Local and Systemic Regulation of Plant Root System Architecture and Symbiotic Nodulation by a Receptor-Like Kinase

PLoS Genetics

Volumn 10, Issue 12, 2014, Pages

  Huault, Emeline ^a   Laffont, Carole ^a   Wen, Jiangqi ^b   Mysore, Kirankumar S ^b   Ratet, Pascal ^a   Duc, Gérard ^c   Frugier, Florian ^a  

^a INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

^b PLANT BIOLOGY DIVISION   (United States)

^c UNIV BOURGOGNE FRANCHE COMTÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE RICH REPEAT RECEPTOR LIKE KINASE; PROTEIN KINASE; UNCLASSIFIED DRUG; PROTEIN TYROSINE KINASE; VEGETABLE PROTEIN;

ARTICLE; BARREL MEDIC; CONTROLLED STUDY; CRA2 GENE; GENOTYPE; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MUTANT; NITROGEN FIXATION; NONHUMAN; PHENOTYPE; PHYLOGENY; PLANT GENE; PLANT ROOT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROOT DEVELOPMENT; SHOOT; SYMBIOSIS; SYMBIOTIC NODULATION; TRANSPOSON; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; MICROBIOLOGY; NODULATION; PHYSIOLOGY; RHIZOBIUM;

MEDICAGO TRUNCATULA;

MEDICAGO TRUNCATULA; MERISTEM; PHYLOGENY; PLANT PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RHIZOBIUM; ROOT NODULES, PLANT; SYMBIOSIS;

EID: 84919625970     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004891     Document Type: Article

References (51)

1. Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA, (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4: 442.
2. Gonzalez-Rizzo S, Laporte P, Crespi M, Frugier F (2009) Legume root architecture: a peculiar root system. In: Beeckman T editor, Blackwell, Oxford, United Kingdom. Annual Plant Reviews: Chapter 10, Root Development. pp.239–87.
3. Desbrosses GJ, Stougaard J, (2011) Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe 10: 348–58.
4. Oldroyd GE, Murray JD, Poole PS, Downie JA, (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45: 119–44.
5. Malamy JE, (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67–77.
6. Crespi M, Frugier F, (2008) De novo organ formation from differentiated cells: root nodule organogenesis. Sci Signal 1: re11.
7. Reid DE, Ferguson BJ, Hayashi S, Lin YH, Gresshoff PM, (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108: 789–95.
8. Herrbach V, Remblière C, Gough C, Bensmihen S, (2014) Lateral root formation and patterning in Medicago truncatula. J Plant Physiol 171: 301–10.
9. Fukaki H, Tasaka M, (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69: 437–49.
10. Murphy E, Smith S, De Smet I, (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24: 3198–217.
11. Chen X, (2012) Small RNAs in development - insights from plants. Curr Opin Genet Dev 22: 361–7.
12. 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: 575–85.
13. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM, (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911–4.
14. Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu CM, Heidstra R, et al. (2003) Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr Biol 13: 1435–41.
15. Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, et al. (2005) The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17: 2542–53.
16. Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S, et al. (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23: 362–71.
17. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, et al. (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313: 842–5.
18. Fisher K, Turner S, (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17: 1061–6.
19. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, et al. (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci U S A 105: 15208–13.
20. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, et al. (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420: 422–6.
21. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, et al. (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420: 426–9.
22. Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, et al. (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299: 109–12.
23. 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: 809–22.
24. Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu GJ, et al. (2010) The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137: 4317–25.
25. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, et al. (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50: 67–77.
26. Saur IM, Oakes M, Djordjevic MA, Imin N, (2011) Crosstalk between the nodulation signaling pathway and the autoregulation of nodulation in Medicago truncatula. New Phytol 190: 865–74.
27. Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S, (2012) Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70: 367–76.
28. Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M, (2013) Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat Commun 4: 2191.
29. Wopereis J, Pajuelo E, Dazzo FB, Jiang Q, Gresshoff PM, et al. (2000) Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype. Plant J 23: 97–114.
30. Tadege M, Wen J, He J, Tu H, Kwak Y, et al. (2008) Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J 54: 335–47.
31. Tadege M, Wang TL, Wen J, Ratet P, Mysore KS, (2009) Mutagenesis and beyond! Tools for understanding legume biology. Plant Physiol 151: 978–84.
32. Laffont C, Blanchet S, Lapierre C, Brocard L, Ratet P, et al. (2010) The compact root architecture1 gene regulates lignification, flavonoid production, and polar auxin transport in Medicago truncatula. Plant Physiol 153: 1597–607.
33. Kamiya N, Nagasaki H, Morikami A, Sato Y, Matsuoka M, (2003) Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J 35: 429–41.
34. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, et al. (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657–68.
35. Osipova MA, Mortier V, Demchenko KN, Tsyganov VE, Tikhonovich IA, et al. (2012) Wuschel-related homeobox5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiol 158: 1329–41.
36. Betsuyaku S, Sawa S, Yamada M, (2011) The Function of the CLE Peptides in Plant Development and Plant-Microbe Interactions. Arabidopsis Book 9: e0149.
37. Bryan AC, Obaidi A, Wierzba M, Tax FE, (2012) XYLEM INTERMIXED WITH PHLOEM1, a leucine-rich repeat receptor-like kinase required for stem growth and vascular development in Arabidopsis thaliana. Planta 235: 111–22.
38. Nontachaiyapoom S, Scott PT, Men AE, Kinkema M, Schenk PM, et al. (2007) Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Mol Plant Microbe Interact 20: 769–80.
39. Schnabel E, Karve A, Kassaw T, Mukherjee A, Zhou X, et al. (2012) The M. truncatula SUNN gene is expressed in vascular tissue, similarly to RDN1, consistent with the role of these nodulation regulation genes in long distance signaling. Plant Signal Behav 7: 4–6.
40. Oka-Kira E, Tateno K, Miura K, Haga T, Hayashi M, et al. (2005) klavier (klv), a novel hypernodulation mutant of Lotus japonicus affected in vascular tissue organization and floral induction. Plant J 44: 505–15.
41. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, et al. (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322: 594–7.
42. Gonzalez-Rizzo S, Crespi M, Frugier F, (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18: 2680–93.
43. Truchet G, Debellé F, Vasse J, Terzaghi B, Garnerone AM, et al. (1985) Identification of a Rhizobium meliloti pSym2011 region controlling the host specificity of root hair curling and nodulation. J Bacteriol 164: 1200–10.
44. d'Erfurth I, Cosson V, Eschstruth A, Lucas H, Kondorosi A, et al. (2003) Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. Plant J 34: 95–106.
45. Ratet P, Wen J, Cosson V, Tadege M, Mysore KS (2009) Tnt1 induced mutations in Medicago: characterisation and applications. In: Meksem K and Kahl G editors, Wiley, Oxford, United Kingdom. The Handbook of Plant Mutation Screening. pp. 83–99.
46. Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, et al. (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant Microbe Interact 14: 695–700.
47. Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, et al. (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell 20: 1494–503.
48. Plet J, Wasson A, Ariel F, Le Signor C, Baker D, et al. (2011) MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J 65: 622–33.
49. Koch B, Evans HJ, (1966) Reduction of acetylene to ethylene by soybean root nodules. Plant Physiol 41: 748–50.
50. Gouy M, Guindon S, Gascuel O, (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221–4.
51. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–21.