume ethylene-Insensitive mutant hyperinfected by its rhizobial symbiont. Science 275, 527-530. (Pubitemid 27051907)
73. 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.
74. Perret, X., Staehelin, C., and Broughton, W.J. (2000). Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180-201. (Pubitemid 30143845)
75. 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.
76. 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.
77. 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. (Pubitemid 37280137)
78. 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. (Pubitemid 47367494)
79. Ronald, P.C., and Beutler, B. (2010). Plant and animal sensors of conserved microbial signatures. Science 330, 1061-1064.
80. 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. (Pubitemid 32406367)
81. 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. (Pubitemid 35014767)
82. 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. (Pubitemid 32062631)
83. Schauser, L., Roussis, A., Stiller, J., and Stougaard, J. (1999). A plant regulator controlling development of symbiotic root nodules. Nature 402, 191-195.
84. 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. (Pubitemid 36042413)
85. 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.
86. 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. (Pubitemid 40848007)
87. 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.
88. 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. (Pubitemid 44223297)
89. Stahl, Y., and Simon, R. (2010). Plant primary meristems: Shared functions and regulatory mechanisms. Curr. Opin. Plant Biol. 13, 53-58.
90. 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. (Pubitemid 34716873)
91. 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. (Pubitemid 44484867)
92. 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.
93. 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. (Pubitemid 39123405)
94. 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. (Pubitemid 39182798)
95. Taylor, L.P., and Grotewold, E. (2005). Flavonoids as developmental regulators. Curr. Opin. Plant Biol. 8, 317-323. (Pubitemid 40599985)
96. Terakado, J., Yoneyama, T., and Fujihara, S. (2006). Shoot-Applied polyamines suppress nodule formation in soybean (Glycine max). J. Plant Physiol. 163, 497-505. (Pubitemid 43220120)
97. 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. (Pubitemid 43990736)
98. 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. (Pubitemid 46196990)
99. 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.
100. 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. (Pubitemid 43956232)
101. 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. (Pubitemid 46944773)
102. 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. (Pubitemid 352844585)
103. 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. (Pubitemid 44025547)
104. Xie, X.N., Yoneyama, K., and Yoneyama, K. (2010). The strigolactone story. Ann. Rev. Phytopathol. 48, 93-117.
105. 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.
106. 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. (Pubitemid 351991415)
107. 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. (Pubitemid 351253163)
108. Zhang, S., and Klessig, D.F. (2001). MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520-527. (Pubitemid 33145971)