Identification at the species and symbiovar levels of strains nodulating Phaseolus vulgaris in saline soils of the Marrakech region (Morocco) and analysis of the otsA gene putatively involved in osmotolerance

Systematic and Applied Microbiology

Volumn 35, Issue 3, 2012, Pages 156-164

  Faghire, M ^a,b,c   Mandri, B ^a,b   Oufdou, K ^a   Bargaz, A ^a,b   Ghoulam, C ^b   Ramirez Bahena M H ^c,d   Velazquez E ^d   Peix, A ^c,d  

^a FACULTÉ DES SCIENCES SEMLALIA   (Morocco)

^b FACULTÉ DES SCIENCES ET TECHNIQUES GUÉLIZ   (Morocco)

^c INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^d UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

OtsA; Phaseolus vulgaris; Phylogeny; Rhizobia; Salt stress; Trehalose

Indexed keywords

TREHALOSE;

ARTICLE; BACTERIAL STRAIN; MOROCCO; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASEOLUS VULGARIS; PHYLOGENY; PRIORITY JOURNAL; RHIZOBIUM ETLI; RHIZOBIUM GALLICUM; RHIZOBIUM PHASEOLI; RHIZOBIUM TROPICI; SPECIES IDENTIFICATION; SYMBIOSIS;

ENSIFER; PHASEOLUS VULGARIS; RHIZOBIUM; RHIZOBIUM ETLI; RHIZOBIUM GALLICUM; RHIZOBIUM PHASEOLI; RHIZOBIUM TROPICI;

EID: 84858674150     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2012.02.003     Document Type: Article

References (62)

1. Aguilar O.M., Riva O., Peltzer E. Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13548-13553.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
3. Amarger N., Macheret V., Laguerre G. Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov. from Phaseolus vulgaris nodules. Int. J. Syst. Bacteriol. 1997, 47:996-1006.
4. Anyango B., Wilson K.J., Beynon J.L., Giller K.E. Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. Appl. Environ. Microbiol. 1995, 61:4016-4021.
5. Beyene D., Kassa S., Ampy F., Asseffa A., Gebremedhin T., van Berkum P. Ethiopian soils harbor natural populations of rhizobia that form symbioses with common bean (Phaseolus vulgaris L.). Arch. Microbiol. 2004, 181:129-136.
6. Botsford J.L., Lewis T.A. Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress. Appl. Environ. Microbiol. 1990, 56:488-494.
7. Bouhmouch I., Brhada F., Filali-Maltouf A., Aurag J. Selection of osmotolerant and effective strains of Rhizobiaceae for inoculation of common bean (Phaseolus vulgaris) in Moroccan saline soils. Agronomie 2001, 21:591-599.
8. Bouhmouch I., Souad-Mouhsine B., Brhada F., Aurag J. Influence of host cultivars and Rhizobium species on the growth and symbiotic performance of Phaseolus vulgaris under salt stress. J. Plant Physiol. 2005, 162:1103-1113.
9. Brique A., Devassine J., Pilard S., Cailleub D., Gosselin I. Osmoregulated trehalose-derived oligosaccharides in Sinorhizobium meliloti. FEBS Lett. 2010, 584:3661-3666.
10. Diouf A., de Lajudie P., Neyra M., Kersters K., Gillis M., Martinez-Romero E., Gueye M. Polyphasic characterization of rhizobia that nodulate Phaseolus vulgaris in West Africa (Senegal and Gambia). Int. J. Syst. Evol. Microbiol. 2000, 50:159-170.
11. Estévez J., Soria-Díaz M.E., de Córdoba F.F., Morón B., Manyani H., Gil A., Thomas-Oates J., van Brussel A.A., Dardanelli M.S., Sousa C., Megías M. Different and new Nod factors produced by Rhizobium tropici CIAT899 following Na+ stress. FEMS Microbiol. Lett. 2009, 293:220-231.
12. Fernández-Aunión C., Ben Hamouda T., Iglesias-Guerra F., Argandoña M., Reina-Bueno M., Nieto J.J., Aouani M.E., Vargas C. Biosynthesis of compatible solutes in rhizobial strains isolated from Phaseolus vulgaris nodules in Tunisian fields. BMC Microbiol. 2010, 192.
13. Ferreira L., Sánchez-Juanes F., García-Fraile P., Rivas R., Mateos P.F., Martínez-Molina E., González-Buitrago J.M., Velázquez E. MALDI-TOF mass spectrometry is a fast and reliable platform for identification and ecological studies of species from family Rhizobiaceae. PLoS One 2011, 6:e20223.
14. Food and Agricultural Organization of United Nations (FAO) Economic and Social Department: The Statistical Division 2009, http://faostat.fao.org/site/567/DesktopDefault.aspx%3FPageID=567%23ancor.
15. García-Fraile P., Mulas-García D., Peix A., Rivas R., González-Andrés F., Velázquez E. Phaseolus vulgaris is nodulated in northern Spain by Rhizobium leguminosarum strains harboring two nodC alleles present in American Rhizobium etli strains: biogeographical and evolutionary implications. Can. J. Microbiol. 2010, 56:657-666.
16. Gaunt M.W., Turner S.L., Rigottier-Gois L., Lloyd-Macgilp S.A., Young J.W.P. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 2001, 51:2037-2048.
17. González V., Santamaría R.I., Bustos P., Hernández-González I., Medrano-Soto A., Moreno-Hagelsieb G., Janga S.C., Ramírez M.A., Jiménez-Jacinto V., Collado-Vides J., Dávila G. The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3834-3839.
18. Hasegawa P.M., Bressan R.A., Zhu J.K., Bohnert H.J. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000, 51:463-499.
19. Iglesias O., Rivas R., García-Fraile P., Abril A., Mateos P.F., Martínez-Molina E., Velázquez E. Genetic characterization of fast-growing rhizobia able to nodulate Prosopis alba in North Spain. FEMS Microbiol. Lett. 2007, 277:210-216.
20. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980, 16:111-120.
21. Laguerre G., Fernandez M.P., Edel V., Normand P., Amarger N. Genomic heterogeneity among French Rhizobium strains isolated from Phaseolus vulgaris L. Int. J. Syst. Bacteriol. 1993, 43:761-767.
22. Laguerre G., Nour S.M., Macheret V., Sanjuan J., Drouin P., Amarger N. Classification of rhizobia based on nodC and nifH gene analysis reveals a close phylogenetic relationship among Phaseolus vulgaris symbionts. Microbiology 2001, 147:981-993.
23. León-Barrios M., Lorite M.J., Donate-Correa J., Sanjuán J. Ensifer meliloti bv. lancerottense establishes nitrogen-fixing symbiosis with Lotus endemic to the Canary Islands and shows distinctive symbiotic genotypes and host range. Syst. Appl. Microbiol. 2009, 32:413-420.
24. Martínez-Romero E., Caballero-Mellado J. Rhizobium phylogenies and bacterial genetic diversity. Crit. Rev. Plant Sci. 1996, 15:113-140.
25. Martínez-Romero E., Segovia L., Mercante F.M., Franco A.A., Graham P., Pardo M.A. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 1991, 41:417-426.
26. Mhamdi R., Jebara M., Aouani M.E., Ghrir R., Mars M. Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. Biol. Fertil. Soils 1999, 28:313-320.
27. McIntyre H.J., Davies H., Hore T.A., Miller S.H., Dufour J.P., Ronson C.W. Trehalose biosynthesis in Rhizobium leguminosarum bv. trifolii and its role in desiccation tolerance. Appl. Environ. Microbiol. 2007, 73:3984-3992.
28. Miller K.J., Wood J.M. Osmoadaptation by rhizosphere bacteria. Annu. Rev. Microbiol. 1996, 50:101-136.
29. Mnasri B., Mrabet M., Laguerre G., Aouani M.E., Mhamdi R. Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N2-fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch. Microbiol. 2007, 187:79-85.
30. Moschetti G., Peluso A., Protopapa A., Anastasio M., Pepe O., Defez R. Use of nodulation pattern, stress tolerance, nodC gene amplification, RAPD-PCR and RFLP-16S rDNA to discriminate genotypes of Rhizobium leguminosarum biovar viciae. Syst. Appl. Microbiol. 2005, 28:619-631.
31. Mouhsine B., Prell J., Filali-Maltouf A., Priefer U.B., Aurag J. Diversity, phylogeny and distribution of bean rhizobia in salt-affected soils of North-West Morocco. Symbioses 2007, 43:83-96.
32. Mulas D., García-Fraile P., Carro L., Ramírez-Bahena M.H., Casquero P., Velázquez E., González-Andrés F. Distribution and efficiency of Rhizobium leguminosarum strains nodulating Phaseolus vulgaris in Northern Spanish soils: selection of native strains that replace conventional N fertilization. Soil Biol. Biochem. 2011, 43:2283-2293.
33. Nandasena K.G., O'Hara G.W., Tiwari R.P., Willlems A., Howieson J.G. Mesorhizobium ciceri biovar biserrulae, a novel biovar nodulating the pasture legume Biserrula pelecinus L. Int. J. Syst. Evol. Microbiol. 2007, 57:1041-1045.
34. Pérez-Ramírez N.O., Rogel M.A., Wang E., Castellanos J.Z., Martínez-Romero E. Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol. Ecol. 1998, 26:289-296.
35. Priefer U.B., Aurag J., Boesten B., Bouhmouch I., Defez R., Filali-Maltouf A., Miklis M., Moawad H., Mouhsine B., Prell J., Schlüter A., Senatore B. Characterisation of Phaseolus symbionts isolated from Mediterranean soils and analysis of genetic factors related to pH tolerance. J. Biotechnol. 2001, 91:223-236.
36. Radeva G., Jurgens G., Niemi M., Nick G., Suominen L., Lindström K. Description of two biovars in the Rhizobium galegae species: biovar orientalis and biovar officinalis. Syst. Appl. Microbiol. 2001, 24:192-205.
37. Ramírez-Bahena M.H., Velázquez E., Fernández-Santos F., Peix A., Martínez-Molina E., Mateos P.F. Phenotypic, genotypic and symbiotic diversity in strains nodulating clover in different soils in Spain. Can. J. Microbiol. 2009, 55:1207-1216.
38. Ribeiro, R.A., Rogel, M.A., López-López, A., Ormeño-Orrillo, E., Gomes-Barcellos, F., Martínez, J., Lopes-Thompson, F., Martínez-Romero, E., Hungria, M. (2011) Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int. J. Syst. Evol. Microbiol.,, ahead of print. doi:10.1099/ijs.0.032912-0.
39. Rivas R., García-Fraile P., Mateos P.F., Martínez-Molina E., Velázquez E. Characterization of xylanolytic bacteria present in the bract phyllosphere of the date palm Phoenix dactylifera. Lett. Appl. Microbiol. 2007, 44:181-187.
40. Rivas R., Laranjo M., Velázquez E., Mateos P.F., Oliveira S., Martínez-Molina E. Strains of Mesorhizobium amorphae and M. tianshanense carrying symbiotic genes of common chickpea endosymbiotic species constitute a novel biovar (ciceri) able to nodulate Cicer arietinum. Lett. Appl. Microbiol. 2007, 44:412-418.
41. Rivas R., Peix A., Mateos P.F., Trujillo M.E., Martinez-Molina E., Velázquez E. Biodiversity of populations of phosphate solubilizing rhizobia that nodulate chickpea in different Spanish soils. Plant Soil 2006, 287:23-33.
42. Rivas R., Velázquez E., Palomo J.L., Mateos P., García-Benavides P., Martínez-Molina E. Rapid identification of Clavibacter michiganensis subspecies sepedonicus using two primers random amplified polymorphic DNA (TP-RAPD) fingerprints. Eur. J. Plant Pathol. 2002, 108:179-184.
43. Robledo M., Velázquez E., Ramírez-Bahena M.H., García-Fraile P., Pérez-Alonso A., Rivas R., Martínez-Molina E., Mateos P.F. The celC gene, a new phylogenetic marker useful for taxonomic studies in Rhizobium. Syst. Appl. Microbiol. 2011, 34:393-399.
44. Rogel M.A., Ormeño-Orrillo E., Martinez Romero E. Symbiovars in rhizobia reflect bacterial adaptation to legumes. Syst. Appl. Microbiol. 2011, 34:96-104.
45. Saïdi S., Mnasri B., Mhamdi R. Diversity of nodule-endophytic agrobacteria-like strains associated with different grain legumes in Tunisia. Syst. Appl. Microbiol. 2011, 34:524-530.
46. Saitou N., Nei M. A neighbor-joining method: a new method for reconstructing phylogenetics trees. Mol. Biol. Evol. 1987, 44:406-425.
47. Shamseldin A., Werner D. High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr. Microbiol. 2005, 50:11-16.
48. Silva C., Vinuesa P., Eguiarte L.E., Martínez-Romero E., Souza V. Rhizobium etli and Rhizobium gallicum nodulate common bean (Phaseolus vulgaris) in a traditionally managed milpa plot in Mexico: population genetics and biogeographic implications. Appl. Environ. Microbiol. 2003, 69:884-893.
49. Silva C., Vinuesa P., Eguiarte L.E., Souza V., Martínez-Romero E. Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol. Ecol. 2005, 14:4033-4050.
50. Singleton P.W., El-Swaifi S.A., Bohlool B.B. Effect of salinity on Rhizobium growth and survival. Appl. Environ. Microbiol. 1982, 44:884-890.
51. Sugawara M., Cytryn E.J., Sadowsky M.J. Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl. Environ. Microbiol. 2010, 76:1071-1081.
52. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 4. 10.1093/molbev/msr121.
53. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
54. Valverde A., Igual J.M., Peix A., Cervantes E., Velázquez E. Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int. J. Syst. Evol. Microbiol. 2006, 56:2631-2637.
55. Valverde A., Velázquez E., Cervantes E., Igual J.M., van Berkum P. Evidence of an American origin for symbiosis-related genes in Rhizobium lusitanum. Appl. Environ. Microbiol. 2011, 77:5665-5670.
56. van Berkum P., Beyene D., Eardly B.D. Phylogenetic relationships among Rhizobium species nodulating the common bean (Phaseolus vulgaris L.). Int. J. Syst. Bacteriol. 1996, 46:240-244.
57. Villegas M.C., Rome S., Mauré L., Domergue O., Gardan L., Bailly X., Cleyet-Marel J.C., Brunel B. Nitrogen-fixing sinorhizobia with Medicago laciniata constitute a novel biovar (bv. medicaginis) of S. meliloti. Syst. Appl. Microbiol. 2006, 29:526-538.
58. Vincent J.M. The cultivation isolation and maintenance of rhizobia. A manual for the practical study of root-nodule 1970, 1-13. Blackwell Scientific Publications, Oxford. J.M. Vincent (Ed.).
59. Vinuesa P., León-Barrios M., Silva C., Willems A., Jarabo-Lorenzo A., Pérez-Galdona R., Werner D., Martínez-Romero E. Bradyrhizobium canariense sp. nov., an acid-tolerant endosymbiont that nodulates endemic genistoid legumes (Papilionoideae: Genisteae) from the Canary Islands, along with Bradyrhizobium japonicum bv. genistearum, Bradyrhizobium genospecies alpha and Bradyrhizobium genospecies beta. Int. J. Syst. Evol. Microbiol. 2005, 55:569-575.
60. Zahran H.H., Sprent J.I. Effects of sodium chloride and polyethylene glycol on root-hair infection and nodulation of Vicia faba L. plants by Rhizobium leguminosarum. Planta 1986, 167:303-309.
61. Zahran H.H. Rhizobium - legume symbiosis and nitrogen fixation under severe conditions and in arid climate. Microbiol. Mol. Biol. Rev. 1999, 12:968-998.
62. Zhang X., Blair M.W., Wang S. Genetic diversity of Chinese common bean (Phaseolus vulgaris L.) landraces assessed with simple sequence repeat markers. Theor. Appl. Genet. 2008, 117:629-640.