Diversity analyses of Aeschynomene symbionts in Tropical Africa and Central America reveal that nod-independent stem nodulation is not restricted to photosynthetic bradyrhizobia

Environmental Microbiology

Volumn 12, Issue 8, 2010, Pages 2152-2164

  Miché, Lucie ^a,f   Moulin, Lionel ^a   Chaintreuil, Clémence ^a   Contreras Jimenez, José Luis ^b   Munive Hernández, José Antonio ^c   del Carmen Villegas Hernandez, María ^d   Crozier, Françoise ^e   Béna, Gilles ^a,g  

^a LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

^b Herbario and   (Mexico)

^c BENEMÉRITA UNIVERSIDAD AUTÓNOMA DE PUEBLA   (Mexico)

^d Centro de Investigacion en Biotecnologia Aplicada   (Mexico)

^e INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^f AVIGNON UNIVERSITÉ   (France)

^g MOHAMMED V UNIVERSITY   (Morocco)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

AFRICA; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; BACTERIAL GENOME; BRADYRHIZOBIACEAE; CENTRAL AMERICA; CLASSIFICATION; COMPARATIVE STUDY; EVOLUTION; FABACEAE; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; PLANT STEM; SYMBIOSIS;

AFRICA; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; BIOLOGICAL EVOLUTION; BRADYRHIZOBIACEAE; CENTRAL AMERICA; DNA, BACTERIAL; FABACEAE; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHOTOSYNTHESIS; PHYLOGENY; PLANT STEMS; SYMBIOSIS;

AESCHYNOMENE INDICA; BACTERIA (MICROORGANISMS); BRADYRHIZOBIACEAE; PHOTORHIZOBIUM;

EID: 77955232744     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.02090.x     Document Type: Article

References (42)

1. Alazard D. Stem and root nodulation in Aeschynomene spp. Appl Environ Microbiol 1985, 50:732-734.
2. Alazard D. La nodulation caulinaire dans le genre Aeschynomene. 1991, PhD Thesis, Université Claude Bernard-Lyon I, France.
3. Alazard D, Duhoux E. Diversity of stem nodulation sites in Aeschynomene spp. J Plant Physiol 1988, 132:123-125.
4. Alazard D, Duhoux E. Development of stem nodules in a tropical forage legume, Aeschynomene afraspera. J Exp Bot 1990, 41:1199-1206.
5. Becker M, Ladha JK, Ottow JCG. Growth and N2-fixation of two stem-nodulating legumes and their effect as green manure on lowland rice. Soil Biol Biochem 1990, 22:1109-1119.
6. van Berkum P, Tully RE, Keister DL. Nonpigmented and bacteriochlorophyll-containing bradyrhizobia isolated from Aeschynomene indica. Appl Environ Microbiol 1995, 61:623-629.
7. van Berkum P, Leibold JM, Eardly BD. Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst Appl Microbiol 2006, 29:207-215.
8. Bikandi J, San Millan R, Rementeria A, Garaizar J. In silico analysis of complete bacterial genomes: PCR, AFLP-PCR and endonuclease restriction. Bioinformatics 2004, 20:798-799.
9. Boivin C, Ndoye I, Molouba F, De Lajudie P, Dupuy N, Dreyfus B. Stem nodulation in legumes: diversity, mechanisms, and unusual characteristics. Crit Rev Plant Sci 1997, 16:1-30.
10. Boogerd FC, Rossum D. Nodulation of groundnut by Bradyrhizobium: a simple infection process by crack entry. FEMS Microbiol Rev 1997, 21:5-27.
11. Chaintreuil C, Giraud E, Prin Y, Lorquin J, Ba A, Gillis M. Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 2000, 66:5437-5447.
12. Chaintreuil C, Boivin C, Dreyfus B, Giraud E. Characterization of the common nodulation genes of the photosynthetic Bradyrhizobium sp ORS285 reveals the presence of a new insertion sequence upstream of nodA. FEMS Microbiol Lett 2001, 194:83-86.
13. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36:W465-W469.
14. Doyle JJ, Luckow MA. The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol 2003, 131:900-910.
15. Eaglesham ARJ, Szalay AA. Aerial stem nodules on Aeschynomene spp. Plant Sci Lett 1983, 29:265-272.
16. Evans WR, Fleischman DE, Calvert HE, Pyati PV, Alter GM, Rao NS. Bacteriochlorophyll and photosynthetic reaction centers in Rhizobium strain BTAi 1. Appl Environ Microbiol 1990, 56:3445-3449.
17. Fleischman D, Kramer D. Photosynthetic rhizobia. BBA-Bioenergetics 1998, 1364:17-36.
18. Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JP. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 2001, 51:2037-2048.
19. Giraud E, Fleischman D. Nitrogen-fixing symbiosis between photosynthetic bacteria and legumes. Photosynth Res 2004, 82:115-130.
20. Giraud E, Hannibal L, Fardoux L, Vermeglio A, Dreyfus B. Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc Natl Acad Sci USA 2000, 97:14795-14800.
21. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC. Legumes symbioses: absence of nod genes in photosynthetic bradyrhizobia. Science 2007, 316:1307-1312.
22. Hirsch P, Müller M. Blastobacter aggregatus sp.nov., Blastobacter capsulatus sp.nov., and Blastobacter denitrificans sp.nov., new budding bacteria from freshwater habitats. Syst Appl Microbiol 1985, 6:281-286.
23. Jarvis BDW, Gillis M, De Ley J. Intra- and intergeneric similarities between the ribosomal ribonucleic acid cistrons of Rhizobium and Bradyrhizobium species and some related bacteria. Int J Syst Bacteriol 1986, 36:129-138.
24. Ladha JK, So RB. Numerical taxonomy of photosynthetic rhizobia nodulating Aeschynomene species. Int J Syst Bacteriol 1994, 44:62-73.
25. Lavin M, Thulin M, Labat J, Pennington R. Africa, the Odd Man out: molecular biogeography of dalbergioid legumes (Fabaceae) suggests otherwise. Syst Bot 2000, 25:449-467.
26. Lavin M, Pennington RT, Klitgaard BB, Sprent JI, de Lima HC, Gasson PE. The dalbergioid legumes (Fabaceae): delimitation of a pantropical monophyletic clade. Am J Bot 2001, 88:503-533.
27. Lorquin J, Molouba F, Dreyfus BL. Identification of the carotenoid pigment canthaxanthin from photosynthetic Bradyrhizobium strains. Appl Environ Microbiol 1997, 63:1151-1154.
28. Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B. Photosynthetic bradyrhizobia from Aeschynomene spp. are specific to stem-nodulated species and form a separate 16S ribosomal DNA restriction fragment length polymorphism group. Appl Environ Microbiol 1999, 65:3084-3094.
29. Montecchia MS, Kerber NL, Pucheu NL, Perticari A, Garcia AF. Analysis of genomic diversity among photosynthetic stem-nodulating rhizobial strains from northeast Argentina. Syst Appl Microbiol 2002, 25:423-433.
30. Mueller UG, Lipari SE, Milgroom MG. Amplified fragment length polymorphism (AFLP) fingerprinting of symbiotic fungi cultured by the fungus-growing ant Cyphomyrmex minutus. Mol Ecol 1996, 5:119-122.
31. Normand P, Cournoyer B, Simonet P, Nazaret S. Analysis of a ribosomal RNA operon in the actinomycete Frankia. Gene 1992, 111:119-124.
32. Sprent J. Evolution, structure and function of nitrogen-fixing root nodules: confessions of ignorance. Nitrogen-Fixation: Achievements and Objectives. 1990, 45-54. Gresshoff PMRoth LEStacey GNewton WE. In, London, UK, Chapman & Hall, pp.
33. Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P. Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 2001, 183:214-220.
34. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
35. Vinuesa P, Silva C, Werner D, Martinez-Romero E. Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 2005, 34:29-54.
36. Willems A, Doignon-Bourcier F, Coopman R, Hoste B, de Lajudie P, Gillis M. AFLP fingerprint analysis of Bradyrhizobium strains isolated from Faidherbia albida and Aeschynomene species. Syst Appl Microbiol 2000, 23:137-147.
37. Willems A, Doignon-Bourcier F, Goris J, Coopman R, de Lajudie P, De Vos P, Gillis M. DNA-DNA hybridization study of Bradyrhizobium strains. Int J Syst Evol Microbiol 2001a, 51:1315-1322.
38. Willems A, Doignon-Bourcier F, Gillis M, de Lajudie P. Evaluation of AFLP for the grouping of Bradyrhizobium strains. Genet Sel Evol 2001b, 33:S365-S377.
39. Willems A, Munive A, de Lajudie P, Gillis M. In most Bradyrhizobium groups sequence comparison of 16S-23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations. Syst Appl Microbiol 2003, 26:203-210.
40. Wong FY, Stackebrandt E, Ladha JK, Fleischman DE, Date RA, Fuerst JA. Phylogenetic analysis of Bradyrhizobium japonicum and photosynthetic stem-nodulating bacteria from Aeschynomene species grown in separated geographical regions. Appl Environ Microbiol 1994, 60:940-946.
41. Young JP, Downer HL, Eardly BD. Phylogeny of the phototrophic rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J Bacteriol 1991, 173:2271-2277.
42. Yurkov VV, Beatty JT. Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 1998, 62:695-724.