Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago

Molecular Ecology

Volumn 15, Issue 10, 2006, Pages 2719-2734

  Bailly, Xavier ^a,b   Olivieri, Isabelle ^b   De Mita, Stéphane ^a   Cleyet Marel, Jean Claude ^a   Béna, Gilles ^a  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Medicago; Mutualism; Recombination; Selection; Sinorhizobium; Symbiosis

Indexed keywords

ARTICLE; EPIDEMIOLOGY; GENE LINKAGE DISEQUILIBRIUM; GENETIC DATABASE; GENETIC MARKER; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOTYPE; MEDICAGO; MICROBIOLOGY; MOLECULAR GENETICS; NITROGEN FIXATION; PHYSIOLOGY; SINORHIZOBIUM; SPECIES DIFFERENCE; SYMBIOSIS;

DATABASES, GENETIC; GENETIC MARKERS; GENOTYPE; LINKAGE DISEQUILIBRIUM; MEDICAGO; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; RECOMBINATION, GENETIC; SAMPLING STUDIES; SELECTION (GENETICS); SINORHIZOBIUM; SPECIES SPECIFICITY; SYMBIOSIS; VARIATION (GENETICS);

BACTERIA (MICROORGANISMS); MEDICAGO; SINORHIZOBIUM; SINORHIZOBIUM MEDICAE; SINORHIZOBIUM MELILOTI; SINORHIZOBIUM SP.;

EID: 33747060705     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2006.02969.x     Document Type: Article

References (71)

1. Battisti L, Lara J, Leigh J (1992) Specific oligosaccharide form of the Rhizobium meliloti exopolysaccharide promotes nodule invasion in alfalfa. Proceedings of the National Academy of Sciences, USA, 89, 5625-5629.
2. Bena G, Lejeune B, Prosperi JM, Olivieri I (1998a) Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L. Proceedings of the Royal Society of London. Series B, Biological Sciences, 265, 1141-1151.
3. Bena G, Prosperi JM, Lejeune B, Olivieri I (1998b) Evolution of annual species of the genus Medicago: a molecular phylogenetic approach. Molecular Phylogenetics and Evolution, 9, 552-559.
4. Bena G, Lyet A, Huguet T, Olivieri I (2005) Medicago-Sinorhizobium symbiotic specificity evolution and the geographic expansion of Medicago. Journal of Evolutionary Biology, 18, 1547-1558.
5. Brisson D, Dykhuizen DE (2004) ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics, 168, 713-722.
6. Bryant D, Moulton V (2004) NEIGHBOUR-NET: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution, 21, 255-265.
7. Carelli M, Gnocchi S, Fancelli S et al. (2000) Genetic diversity and dynamics of Sinorhizobium meliloti populations nodulating different alfalfa cultivars in Italian soils. Applied and Environmental Microbiology, 66, 4785-4789.
8. Cook DR (1999) Medicago truncatula - a model in the making! Current Opinion in Plant Biology, 2, 301-304.
9. Eardly BD, Materon LA, Smith NH et al. (1990) Genetic structure of natural populations of the nitrogen-fixing bacterium Rhizobium meliloti. Applied and Environmental Microbiology, 56, 187-194.
10. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
11. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis. European Journal of Biochemistry, 270, 1365-1380.
12. Galibert F, Finan TM, Long SR et al. (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science, 293, 668-672.
13. Gonzalez JE, Reuhs BL, Walker GC (1996a) Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proceedings of the National Academy of Sciences, USA, 93, 8636-8641.
14. Gonzalez JE, York GM, Walker GC (1996b) Rhizobium meliloti exopolysaccharides: synthesis and symbiotic function. Gene, 179, 141-146.
15. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86, 485-486.
16. Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium series, 95-98.
17. Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160-174.
18. Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage analysis. Bioinformatics, 16, 847-848.
19. Haubold B, Travisano M, Rainey PB, Hudson RR (1998) Detecting linkage disequilibrium in bacterial populations. Genetics, 150, 1341-1348.
20. Hedrick PW (1987) Gametic disequilibrium measures: proceed with caution. Genetics, 117, 331-341.
21. Herrera-Cervera JA, Sanjuan-Pinilla JM, Olivares J, Sanjuan J (1998) Cloning and identification of conjugative transfer origins in the Rhizobium meliloti genome. Journal of Bacteriology, 180, 4583-4590.
22. Hughes AL (2005) Evidence for abundant slightly deleterious polymorphisms in bacterial populations. Genetics, 169, 533-538.
23. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254-267.
24. Jiggins FM, Hurst GD, Yang Z (2002) Host-symbiont conflicts: positive selection on an outer membrane protein of parasitic but not mutualistic Rickettsiaceae. Molecular Biology and Evolution, 19, 1341-1349.
25. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Mammalian Protein Metabolism (ed. Munro HN). Academic Press, New York.
26. Kereszt A, Kiss E, Reuhs BL (1998) Novel rkp gene clusters of Sinorhizobium meliloti involved in capsular polysaccharide production and invasion of the symbiotic nodule: the rkpK gene encodes a UDP-glucose dehydrogenase. Journal of Bacteriology, 180, 5426-5431.
27. Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature, 425, 78-81.
28. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
29. Kiss E, Huguet T, Poinsot V, Batut J (2004) The typA gene is required for stress adaptation as well as for symbiosis of Sinorhizobium meliloti 1021 with certain Medicago truncatula lines. Molecular Plant-Microbe Interactions, 17, 235-244.
30. Konstantinidis KT, Tiedje JM (2004) Trends between gene content and genome size in prokaryotic species with larger genomes. Proceedings of the National Academy of Sciences, USA, 101, 3160-3165.
31. de Lajudie P, Willems A, Pot B et al. (1994) Polyphasic taxonomy of rhizobia: emendation of the genus Sinorhizobium and description of Sinorhizobium meliloti comb. nov., Sinorhizobium saheli sp. nov. and Sinorhizobium teranga sp. nov. International Journal of Systematic Bacteriology, 44, 715-733.
32. Lewontin RC (1964) The interaction of selection and linkage. I. General considerations, heterotic models. Genetics, 49, 49-67.
33. Maiden MC, Bygraves JA, Feil E et al. (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences, USA, 95, 3140-3145.
34. Materon LA (1991) Symbiotic characteristics of Rhizobium meliloti in west asian soils. Soil Biology and Biochemistry, 23, 429-434.
35. Maynard Smith J, Haigh J (1974) The hitchhiking effect of a favourable gene. Genetical Research, 23, 23-35.
36. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proceedings of the National Academy of Sciences, USA, 90, 4384-4388.
37. McAdams HH, Srinivasan B, Arkin AP (2004) The evolution of genetic regulatory systems in bacteria. Nature Reviews Genetics, 5, 169-178.
38. Mithofer A (2002) Suppression of plant defence in rhizobia-legume symbiosis. Trends in Plant Science, 7, 440-444.
39. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
40. Paffetti D, Daguin F, Fancelli S et al. (1998) Influence of plant genotype on the selection of nodulating Sinorhizobium meliloti strains by Medicago sativa. Antonie van Leeuwenhoek, 73, 3-8.
41. Parker MA (1999) Mutualism in metapopulations of legumes and rhizobia. American Naturalist, 153, S48-S60.
42. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews, 64, 180-201.
43. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
44. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
45. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092-2100.
46. Raymond M, Rousset F (1995a) An exact test for population differentiation. Evolution; International Journal of Organic Evolution, 49, 1280-1283.
47. Raymond M, Rousset F (1995b) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
48. Reuber TL, Walker GC (1993) Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell, 74, 269-280.
49. Rome S, Fernandez MP, Brunel B, Normand P, Cleyet-Marel JC (1996) Sinorhizobium medicae sp. nov., isolated from annual Medicago spp. International Journal of Systematic Bacteriology, 46, 972-980.
50. Roumiantseva ML, Yakutkina VV, Damman-Kalinowski T et al. (1999) Comparative analysis of structural organization of the genome in alfalfa nodule bacteria Sinorhizobium medicae and Sinorhizobium meliloti. Russian Journal of Genetics, 35, 128-135.
51. Roumiantseva ML, Andronov EE, Sharypova LA et al. (2002) Diversity of Sinorhizobium meliloti from the Central Asian Alfalfa Gene Center. Applied and Environmental Microbiology, 68, 4694-4697.
52. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) dnasp, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496-2497.
53. Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406-425.
54. Silva C, Vinuesa P, Eguiarte LE, Souza V, Martinez-Romero E (2005) Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Molecular Ecology, 14, 4033-4050.
55. Souza V, Nguyen TT, Hudson RR, Pinero D, Lenski RE (1992) Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proceedings of the National Academy of Sciences, USA, 89, 8389-8393.
56. Spaink HP (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annual Review of Microbiology, 54, 257-288.
57. Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusetts.
58. Tachida H, Cockerham CC (1986) Analysis of linkage disequilibrium in an island model. Theoretical Population Biology, 29, 161-197.
59. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
60. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
61. Tibayrenc M (1996) Towards a unified evolutionary genetics of microorganisms. Annual Review of Microbiology, 50, 401-429.
62. Van Berkum P, Beyene D, Bao G, Campbell TA, Eardly BD (1998) Rhizobium mongolense sp. nov. is one of the three rhizobial genotypes identified which nodulate and form nitrogen fixing symbiosis with Medicago ruthenica [(L.) Ledebour]. International Journal of Systematic Bacteriology, 48, 13-22.
63. van Baalen M, Jansen VAA (2001) Dangerous liaisons: the ecology of private interest and common good. Oikos, 95, 211-224.
64. Villegas MDC, Rome S, Maure L et al. (2006) Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. laciniata) of S. meliloti. Systematic and Applied Microbiology, in press, doi: 10.1016/j.syapm.2005.1012.1008.
65. Vincent JM (1970) A Manual for the Practical Study of Root-nodule Bacteria. Blackwell Scientific Publications Ltd, Oxford.
66. Vinuesa P, Silva C, Werner D, Martinez-Romero E (2005) Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Molecular Phylogenetics and Evolution, 34, 29-54.
67. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution: International Journal of Organic Evolution, 38, 1358-1370.
68. West SA, Kiers ET, Simms EL, Denison RF (2002) Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proceedings of the Royal Society of London. Series B, Biological Sciences, 269, 685-694.
69. Wilkinson M, Lapointe FJ, Gower DJ (2003) Branch lengths and support. Systematic Biology, 52, 127-130.
70. Wirth T, Wang X, Linz B et al. (2004) Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proceedings of the National Academy of Sciences, USA, 101, 4746-4751.
71. Young ND, Cannon SB, Sato S et al. (2005) Sequencing the gene-spaces of Medicago truncatula and Lotus japonicus. Plant Physiology, 137, 1174-1181.