Cellular and Molecular Life Sciences

, Volume 68, Issue 8, pp 1341–1351 | Cite as

Function and evolution of nodulation genes in legumes

  • Keisuke Yokota
  • Makoto HayashiEmail author
Multi-author review


Root nodule (RN) symbiosis has a unique feature in which symbiotic bacteria fix atmospheric nitrogen. The symbiosis is established with a limited species of land plants, including legumes. How RN symbiosis evolved is still a mystery, but recent findings on legumes genes that are necessary for RN symbiosis may give us a clue.


Root nodule symbiosis Arbuscular mycorrhiza symbiosis Actinorhiza symbiosis Legumes Lotus japonicus Medicago truncatula Nitrogen fixation Infection threads 



We are grateful to Jeff J. Doyle (Cornell University) for critical reading of the manuscript. We thank Shusei Sato (Kazusa DNA Research Institute) and Takeshi Izawa (National Institute of Agrobiological Sciences) for NLP clustering. This work was supported by the Ministry of Agriculture, Forestry and Fisheries of Japan (Rice Genome Project Grant PMI-0001 to M.H.).


  1. 1.
    Doyle JJ, Luckow MA (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 131:900–910PubMedGoogle Scholar
  2. 2.
    Swensen SM, Mullin BC (1997) Phylogenetic relationships among actinorhizal plants. The impact of molecular systematics and implications for the evolution of actinorhizal symbioses. Physiol Plant 99:565–573Google Scholar
  3. 3.
    Sprent JI (2001) Nodulation in Legumes. Royal Botanic Gardens, KewGoogle Scholar
  4. 4.
    Sprent JI, James EK (2007) Legume evolution: where do nodules and mycorrhizas fit in? Plant Physiol 144:575–581PubMedGoogle Scholar
  5. 5.
    Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182PubMedGoogle Scholar
  6. 6.
    Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546PubMedGoogle Scholar
  7. 7.
    Doyle JJ (1994) Phylogeny of the legume family: an approach to understanding the origins of nodulation. Annu Rev Ecol Syst 25:325–349Google Scholar
  8. 8.
    Pawlowski K, Bisseling T (1996) Rhizobial and actinorhizal symbioses: what are the shared features? Plant Cell 8:1899–1913PubMedGoogle Scholar
  9. 9.
    Doyle JJ (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3:473–478Google Scholar
  10. 10.
    Gualtieri G, Bisseling T (2000) The evolution of nodulation. Plant Mol Biol 42:181–194PubMedGoogle Scholar
  11. 11.
    Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518PubMedGoogle Scholar
  12. 12.
    Szczyglowski K, Amyot L (2003) Symbiosis, inventiveness by recruitment? Plant Physiol 131:935–940PubMedGoogle Scholar
  13. 13.
    Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedGoogle Scholar
  14. 14.
    Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14:77–86PubMedGoogle Scholar
  15. 15.
    Held M, Hossain MS, Yokota K, Bonfante P, Stougaard J, Szczyglowski K (2010) Common and not so common symbiotic entry. Trends Plant Sci 15:540–545PubMedGoogle Scholar
  16. 16.
    Spaink HP (2004) Specific recognition of bacteria by plant LysM domain receptor kinases. Trends Microbiol 12:201–204PubMedGoogle Scholar
  17. 17.
    Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592PubMedGoogle Scholar
  18. 18.
    Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640PubMedGoogle Scholar
  19. 19.
    Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633PubMedGoogle Scholar
  20. 20.
    Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Gherardi M, Huguet T, Geurts R, Denarie J, Rouge P, Gough C (2006) The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:265–279PubMedGoogle Scholar
  21. 21.
    Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C, Bisseling T (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145:183–191PubMedGoogle Scholar
  22. 22.
    Zhukov V, Radutoiu S, Madsen LH, Rychagova T, Ovchinnikova E, Borisov A, Tikhonovich I, Stougaard J (2008) The pea Sym37 receptor kinase gene controls infection-thread initiation and nodule development. Mol Plant Microbe Interact 21:1600–1608PubMedGoogle Scholar
  23. 23.
    Doyle JJ, Doyle JL, Ballenger JA, Dickson EE, Kajita T, Ohashi H (1997) A phylogeny of the chloroplast gene rbcL in the Leguminosae: taxonomic correlations and insights into the evolution of nodulation. Am J Bot 84:541–554Google Scholar
  24. 24.
    Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26:3923–3935PubMedGoogle Scholar
  25. 25.
    Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104:19613–19618PubMedGoogle Scholar
  26. 26.
    Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481PubMedGoogle Scholar
  27. 27.
    Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103:11086–11091PubMedGoogle Scholar
  28. 28.
    Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214PubMedGoogle Scholar
  29. 29.
    Zhang XC, Wu X, Findley S, Wan J, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144:623–636PubMedGoogle Scholar
  30. 30.
    Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol 9:10PubMedGoogle Scholar
  31. 31.
    Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962PubMedGoogle Scholar
  32. 32.
    Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531PubMedGoogle Scholar
  33. 33.
    Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364PubMedGoogle Scholar
  34. 34.
    Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624PubMedGoogle Scholar
  35. 35.
    Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, 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 22:2509–2526PubMedGoogle Scholar
  36. 36.
    Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci USA 105:20540–20545PubMedGoogle Scholar
  37. 37.
    Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH, Miwa H, Nakagawa T, Sandal N, Albrektsen AS, Kawaguchi M, Downie A, Sato S, Tabata S, Kouchi H, Parniske M, Kawasaki S, Stougaard J (2006) Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:1153–1156PubMedGoogle Scholar
  38. 38.
    Godfroy O, Debelle F, Timmers T, Rosenberg C (2006) A rice calcium- and calmodulin-dependent protein kinase restores nodulation to a legume mutant. Mol Plant Microbe Interact 19:495–501PubMedGoogle Scholar
  39. 39.
    Chen C, Gao M, Liu J, Zhu H (2007) Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase. Plant Physiol 145:1619–1628PubMedGoogle Scholar
  40. 40.
    Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6:e68PubMedGoogle Scholar
  41. 41.
    Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, Imaizumi-Anraku H (2008) Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol 49:1659–1671PubMedGoogle Scholar
  42. 42.
    Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial nod factor-induced transcription. Science 308:1789–1791PubMedGoogle Scholar
  43. 43.
    Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308:1786–1789PubMedGoogle Scholar
  44. 44.
    Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142:1739–1750PubMedGoogle Scholar
  45. 45.
    Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie JA, Kawaguchi M, 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 13:255–265PubMedGoogle Scholar
  46. 46.
    Hirsch S, Oldroyd GE (2009) GRAS-domain transcription factors that regulate plant development. Plant Signal Behav 4:698–700PubMedGoogle Scholar
  47. 47.
    Yokota K, Soyano T, Kouchi H, Hayashi M (2010) Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice. Plant Cell Physiol 51:1436–1442PubMedGoogle Scholar
  48. 48.
    Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557PubMedGoogle Scholar
  49. 49.
    Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol 182:200–212PubMedGoogle Scholar
  50. 50.
    Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195PubMedGoogle Scholar
  51. 51.
    Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60:229–237PubMedGoogle Scholar
  52. 52.
    Aravind L, Ponting CP (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22:458–459PubMedGoogle Scholar
  53. 53.
    Rybalkin SD, Rybalkina IG, Shimizu-Albergine M, Tang XB, Beavo JA (2003) PDE5 is converted to an activated state upon cGMP binding to the GAF A domain. EMBO J 22:469–478PubMedGoogle Scholar
  54. 54.
    Little R, Dixon R (2003) The amino-terminal GAF domain of Azotobacter vinelandii NifA binds 2-oxoglutarate to resist inhibition by NifL under nitrogen-limiting conditions. J Biol Chem 278:28711–28718PubMedGoogle Scholar
  55. 55.
    Ponting CP, Ito T, Moscat J, Diaz-Meco MT, Inagaki F, Sumimoto H (2002) OPR, PC and AID: all in the PB1 family. Trends Biochem Sci 27:10PubMedGoogle Scholar
  56. 56.
    Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435PubMedGoogle Scholar
  57. 57.
    Nutman PS (1952) Host-factors influencing infection and nodule development in leguminous plants. Proc R Soc Lond B Biol Sci 139:176–185 discussion 202–207PubMedGoogle Scholar
  58. 58.
    Pierce M, Bauer WD (1983) A rapid regulatory response governing nodulation in soybean. Plant Physiol 73:286–290PubMedGoogle Scholar
  59. 59.
    Kosslak RM, Bohlool BB (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 75:125–130PubMedGoogle Scholar
  60. 60.
    Malik NS, Bauer WD (1988) When does the self-regulatory response elicited in soybean root after inoculation occur? Plant Physiol 88:537–539PubMedGoogle Scholar
  61. 61.
    Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426PubMedGoogle Scholar
  62. 62.
    Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429PubMedGoogle Scholar
  63. 63.
    Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109–112PubMedGoogle Scholar
  64. 64.
    Oka-Kira E, Kawaguchi M (2006) Long-distance signaling to control root nodule number. Curr Opin Plant Biol 9:496–502PubMedGoogle Scholar
  65. 65.
    Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585PubMedGoogle Scholar
  66. 66.
    Suzaki T, Sato M, Ashikari M, Miyoshi M, Nagato Y, Hirano HY (2004) The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131:5649–5657PubMedGoogle Scholar
  67. 67.
    Schnabel E, Journet EP, de Carvalho-Niebel F, Duc G, 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 58:809–822PubMedGoogle Scholar
  68. 68.
    Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460–469PubMedGoogle Scholar
  69. 69.
    Oka-Kira E, Tateno K, Miura K, Haga T, Hayashi M, Harada K, Sato S, Tabata S, Shikazono N, Tanaka A, Watanabe Y, Fukuhara I, Nagata T, Kawaguchi M (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J 44:505–515PubMedGoogle Scholar
  70. 70.
    Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu GJ, Sato S, Hayashi M, Betsuyaku S, Nakazono M, Tabata S, Harada K, Sawa S, Fukuda H, Kawaguchi M (2010) The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137:4317–4325PubMedGoogle Scholar
  71. 71.
    Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–3920PubMedGoogle Scholar
  72. 72.
    Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238:106–119PubMedGoogle Scholar
  73. 73.
    Charon C, Johansson C, Kondorosi E, Kondorosi A, Crespi M (1997) enod40 induces dedifferentiation and division of root cortical cells in legumes. Proc Natl Acad Sci USA 94:8901–8906PubMedGoogle Scholar
  74. 74.
    Yang WC, Katinakis P, Hendriks P, Smolders A, de Vries F, Spee J, van Kammen A, Bisseling T, Franssen H (1993) Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3:573–585PubMedGoogle Scholar
  75. 75.
    Kouchi H, Takane K, So RB, Ladha JK, Reddy PM (1999) Rice ENOD40: isolation and expression analysis in rice and transgenic soybean root nodules. Plant J 18:121–129PubMedGoogle Scholar
  76. 76.
    Takeda N, Okamoto S, Hayashi M, Murooka Y (2005) Expression of LjENOD40 genes in response to symbiotic and non-symbiotic signals: LjENOD40–1 and LjENOD40–2 are differentially regulated in Lotus japonicus. Plant Cell Physiol 46:1291–1298PubMedGoogle Scholar
  77. 77.
    Gultyaev AP, Roussis A (2007) Identification of conserved secondary structures and expansion segments in enod40 RNAs reveals new enod40 homologues in plants. Nucleic Acids Res 35:3144–3152PubMedGoogle Scholar
  78. 78.
    Cole RA, Fowler JE (2006) Polarized growth: maintaining focus on the tip. Curr Opin Plant Biol 9:579–588PubMedGoogle Scholar
  79. 79.
    Smith LG (2003) Cytoskeletal control of plant cell shape: getting the fine points. Curr Opin Plant Biol 6:63–73PubMedGoogle Scholar
  80. 80.
    Geitmann A, Emons AM (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245PubMedGoogle Scholar
  81. 81.
    Gage DJ, Margolin W (2000) Hanging by a thread: invasion of legume plants by rhizobia. Curr Opin Microbiol 3:613–617PubMedGoogle Scholar
  82. 82.
    van Brussel AA, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T, Lugtenberg BJ, Kijne JW (1992) Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257:70–72PubMedGoogle Scholar
  83. 83.
    Brewin NJ (2004) Plant cell wall remodelling in the rhizobium–legume symbiosis. Crit Rev Plant Sci 23:293–316Google Scholar
  84. 84.
    Yokota K, Fukai E, Madsen LH, Jurkiewicz A, Rueda P, Radutoiu S, Held M, Hossain MS, Szczyglowski K, Morieri G, Oldroyd GE, Downie JA, Nielsen MW, Rusek AM, Sato S, Tabata S, James EK, Oyaizu H, Sandal N, Stougaard J (2009) Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21:267–284PubMedGoogle Scholar
  85. 85.
    Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136:3864–3876PubMedGoogle Scholar
  86. 86.
    Tansengco ML, Hayashi M, Kawaguchi M, Imaizumi-Anraku H, Murooka Y (2003) crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair, trichome, and seed development in Lotus japonicus. Plant Physiol 131:1054–1063PubMedGoogle Scholar
  87. 87.
    Tansengco ML, Imaizumi-Anraku H, Yoshikawa M, Takagi S, Kawaguchi M, Hayashi M, Murooka Y (2004) Pollen development and tube growth are affected in the symbiotic mutant of Lotus japonicus, crinkle. Plant Cell Physiol 45:511–520PubMedGoogle Scholar
  88. 88.
    Yano K, Shibata S, Chen WL, Sato S, Kaneko T, Jurkiewicz A, Sandal N, Banba M, Imaizumi-Anraku H, Kojima T, Ohtomo R, Szczyglowski K, Stougaard J, Tabata S, Hayashi M, Kouchi H, Umehara Y (2009) CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume–rhizobium symbiosis. Plant J 60:168–180PubMedGoogle Scholar
  89. 89.
    Yano K, Tansengco ML, Hio T, Higashi K, Murooka Y, Imaizumi-Anraku H, Kawaguchi M, Hayashi M (2006) New nodulation mutants responsible for infection thread development in Lotus japonicus. Mol Plant Microbe Interact 19:801–810PubMedGoogle Scholar
  90. 90.
    Lombardo F, Heckmann AB, Miwa H, Perry JA, Yano K, Hayashi M, Parniske M, Wang TL, Downie JA (2006) Identification of symbiotically defective mutants of Lotus japonicus affected in infection thread growth. Mol Plant Microbe Interact 19:1444–1450PubMedGoogle Scholar
  91. 91.
    Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, Ronson CW, James EK, Stougaard J (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1:1–12Google Scholar
  92. 92.
    Hayashi T, Banba M, Shimoda Y, Kouchi H, Hayashi M, Imaizumi-Anraku H (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J 63:141–154PubMedGoogle Scholar
  93. 93.
    Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu Rev Plant Physiol Plant Mol Biol 48:493–523PubMedGoogle Scholar
  94. 94.
    Garrocho-Villegas V, Gopalasubramaniam SK, Arredondo-Peter R (2007) Plant hemoglobins: what we know six decades after their discovery. Gene 398:78–85PubMedGoogle Scholar
  95. 95.
    Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531–535PubMedGoogle Scholar
  96. 96.
    Dordas C (2009) Nonsymbiotic hemoglobins and stress tolerance in plants. Plant Sci 176:433–440Google Scholar
  97. 97.
    Shimoda Y, Nagata M, Suzuki A, Abe M, Sato S, Kato T, Tabata S, Higashi S, Uchiumi T (2005) Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol 46:99–107PubMedGoogle Scholar
  98. 98.
    Shimoda Y, Shimoda-Sasakura F, Kucho K, Kanamori N, Nagata M, Suzuki A, Abe M, Higashi S, Uchiumi T (2009) Overexpression of class 1 plant hemoglobin genes enhances symbiotic nitrogen fixation activity between Mesorhizobium loti and Lotus japonicus. Plant J 57:254–263PubMedGoogle Scholar
  99. 99.
    Hunt PW, Watts RA, Trevaskis B, Llewelyn DJ, Burnell J, Dennis ES, Peacock WJ (2001) Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Mol Biol 47:677–692PubMedGoogle Scholar
  100. 100.
    Frugier F, Kosuta S, Murray JD, Crespi M, Szczyglowski K (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci 13:115–120PubMedGoogle Scholar
  101. 101.
    Guldner E, Godelle B, Galtier N (2004) Molecular adaptation in plant hemoglobin, a duplicated gene involved in plant–bacteria symbiosis. J Mol Evol 59:416–425PubMedGoogle Scholar
  102. 102.
    Gopalasubramaniam SK, Kovacs F, Violante-Mota F, Twigg P, Arredondo-Peter R, Sarath G (2008) Cloning and characterization of a caesalpinoid (Chamaecrista fasciculata) hemoglobin: the structural transition from a nonsymbiotic hemoglobin to a leghemoglobin. Proteins 72:252–260PubMedGoogle Scholar
  103. 103.
    Franche C, Diouf D, Laplaze L, Auguy F, Frutz T, Rio M, Duhoux E, Bogusz D (1998) Soybean (lbc3), Parasponia, and Trema hemoglobin gene promoters retain symbiotic and nonsymbiotic specificity in transgenic Casuarinaceae: implications for hemoglobin gene evolution and root nodule symbioses. Mol Plant Microbe Interact 11:887–894Google Scholar
  104. 104.
    Sturms R, Kakar S, Trent J 3rd, Hargrove MS (2010) Trema and Parasponia hemoglobins reveal convergent evolution of oxygen transport in plants. Biochemistry 49:4085–4093PubMedGoogle Scholar
  105. 105.
    Hakoyama T, Niimi K, Watanabe H, Tabata R, Matsubara J, Sato S, Nakamura Y, Tabata S, Jichun L, Matsumoto T, Tatsumi K, Nomura M, Tajima S, Ishizaka M, Yano K, Imaizumi-Anraku H, Kawaguchi M, Kouchi H, Suganuma N (2009) Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature 462:514–517PubMedGoogle Scholar
  106. 106.
    Hoover TR, Robertson AD, Cerny RL, Hayes RN, Imperial J, Shah VK, Ludden PW (1987) Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate. Nature 329:855–857PubMedGoogle Scholar
  107. 107.
    Hoover TR, Imperial J, Ludden PW, Shah VK (1989) Homocitrate is a component of the iron–molybdenum cofactor of nitrogenase. Biochemistry 28:2768–2771PubMedGoogle Scholar
  108. 108.
    Hoover TR, Imperial J, Ludden PW, Shah VK (1988) Homocitrate cures the NifV-phenotype in Klebsiella pneumoniae. J Bacteriol 170:1978–1979PubMedGoogle Scholar
  109. 109.
    Zheng L, White RH, Dean DR (1997) Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase. J Bacteriol 179:5963–5966PubMedGoogle Scholar
  110. 110.
    de Kraker JW, Luck K, Textor S, Tokuhisa JG, Gershenzon J (2007) Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branchpoint step in the biosynthesis of leucine. Plant Physiol 143:970–986PubMedGoogle Scholar
  111. 111.
    Oke V, Long SR (1999) Bacteroid formation in the rhizobium–legume symbiosis. Curr Opin Microbiol 2:641–646PubMedGoogle Scholar
  112. 112.
    Graham MA, Silverstein KA, Cannon SB, VandenBosch KA (2004) Computational identification and characterization of novel genes from legumes. Plant Physiol 135:1179–1197PubMedGoogle Scholar
  113. 113.
    Silverstein KA, Graham MA, Paape TD, VandenBosch KA (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610PubMedGoogle Scholar
  114. 114.
    Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700PubMedGoogle Scholar
  115. 115.
    Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361PubMedGoogle Scholar
  116. 116.
    Silverstein KA, Graham MA, VandenBosch KA (2006) Novel paralogous gene families with potential function in legume nodules and seeds. Curr Opin Plant Biol 9:142–146PubMedGoogle Scholar
  117. 117.
    Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaitre B, Alunni B, Bourge M, Kucho K, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126PubMedGoogle Scholar
  118. 118.
    Wang D, Griffitts J, Starker C, Fedorova E, Limpens E, Ivanov S, Bisseling T, Long S (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327:1126–1129PubMedGoogle Scholar
  119. 119.
    Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3:238–250PubMedGoogle Scholar
  120. 120.
    Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A, Kondorosi E (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132:161–173PubMedGoogle Scholar
  121. 121.
    Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862Google Scholar
  122. 122.
    Alunni B, Kevei Z, Redondo-Nieto M, Kondorosi A, Mergaert P, Kondorosi E (2007) Genomic organization and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula. Mol Plant Microbe Interact 20:1138–1148PubMedGoogle Scholar
  123. 123.
    Fedorova M, van de Mortel J, Matsumoto PA, Cho J, Town CD, VandenBosch KA, Gantt JS, Vance CP (2002) Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol 130:519–537PubMedGoogle Scholar
  124. 124.
    Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 54:575–594PubMedGoogle Scholar
  125. 125.
    Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92:2647–2651PubMedGoogle Scholar
  126. 126.
    Monteiro A, Podlaha O (2009) Wings, horns, and butterfly eyespots: how do complex traits evolve? PLoS Biol 7:e37PubMedGoogle Scholar
  127. 127.
    Pawlowski K, Newton WE (2008) Nitrogen-fixing actinorhizal symbioses. Springer, Berlin Heidelberg New YorkGoogle Scholar
  128. 128.
    Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335PubMedGoogle Scholar
  129. 129.
    Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD, Stacey G (2010) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 152:541–552PubMedGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  1. 1.National Institute of Agrobiological SciencesTsukubaJapan

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