Nonlegume Parasponia andersonii deploys a broad rhizobium host range strategy resulting in largely variable symbiotic effectiveness

Molecular Plant-Microbe Interactions

Volumn 25, Issue 7, 2012, Pages 954-963

  Den Camp, Rik H M Op ^a   Polone, Elisa ^a,b   Fedorova, Elena ^a   Roelofsen, Wim ^a   Squartini, Andrea ^b   Den Camp, Huub J M Op ^c   Bisseling, Ton ^a,d   Geurts, René ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF PADOVA   (Italy)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; CANNABACEAE; CELL DEATH; CHEMISTRY; DNA SEQUENCE; FABACEAE; GENETICS; HOST RANGE; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NITROGEN FIXATION; NODULATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PROTEOBACTERIA; RHIZOBIUM TROPICI; SINORHIZOBIUM; SYMBIOSIS; ULTRASTRUCTURE;

BASE SEQUENCE; CANNABACEAE; CELL DEATH; FABACEAE; GENES, BACTERIAL; GENOME, BACTERIAL; HOST SPECIFICITY; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; PHYLOGENY; PLANT ROOT NODULATION; PROTEOBACTERIA; RHIZOBIUM TROPICI; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; ROOT NODULES, PLANT; SEQUENCE ANALYSIS, DNA; SINORHIZOBIUM; SYMBIOSIS;

PARASPONIA; PARASPONIA ANDERSONII; RHIZOBIACEAE; RHIZOBIUM; RHIZOBIUM SP. ANU289; RHIZOBIUM TROPICI;

EID: 84863314775     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-11-11-0304     Document Type: Article

References (75)

1. Ardourel, M., Demont, N., Debelle, F., Maillet, F., de Billy, F., Prome, J. C., Denarie, J., and Truchet, G. 1994. 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 6:1357-1374. (Pubitemid 24976493)
2. Arrighi, J. F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L. C., Mirabella, R., de Carvalho-Niebel, F., Journet, E. P., Gherardi, M., Huguet, T., Geurts, R., Denarie, J., Rouge, P., and Gough, C. 2006. The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142:265-279. (Pubitemid 44412246)
3. Becking, J. H. 1983. The Parasponia parviflora-Rhizobium symbiosis-host specificity, growth and nitrogen-fixation under various conditions. Plant Soil 75:309-342.
4. Becking, J. H. 1992. The rhizobium symbiosis of the nonlegume Parasponia. Pages 497-559 in: Biological Nitrogen Fixation. G. Stacey, R. H. Burris, and H. J. Evans, eds. Chapman and Hall, New York.
5. Bergersen, F. 1970. The quantitative relationship between nitrogen fixation and the acetylene-reduction assay. Aust. J. Biol. Sci. 23:1015-1026.
6. Bloemberg, G. V., Thomas-Oates, J. E., Lugtenberg, B. J., Spaink, H. P. 1994. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Mol Microbiol. 4:793-804.
7. Boogerd, F. C., and van Rossum, D. 1997. Nodulation of groundnut by Bradyrhizobium: A simple infection process by crack entry. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 21:5-27. (Pubitemid 27376756)
8. Capoen, W., Goormachtig, S., and Holsters, M. 2010. Water-tolerant legume nodulation. J. Exp. Bot. 61:1251-1255.
9. Charpentier, M., and Oldroyd, G. 2010. How close are we to nitrogen-fixing cereals? Curr. Opin. Plant Biol. 13:556-564.
10. Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Marsh, T., Garrity, G. M., and Tiedje, J. M. 2009. The Ribosomal Database Project: Improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-145.
11. Debellé, F., Plazanet, C., Roche, P., Pujol, C., Savagnac, A., Rosenberg, C., Promé, J. C., and Dénarié J. 1996. The NodA proteins of Rhizobium meliloti and Rhizobium tropici specify the N-acylation of Nod factors by different fatty acids. Mol. Microbiol. 22:303-314. (Pubitemid 26352695)
12. Den Herder, G., and Parniske, M. 2009. The unbearable naivety of legumes in symbiosis. Curr. Opin. Plant Biol. 12:491-499.
13. D'Haeze, W., and Holsters, M. 2002. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R-105R.
14. Downie, J. A. 2010. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 34:150-170.
15. Estévez, J., Soria-Díaz, M. E., de Córdoba, F. F., Morón, B., Manyani, H., Gil, A., Thomas-Oates, J., Van Brussel, A. A. N., Dardanelli, M. S., Sousa, C., and Megías, M. 2009. Different and new Nod factors produced by Rhizobium tropici CIAT899 following Na+ stress. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 293:220-231.
16. Fahraeus, G. 1957. The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16:374-381.
17. Folch-Mallol, J. L., Marroqui, S., Sousa, C., Manyani, H., López-Lara, I. M., van der Drift, K. M., Haverkamp, J., Quinto, C., Gil-Serrano, A., Thomas-Oates, J., Spaink, H. P., and Megías, M. 1996. Characterization of Rhizobium tropici CIAT899 nodulation factors: The role of nodH and nodPQ genes in their sulfation. Mol. Plant-Microbe Interact. 9:151-163.
18. Goormachtig, S., Capoen, W., James, E. K., and Holsters, M. 2004. Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proc. Natl. Acad. Sci. U. S. A. 101:6303-6308. (Pubitemid 38520569)
19. Heath, K. D., and Tiffin, P. 2007. Context dependence in the coevolution of plant and rhizobial mutualists. Proc. Biol. Sci. 274:1905-1912. (Pubitemid 47377909)
20. Hirsch, A. M., and Smith, C. A. 1987. Effects of Rhizobium meliloti nif and fix mutants on alfalfa root nodule development. J. Bacteriol. 169:1137-1146. (Pubitemid 17043379)
21. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Mochizuki, Y., Nakayama, S., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeucki, C., Yamada, M., and Tabata, S. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7:331-338.
22. Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Watanabe, A., Idesawa, K., Iriguchi, M., Kawashima, K., Kohara, M., Matsumoto, M., Shimpo, S., Tsuruoka, H., Wada, T., Yamada, M., and Tabata, S. 2002. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9:189-197. (Pubitemid 36307023)
23. Kiers, E. T., Rousseau, R. A., West, S. A., and Denison, R. F. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81. (Pubitemid 37101720)
24. Kouchi, H., Imaizumi-Anraku, H., Hayashi, M., Hakoyama, T., Nakagawa, T., Umehara, Y., Suganuma, N., and Kawaguchi, M. 2010. How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol. 51:1381-1397.
25. Laeremans, T., Caluwaerts, I., Verreth, C., Rogel, M. A., Vanderleyden, J., and Martínez-Romero, E. 1996. Isolation and characterization of Rhizobium tropici Nod factor sulfation genes. Mol. Plant-Microbe Interact. 9:492-500. (Pubitemid 26324264)
26. Lewin, A., Rosenberg, C., Meyer, H. A., A, Z., Wong, C. H., Nelson, L., Manen, J. F., Stanley, J., Dowling, D. N., Denarie, J., and Broughton, W. J. 1987. Multiple host-specificity loci of the broad host-range Rhizobium sp. NGR234 selected using the widely compatible legume Vigna unguiculata. Plant Mol. Biol. 8:447-459.
27. 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. (Pubitemid 37310916)
28. Limpens, E., Ivanov, S., van Esse, W., Voets, G., Fedorova, E., and Bisseling, T. 2009. Medicago N2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell 21:2811-2828.
29. López-Lara, I M., Kafetzopoulos, D., Spaink, H. P., and Thomas-Oates, J. E. 2001. Rhizobial NodL O-acetyl transferase and NodS N-methyl transferase functionally interfere in production of modified Nod factors. J. Bacteriol. 183:3408-3416. (Pubitemid 32454499)
30. Madsen, L. H., Tirichine, L., Jurkiewicz, A., Sullivan, J. T., Heckmann, A. B., Bek, A. S., Ronson, C. W., James, E. K., and Stougaard, J. 2010. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1, article number 10. doi:10.1038/ ncomms1009. Published online.
31. Maillet, F., Poinsot, V., Andre, O., Puech-Pages, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E. A., Driguez, H., Becard, G., and Denarie, J. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58-63.
32. Marchesi, J. R., Sato, T., Weightman, A. J., Martin, T. A., Fry, J. C., Hiom, S. J., Dymock, D., and Wade, W. G. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 64:795-799. (Pubitemid 28079862)
33. Martinez-Romero, E. 2009. Coevolution in rhizobium-legume symbiosis? DNA Cell Biol. 28:361-370.
34. Masson-Boivin, C., Giraud, E., Perret, X., and Batut, J. 2009. Establishing nitrogen-fixing symbiosis with legumes: How many rhizobium recipes? Trends Microbiol. 17:458-466.
35. Mergaert, P., Van Montagu, M., and Holsters, M. 1997. Molecular mechanisms of Nod factor diversity. Mol. Microbiol. 25:811-817. (Pubitemid 27397510)
36. Morón, B., Soria-Díaz, M. E., Ault, J., Verroios, G., Noreen, S., Rodríguez-Navarro, D. N., Gil-Serrano, A., Thomas-Oates, J., Megías, M., and Sousa, C. 2005. Low pH changes the profile of nodulation factors produced by Rhizobium tropici CIAT899. Chem. Biol. 12:1029-1040. (Pubitemid 41338813)
37. Op den Camp, R., Streng, A., De Mita, S., Cao, Q., Polone, E., Liu, W., Ammiraju, J. S., Kudrna, D., Wing, R., Untergasser, A., Bisseling, T., and Geurts, R. 2011 LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia. Science 331:909-912.
38. Osborn, A. M., Moore, E. R., and Timmis, K. N. 2000. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ. Microbiol. 2:39-50. (Pubitemid 33124580)
39. Pajuelo, E., and Stougaard, J. 2005. Lotus japonicus as a model system. Pages 3-24 in: The Lotus japonicus Handbook. A. J. Marquez, ed. Springer, Dordrecht, The Netherlands.
40. Perret, X., Staehelin, C., and Broughton, W. J. 2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64:180-201. (Pubitemid 30143845)
41. Price, N. P., Relic, B., Talmont, F., Lewin, A., Prome, D., Pueppke, S. G., Maillet, F., Denarie, J., Prome, J. C., and Broughton, W. J. 1992. Broadhost-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6:3575-3584. (Pubitemid 23002412)
42. Provorov, N. A., and Vorobyov, N. I. 2008. Equilibrium between the "genuine mutualists" and "symbiotic cheaters" in the bacterial population co-evolving with plants in a facultative symbiosis. Theor. Popul. Biol. 74:345-355.
43. Pueppke, S. G., and Broughton, W. J. 1999. Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant-Microbe Interact. 12:293-318. (Pubitemid 29167304)
44. Puppo, A., Groten, K., Bastian, F., Carzaniga, R., Soussi, M., Lucas, M. M., de Felipe, M. R., Harrison, J., Vanacker, H., and Foyer, C. H. 2005. Legume nodule senescence: Roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol. 165:683-701. (Pubitemid 40284831)
45. 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. (Pubitemid 37280137)
46. Radutoiu, S., Madsen, L. H., Madsen, E. B., Jurkiewicz, A., Fukai, E., Quistgaard, E. 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. (Pubitemid 47367494)
47. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M. A., and Barrell, B. 2000. Artemis: Sequence visualization and annotation. Bioinformatics 16:944-945.
48. Schmeisser, C., Liesegang, H., Krysciak, D., Bakkou, N., Le Quere, A., Wollherr, A., Heinemeyer, I., Morgenstern, B., Pommerening-Roser, A., Flores, M., Palacios, R., Brenner, S., Gottschalk, G., Schmitz, R. A., Broughton, W. J., Perret, X., Strittmatter, A. W., and Streit, W. R. 2009. Rhizobium sp. strain NGR234 possesses a remarkable number of secretion systems. Appl. Environ. Microbiol. 75:4035-4045.
49. Schumpp, O., Crevecoeur, M., Broughton, W. J., and Deakin, W. J. 2009. Delayed maturation of nodules reduces symbiotic effectiveness of the Lotus japonicus-Rhizobium sp. NGR234 interaction. J. Exp. Bot. 60:581-590.
50. Schwedock, J., and Long, S. R. 1990. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348:644-647. (Pubitemid 120015128)
51. Schwedock, J. S., Liu, C., Leyh, T. S., and Long, S. R. 1994. Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity. J. Bacteriol. 176:7055-7064. (Pubitemid 24349449)
52. 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. (Pubitemid 47416492)
53. Sprent, J. I. 1994. Evolution and diversity in the legume-rhizobium symbiosis: Chaos theory? Plant Soil 161:1-10.
54. Sprent, J. I. 2007. Evolving ideas of legume evolution and diversity: A taxonomic perspective on the occurrence of nodulation. New Phytol. 174:11-25. (Pubitemid 46333284)
55. Squartini, A., Struffi, P., Doring, H., Selenska-Pobell, S., Tola, E., Giacomini, A., Vendramin, E., Velazquez, E., Mateos, P. F., Martinez-Molina, E., Dazzo, F. B., Casella, S., and Nuti, M. P. 2002. Rhizobium sullae sp. nov. (formerly 'Rhizobium hedysari'), the root-nodule microsymbiont of Hedysarum coronarium L. Int. J. Syst. Evol. Microbiol. 52:1267-1276. (Pubitemid 34846427)
56. Sytsma, K. J., Morawetz, J., Pires, J. C., Nepokroeff, M., Conti, E., Zjhra, M., Hall, J. C., and Chase, M. W. 2002. Urticalean rosids: Circumscription, rosid ancestry, and phylogenetics based on rbcL, trnL-F, and ndhF sequences. Am. J. Bot. 89:1531-1546.
57. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
58. Terpolilli, J. J., O'Hara, G. W., Tiwari, R. P., Dilworth, M. J., and Howieson, J. G. 2008, The model legume Medicago truncatula A17 is poorly matched for N2 fixation with the sequenced microsymbiont Sinorhizobium meliloti 1021. New Phytol. 179:62-66. (Pubitemid 351783181)
59. Torres Tejerizo, G., Del Papa, M. F., Soria-Diaz, M. E., Draghi, W., Lozano, M., Giusti Mde, L., Manyani, H., Megias, M., Gil Serrano, A., Puhler, A., Niehaus, K., Lagares, A., and Pistorio, M. 2011. The nodulation of alfalfa by the acid-tolerant Rhizobium sp. strain LPU83 does not require sulfated forms of lipochitooligosaccharide nodulation signals. J. Bacteriol. 193:30-39.
60. Trinick, M. J. 1973. Symbiosis between Rhizobium and the non-legume, Trema aspera. Nature 244:459-460.
61. Trinick, M. J. 1979. Structure of nitrogen-fixing nodules formed by Rhizobium on roots of Parasponia andersonii Planch. Can. J. Microbiol. 25:565-578. (Pubitemid 9201410)
62. Trinick, M. J. 1980a. Growth of Parasponia in agar tube culture and symbiotic effectiveness of isolates from Pa r a s p o n i a spp. New Phytol. 85:37-45.
63. Trinick, M. J. 1980b. Relationships amongst the fast-growing rhizobia of Lablab purpureus, Leucaena leucocephala, Mimosa spp., Acacia farnesiana and Sesbania grandiflora and their affinities with other rhizobial groups. J. Appl. Bacteriol. 49:39-53.
64. Trinick, M. J., and Galbraith, J. 1976. Structure of root nodules formed by Rhizobium on the non-legume Trema cannabina var. scabra. Arch. Microbiol. 108:159-166.
65. Trinick, M. J., and Galbraith, J. 1980. The Rhizobium requirements of the non-legume Parasponia in relationship to the cross-inoculation group concept of legumes. New Phytol. 86:17-26.
66. Trinick, M. J., and Hadobas, P. A. 1988. Biology of the Parasponia-Bradyrhizobium symbiosis. Plant Soil 110:177-185.
67. Trinick, M. J., Goodchild, D. J., and Miller, C. 1989. Localization of bacteria and hemoglobin in root nodules of Parasponia andersonii containing both Bradyrhizobium strains and Rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 55:2046-2055.
68. Van de Velde, W., Guerra, J. C., De Keyser, A., De Rycke, R., Rombauts, S., Maunoury, N., Mergaert, P., Kondorosi, E., Holsters, M., and Goormachtig, S. 2006. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol. 141:711-720. (Pubitemid 43974563)
69. Van Domselaar, G. H., Stothard, P., Shrivastava, S., Cruz, J. A., Guo, A., Dong, X., Lu, P., Szafron, D., Greiner, R., and Wishart, D. S. 2005. BASys: A web server for automated bacterial genome annotation. Nucleic Acids Res. 33:W455-W459. (Pubitemid 44529961)
70. Waelkens, F., Voets, T., Vlassak, K., Vanderleyden, J., and Van Rhijn, P. 1995. The nodS gene of Rhizobium tropici strain CIAT899 is necessary for nodulation on Phaseolus vulgaris and on Leucaena leucocephala. Mol. Plant-Microbe Interact. 8:147-154.
71. Wang, D., Griffitts, J., Starker, C., Fedorova, E., Limpens, E., Ivanov, S., Bisseling, T., and Long, S. 2010. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327:1126-1129.
72. Webster, G., Poulton, P. R., Cocking, E. C., and Davey, M. R. 1995. The nodulation of micro-propagated plants of Parasponia andersonii by tropical legume rhizobia. J. Exp. Bot. 46:1131-1137.
73. Witzany, G. 2011. Rhizobia, legumes and nitrogen fixation. Pages 309-311 in: Biocommunication in soil microorganisms, Ed. 1, Vol. 1. G. Witzany, ed. Springer, Heidelberg, Germany.
74. Wong, C. H., and Patchamuthu, R. 1988. Rhizobia in tropical legumes: Ineffective nodulation of Arachis hypogaea L. by fast-growing strains. Soil Biol. Biochem. 20:677-681.
75. Yasuta, T., Okazaki, S., Mitsui, H., Yuhashi, K. I., Ezura, H., and Minamisawa, K. 2001. DNA sequence and mutational analysis of Rhizobitoxine biosynthesis genes in Bradyrhizobium elkanii. Appl. Environ. Microbiol. 67:4999-5009. (Pubitemid 33701262)