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PMID: 20660226 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

How many peas in a pod? Legume genes responsible for mutualistic symbioses underground.

Plant & cell physiology ·Vol. 51 ·No. 9 ·2010-09-00 ·Pages 1381-97

Kouchi H, Imaizumi-Anraku H, Hayashi M, Hakoyama T, Nakagawa T, Umehara Y, Suganuma N, Kawaguchi M

Abstract

The nitrogen-fixing symbiosis between legume plants and Rhizobium bacteria is the most prominent plant-microbe endosymbiotic system and, together with mycorrhizal fungi, has critical importance in agriculture. The introduction of two model legume species, Lotus japonicus and Medicago truncatula, has enabled us to identify a number of host legume genes required for symbiosis. A total of 26 genes have so far been cloned from various symbiotic mutants of these model legumes, which are involved in recognition of rhizobial nodulation signals, early symbiotic signaling cascades, infection and nodulation processes, and regulation of nitrogen fixation. These accomplishments during the past decade provide important clues to understanding not only the molecular mechanisms underlying plant-microbe endosymbiotic associations but also the evolutionary aspects of nitrogen-fixing symbiosis between legume plants and Rhizobium bacteria. In this review we survey recent progress in molecular genetic studies using these model legumes.

MeSH Terms
Fabaceae/genetics,microbiology Gene Expression Regulation, Plant Genes, Plant Nitrogen Fixation Plant Root Nodulation/genetics Rhizobium/physiology Signal Transduction Symbiosis/genetics
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Kouchi Hiroshi
Department of Plant Sciences, National Institute of Agrobiological Sciences, Tsukuba 305-8602, Japan. kouchih@nias.affrc.go.jp
Imaizumi-Anraku Haruko
Hayashi Makoto
Hakoyama Tsuneo
Nakagawa Tomomi
Umehara Yosuke
Suganuma Norio
Kawaguchi Masayoshi
References (129)
129 references, click to expand
  1. A plant regulator controlling development of symbiotic root nodules.
    Nature. 1999 Nov 11;402(6758):191-5 PMID: 10647012
  2. An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction.
    Plant Cell. 2007 Apr;19(4):1221-34 PMID: 17449807
  3. Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti.
    Plant J. 2009 Jan;57(1):171-83 PMID: 18786000
  4. Control of nodule number by the phytohormone abscisic Acid in the roots of two leguminous species.
    Plant Cell Physiol. 2004 Jul;45(7):914-22 PMID: 15295075
  5. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes.
    Science. 2004 Feb 27;303(5662):1364-7 PMID: 14963334
  6. [Creation and genetic study of a collection of symbiotic mutants of the pea (Pisum sativum L.)].
    Genetika. 2003 Apr;39(4):501-9 PMID: 12760250
  7. Shoot-applied MeJA suppresses root nodulation in Lotus japonicus.
    Plant Cell Physiol. 2006 Jan;47(1):176-80 PMID: 16258071
  8. Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules.
    Plant Physiol. 2003 Mar;131(3):1080-90 PMID: 12644660
  9. Derepression of the plant Chromovirus LORE1 induces germline transposition in regenerated plants.
    PLoS Genet. 2010 Mar 05;6(3):e1000868 PMID: 20221264
  10. Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.).
    Plant Cell Physiol. 2010 Feb;51(2):201-14 PMID: 20007291
  11. Microtubule dynamics in living root hairs: transient slowing by lipochitin oligosaccharide nodulation signals.
    Plant Cell. 2005 Jun;17(6):1777-87 PMID: 15863517
  12. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection.
    Science. 2003 Oct 24;302(5645):630-3 PMID: 12947035
  13. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development.
    Mol Gen Genet. 1993 Apr;238(1-2):106-19 PMID: 7683079
  14. 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. 2006 Dec 31;13(6):255-65 PMID: 17244637
  15. Too much love, a root regulator associated with the long-distance control of nodulation in Lotus japonicus.
    Mol Plant Microbe Interact. 2009 Mar;22(3):259-68 PMID: 19245320
  16. Genetics of symbiosis in Lotus japonicus: recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci.
    Mol Plant Microbe Interact. 2006 Jan;19(1):80-91 PMID: 16404956
  17. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype.
    Plant J. 2000 Jul;23(1):97-114 PMID: 10929105
  18. 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. 2008 Nov;49(11):1659-71 PMID: 18852152
  19. 3-hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula.
    Plant Cell. 2007 Dec;19(12):3974-89 PMID: 18156218
  20. Plant genetic control of nodulation.
    Annu Rev Microbiol. 1991;45:345-82 PMID: 1741618
  21. HAR1 mediates systemic regulation of symbiotic organ development.
    Nature. 2002 Nov 28;420(6914):426-9 PMID: 12442172
  22. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals.
    Cell. 1996 May 31;85(5):673-81 PMID: 8646776
  23. A remorin protein interacts with symbiotic receptors and regulates bacterial infection.
    Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2343-8 PMID: 20133878
  24. A plant receptor-like kinase required for both bacterial and fungal symbiosis.
    Nature. 2002 Jun 27;417(6892):959-62 PMID: 12087405
  25. A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus.
    Plant Physiol. 2007 Mar;143(3):1293-305 PMID: 17277093
  26. Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula.
    Plant Cell. 2008 Oct;20(10):2681-95 PMID: 18931020
  27. Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent, low molecular mass fraction.
    New Phytol. 2010 Mar;185(4):1074-86 PMID: 20100211
  28. The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus.
    Plant Physiol. 2003 Mar;131(3):1009-17 PMID: 12644653
  29. Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses.
    Genetics. 2006 Apr;172(4):2491-9 PMID: 16452143
  30. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range.
    EMBO J. 2007 Sep 5;26(17):3923-35 PMID: 17690687
  31. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses.
    Plant Cell. 1994 Oct;6(10):1357-74 PMID: 7994171
  32. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots.
    Nature. 2005 Feb 3;433(7025):527-31 PMID: 15616514
  33. Dissection of symbiosis and organ development by integrated transcriptome analysis of lotus japonicus mutant and wild-type plants.
    PLoS One. 2009 Aug 07;4(8):e6556 PMID: 19662091
  34. Antiquity and function of CASTOR and POLLUX, the twin ion channel-encoding genes key to the evolution of root symbioses in plants.
    Plant Physiol. 2009 Jan;149(1):306-17 PMID: 18978069
  35. The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules.
    Plant Cell. 2005 May;17(5):1625-36 PMID: 15805486
  36. Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant.
    Plant Physiol. 2006 Apr;140(4):1494-506 PMID: 16489131
  37. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway.
    Plant Cell. 2008 Nov;20(11):2989-3005 PMID: 19033527
  38. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain.
    Science. 2008 Jan 18;319(5861):294 PMID: 18202283
  39. Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase.
    J Bacteriol. 1997 Sep;179(18):5963-6 PMID: 9294461
  40. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis.
    Science. 2007 Jan 5;315(5808):101-4 PMID: 17110535
  41. Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development.
    Curr Biol. 2005 Mar 29;15(6):531-5 PMID: 15797021
  42. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium.
    Science. 1992 Jul 3;257(5066):70-2 PMID: 17800714
  43. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis.
    Science. 2010 Feb 26;327(5969):1126-9 PMID: 20185723
  44. The cytoskeleton as a regulator and target of biotic interactions in plants.
    Plant Physiol. 2004 Dec;136(4):3864-76 PMID: 15591444
  45. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria.
    PLoS Biol. 2008 Mar 4;6(3):e68 PMID: 18318603
  46. Long-distance control of nodulation: molecules and models.
    Mol Cells. 2009 Feb 28;27(2):129-34 PMID: 19277493
  47. A gene expression atlas of the model legume Medicago truncatula.
    Plant J. 2008 Aug;55(3):504-13 PMID: 18410479
  48. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus.
    Nat Commun. 2010 Apr 12;1:10 PMID: 20975672
  49. New nodulation mutants responsible for infection thread development in Lotus japonicus.
    Mol Plant Microbe Interact. 2006 Jul;19(7):801-10 PMID: 16838792
  50. klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction.
    Plant J. 2005 Nov;44(3):505-15 PMID: 16236159
  51. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula.
    Plant Cell. 2009 Feb;21(2):545-57 PMID: 19252081
  52. Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus.
    Mol Plant Microbe Interact. 2006 Aug;19(8):914-23 PMID: 16903357
  53. Shoot control of root development and nodulation is mediated by a receptor-like kinase.
    Nature. 2002 Nov 28;420(6914):422-6 PMID: 12442170
  54. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis.
    Cell. 1997 May 16;89(4):575-85 PMID: 9160749
  55. The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection.
    Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9817-22 PMID: 18621693
  56. Plant science. Nodules and hormones.
    Science. 2007 Jan 5;315(5808):52-3 PMID: 17204633
  57. Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation.
    Nature. 2009 Nov 26;462(7272):514-7 PMID: 19940927
  58. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus.
    Plant Cell. 2007 Feb;19(2):610-24 PMID: 17307929
  59. Evolution and regulation of the Lotus japonicus LysM receptor gene family.
    Mol Plant Microbe Interact. 2010 Apr;23(4):510-21 PMID: 20192837
  60. CYCLOPS, a mediator of symbiotic intracellular accommodation.
    Proc Natl Acad Sci U S A. 2008 Dec 23;105(51):20540-5 PMID: 19074278
  61. Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids.
    Proc Natl Acad Sci U S A. 2009 Jul 28;106(30):12477-82 PMID: 19597156
  62. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development.
    Nature. 2006 Jun 29;441(7097):1153-6 PMID: 16810257
  63. LIN, a novel type of U-box/WD40 protein, controls early infection by rhizobia in legumes.
    Plant Physiol. 2009 Nov;151(3):1239-49 PMID: 19776163
  64. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots.
    Plant J. 2007 Jan;49(2):208-16 PMID: 17173544
  65. CLV3/ESR-related (CLE) peptides as intercellular signaling molecules in plants.
    Chem Rec. 2006;6(6):303-10 PMID: 17304552
  66. Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition.
    Nature. 2006 Jun 29;441(7097):1149-52 PMID: 16810256
  67. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis.
    Plant Cell. 2008 Dec;20(12):3467-79 PMID: 19106374
  68. A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts.
    Plant J. 2010 Jul 1;63(1):141-54 PMID: 20409002
  69. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length.
    Plant Mol Biol. 2005 Aug;58(6):809-822 PMID: 16240175
  70. The pea Sym37 receptor kinase gene controls infection-thread initiation and nodule development.
    Mol Plant Microbe Interact. 2008 Dec;21(12):1600-8 PMID: 18986256
  71. Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome.
    Plant Physiol. 2007 Dec;145(4):1600-18 PMID: 17951459
  72. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses.
    Science. 2004 Feb 27;303(5662):1361-4 PMID: 14963335
  73. Isolation and properties of soybean [Glycine max (L.) Merr.] mutants that nodulate in the presence of high nitrate concentrations.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4162-6 PMID: 16593577
  74. Insights into symbiotic nitrogen fixation in Medicago truncatula.
    Mol Plant Microbe Interact. 2006 Mar;19(3):330-41 PMID: 16570662
  75. The Medicago truncatula lysin [corrected] motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes.
    Plant Physiol. 2006 Sep;142(1):265-79 PMID: 16844829
  76. Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem.
    J Plant Res. 2009 Jan;122(1):31-9 PMID: 19104754
  77. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators.
    Science. 2005 Jun 17;308(5729):1786-9 PMID: 15961668
  78. GmN56, a novel nodule-specific cDNA from soybean root nodules encodes a protein homologous to isopropylmalate synthase and homocitrate synthase.
    Mol Plant Microbe Interact. 1995 Jan-Feb;8(1):172-6 PMID: 7539640
  79. 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. 2009 Oct;60(1):168-80 PMID: 19508425
  80. Plant peptides govern terminal differentiation of bacteria in symbiosis.
    Science. 2010 Feb 26;327(5969):1122-6 PMID: 20185722
  81. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase.
    Plant Physiol. 2007 May;144(1):324-35 PMID: 17369436
  82. Hanging by a thread: invasion of legume plants by rhizobia.
    Curr Opin Microbiol. 2000 Dec;3(6):613-7 PMID: 11121782
  83. Identification of "nodule-specific" host proteins (nodoulins) involved in the development of rhizobium-legume symbiosis.
    Cell. 1980 May;20(1):153-63 PMID: 7388942
  84. The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis.
    Annu Rev Phytopathol. 1995;33:345-68 PMID: 18999965
  85. A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula.
    Plant J. 2010 Apr 1;62(1):100-12 PMID: 20088899
  86. 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. 2003 Mar;131(3):1054-63 PMID: 12644658
  87. The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations.
    Plant J. 2008 Aug;55(4):580-95 PMID: 18435823
  88. Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium-pea (Pisum sativum L.) symbiosis.
    Ann Bot. 2002 Apr;89(4):357-66 PMID: 12096795
  89. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes.
    Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9823-8 PMID: 18606999
  90. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling.
    Plant Physiol. 2007 Sep;145(1):183-91 PMID: 17586690
  91. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti.
    J Bacteriol. 2009 Mar;191(5):1519-27 PMID: 19074376
  92. Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti.
    Plant Cell. 2009 Jan;21(1):267-84 PMID: 19136645
  93. Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2.
    Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10375-80 PMID: 16006515
  94. Shoot-applied polyamines suppress nodule formation in soybean (Glycine max).
    J Plant Physiol. 2006 Mar;163(5):497-505 PMID: 16473654
  95. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements.
    Development. 1999 Aug;126(16):3617-28 PMID: 10409507
  96. Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress.
    Plant Physiol. 2007 Jul;144(3):1495-507 PMID: 17545507
  97. A receptor kinase gene regulating symbiotic nodule development.
    Nature. 2002 Jun 27;417(6892):962-6 PMID: 12087406
  98. A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula.
    Mol Plant Microbe Interact. 2007 Aug;20(8):912-21 PMID: 17722695
  99. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis.
    Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5230-5 PMID: 16547129
  100. Coordinating nodule morphogenesis with rhizobial infection in legumes.
    Annu Rev Plant Biol. 2008;59:519-46 PMID: 18444906
  101. A Lotus basic leucine zipper protein with a RING-finger motif negatively regulates the developmental program of nodulation.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):15206-10 PMID: 12397181
  102. Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus.
    DNA Res. 2004 Aug 31;11(4):263-74 PMID: 15500251
  103. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume.
    Plant Physiol. 2006 Dec;142(4):1739-50 PMID: 17071642
  104. The nuclear pore and plant development.
    Curr Opin Plant Biol. 2009 Feb;12(1):87-95 PMID: 18938103
  105. Phosphoenolpyruvate carboxylase plays a crucial role in limiting nitrogen fixation in Lotus japonicus nodules.
    Plant Cell Physiol. 2006 May;47(5):613-21 PMID: 16524873
  106. 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. 2003 May;34(4):495-506 PMID: 12753588
  107. A Legume Ethylene-Insensitive Mutant Hyperinfected by Its Rhizobial Symbiont
    Science. 1997 Jan 24;275(5299):527-30 PMID: 8999796
  108. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19613-8 PMID: 18042724
  109. The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling.
    Development. 2001 May;128(9):1507-18 PMID: 11290290
  110. C(4)-dicarboxylate transport mutants of Rhizobium trifolii form ineffective nodules on Trifolium repens.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4284-8 PMID: 16593058
  111. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals.
    Nature. 2003 Oct 9;425(6958):637-40 PMID: 14534591
  112. Evolution of root endosymbiosis with bacteria: How novel are nodules?
    Trends Plant Sci. 2009 Feb;14(2):77-86 PMID: 19167260
  113. Pollen development and tube growth are affected in the symbiotic mutant of Lotus japonicus, crinkle.
    Plant Cell Physiol. 2004 May;45(5):511-20 PMID: 15169932
  114. Chimeric plant calcium/calmodulin-dependent protein kinase gene with a neural visinin-like calcium-binding domain.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):4897-901 PMID: 7761420
  115. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis.
    Science. 2007 Jan 5;315(5808):104-7 PMID: 17110537
  116. Long-distance signaling to control root nodule number.
    Curr Opin Plant Biol. 2006 Oct;9(5):496-502 PMID: 16877028
  117. Interactions between plants and arbuscular mycorrhizal fungi.
    Int Rev Cell Mol Biol. 2010;281:1-48 PMID: 20460182
  118. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation.
    New Phytol. 2007;174(1):11-25 PMID: 17335493
  119. Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus.
    Plant J. 2004 Aug;39(4):487-512 PMID: 15272870
  120. CLE peptides control Medicago truncatula nodulation locally and systemically.
    Plant Physiol. 2010 May;153(1):222-37 PMID: 20348212
  121. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1.
    Development. 2004 Nov;131(22):5649-57 PMID: 15509765
  122. A novel ARID DNA-binding protein interacts with SymRK and is expressed during early nodule development in Lotus japonicus.
    Plant Physiol. 2008 Sep;148(1):337-47 PMID: 18633121
  123. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation.
    Plant Cell Physiol. 2009 Jan;50(1):67-77 PMID: 19074184
  124. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis.
    Proc Natl Acad Sci U S A. 2006 Jan 10;103(2):359-64 PMID: 16407163
  125. Dual genetic pathways controlling nodule number in Medicago truncatula.
    Plant Physiol. 2003 Mar;131(3):998-1008 PMID: 12644652
  126. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti.
    Plant Cell. 2006 Oct;18(10):2680-93 PMID: 17028204
  127. Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate.
    Nature. 1987 Oct 29-Nov 4;329(6142):855-7 PMID: 3313054
  128. Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13407-12 PMID: 11078514
  129. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases.
    Nature. 2003 Oct 9;425(6958):585-92 PMID: 14534578
Article Info
Journal
Plant & cell physiology
Abbr.
Plant Cell Physiol
ISSN
1471-9053
Published
2010-09-00
Epub
2010-00-21
Pages
1381-97
Language
English
Region
Japan
NLM ID
9430925
PMCID
PMC2938637
Subset
IM
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