Pharmacological 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 expression

Plant Physiology

Volumn 136, Issue 3, 2004, Pages 3582-3593

  Charron, Dorothée ^a   Pingret, Jean Luc ^a   Chabaud, Mireille ^a   Journet, Etienne Pascal ^a   Barker, David G ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GENES; OLIGOMERS; PHOSPHOLIPIDS; POLYSACCHARIDES; SIGNALING;

GENE EXPRESSION; LIPPCHITO-OLIGOSACCHARIDE SIGNALS; PHARMALOGICAL EVIDENCE; PHOSPHOLIPID SIGNALING PATHWAYS;

PLANTS (BOTANY);

ENZYMES; GENES; LIPIDS; OLIGOMERS; POLYSACCHARIDES; ROOTS;

MEDICAGO; MEDICAGO TRUNCATULA; RHIZOBIUM;

CALCIUM; ENOD11 PROTEIN, MEDICAGO TRUNCATULA; MASTOPARAN; OLIGOSACCHARIDE; PEPTIDE; PHOSPHOLIPID; VEGETABLE PROTEIN; WASP VENOM;

ARTICLE; BARREL MEDIC; BIOSYNTHESIS; DRUG EFFECT; GENE EXPRESSION REGULATION; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHYSIOLOGY; PLANT ROOT; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; TRANSGENIC PLANT;

CALCIUM; GENE EXPRESSION REGULATION, PLANT; MEDICAGO TRUNCATULA; NITROGEN FIXATION; OLIGOSACCHARIDES; PEPTIDES; PHOSPHOLIPIDS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; WASP VENOMS;

EID: 16544386635     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.051110     Document Type: Article

References (63)

1. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, et al (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303: 1364-1367
2. Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bögre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23: 572-581
3. Ben Amor B, Shaw SL, Oldroyd GE, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, 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
4. Calantzis C, Morandi D, Arnould C, Gianinazzi PV (2001) Cellular interactions between G-mosseae and a Myc(-) dmi2 mutant in Medicago truncatula. Symbiosis 30: 97-108
5. Cárdenas L, Feijó JA, Kunkel JG, Sánchez F, Holdaway-Clarke T, Hepler PK, Quinto C (1999) Rhizobium Nod factors induce increases in intracellular free calcium and extracellular calcium influxes in bean root hairs. Plant J 19: 347-352
6. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1665
7. Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of barrel medic (Medicago truncatula Gaertn.) by Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the MtENOD12 nodulin promoter fused to the GUS reporter gene. Plant Cell Rep 15: 305-310
8. Chen J-G, Pandey S, Huang J, Alonso JM, Ecker JR, Assmann SM, Jones AM (2004) GCR1 can act independently of heterotrimeric G-protein in response to brassinosteroids and gibberellins in Arabidopsis seed germination. Plant Physiol 135: 907-915
9. Cook DR (2004) Unravelling the mystery of Nod factor signaling by a genomic approach in Medicago truncatula. Proc Natl Acad Sci USA 101: 4339-4340
10. Cullimore J, Dénarié J (2003) How legumes select their sweet talking symbionts. Science 302: 575-578
11. Demont-Caulet N, Maillet F, Tailler D, Jacquinet JC, Promé JC, Nicolaou KC, Truchet G, Beau JM, Dénarié J (1999) Nodule-inducing activity of synthetic Sinorhizobium meliloti nodulation factors and related lipochito-oligosaccharides on alfalfa. Importance of the acyl chain structure. Plant Physiol 120: 83-92
12. den Hartog M, Musgrave A, Munnik T (2001) Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J 25: 55-65
13. den Hartog M, Verhoef N, Munnik T (2003) Nod factors and elicitors activate different phospholipid signalling pathways in suspension-cultured alfalfa cells. Plant Physiol 132: 311-317
14. de Ruijter NCA, Bisseling T, Emons AMC (1999) Rhizobium Nod factors induce an increase in sub-apical fine bundles of actin filaments in Vicia sativa root hairs within minutes. Mol Plant Microbe Interact 12: 829-832
15. de Ruijter NCA, Rook MB, Bisseling T, Emons AMC (1998) Lipochito-oligosaccharides re-initiate root hair tip growth in Vicia sativa with high calcium and spectrin-like antigen at the tip. Plant J 13: 341-350
16. Dhonukshe P, Laxalt AM, Goedhart J, Gadella TW, Munnik T (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15: 2666-2679
17. Ehrhardt DW, Atkinson EM, Long SR (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256: 998-1000
18. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673-681
19. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966
20. Engstrom EM, Ehrhardt DW, Mitra RM, Long SR (2002) Pharmacological analysis of Nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol 128: 1390-1401
21. Esseling JJ, Lhuissier FG, Emons AM (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of Nod factor application. Plant Physiol 132: 1982-1988
22. Esseling JJ, Lhuissier FG, Emons AM (2004) A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16: 933-944
23. Felle HH, Kondorosi E, Kondorosi A, Schultze M (1995) Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant J 7: 939-947
24. Felle HH, Kondorosi E, Kondorosi A, Schultze M (1998) The role of ion fluxes in Nod factor signalling in Medicago sativa. Plant J 13: 455-463
25. 2+] is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol 121: 273-279
26. Geurts R, Bisseling T (2002) Rhizobium Nod factor perception and signalling. Plant Cell 14(Suppl): S239-S249
27. Harris JM, Wais K, Long SR (2003) Rhizobium-induced calcium spiking in Lotus japonicus. Mol Plant Microbe Interact 16: 335-341
28. o by mastoparan, related amphiphilic peptides, and hydrophobic amines. Mechanism and structural determinants of activity. J Biol Chem 265: 14176-14186
29. Higashijima T, Uzu S, Nakajima T, Ross EM (1988) Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J Biol Chem 263: 6491-6494
30. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14: 737-748
31. Journet EP, Pichon M, Dedieu A, de Billy F, Truchet G, Barker DG (1994) Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J 6: 241-249
32. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364
33. 2+ pump, ECA1, from the endoplasmic reticulum is inhibited by cyclopiazonic acid but not by thapsigargin. Plant Physiol 118: 817-825
34. 2+ entry channels. J Biol Chem 276: 18888-18896
35. Madsen EB, Madsen LH, 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
36. Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54: 265-306
37. Miles GP, Samuel MA, Jones AM, Ellis BE (2004) Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins. Plant Physiol 134: 1332-1336
38. 2+ /calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101: 4701-4705
39. Mueller-Roeber B, Pical C (2002) Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol 130: 22-46
40. Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6: 227-233
41. Munnik T, Arisz SA, de Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7: 2197-2210
42. 2-dependent phospholipase D activity is regulated by phosphorylation. FEBS Lett 554: 50-54
43. Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5: 566-576
44. Oldroyd GED, Mitra RM, Wais RJ, Long SR (2001) Evidence for structurally specific negative feedback in the Nod factor signal transduction pathway. Plant J 28: 191-199
45. Pandey S, Assmann SM (2004) The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein α subunit GPA1 and regulates abscisic acid. Plant Cell 16: 1616-1632
46. Pichon M, Journet EP, Dedieu A, de Billy F, Truchet G, Barker DG (1992) Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4: 1199-1211
47. Pingret JL, Journet EP, Barker DG (1998) Rhizobium Nod factor signaling: evidence for a G protein-mediated transduction mechanism. Plant Cell 10: 659-671
48. Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDζ 1 with distinct regulatory domains. Plant Physiol 128: 1057-1068
49. Radutoiu S, Madsen LH, Madsen EB, Felle HH, 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
50. Ross EM, Higashijima T (1994) Regulation of G-protein activation by mastoparans and other cationic peptides. Methods Enzymol 237: 26-37
51. Sagan M, de Larambergue H, Morandi D (1998) Genetic analysis of symbiosis mutants in Medicago truncatula. In C Elmerich, A Kondorosi, WE Newton, eds, Biological Nitrogen Fixation for the 21st Century, Vol 31. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 317-318
52. Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after γ-ray mutagenesis. Plant Sci 111: 63-71
53. 2+ from vacuolar membrane vesicles of oat roots. J Biol Chem 262: 3944-3946
54. Shaw SL, Long SR (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 131: 976-984
55. Szabados L, Charrier B, Kondorosi A, de Bruijn FJ, Ratet P (1995) New plant promoter and enhancer testing vectors. Mol Breed 1: 419-423
56. 2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol 51: 433-162
57. Thoquet P, Ghérardi M, Journet EP, Kereszt A, Ané JM, Prosperi JM, Huguet T (2002) The molecular genetic linkage map of the model legume M. truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biol 2: 1
58. Vernoud V, Journet E-P, Barker DG (1999a) MtENOD20, a Nod factor-inducible molecular marker for root cortical cell activation. Mol Plant Microbe Interact 12: 604-614
59. - mutants TR25/26. In PJGM De Wit, T Bisseling, WJ Stiekema, eds, Proceedings of the Ninth International Congress on Molecular Plant-Microbe Interactions. ISMPMI, St. Paul, pp 114-119
60. Wais RJ, Galera C, Oldroyd G, Catoira R, Penmetsa RV, Cook D, Gough C, Dénarié J, Long SR (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proc Natl Acad Sci USA 97: 13407-13412
61. Walker SA, Viprey V, Downie JA (2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. Proc Natl Acad Sci USA 97: 13413-13418
62. Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proc Natl Acad Sci USA 101: 9508-9513
63. Zhao J, Wang X (2004) Arabidopsis phospholipase Dα1 interacts with the heterotrimeric G-protein α-subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem 279: 1794-1800