Plant Molecular Biology

, Volume 58, Issue 6, pp 809–822 | Cite as

The Medicago truncatula SUNN Gene Encodes a CLV1-like Leucine-rich Repeat Receptor Kinase that Regulates Nodule Number and Root Length

  • Schnabel Elise
  • Journet Etienne-Pascal
  • Carvalho-Niebel de Fernanda
  • Duc Gérard
  • Frugoli Julia


Four Medicago truncatula sunn mutants displayed shortened roots and hypernodulation under all conditions examined. The mutants, recovered in three independent genetic screens, all contained lesions in a leucine-rich repeat (LRR) receptor kinase. Although the molecular defects among alleles varied, root length and the extent of nodulation were not significantly different between the mutants. SUNN is expressed in shoots, flowers and roots. Although previously reported grafting experiments showed that the presence of the mutated SUNN gene in roots does not confer an obvious phenotype, expression levels of SUNN mRNA were reduced in sunn-1 roots. SUNN and the previously identified genes HAR1 (Lotus japonicus) and NARK (Glycine max) are orthologs based on gene sequence and synteny between flanking sequences. Comparison of related LRR receptor kinases determined that all nodulation autoregulation genes identified to date are the closest legume relatives of AtCLV1 by sequence, yet sunn, har and nark mutants do not display the fasciated clv phenotype. The M. truncatula region is syntenic with duplicated regions of Arabidopsis chromosomes 2 and 4, none of which harbor CLV1 or any other LRR receptor kinase genes. A novel truncated copy of the SUNN gene lacking a kinase domain, RLP1, is found immediately upstream of SUNN and like SUNN is expressed at a reduced level in sunn-1 roots.


Medicago truncatula nodule regulation RLP1 SUNN supernodulation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Albertsen, M.C., Curry, T.M., Palmer, R.G., Lamotte, C.E. 1983Genetics and comparative growth morphology of fasciation in soybeans (Glycine max [L.] Merr.)Bot. Gaz.144263275CrossRefGoogle Scholar
  2. Ane, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G., Ayax, C., Levy, J., Debelle, F., Baek, J.M., Kalo, P., Rosenberg, C., Roe, B.A., Long, S.R., Denarie, J., Cook, D. 2004Medicago truncatula DMI1 required for bacterial and fungal symbiosis in legumesScience39313641366CrossRefGoogle Scholar
  3. Benlloch, R., Navarro, C., Beltran, J.P., Canas, L.A. 2003Floral development of the model legume Medicago truncatula: ontogeny studies as a tool to better characterize homeotic mutationsSex Plant Reprod.15231241Google Scholar
  4. Bladergroen, M.R., Spaink, H.P. 1998Genes and signal molecules involved in the rhizobia–Leguminoseae symbiosisCurr. Opin. Plant Biol.1353359CrossRefPubMedGoogle Scholar
  5. Blanc, G., Barakat, A., Guyot, R., Cooke, R., Delseny, I. 2000Extensive duplication and reshuffling in the Arabidopsis genomePlant Cell1210931101CrossRefPubMedGoogle Scholar
  6. Bommert, P., Lunde, C., Nardmann, J., Volbrecht, E., Running, M., Jackson, D., Hake, S., Werr, W. 2005Thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinaseDevelopment13212351245CrossRefPubMedGoogle Scholar
  7. Carroll, B.J., McNeil, D.L., Gresshoff, P.M. 1985aIsolation and properties of soybean (Glycine max (L.) Merr.) mutants that nodulate in the presence of high nitrate concentrationsProc. Natl. Acad. Sci. USA8241624166Google Scholar
  8. Carroll, B.J., McNeil, D.L., Gresshoff, P.M. 1985bA super-nodulation and nitrate-tolerant symbiotic (nts) soybean mutantPlant Physiol.783440Google Scholar
  9. Charron, D., Pingret, J.L., Chabaud, M., Journet, E.P., Barker, D.G. 2004Pharmacological evidence that multiple phospholipid signaling pathways link rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses,including Ca2+ spiking and specific ENOD gene expressionPlant Physiol.13635823593CrossRefPubMedGoogle Scholar
  10. Clark, S.E., Williams, R.W., Meyerowitz, E.M. 1997The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in ArabidopsisCell89575585CrossRefPubMedGoogle Scholar
  11. Cohn, J., Day, R.B., Stacey, G. 1998Legume nodule organogenesisTrends Plant Sci.3105110CrossRefGoogle Scholar
  12. Crawford, N.M., Kahn, M.L., Leustek, T., Long, S.R. 2000 Nitrogen and sulfurBuchanan, B.B.Gruissem, W.Jones, R.L. eds. Biochemistry and Molecular Biology of PlantsAmerican Association of Plant PhysiologistsRockville, MD787849Google Scholar
  13. Diévart, A., Dalal, M., Tax, F.E., Lacey, A.D., Huttly, A., Li, J., Clark, S.E. 2003CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ developmentPlant Cell1511981211CrossRefPubMedGoogle Scholar
  14. Gottschalk, W. 1977Fasciated peas-unusual mutants for breeding and researchJ. Nucl. Agr. Biol.62733Google Scholar
  15. Hanks, S.K., Quinn, A.M. 1991Protein kinase catalytic domain sequence database: identification of conserved features of primary structure and classification of family membersMeth. Enzym.2003881PubMedGoogle Scholar
  16. Initiative, The Arabidopsis Genome2000Analysis of the genome sequence of the flowering plant Arabidopsis thalianaNature408796815Google Scholar
  17. Jeong, S., Clark, S.E. 2005Photoperiod regulates flower meristem development in Arabidopsis thalianaGenetics169907915CrossRefPubMedGoogle Scholar
  18. Journet, E.-P., El-Gachtouli, N., Vernoud, V., Billy, F., Pichon, M., Dedieu, A., Arnould, C., Morandi, D., Barker, D.G., Gianinazzi-Pearson, V. 2001aMedicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cellsMol. Plant–Microbe Inter.14737748Google Scholar
  19. Journet E.-P., Barker D., Harrison H.J. and Kondorosi E., 2001b. M. truncatula as biological material. In: EMBO Practical Course on the New Plant Model System Medicago truncatula, Scholar
  20. Kellogg, E.A. 2003aIt’s all relativeNature422383384CrossRefGoogle Scholar
  21. Kellogg, E.A. 2003bWhat happens to genes in duplicated genomesProc. Natl. Acad. Sci. USA10043604362CrossRefGoogle Scholar
  22. Kim, C.H., Jeong, D.H., An, G.H. 2000Molecular cloning and characterization of OsLRK1 encoding a putative receptor-like protein kinase from Oryza sativaPlant Sci.1521726CrossRefGoogle Scholar
  23. Koonin, E.V. 2001An apology for orthologs-or brave new memesGen. Biol.21005110052Google Scholar
  24. Krusell, L., Madsen, L.H., Sato, S., Aubert, G., Genua, A., Szczyglowski, K., Duc, G., Kaneko, T., Tabata, S., De Bruijn, F.J., Pajuelo, E., Sandal, N., Stougaard, J. 2002Shoot control of root development and nodulation is mediated by a receptor-like kinaseNature420422426CrossRefPubMedGoogle Scholar
  25. Kuppusamy, K., Endre, G., Prabhu, R., Penmetsa, R.V., Veershlingam, H., Cook, D.R., Dickstein, R., VandenBosch, K.A. 2004LIN, a Medicago truncatula gene required for nodule differentiation and persistance of rhizobial infectionsPlant Physiol.13636823691CrossRefPubMedGoogle Scholar
  26. Leong, S.A., Williams, P.H., Ditta, G.S. 1985Analysis of the 5′ regulatory region of the gene for delta-aminolevulinic acid synthetase of Rhizobium melilotiNucleic Acids Res.1359655976PubMedGoogle Scholar
  27. Levy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E. P., Ane, J.M., Lauber, E., Bisseling, T., Denarie, J., Rosenberg, C., Debelle, F. 2004A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbiosesScience30313611364CrossRefPubMedGoogle Scholar
  28. Limpens, E., Bisseling, T. 2003Signaling in symbiosisCurr. Opin. Plant Biol.6343350CrossRefPubMedGoogle Scholar
  29. Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., Geurts, R. 2003LysM receptor kinases regulating rhizobial Nod-factor induced infectionScience302630633CrossRefPubMedGoogle Scholar
  30. Mylona, P., Pawlowski, K., Bisseling, T. 1995Symbiotic nitrogen fixationPlant Cell7869885CrossRefPubMedGoogle Scholar
  31. Nishimura, R., Hayashi, M., Wu, G.J., Kouchi, H., Imaizumu-Anraku, H., Murakami, Y., Kawasaki, S., Akao, S., Ohmori, M., Nagasawa, M., Harada, K., Kawaguchi, M. 2002HAR1 mediates systemic regulation of symbiotic organ developmentNature420426429CrossRefPubMedGoogle Scholar
  32. Osborn, T.C., Pires, J.C., Birchler, J.A., Auger, D.L., Chen, Z.J., Lee, H.S., Comai, L., Madlung, A., Doerge, R., Colot, V., Martienssen, R.A. 2003Understanding mechanisms of novel gene expression in polyploidsTrends Genet.19141147CrossRefPubMedGoogle Scholar
  33. Paterson, A.H., Bowers, J.E., Burow, M.D., Draye, X., Elsik, C.G., Jiang, C.X., Katsar, C.S., Lan, T.H., Lin, Y.R., R.G., M., Wright, R.J. 2000Comparative genomics of plant chromosomesPlant Cell1215231539CrossRefPubMedGoogle Scholar
  34. Penmetsa, R.V., Cook, D.R. 1997A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiontScience275527530CrossRefPubMedGoogle Scholar
  35. Penmetsa, R.V., Frugoli, J., Smith, L., Long, S.R., Cook, D. 2003Genetic evidence for dual pathway control of nodule number in Medicago truncatulaPlant Physiol.1319981008CrossRefPubMedGoogle Scholar
  36. Pfaffl, M.W. 2001A new mathematical model for relative quantification in real-time RT-PCRNuc Acids Res.294550CrossRefGoogle Scholar
  37. Riely, B.K., Ane, J.M., Penmetsa, R.V., Cook, D. 2004Genetic and genomic analysis in model legumes bring Nod-factor signaling to center stageCurr. Opin. Plant Biol.7408413CrossRefPubMedGoogle Scholar
  38. Rosenberg, C., Boistard, P., Denarie, J., Casse-Delbart, F. 1981Genes controlling early and late functions in symbiosis are located on a megaplasmid in Rhizobium melilotiMol. Gen. Genet.184326333PubMedGoogle Scholar
  39. Sagan, M., Larambergue, H., Morandi, D. 1998Genetic analysis of symbiosis mutants in Medicago truncatulaElmerich, C.Kondorosi, A.Newton, W.E. eds. Biological Nitrogen Fixation for the 21st CenturyKluwer Academic PublishersDordrecht, The Netherlands317318Google Scholar
  40. Sagan, M., Duc, G. 1996Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.)Symbiosis20229245Google Scholar
  41. Sagan, M., Morandi, D., Tarenghi, E., Duc, G. 1995Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after g-ray mutagenesisPlant Sci.1116371CrossRefGoogle Scholar
  42. Salamov, A., Solovyev, V. 2000Ab initio gene finding in Drosophila genomic DNAGenome Res.10516522CrossRefPubMedGoogle Scholar
  43. Schnabel, E., Kulikova, O., Bisseling, T., Penmetsa, V., Cook, D., Frugoli, J. 2003An integrated physical, genetic and cytogenetic map around the sunn locus of M. truncatulaGenome4666572CrossRefPubMedGoogle Scholar
  44. Schultze, M., Kondorosi, A. 1998Regulation of symbiotic root nodule developmentAnn. Rev. Genet.323357CrossRefPubMedGoogle Scholar
  45. Searle, I.R., Men, A.E., Laniya, T., Buzas, D., Iturbe-Ormaetxe, I., Carroll, B.J., Gresshoff, P.M. 2003Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinaseScience299109112CrossRefPubMedGoogle Scholar
  46. Shiu S.H. and Bleecker A.B. 2001. Plant receptor-like kinase gene family:diversity, function and signaling. Science’s STKE 113(RE22): 1–13.Google Scholar
  47. Stougaard, J. 2000Regulators and regulation of legume root nodule developmentPlant Physiol.124531540CrossRefPubMedGoogle Scholar
  48. Suzaki, T., Sato, M., Ashikari, M., Miyoshi, M., Nagato, Y., Hirano, H.K. 2004The gene FLORAL ORGAN NUMBER1 regulated floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA 1Development13156495657CrossRefPubMedGoogle Scholar
  49. Taguchi-Shiobara, F., Yuan, Z., Hake, S., Jackson, D. 2001The fasciated ear2 gene encodes a leucine-rich repeat receptor- like protein that regulates shoot meristem proliferation in maizeGenes Develop.1527552766CrossRefPubMedGoogle Scholar
  50. Tang, Y., Knap, H.T. 1998Fasciation mutation enhances meristematic activity and alters pattern formation in soybeanInter. J. Plant. Sci.159249260CrossRefGoogle Scholar
  51. Thoquet, P., Gherardi, M., Journet, E.P., Kereszt, A., Ane, J.M., Prosperi, J.M., Huguet, T. 2002The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genesBioMed. Central Plant Biol.21Google Scholar
  52. Tör, M., Brown, D., Cooper, A., Woods-Tör, A., Sjölander, K., Jones, J.D.J., Holub, E.B. 2004Arabidopsis Downy Mildew Resistance Gene RPP27 Encodes a Receptor-Like Protein Similar to CLAVATA2 and Tomato Cf-9Plant Physiol.13511001112CrossRefPubMedGoogle Scholar
  53. Vision, T., Brown, D., Tanksley, S. 2000The origins of genomic duplications in ArabidopsisScience29021142117CrossRefPubMedGoogle Scholar
  54. Wolfe, K.H. 2001Yesterday’s polyploids and the mystery of diploidizationNature Rev. Genet.2333341CrossRefGoogle Scholar
  55. Wopereis, J., Pajuelo, E., Dazzo, F., Jiang, Q., Gresshoff, P., Bruijn, F., Stougaard, J., Szczyglowski, K. 2000Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotypePlant J.2397114CrossRefPubMedGoogle Scholar
  56. Yamamoto, E., Karakaya, H.C., Knap, H.T. 2000Molecular characterization of two soybean homologs of Arabidopsis thaliana CLAVATA1 from the wild type and fasciation mutantBiochem. Biophys. Acta1491333340PubMedGoogle Scholar
  57. Yamamoto, E., Knap, H.T. 2001Soybean receptor-like protein kinase genes: Paralogous divergence of a gene familyMol. Biol. Evol.1815221531PubMedGoogle Scholar
  58. Zhu, H.Y., Kim, D.J., Baek, J.M., Choi, H.K., Ellis, L.C., Kuester, H., McCombie, W.R., Peng, H.M., Cook, D.R. 2003Syntenic relationships between Medicago truncatula and Arabidopsis reveal extensive divergence of genome organizationPlant Physiol.13110181026CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Schnabel Elise
    • 1
  • Journet Etienne-Pascal
    • 2
  • Carvalho-Niebel de Fernanda
    • 2
  • Duc Gérard
    • 3
  • Frugoli Julia
    • 1
  1. 1.Department of Genetics, Biochemistry and Life Science StudiesClemson UniversityClemsonUSA
  2. 2.Laboratoire des Interactions Plantes-MicroorganismesUnité Mixte de Recherche, CNRS-INRACastanet-Tolosan cédexFrance
  3. 3.lNRA Unité de Recherches en Génétique et Ecophysiologie des légumineuses à grainesDIJON cédexFrance

Personalised recommendations