Shaping bacterial symbiosis with legumes by experimental evolution

Molecular Plant-Microbe Interactions

Volumn 27, Issue 9, 2014, Pages 956-964

  Marchetti, Marta ^a   Jauneau, Alain ^b,c   Capela, Delphine ^a   Remigi, Philippe ^a   Gris, Carine ^a   Batut, Jacques ^a   Masson Boivin, Catherine ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b CNRS   (France)

^c Plateforme d'Imagerie TRI   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LEGHEMOGLOBIN; REACTIVE OXYGEN METABOLITE;

ARTICLE; CUPRIAVIDUS; CYTOLOGY; DIRECTED MOLECULAR EVOLUTION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MIMOSA; NITROGEN FIXATION; NODULATION; PHENOTYPE; PHYSIOLOGY; PLANT IMMUNITY; PLANT ROOT; PLASMID; RALSTONIA SOLANACEARUM; SYMBIOSIS;

CUPRIAVIDUS; DIRECTED MOLECULAR EVOLUTION; LEGHEMOGLOBIN; MIMOSA; NITROGEN FIXATION; PHENOTYPE; PLANT IMMUNITY; PLANT ROOT NODULATION; PLANT ROOTS; PLASMIDS; RALSTONIA SOLANACEARUM; REACTIVE OXYGEN SPECIES; SYMBIOSIS;

EID: 84906279648     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-03-14-0083-R     Document Type: Article

References (55)

1. Allan, A. C., and Fluhr, R. 1997. Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559-1572.
2. Amadou, C., Pascal, G., Mangenot, S., Glew, M., Bontemps, C., Capela, D., Carrere, S., Cruveiller, S., Dossat, C., Lajus, A., Marchetti, M., Poinsot, V., Rouy, Z., Servin, B., Saad, M., Schenowitz, C., Barbe, V., Batut, J., Medigue, C., and Masson-Boivin, C. 2008. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 18:1472-1483.
3. Barrick, J. E., and Lenski, R. E. 2013. Genome dynamics during experimental evolution. Nat. Rev. Genet. 14:827-839.
4. Barrick, J. E., Yu, D. S., Yoon, S. H., Jeong, H., Oh, T. K., Schneider, D., Lenski, R. E., and Kim, J. F. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461:1243-1274.
5. Bensadoun, A., and Weinstein, D. 1976. Assay of protein in presence of interfering materials. Anal. Biochem. 70:241-250.
6. Berendsen, R. L., Pieterse, C. M. J., and Bakker, P. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17:478-486.
7. Boucher, C. A., Barberis, P. A., Trigalet, A. P., and Demery, D. A. 1985. Transposon mutagenesis of Pseudomonas solanacearum-Isolation of TN5-induced avirulent mutants. J. Gen. Microbiol. 131:2449-2457.
8. Buckling, A., Maclean, R. C., Brockhurst, M. A., and Colegrave, N. 2009. The Beagle in a bottle. Nature 457:824-829.
9. Bulgarelli, D., Rott, M., Schlaeppi, K., Van Themaat, E. V. L., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., Peplies, J., Gloeckner, F. O., Amann, R., Eickhorst, T., and Schulze-Lefert, P. 2012. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91-95.
10. Capela C., Guan S., and Masson-Boivin C. 2013. In: Diversity and Evolution of Nitrogen-Fixing Legume Symbionts. F. de Bruijn, ed. Wiley-Blackwell, Hoboken, NJ, U.S.A.
11. Chen, W. M., Moulin, L., Bontemps, C., Vandamme, P., Bena, G., and Boivin-Masson, C. 2003. Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J. Bacteriol. 185:7266-7272.
12. Deslandes, L., Pileur, F., Liaubet, L., Camut, S., Can, C., Williams, K., Holub, E., Beynon, J., Arlat, M., and Marco, Y. 1998. Genetic characterization of RRS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soilborne pathogen Ralstonia solanacearum. Mol. Plant-Microbe Interact. 11:659-667.
13. Dixon, R., and Kahn, D. 2004. Genetic regulation of biological nitrogen fixation. Nat. Rev. Microbiol. 2:621-631.
14. Elliott, G. N., Chou, J. H., Chen, W. M., Bloemberg, G. V., Bontemps, C., Martinez-Romero, E., Velazquez, E., Young, J. P. W., Sprent, J. I., and James, E. K. 2009. Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ. Microbiol. 11:762-778.
15. Felix, G., Duran, J. D., Volko, S., and Boller, T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265-276.
16. Feng, D. X., Tasset, C., Hanemian, M., Barlet, X., Hu, J., Tremousaygue, D., Deslandes, L., and Marco, Y. 2012. Biological control of bacterial wilt in Arabidopsis thaliana involves abscissic acid signalling. New Phytol. 194:1035-1045.
17. Fones, H., and Preston, G. M. 2012. Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 327:1-8.
18. Galibert, F., Finan, T. M., Long, S. R., Puhler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A., Boistard, P., Bothe, G., Boutry, M., Bowser, L., Buhrmester, J., Cadieu, E., Capela, D., Chain, P., Cowie, A., Davis, R. W., Dreano, S., Federspiel, N. A., Fisher, R. F., Gloux, S., Godrie, T., Goffeau, A., Golding, B., Gouzy, J., Gurjal, M., Hernandez-Lucas, I., Hong, A., Huizar, L., Hyman, R. W., Jones, T., Kahn, D., Kahn, M. L., Kalman, S., Keating, D. H., Kiss, E., Komp, C., Lalaure, V., Masuy, D., Palm, C., Peck, M. C., Pohl, T. M., Portetelle, D., Purnelle, B., Ramsperger, U., Surzycki, R., Thebault, P., Vandenbol, M., Vorholter, F. J., Weidner, S., Wells, D. H., Wong, K., Yeh, K. C., and Batut, J. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
19. Gehlot, H. S., Tak, N., Kaushik, M., Mitra, S., Chen, W. M., Poweleit, N., Panwar, D., Poonar, N., Parihar, R., Tak, A., Sankhla, I. S., Ojha, A., Rao, S. R., Simon, M. F., Reis Junior, F. B., Perigolo, N., Tripathi, A. K., Sprent, J. I., Young, J. P. W., James, E. K., and Gyaneshwar, P. 2013. An invasive Mimosa in India does not adopt the symbiont of its native relatives. Ann. Bot. 112:179-96.
20. Gibson, K. E., Kobayashi, H., and Walker, G. C. 2008. Molecular determinants of a symbiotic chronic infection. Annu. Rev. Genet. 42:413-441.
21. Guan, S. H., Gris, C., Cruveiller, S., Pouzet, C., Tasse, L., Leru, A., Maillard, A., Medigue, C., Batut, J., Masson-Boivin, C., and Capela, D. 2013. Experimental evolution of nodule intracellular infection in legume symbionts. ISME J. 7:1367-1377.
22. Gyaneshwar, P., Hirsch, A. M., Moulin, L., Chen, W. M., Elliott, G. N., Bontemps, C., Estrada-de los Santos, P., Gross, E., dos Reis, F. B., Sprent, J. I., Young, J. P. W., and James, E. K. 2011. Legume-nodulating betaproteobacteria: Diversity, host range, and future prospects. Mol. Plant-Microbe Interact. 24:1276-1288.
23. Hirsch, A., Lum, M., and Downie, J. 2001. What makes the rhizobia-legume symbiosis so special? Plant Physiol. 127:1484-1492.
24. Ivanov, S., Fedorova, E., and Bisseling, T. 2010. Intracellular plant microbe associations: Secretory pathways and the formation of perimicrobial compartments. Curr. Opin. Plant Biol. 13:372-377.
25. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
26. Jones, K. M., Kobayashi, H., Davies, B. W., Taga, M. E., and Walker, G.C. 2007. How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5:619-633.
27. Kiers, E., Rousseau, R., West, S., and Denison, R. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78-81.
28. Lamb, C., and Dixon, R. A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
29. Le Gac, M., Cooper, T. F., Cruveiller, S., Edigue, C. M., and Schneider, D. 2013. Evolutionary history and genetic parallelism affect correlated responses to evolution. Mol. Ecol. 22:3292-3303.
30. Lenski, R. E., and Travisano, M. 1994. Dynamics of adaptation and diversification-A 10,000 generation experiment with bacterial populations. Proc. Natl. Acad. Sci. U.S.A. 91:6808-6814.
31. Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., del Rio, T. G., Edgar, R. C., Eickhorst, T., Ley, R. E., Hugenholtz, P., Tringe, S. G., and Dangl, J. L. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90.
32. Marchetti, M., Capela, D., Glew, M., Cruveiller, S., Chane-Woon-Ming, B., Gris, C., Timmers, T., Poinsot, V., Gilbert, L. B., Heeb, P., Medigue, C., Batut, J., and Masson-Boivin, C. 2010. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8:e1000280.
33. Marchetti, M., Catrice, O., Batut, J., and Masson-Boivin, C. 2011. Cupriavidus taiwanensis bacteroids in Mimosa pudica indeterminate nodules are not terminally differentiated. Appl. Environ. Microbiol. 77:2161-2164.
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. Mithofer, A. 2002. Suppression of plant defence in rhizobia-legume symbiosis. Trends Plant Sci. 7:440-444.
36. Moreau, S., Verdenaud, M., Ott, T., Letort, S., de Billy, F., Niebel, A., Gouzy, J., de Carvalho-Niebel, F., and Gamas, P. 2011. Transcription reprogramming during root nodule development in Medicago truncatula. PLoS One 6:e16463.
37. Moulin, L., Munive, A., Dreyfus, B., and Boivin-Masson, C. 2001. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411:948-950.
38. Oke, V., and Long, S. R. 1999. Bacteroid formation in the Rhizobium-Legume symbiosis. Curr. Opin. Microbiol. 2:641-646.
39. Oldroyd, G. E. D., and Downie, J. M. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59:519-546.
40. Oono, R., Anderson, C. G., and Denison, R. F. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proc. Royal Soc. B Biol. Sci. 278:2698-2703.
41. Ramsay, J. P., Sullivan, J. T., Jambari, N., Ortori, C. A., Heeb, S., Williams, P., Barrett, D. A., Lamont, I. L., and Ronson, C. W. 2009. A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Mol. Microbiol. 73:1141-1155.
42. Remigi, P., Anisimova, M., Guidot, A., Genin, S., and Peeters, N. 2011. Functional diversification of the GALA type III effector family contributes to Ralstonia solanacearum adaptation on different plant hosts. New Phytol. 192:976-987.
43. Rodriguez-Lopez, J. N., Lowe, D. J., Hernandez-Ruiz, J., Hiner, A. N. P., Garcia-Canovas, F., and Thorneley, R. N. F. 2001. Mechanism of reaction of hydrogen peroxide with horseradish peroxidase: Identification of intermediates in the catalytic cycle. J. Am. Chem. Soc. 123:11838-11847.
44. Rogel, M., Hernández-Lucas, I., Kuykendall, L., Balkwill, D., and Martinez-Romero, E. 2001. Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl. Environ. Microbiol. 67:3264-3268.
45. Saeki, K. 2011. Rhizobial measures to evade host defense strategies and endogenous threats to persistent symbiotic nitrogen fixation: A focus on two legume-rhizobium model systems. Cell. Mol. Life Sci. 68:1327-1339.
46. Sprent, J. I. 2001. Nodulation in Legumes. Royal Botanic Gardens, Kew, U.K.
47. Sprent, J. I. 2007. Evolving ideas of legume evolution and diversity: A taxonomic perspective on the occurrence of nodulation. New Phytol. 174:11-25.
48. Sullivan, J., and Ronson, C. 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.
49. Sy, A., Giraud, E., Jourand, P., Garcia, N., Willems, A., de Lajudie, P., Prin, Y., Neyra, M., Gillis, M., Boivin-Masson, C., and Dreyfus, B. 2001. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J. Bacteriol. 183:214-220.
50. Terpolilli, J. J., Hood, G. A., and Poole, P. S. 2012. What determines the efficiency of N2-fixing rhizobium-legume symbioses? Adv. Microb. Physiol. 60:325-389.
51. Tian, C. F., Zhou, Y. J., Zhang, Y. M., Li, Q. Q., Zhang, Y. Z., Li, D. F., Wang, S., Wang, J., Gilbert, L. B., Li, Y. R., and Chen, W. X. 2012. Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc. Natl. Acad. Sci. U.S.A. 109:8629-8634.
52. Timmers, A. C. J., Soupene, E., Auriac, M. C., de Billy, F., Vasse, J., Boistard, P., and Truchet, G. 2000. Saprophytic intracellular rhizobia in alfalfa nodules. Mol. Plant-Microbe Interact. 13:1204-1213.
53. Udvardi, M., and Poole, P. S. 2013. Transport and metabolism in legumerhizobia symbioses. Annu. Rev. Plant Biol. 64:781-805.
54. Virta, M., Lineri, S., Kankaapaa, P., Karp, M., Peltonen, K., Nuutila, J., and Lilius, E. M. 1998. Determination of complement-mediated killing of bacteria by viability staining and bioluminescence. Appl. Environ. Microbiol. 64:515-519.
55. Zamioudis, C., and Pieterse, C. M. J. 2012. Modulation of host immunity by beneficial microbes. Mol. Plant-Microbe Interact. 25:139-150.