Nod factors induce Nod factor cleaving enzymes in pea roots. Genetic and pharmacological approaches indicate different activation mechanisms

Plant Physiology

Volumn 139, Issue 2, 2005, Pages 1051-1064

  Ovtsyna, Alexandra O ^a   Dolgikh, Elena A ^a   Kilanova, Alexandra S ^b   Tsyganov, Viktor E ^a   Borisov, Alexey Y ^a   Tikhonovich, Igor A ^a   Staehelin, Christian ^c  

^a ALL RUSSIA RESEARCH INSTITUTE FOR AGRICULTURAL MICROBIOLOGY   (Russian Federation)

^b ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; MUTAGENESIS; PLANTS (BOTANY); POLYSACCHARIDES;

MUTANTS; NOD FACTORS (NFS); SIGNAL TRANSDUCTION;

ENZYMES;

ENZYMES; PLANTS;

BACTERIA (MICROORGANISMS); PISUM SATIVUM; RHIZOBIACEAE; RHIZOBIUM LEGUMINOSARUM; SINORHIZOBIUM MELILOTI;

CHITINASE; HYDROLASE; LIPID LINKED OLIGOSACCHARIDES; LIPID-LINKED OLIGOSACCHARIDES; LIPOPOLYSACCHARIDE; NOD FACTOR IV, RHIZOBIUM MELILOTI;

ARTICLE; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENE; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PEA; PLANT ROOT; RHIZOBIUM LEGUMINOSARUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

CHITINASE; ENZYME ACTIVATION; GENES, PLANT; HYDROLASES; LIPOPOLYSACCHARIDES; MUTATION; PEAS; PLANT ROOTS; RHIZOBIUM LEGUMINOSARUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 33644653446     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.061705     Document Type: Article

References (76)

1. Albrecht C, Geurts R, Lapeyrie F, Bisseling T (1998) Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J 15: 605-614
2. Ane 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
3. Blauenfeldt J, Joshi PA, Gresshoff PM, Caetano-Anollés G (1994) Nodulation of white clover (Trifolium repens) in the absence of Rhizobium. Protoplasma 179: 106-110
4. Borisov AY, Barmicheva EM, Jacobi LM, Tsyganov VE, Voroshilova VA, Tikhonovich IA (2000) Pea (Pisum sativum L.) mendelian genes controlling development of nitrogen-fixing nodules and arbuscular mycorrhiza. Czech J Genet Plant Breed 36: 106-110
5. Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, Batagov AO, Sandal N, Mortensen A, Schauser L, Ellis N, Tikhonovich IA, Stougaard J (2003) The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol 131: 1009-1017
6. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 243-254
7. Catford JG, Staehelin C, Lérat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54: 1481-1487
8. 2+ spiking and specific ENOD gene expression. Plant Physiol 136: 3582-3593
9. Dassi B, Dumas-Gaudot E, Asselin A, Richard C, Gianinazzi S (1996) Chitinase and β-1,3-glucanse isoforms expressed in pea roots inoculated with arbuscular mycorrhizal or pathogenic fungi. Eur J Plant Pathol 102: 105-108
10. Davis BJ (1964) Disc electrophoresis. II. Method and application to human serum proteins. Ann N Y Acad Sci 121: 404-427
11. 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
12. Duc G, Messager A (1989) Mutagenesis of pea (Pisum sativum L.) and the isolation of mutants for nodulation and nitrogen fixation. Plant Sci 60: 207-213
13. Dumas-Gaudot E, Asselin A, Gianinazzi-Pearson V, Gollotte A, Gianinazzi S (1994) Chitinase isoforms in roots of various pea genotypes infected with arbuscular mycorrhizal fungi. Plant Sci 99: 27-37
14. Duodu S, Bhuvaneswari TV, Stokkermans TJW, Peters NK (1999) A positive role for rhizobitoxine in Rhizobium-legume symbiosis. Mol Plant Microbe Interact 12: 1082-1089
15. Ehrhardt DW, Atkinson EM, Long SR (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256: 998-1000
16. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 88: 673-681
17. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss G (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966
18. 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
19. Engvild J (1987) Modulation and nitrogen fixation mutants of pea (Pisum sativum). Theor Appl Genet 74: 711-713
20. 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 lipochitooligusaccharide. Plant J 7: 939-947
21. 2+ is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiol 121: 273-280
22. Felle HH, Kondorosi E, Kondorosi A, Schultze M (2000) How alfalfa root hairs discriminate between Nod factors and oligochitin elicitors. Plant Physiol 124: 1373-1380
23. Felix G, Regenass M, Spanu P, Boller T (1994) The protein phosphatase inhibitor calyculin A mimics elicitor action in plant cells and induces rapid hyperphosphorylation of specific proteins as revealed by pulse labeling with [33P] phosphate. Proc Natl Acad Sci USA 91: 952-956
24. Goormachtig S, Lievens S, Van de Velde W, Van Montagu M, Holsters M (1998) Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. Plant Cell 10: 905-915
25. Guinel FC, Geil RD (2002) A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses. Can J Bot 80: 695-720
26. He C-Y, Zhang J-S, Chen S-Y (2002) A soybean gene encoding a proline-rich protein is regulated by salicylic acid, an endogenous circadian rhythm and by various stresses. Theor Appl Genet 104: 1125-1131
27. Heidstra R, Geurts R, Franssen H, Spaink HP, van Kammen A, Bisseling T (1994) Root hair deformation activity of nodulation factors and their fate on Vicia sativa. Plant Physiol 105: 787-797
28. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, et al (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433: 527-531
29. Kelly MN, Irving HR (2001) Nod factors stimulate plasma membrane delimited phospholipase C activity in vitro. Physiol Plant 113: 461-468
30. Kelly MN, Irving HR (2003) Nod factors activate both heterotrimeric and monomeric G-proteins in Vigna unguiculata (L.) Walp. Planta 216: 674-685
31. Kneen BE, LaRue TA (1984) Nodulation resistant mutant of Pisum sativum (L.). J Hered 75: 238-240
32. Kneen BE, LaRue TA, Hirsch AM, Smith CA, Weeden NF (1990) sym13-a gene conditioning ineffective nodulation in Pisum sativum. Plant Physiol 94: 899-905
33. Kneen BE, Weeden NF, LaRue TA (1994) Non-nodulating mutants of Pisum sativum (L.) cv. Sparkle. J Hered 85: 129-133
34. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, et al (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420: 422-426
35. Lee KH, LaRue TA (1992) Pleiotropic effects of sym-17. A mutation in Pisum sativum L. cv Sparkle causes decreased nodulation, altered root and shoot growth, and increased ethylene production. Plant Physiol 100: 1326-1333
36. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364
37. 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: 630-633
38. 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: 637-640
39. Markwei CP, LaRue TA (1992) Phenotypic characterization of sym8 and sym9 genes conditioning non-nodulation in Pisum sativum "Sparkle". Can J Microbiol 38: 543-554
40. Michaud D, Asselin A (1995) Application to plant proteins of gel electrophoretic methods. J Chromatogr A 698: 263-279
41. Minic Z, Brown S, De Kouchkovsky Y, Schultze M, Staehelin C (1998) Purification and characterization of a novel chitinase-lysozyme, of another chitinase, both hydrolysing Rhizobium meliloti Nod factors, and of a pathogenesis-related protein from Medicago sativa roots. Biochem J 332: 329-335
42. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101: 4701-4705
43. Nishimura R, Hayashi M, Wu G-J, 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: 426-429
44. Novak K, Lisa L, Skrdleta V (2004) Rhizobial nod gene-inducing activity in pea nodulation mutants: dissociation of nodulation and flavonoid response. Physiol Plant 120: 546-555
45. Novak K, Skrdleta V, Kropacova M, Lisa L, Nemcova M (1997) Interaction of two genes controlling symbiotic nodule number in pea (Pisum sativum L.). Symbiosis 23: 43-62
46. Oldroyd GED, Engstrom EM, Long SR (2001) Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell 13: 1835-1849
47. Ovtsyna AO, Schultze M, Tikhonovich IA, Spaink HP, Kondorosi E, Kondorosi A, Staehelin C (2000) Nod factors of Rhizobium leguminosarum bv. viciae and their fucosylated derivatives stimulate a Nod factor cleaving activity in pea roots and are hydrolyzed in vitro by plant chitinases at different rates. Mol Plant Microbe Interact 13: 799-807
48. Ovtsyna AO, Staehelin C (2003) Bacterial signals required for the Rhizobium-legume symbiosis. In SG Pandalai, ed, Recent Research Developments in Microbiology, Vol 7 (Part II). Research Signpost, Trivandrum, India, pp 631-648
49. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201
50. Pingret JL, Journet EP, Barker DG (1998) Rhizobium Nod factor signaling. Evidence for a G-protein-mediated transduction mechanism. Plant Cell 10: 659-672
51. 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: 585-592
52. Safronova VI, Novikova NI (1996) Comparison of two methods for root nodule bacteria preservation: lyophilization and liquid nitrogen freezing. J Microbiol Methods 24: 231-237
53. Sagan M, Duc C (1996) Sym28 and sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20: 229-245
54. Sagan M, Huguet T, Duc G (1994) Phenotypic characterization and classification of nodulation mutants of pea (Pisum sativum L.). Plant Sci 100: 59-70
55. Salzer P, Feddermann N, Wiemken A, Boller T, Staehelin C (2004) Sinorhizobium melilotti-induced chitinase gene expression in Medicago truncatula ecotype R108-1: a comparison between symbiosis-specific class V and defence-related class IV chitinases. Planta 219: 626-638
56. Schneider A, Walker SA, Sagan M, Duc G, Ellis THN, Downie JA (2002) Mapping of the nodulation loci sym9 and sym10 of pea (Pisum sativum L.). Theor Appl Genet 104: 1312-1316
57. Schultze M, Quiclet-Sire B, Kondorosi E, Virelizier H, Glushka JN, Endre G, Gero SD, Kondorosi A (1992) Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity. Proc Natl Acad Sci USA 89: 192-196
58. Schultze M, Staehelin C, Brunner F, Genetet I, Legrand M, Fritig B, Kondorosi E, Kondorosi A (1998) Plant chitinase/lysozyme isoforms show distinct substrate specificity and cleavage site preference towards lipochitooligosaccharide Nod signals. Plant J 16: 571-580
59. 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: 109-112
60. Spaink HP, Sheeley DM, Van Brussel AAN, Glushka J, York WS, Tak T, Geiger O, Kennedy EP, Reinhold VN, Lugtenberg BJJ (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354: 125-130
61. +) and ineffective (fix) soybean nodules. Planta 187: 295-300
62. Staehelin C, Schultze M, Kondorosi E, Kondorosi A (1995) Lipochitooligosaccharide nodulation signals from Rhizobium meliloti induce their rapid degradation by the host plant alfalfa. Plant Physiol 108: 1607-1614
63. Staehelin C, Schultze M, Kondorosi E, Mellor RB, Boller T, Kondorosi A (1994) Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J 5: 319-330
64. Staehelin C, Schultze M, Tokuyasu K, Poinsot V, Promé JC, Kondorosi E, Kondorosi A (2000) N-deacetylation of Sinorhizobium meliloti Nod factors increases their stability in the Medicago sativa rhizosphere and decreases their biological activity. Mol Plant Microbe Interact 13: 72-79
65. Staehelin C, Vanney M, Foucher F, Kondorosi E, Schultze M, Kondorosi A (1997) Degradation of nodulation signals from Rhizobium meliloti by its host plants. In A Legocki, H Bothe, A Pühler, eds, Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture. Springer, Berlin, pp 43-46
66. 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: 959-962
67. Truchet G, Barker DG, Camut S, de Billy F, Vasse J, Huguet T (1989) Alfalfa nodulation in the absence of Rhizobium. Mol Gen Genet 219: 65-68
68. Trudel J, Asselin A (1989) Detection of chitinase activity after polyacrylamide gel electrophoresis. Anal Biochem 178: 362-366
69. Tsyganov VE, Voroshilova VA, Priefer UB, Borisv AY, Tikhonovich IA (2002) Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium-pea (Pisum sativum L.) symbiosis. Ann Bot (Lond) 89: 357-366
70. van Brussel AAN, Planque K, Quispel A (1977) The wall of Rhizobium leguminosarum in bacteroid and free-living forms. J Gen Microbiol 101: 51-56
71. van Brussel AAN, Tak T, Boot KJM, Kijne JW (2002) Autoregulation of root nodule formation: signals of both symbiotic partners studied in a split-root system of Vicia sativa. subsp. nigra. Mol Plant Microbe Interact 15: 341-349
72. van Brussel AAN, Tak T, Wetselaar A, Pees E, Wijffelman CA (1982) Small Leguminosae as test plants for nodulation of Rhizobium leguminosarum and other rhizobia and agrobacteria harbouring a leguminosarum Sym plasmid. Plant Sci Lett 27: 317-325
73. Vasse J, De Billy F, Truchet G (1993) Abortion of infection during the Rhizobium mileloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J 4: 555-566
74. 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
75. Wijffelman CA, Pees E, van Brussel AAN, Okker RJH, Lugtenberg BJJ (1985) Genetic and functional analysis of the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Arch Microbiol 143: 225-232
76. Xie ZP, Staehelin C, Wiemken A, Broughton WJ, Müller J, Boller T (1999) Symbiosis-stimulated chitinase isoenzymes of soybean (Glycine max (L.) Merr.). J Exp Bot 50: 327-333