The geographical patterns of symbiont diversity in the invasive legume Mimosa pudica can be explained by the competitiveness of its symbionts and by the host genotype

Environmental Microbiology

Volumn 16, Issue 7, 2014, Pages 2099-2111

  Melkonian, Rémy ^a   Moulin, Lionel ^a   Béna, Gilles ^a   Tisseyre, Pierre ^a   Chaintreuil, Clémence ^a   Heulin, Karine ^b   Rezkallah, Naïma ^a   Klonowska, Agnieszka ^a   Gonzalez, Sophie ^c   Simon, Marcelo ^d   Chen, Wen Ming ^e   James, Euan K ^f   Laguerre, Gisèle ^b  

^a LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

^b CEMAGREF   (France)

^c INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^d EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^e NATIONAL KAOHSIUNG UNIVERSITY OF APPLIED SCIENCES   (Taiwan)

^f SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BURKHOLDERIA; BURKHOLDERIA PHYMATUM; CUPRIAVIDUS; CUPRIAVIDUS TAIWANENSIS; MIMOSA PUDICA; RHIZOBIACEAE;

RNA 16S;

ARTICLE; BURKHOLDERIA; CLASSIFICATION; CUPRIAVIDUS; GENETICS; GENOTYPE; INTRODUCED SPECIES; MICROBIOLOGY; MIMOSA; MOLECULAR GENETICS; NODULATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLOGEOGRAPHY; PHYSIOLOGY; REPRODUCIBILITY; RHIZOBIUM; SYMBIOSIS; TAIWAN;

BURKHOLDERIA; CUPRIAVIDUS; GENOTYPE; INTRODUCED SPECIES; MIMOSA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; PLANT ROOT NODULATION; REPRODUCIBILITY OF RESULTS; RHIZOBIUM; RNA, RIBOSOMAL, 16S; SYMBIOSIS; TAIWAN;

EID: 84903759029     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12286     Document Type: Article

References (58)

1. Amadou, C., Pascal, G., Mangenot, S., Glew, M., Bontemps, C., Capela, D., etal. (2008) Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18: 1472-1483.
2. Amarger, N., and Lobreau, J.P. (1982) Quantitative study of nodulation competitiveness in Rhizobium strains. Appl Environ Microbiol 44: 583-588.
3. Andrus, A.D., Andam, C., and Parker, M.A. (2012) American origin of Cupriavidus bacteria associated with invasive Mimosa legumes in the Philippines. FEMS Microbiol Ecol 80: 747-750.
4. Barneby, R.C. (1991) Sensitivae Censitae: A Description of the Genus Mimosa Linnaeus (Mimosaceae) in the New World. Bronx, NY, USA: The New York Botanical Garden.
5. Barrett, C.F., and Parker, M.A. (2005) Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama. Syst Appl Microbiol 28: 57-65.
6. Barrett, C.F., and Parker, M.A. (2006) Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol 72: 1198-1206.
7. Bontemps, C., Elliott, G.N., Simon, M.F., Dos Reis Junior, F.B., Gross, E., Lawton, R.C., etal. (2010) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19: 44-52.
8. Bournaud, C., De Faria, S.M., Dos Santos, J.M.F., Tisseyre, P., Silva, M., Chaintreuil, C., etal. (2013) Burkholderia species are the most common and preferred nodulating symbionts of the Piptadenia Group (tribe Mimoseae). PLoS ONE 8: e63478.
9. Broughton, W.J., and Dilworth, M.J. (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125: 1075-1080.
10. Chen, W.M., Laevens, S., Lee, T.M., Coenye, T., De Vos, P., Mergeay, M., and Vandamme, P. (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51: 1729-1735.
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. Chen, W.M., James, E.K., Chou, J.H., Sheu, S.Y., Yang, S.Z., and Sprent, J.I. (2005a) Beta-rhizobia from Mimosa pigra, a newly discovered invasive plant in Taiwan. New Phytol 168: 661-675.
13. Chen, W.M., de Faria, S.M., Straliotto, R., Pitard, R.M., Simoes-Araujo, J.L., Chou, J.H., etal. (2005b) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 71: 7461-7471.
14. Denton, M.D., Reeve, W.G., Howieson, J.G., and Coventry, D.R. (2003) Competitive abilities of common field isolates and commercial strain of Rhizobium leguminosarum bv. trifolii for clover nodule occupancy. Soil Biol Biochem 35: 1039-1048.
15. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
16. Elliott, G.N., Chen, W.M., Bontemps, C., Chou, J.H., Young, J.P., Sprent, J.I., and James, E.K. (2007a) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot (Lond) 100: 1403-1411.
17. Elliott, G.N., Chen, W.M., Chou, J.H., Wang, H.C., Sheu, S.Y., Perin, L., etal. (2007b) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta. New Phytol 173: 168-180.
18. Elliott, G.N., Chou, J.H., Chen, W.M., Bloemberg, G.V., Bontemps, C., Martinez-Romero, E., etal. (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11: 762-778.
19. Ferguson, B.J., Indrasumunar, A., Hayashi, S., Lin, M.H., Lin, Y.H., Reid, D.E., and Gresshoff, P.M. (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52: 61-76.
20. Friesen, M.L. (2012) Widespread fitness alignment in the legume-rhizobium symbiosis. New Phytol 194: 1096-1111.
21. Fry, J., Wood, M., and Poole, P.S. (2001) Investigation of myo-inositol catabolism in Rhizobium leguminosarum bv. viciae and its effect on nodulation competitiveness. Mol Plant Microbe Interact 14: 1016-1025.
22. Garau, G., Yates, R.J., Deiana, P., and Howieson, J.G. (2009) Novel strains of nodulating Burkholderia have a role in nitrogen fixation with papilionoid herbaceous legumes adapted to acid, infertile soils. Soil Biol Biochem 41: 125-134.
23. Gehlot, H.S., Tak, N., Kaushik, M., Mitra, S., Chen, W.M., Poweleit, N., etal. (2013) An invasive Mimosa in India does not adopt the symbionts of its native relatives. Ann Bot 112: 179-196.
24. Gyaneshwar, P., Hirsch, A.M., Moulin, L., Chen, W.M., Elliott, G.N., Bontemps, C., etal. (2011) Legume-nodulating betaproteobacteria: diversity, host range and future prospects. Mol Plant Microbe Interact 24: 1276-1288.
25. Howieson, J.G., De Meyer, S.E., Vivas-Marfisi, A.V., Ratnayake, S., Ardley, J.K., and Yates, R.J. (2013) Novel Burkholderia bacteria isolated from Lebeckia ambigua - a perennial suffrutescent legume of the fynbos. Soil Biol Biochem 60: 55-64.
26. Klonowska, A., Chaintreuil, C., Tisseyre, P., Miche, L., Melkonian, R., Ducousso, M., etal. (2012) Biodiversity of Mimosa pudica rhizobial symbionts (Cupriavidus taiwanensis, Rhizobium mesoamericanum) in New Caledonia and their adaptation to heavy metal-rich soils. FEMS Microbiol Ecol 81: 618-635.
27. Lagares, A., Caetano-Anolles, G., Niehaus, K., Lorenzen, J., Ljunggren, H.D., Puhler, A., and Favelukes, G. (1992) A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. J Bacteriol 174: 5941-5952.
28. Liu, X.Y., Wu, W., Wang, E.T., Zhang, B., Macdermott, J., and Chen, W.X. (2012) Phylogenetic relationships and diversity of beta-rhizobia associated with Mimosa species grown in Sishuangbanna, China. Int J Syst Evol Microbiol 61: 334-342.
29. Lodeiro, A.R., Lopez-Garcia, S.L., Vazquez, T.E., and Favelukes, G. (2000) Stimulation of adhesiveness, infectivity, and competitiveness for nodulation of Bradyrhizobium japonicum by its pretreatment with soybean seed lectin. FEMS Microbiol Lett 188: 177-184.
30. López-López, A., Rogel-Hernandez, M.A., Barois, I., Ortiz Ceballos, A.I., Martinez, J., Ormeno-Orrillo, E., and Martinez-Romero, E. (2012) Rhizobium grahamii sp. nov. from Dalea leporina, Leucaena leucocephala, Clitoria ternatea nodules, and Rhizobium mesoamericanum sp. nov. from Phaseolus vulgaris, siratro, cowpea and Mimosa pudica nodules. Int J Syst Evol Microbiol 62: 2264-2271.
31. Malek, W. (1992) The role of motility in the efficiency of nodulation by Rhizobium meliloti. Arch Microbiol 158: 26-28.
32. Martinez-Romero, E. (2009) Coevolution in Rhizobium-legume symbiosis? DNA Cell Biol 28: 361-370.
33. 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.
34. Mishra, R.P., Tisseyre, P., Melkonian, R., Chaintreuil, C., Miche, L., Klonowska, A., etal. (2012) Genetic diversity of Mimosa pudica rhizobial symbionts in soils of French Guiana: investigating the origin and diversity of Burkholderia phymatum and other beta-rhizobia. FEMS Microbiol Ecol 79: 487-503.
35. 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.
36. Murphy, P., Wexler, W., Grzemski, W., Rao, J., and Gordon, D. (1995) Rhizopines - their role in symbiosis and competition. Soil Biol Biochem 27: 525-529.
37. Nicholas, K.B., and Nicholas, B.J. (1997) Genedoc: a tool for editing and annotating multiple sequence alignments. Distributed by the author.
38. Parker, M.A., Wurtz, A., and Paynter, Q. (2007) Nodule symbiosis of invasive Mimosa pigra in Australia and in ancestral habitats: a comparative analysis. Biol Invasions 9: 127-138.
39. Ponsonnet, C., and Nesme, X. (1994) Identification of Agrobacterium strains by PCR-RFLP analysis of pTi and chromosomal regions. Arch Microbiol 161: 300-309.
40. Rangin, C., Brunel, B., Cleyet-Marel, J.C., Perrineau, M.M., and Bena, G. (2008) Effects of Medicago truncatula genetic diversity, rhizobial competition, and strain effectiveness on the diversity of a natural Sinorhizobium species community. Appl Environ Microbiol 74: 5653-5661.
41. Reid, D.E., Ferguson, B.J., Hayashi, S., Lin, Y.H., and Gresshoff, P.M. (2011) Molecular mechanisms controlling legume autoregulation of nodulation. Ann Bot 108: 789-795.
42. dos Reis, F.B., Simon, M.F., Gross, E., Boddey, R.M., Elliott, G.N., Neto, N.E., etal. (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186: 934-946.
43. Robleto, E.A., Kmiecik, K., Oplinger, E.S., Nienhuis, J., and Triplett, E.W. (1998) Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Appl Environ Microbiol 64: 2630-2633.
44. Sheu, S.Y., Chou, J.H., Bontemps, C., Elliott, G.N., Gross, E., James, E.K., etal. (2012) Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil. Int J Syst Evol Microbiol 62: 2272-2278.
45. Sheu, S.Y., Chou, J.H., Bontemps, C., Elliott, G.N., Gross, E., Dos Reis Junior, F.B., etal. (2013) Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp. Int J Syst Evol Microbiol 63: 435-441.
46. da Silva, K., Florentino, L.A., da Silva, K.B., de Brandt, E., Vandamme, P., and de Souza Moreira, F.M. (2012) Cupriavidus necator isolates are able to fix nitrogen in symbiosis with different legume species. Syst Appl Microbiol 35: 175-182.
47. Simon, M.F., Grether, R., Queiroz, L.P., Sarkinen, T.E., Dutra, V.F., and Hughes, C.E. (2011) The evolutionary history of Mimosa (Leguminosae): towards a phylogeny of the sensitive plants. Am J Bot 98: 1201-1221.
48. Soedarjo, M., and Borthakur, D. (1996) Mimosine produced by the tree-legume Leucaena provides growth advantages to some Rhizobium strains that utilize it as a source of carbon and nitrogen. Plant Soil 186: 87-92.
49. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
50. Taulé, C., Zabaleta, M., Mareque, C., Platero, R., Sanjurjo, L., Sicardi, M., etal. (2012) New betaproteobacterial Rhizobium strains able to efficiently nodulate Parapiptadenia rigida (Benth.) Brenan. Appl Environ Microbiol 78: 1692-1700.
51. Toro, N. (1996) Nodulation competitiveness in the rhizobium-legume symbiosis. World J Microbiol Biotech 12: 1557-1162.
52. Triplett, E.W., and Sadowsky, M.J. (1992) Genetics of competition for nodulation of legumes. Annu Rev Microbiol 46: 399-428.
53. Vandamme, P., Goris, J., Chen, W.M., de Vos, P., and Willems, A. (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25: 507-512.
54. Vincent, J.M. (1970) A Manual for the Practical Study of Root-Nodule Bacteria. I.B.P. Handbook, Vol. 15. Oxford, UK: Blackwell Scientific Publications, Ltd.
55. Wang, E.T., Rogel, M.A., Garcia-de los Santos, A., Martinez-Romero, J., Cevallos, M.A., and Martinez-Romero, E. (1999) Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49 (Part 4): 1479-1491.
56. Wielbo, J., Marek-Kozaczuk, M., Kubik-Komar, A., and Skorupska, A. (2007) Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness. Can J Microbiol 53: 957-967.
57. Willems, A., Coopman, R., and Gillis, M. (2001) Comparison of sequence analysis of 16S-23S rDNA spacer regions, AFLP analysis and DNA-DNA hybridizations in Bradyrhizobium. Int J Syst Evol Microbiol 51: 623-632.
58. Wu, S.-H., Chaw, S.-M., and Rejmanek, M. (2003) Naturalized Fabaceae (Leguminosae) species in Taiwan: the first approximation. Bot Bull Acad Sinica (Taiwan) 44: 59-66.