Nodulation gene mutants of Mesorhizobium loti R7A - nodZand nolL mutants have host-specific phenotypes on Lotus spp

Molecular Plant-Microbe Interactions

Volumn 22, Issue 12, 2009, Pages 1546-1554

  Rodpothong, Patsarin ^a,b   Sullivan, John T ^a,b   Songsrirote, Kriangsak ^c   Sumpton, David ^c   Cheung, Kenneth W J T ^c   Thomas Oates, Jane ^c   Radutoiu, Simona ^b   Stougaard, Jens ^b   Ronson, Clive W ^a,b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FUCOSYLTRANSFERASE; NODZ PROTEIN, BACTERIA; NOIL PROTEIN, RHIZOBIUM ETLI;

ALPHAPROTEOBACTERIA; ARTICLE; GENETICS; HOST PATHOGEN INTERACTION; LOTUS; METABOLISM; MICROBIOLOGY; MUTATION; NODULATION; PHENOTYPE; PHYSIOLOGY;

ALPHAPROTEOBACTERIA; BACTERIAL PROTEINS; FUCOSYLTRANSFERASES; HOST-PATHOGEN INTERACTIONS; LOTUS; MUTATION; PHENOTYPE; PLANT ROOT NODULATION;

BACTERIA (MICROORGANISMS); LOTUS CORNICULATUS; LOTUS FILICAULIS; MESORHIZOBIUM; MESORHIZOBIUM LOTI;

EID: 72949118962     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-22-12-1546     Document Type: Article

References (56)

1. Amor, B. B., Shaw, S. L., Oldroyd, G. E., Maillet, F., Penmetsa, R. V., Cook, D., Long, S. R., Denarie, J., and 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.
2. Ardourel, M., Demont, N., Debellé, F., Maillet, F., de Billy, F., Promé, J., Déarié, J., and Truchet, G. 1994. Rhizobium meliloti lipooligosaccha- ride nodulation factors: Different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic development responses. Plant Cell 6:1357-1374.
3. Berck, S., Perret, X., Quesada-Vincens, D., Promé, J. C., Broughton, W. J., and Jabbouri, S. 1999. NolL of Rhizobium sp. strain NGR234 is required for O-acetyltransferase activity. J. Bacteriol. 181:957-964.
4. Cheng, H. P., and Walker, G. C. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 180:5183-91.
5. Corvera, A., Promé, D., Promé, J. C., Martínez- Romero, E., and Romero, D. 1999. The nolL gene from Rhizobium etli determines nodulation efficiency by mediating the acetylation of the fucosyl residue in the nodulation factor. Mol. Plant-Microbe Interact. 13:236-246.
6. Dombrecht, B., Vanderleyden, J., and Michiels, J. 2001. Stable RK2-derived cloning vectors for the analysis of gene expression and gene function in gram-negative bacteria. Mol. Plant-Microbe Interact. 14:426-430.
7. Downie, J. A., and Surin, B. P. 1990. Either of two nod gene loci can complement the nodulation defect of a nod deletion mutant of Rhizobium leguminosarum biovar viciae. Mol. Gen. Genet. 222:81-86.
8. Fisher, R. F., and Long, S. R. 1993. Interaction of NodD at the nod box: NodD binds to two distinct sites on the same face of the helix and induces a bend in the DNA. J. Mol. Biol. 233:336-348.
9. Geurts, R., Fedorova, E., and Bisseling, T. 2005. Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 8:346-352.
10. Hayashi, M., Miyahara, A., Sato, S., Kato, T., Yoshikawa, M., Taketa, M., Hayashi, M., Pedrosa, A., Onda, R., Imaizumi-Anraku, H., Bachmair, A., Sandal, N., Stougaard, J., Murooka, Y., Tabata, S., Kawasaki, S., Kawaguchi, M., and Harada, K. 2001. Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. DNA Res. 8:301-310.
11. Herrero, M., de Lorenzo, V., and Timmis, K. N. 1990. Transposon vectors containing stable non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J. Bacteriol. 172:6557-6567.
12. Hotter, G. S., and Scott, D. B. 1991. Exopolysaccharide mutants of Rhizo-bium loti are fully effective on a determinate nodulating host but are ineffective on an indeterminate nodulating host. J. Bacteriol. 173:851-859.
13. Hubber, A., Vergunst, A. C., Sullivan, J. T., Hooykaas, P. J. J., and Ronson, C. W. 2004. Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol. Microbiol. 54:561-574.
14. Hubber, A., Sullivan, J. T., and Ronson, C. W. 2007. Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 type IV secretion system. Mol. Plant-Microbe Interact. 20:255-261.
15. John, M., Rohrig, H., Schmidt, J., Wieneke, U., and Schell, J. 1993. Rhizo-bium NodB protein involved in nodulation signal synthesis is a chitooli-gosaccharide deacetylase. Proc. Natl. Acad. Sci. U.S.A. 90:625-629.
16. Kawaguchi, M., Pedrosa, A., Yano, K., Hayashi, M., Murooka, Y., Saito, K., Nagata, T., Namai, K., Nishida, H., Shibata, D., Sato, S., Tabata, S., Hayashi, M., Harada, K., Sandal, N., Stougaard, J., Bachmair, A., and Grant, W. F. 2005. Lotus burttii takes a position of the third corner in the Lotus molecular genetics triangle. DNA Res. 12:69-77.
17. Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., and Geurts, R. 2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630-633.
18. López-Lara, I. M., van den Berg, J. D. J., Thomas-Oates, J. E., Glushka, J., Lugtenberg, B. J., and Spaink, H. P. 1995. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol. Microbiol. 15:627-638.
19. López-Lara, I. M., Blok-Tip, L., Quinto, C., Garcia, M. L., Stacey, G., Bloemberg, G. V., Lamers, G. E. M., Lugtenberg, B. J. J., Thomas- Oates, J. E., and Spaink, H. P. 1996. NodZ of Bradyrhizobium extends the nodulation host range of Rhizobium by adding a fucosyl residue to nodulation signals. Mol. Microbiol. 21:397-408.
20. Madsen, E. B., Madsen, L. H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., Sato, S., Kaneko, T., Tabata, S., Sandal, N., and Stougaard, J. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637-640.
21. Marsh, J. F., Rakocevic, A., Mitra, R. M., Brocard, L., Sun, J., Eschstruth, A., Long, S. R., Schultze, M., Ratet, P., and Oldroyd, G. E. 2007. Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol. 144:324-335.
22. Mergaert, P., D'Haeze, W., Fernandez-López, M., Geelen, D., Goethals, K., Promé, J. C., Van Montagu, M., and Holsters, M. 1996. Fucosylation and arabinosylation of Nod factors in Azorhizobium caulinodans: Involvement of nolK, nodZ as well as noeC and/or downstream genes. Mol. Microbiol. 21:409-419.
23. Miller, W. G., Leveau, J. H., and Lindow, S. E. 2000. Improved gfp and inaZ broad-host-range promoter-probe vectors. Mol. Plant-Microbe Interact. 13:1243-1250.
24. Niwa, S., Kawaguchi, M., Imazumi-Anraku, H., Chechetka, S. A., Ishizaka, M., Ikuta, A., and Kouchi, H. 2001. Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. Mol. Plant-Microbe Interact. 14:848-856.
25. Oldroyd, G. E., and Downie, J. A. 2004. Calcium, kinases and nodulation signaling in legumes. Nature Rev. Mol. Cell Biol. 5:566-576.
26. Oldroyd, G. E., and Downie, J. A. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59:519-546.
27. Oldroyd, G. E., Mitra, R. M., Wais, R., and Long, S. R. 2001. Evidence for structurally specific negative feedback in the Nod factor signal trans-duction pathway. Plant J. 28:191-199.
28. Olsthoorn, M. M., López-Lara, I. M., Petersen, B. O., Bock, K., Haverkamp, J., Spaink, H. P., and Thomas-Oates, J. E. 1998. Novel branched Nod factor structure results from alpha-(1→3) fucosyl transferase activity: The major lipo-chitin oligosaccharides from Mesorhizobium loti strain NZP2213 bear an alpha-(1→3) fucosyl substituent on a nonterminal backbone residue. Biochemistry 37:9024-9032.
29. Olsthoorn, M. M., Stokvis, E., Haverkamp, J., Spaink, H. P., and Thomas-Oates, J. E. 2000. Growth temperature regulation of host-specific modifications of rhizobial lipo-chitin oligosaccharides: The function of nodX is temperature regulated. Mol. Plant-Microbe Interact. 13:808-820.
30. Pacios-Bras, C., Jordá, M. A., Wijfjes, A. H. M., Harteveld, M., Stuurman, N., Thomas-Oates, J. E., and Spaink, H. P. 2000. A Lotus japonicus nodulation system based on heterologous expression of the fucosyl transferase NodZ and the acetyl transferase NolL in Rhizobium legumi-nosarum. Mol. Plant-Microbe Interact. 13:475-479.
31. Pellock, B. J., Cheng, H. P., and Walker, G. C. 2000. Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccha- rides. J. Bacteriol. 182:4310-4318.
32. Quandt, J., and Hynes, F. M. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127:15-21.
33. Quesada-Vincens, D., Fellay, R., Nasim, T., Viprey, V., Burger, U., Promé, J. C., Broughton, W. J., and Jabbouri, S. 1997. Rhizobium sp. strain NGR234 NodZ protein is a fucosyltransferase. J. Bacteriol. 179:5087-5093.
34. Radutoiu, S., Madsen, L. H., Madsen, E. B., Felle, H. H., Umehara, Y., Gronlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., and Stougaard, J. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585-592.
35. Radutoiu, S., Madsen, L. H., Madsen, E. B., Jurkiewicz, A., Fukai, E., Quistgaard, M. M., Albrektsen, A. S., James, E. K., Thirup, S., and Stougaard, J. 2007. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO (Eur. Mol. Biol. Organ.) J. 26:3923-3935.
36. Ramsay, J. P., Sullivan, J. T., Stuart, G. S., Lamont, I. L., and Ronson, C. W. 2006. Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol. Microbiol. 62:723-734.
37. Riely, B. K., Mun, J. H., and Ané, J. M. 2006. Unraveling the molecular basis for symbiotic signal transduction in legumes. Mol. Plant Pathol. 7:197-207.
38. Rostas, K., Kondorosi, E., Horvath, B., Simoncsits, A., and Kondorosi, A. 1986. Conservation of extended promoter regions of nodulation genes in Rhizobium. Proc. Natl. Acad. Sci. U.S.A. 83.
39. Sandal, N., Petersen, T. R., Murray, J., Umehara, Y., Karas, B., Yano, K., Kumagai, H., Yoshikawa, M., Saito, K., Hayashi, M., Murakami, Y., Wang, X., Hakoyama, T., Imaizumi-Anraku, H., Sato, S., Kato, T., Chen, W., Hossain, M. S., Shibata, S., Wang, T. L., Yokota, K., Larsen, K., Kanamori, N., Madsen, E. B., Radutoiu, S., Madsen, L. H., Radu, T. G., Krusell, L., Ooki, Y., Banba, M., Betti, M., Rispail, N., Sk0t, L., Tuck, E., Perry, J., Yoshida, S., Vickers, K., Pike, J., Mulder, L., Charpentier, M., Müller, J., Ohtomo, R., Kojima, T., Ando, S., Marquez, A. J., Gresshoff, P. M., Harada, K., Webb, J., Hata, S., Suganuma, N., Kouchi, H., Kawasaki, S., Tabata, S., Hayashi, M., Parniske, M., Szczyglowski, K., Kawaguchi, M., and Stougaard, J. 2006. Genetics of symbiosis in Lotus japonicus: Recombinant inbred lines, comparative genetic maps, and map position of 35 symbiotic loci. Mol. Plant-Microbe Interact. 19:80-91.
40. Scott, D. B., Young, C. A., Collins-Emerson, J. M., Terzaghi, E. A., Rockman, E. S., Lewis, P. E., and Pankhurst, C. E. 1996. Novel and complex chromosomal arrangement of Rhizobium loti nodulation genes. Mol. Plant-Microbe Interact. 9:187-197.
41. Shibata, S., Mitsui, H., and Kouchi, H. 2005. Acetylation of fucosyl residue at the reducing end of Mesorhizobium loti Nod factors is not essential for nodulation of Lotus japonicus. Plant Cell Physiol. 46:1017-1020.
42. Smit, P., Limpens, E., Geurts, R., Fedorova, E., Dolgikh, E., Gough, C., and Bisseling, T. 2007. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 145:183-191.
43. Soria-Díaz, M. E., Tejero-Mateo, P., Espartero, J. L., Rodriguez-Carvajal, M. A., Moron, B., Sousa, C., Megias, M., Amarger, N., Thomas-Oates, J. E., and Gil-Serrano, A. M. 2003. Structural determination of the lipochitin oligosaccharide nodulation signals produced by Rhizobium giardinii bv. giardinii H152. Carbohydr. Res. 338:237-250.
44. Spaink, H. P. 2000. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54:257-288.
45. Spaink, H. P., Okker, R. J., Wijffelman, C. A., Tak, T., Goosen-de Roo, L., Pees, E., van Brussel, A. A., and Lugtenberg, B. J. 1989. Symbiotic properties of rhizobia containing a flavonoid-independent hybrid nodD product. J. Bacteriol. 171:4045-4053.
46. Sullivan, J. T., and Ronson, C. W. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci. U.S.A. 95:5145-5149.
47. Sullivan, J. T., Patrick, H. N., Lowther, W. L., Scott, D. B., and Ronson, C. W. 1995. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc. Natl. Acad. Sci. U.S.A. 92:8985-8989.
48. Sullivan, J. T., Brown, S. D., Yocum, R. R., and Ronson, C. W. 2001. The bio operon on the acquired symbiosis island of Mesorhizobium sp. strain R7A includes a novel gene involved in pimeloyl-CoA synthesis. Microbiology 147:1315-1322.
49. Sullivan, J. T., Trzebiatowski, J. R., Cruickshank, R. W., Gouzy, J., Brown,
50. S. D., Elliott, R. M., Fleetwood, D. J., McCallum, N. G., Rossbach, U., Stuart, G. S., Weaver, J. E., Webby, R. J., de Bruijn, F. J., and Ronson, C. W. 2002. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J. Bacteriol. 184:3086-3095.
51. Szczyglowski, K., Shaw, R. S., Wopereis, J., Copeland, S., Hamburger, D., Kasiborski, B., Dazzo, F. B., and de Bruijn, F. J. 1998. Nodule organo-genesis and symbiotic mutants of the model legume Lotus japonicus. Mol. Plant-Microbe Interact. 11:684-697.
52. van Brussel, A. A., Planqú, K., and Quispel, A. 1977. The wall of Rhizobium leguminosarum in bacteroid and free-living forms. J. Gen. Micro- biol. 101:51-56.
53. Vincent, J. M. 1970. A Manual for the Practical Study of Root Nodule Bacteria. Blackwell Scientific Publications, Oxford.
54. Wais, R. J., Keating, D. H., and Long, S. R. 2002. Structure-function analysis of Nod factor-induced root hair calcium spiking in rhizobium- legume symbiosis. Plant Physiol. 129:211-224.
55. Walker, S. A., and Downie, J. A. 2000. Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal Nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Mol. PlantMicrobe Interact. 13:754-762.
56. Wernegreen, J. J., and Riley, M. A. 1999. Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: A case for the genetic coherence of rhizobial lineages. Mol. Biol. Evol. 16:98-113.