Abstract
Phaseolus vulgaris L. (common bean) is a legume indigenous to American countries currently cultivated in all continents, which is nodulated by different rhizobial species and symbiovars. Most of species able to nodulate this legume worldwide belong to the genus Rhizobium, followed by those belonging to the genera Ensifer (formerly Sinorhizobium) and Pararhizobium (formerly Rhizobium) and minority by species of the genus Bradyrhizobium. All these genera belong to the phylum alpha-Proteobacteria, but the nodulation of P. vulgaris has also been reported for some species belonging to Paraburkholderia and Cupriavidus from the beta-Proteobacteria. Several species nodulating P. vulgaris were originally isolated from nodules of this legume in American countries and are linked to the symbiovars phaseoli and tropici, which are currently present in other continents probably because they were spread in their soils together with the P. vulgaris seeds. In addition, this legume can be nodulated by species and symbiovars originally isolated from nodules of other legumes due its high promiscuity, a concept currently related with the ability of a legume to be nodulated by several symbiovars rather than by several species. In this article we review the species and symbiovars able to nodulate P. vulgaris in different countries and continents and the challenges on the study of the P. vulgaris endosymbionts diversity in those countries where they have not been studied yet, that will allow to select highly effective rhizobial strains in order to guarantee the success of P. vulgaris inoculation.
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Abiala MA, Abdelrahman M, Burritt DJ, Tran LSP (2018) Salt stress tolerance mechanisms and potential applications of legumes for sustainable reclamation of salt-degraded soils. Land Degrad Dev 29:3812–3822
Adhikari D, Itoh K, Suyama K (2013) Genetic diversity of common bean (Phaseolus vulgaris L.) nodulating rhizobia in Nepal. Plant Soil 368:341–353
Aguilar OM, Lopez MV, Riccillo PM (2001) The diversity of rhizobia nodulating beans in Northwest Argentina as a source of more efficient inoculant strains. J Biotechnol 91:181–188
Aguilar OM, Riva O, Peltzer E (2004) Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc Natl Acad Sci USA 101:13548–13553
Álvarez-Martínez ER, Valverde A, Ramírez-Bahena MH, García-Fraile P, Tejedor C, Mateos PF, Santillana N, Zúñiga D, Peix A, Velázquez E (2009) The analysis of core and symbiotic genes of rhizobia nodulating Vicia from different continents reveals their common phylogenetic origin and suggests the distribution of Rhizobium leguminosarum strains together with Vicia seeds. Arch Microbiol 191:659–668
Amarger N, Macheret V, Laguerre G (1997) Rhizobium gallicum sp. nov. and Rhizobium giardinii sp. nov., from Phaseolus vulgaris nodules. Int J Syst Bacteriol 47:996–1006
Andrews M, De Meyer S, James EK, Stępkowski T, Hodge S, Simon MF, Young JPW (2018) Horizontal transfer of symbiosis genes within and between rhizobial genera: occurrence and importance. Genes (Basel). https://doi.org/10.3390/genes9070321
Angioi SA, Rau D, Attene G, Nanni L, Bellucci E, Logozzo G, Negri V, Zeuli PLS, Papa R (2010) Beans in Europe: origin and structure of the European landraces of Phaseolus vulgaris L. Theor Appl Genet 121:829–843
Aserse AA, Räsänen LA, Assefa F, Hailemariam A, Lindström K (2012) Phylogeny and genetic diversity of native rhizobia nodulating common bean (Phaseolus vulgaris L.) in Ethiopia. Syst Appl Microbiol 35:120–131
Aserse AA, Woyke T, Kyrpides NC, Whitman WB, Lindström K (2017) Draft genome sequence of type strain HBR26T and description of Rhizobium aethiopicum sp. nov. Stand Genomic Sci 12:14
Aserse AA, Markos D, Getachew G, Yli-Halla M, Lindström K (2020) Rhizobial inoculation improves drought tolerance, biomass and grain yields of common bean (Phaseolus vulgaris L.) and soybean (Glycine max L.) at Halaba and Boricha in Southern Ethiopia. Arch Agron Soil Sci 66:488–501
Baginsky C, Brito B, Scherson R, Pertuzé R, Seguel O, Cañete A, Araneda C, Johnson WE (2015) Genetic diversity of Rhizobium from nodulating beans grown in a variety of Mediterranean climate soils of Chile. Arch Microbiol 197:419–429
Barraza A, Coss-Navarrete EL, Vizuet-de-Rueda JC, Martínez-Aguilar K, Hernández-Chávez JL, Ordaz-Ortiz JJ, Winkler R, Tiessen A, Alvarez-Venegas R (2018) Down-regulation of PvTRX1h increases nodule number and affects auxin, starch, and metabolic fingerprints in the common bean (Phaseolus vulgaris L.). Plant Sci 274:45–58
Beyene D, Kassa S, Ampy F, Asseffa A, Gebremedhin T, Berkum PV (2004) Ethiopian soils harbor natural populations of rhizobia that form symbioses with common bean (Phaseolus vulgaris L.). Arch Microbiol 181:129–136
Bouhmouch I, Brhada F, Filali-Maltouf A, Aurag J (2001) Selection of osmotolerant and effective strains of Rhizobiaceae for inoculation of common bean (Phaseolus vulgaris) in Moroccan saline soils. Agronomie 21:591–599
Bruning B, Rozema J (2013) Symbiotic nitrogen fixation in legumes: perspectives for saline agriculture. Environ Exp Bot 92:134–143
Buruchara R, Chirwa R, Sperling L, Mukankusi C, Rubyogo JC, Mutonhi R, Abang MM (2011) Development and delivery of bean varieties in Africa: the Pan-Africa Bean Research Alliance (PABRA) model. African Crop Sci J 19:227–245
Butcher K, Wick AF, De Sutter T, Chatterjee A, Harmon J (2016) Soil salinity: a threat to global food security. Agron J 108:2189–2200
Cao Y, Wang ET, Zhao L, Chen WM, Wei GH (2014) Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol Biochem 78:128–137
Carrasco-Castilla J, Ortega-Ortega Y, Jáuregui-Zúñiga D, Juárez-Verdayes MA, Arthikala MK, Monroy-Morales E, Nava N, Santana O, Sánchez-López R, Quinto C (2018) Down-regulation of a Phaseolus vulgaris annexin impairs rhizobial infection and nodulation. Environ Exp Bot 153:108–119
Cordeiro AB, Ribeiro RA, Helene LCF, Hungria M (2017) Rhizobium esperanzae sp. nov., a N2-fixing root symbiont of Phaseolus vulgaris from Mexican soils. Int J Syst Evol Microbiol 67:3937–3945
Costa MR, Chibeba AM, Mercante FM, Hungría M (2018) Polyphasic characterization of rhizobia microsymbionts of common bean [Phaseolus vulgaris (L.)] isolated in Mato Grosso do Sul, a hotspot of Brazilian biodiversity. Symbiosis 76:163–176
Dall'Agnol RF, Ribeiro RA, Ormeno-Orrillo E, Rogel MA, Delamuta JRM, Andrade DS, Martínez-Romero E, Hungria M (2013) Rhizobium freirei sp. nov.: a symbiont of Phaseolus vulgaris that is very effective at fixing nitrogen. Int J Syst Evol Microbiol 63:4167–4173
Dall'Agnol RF, Ribeiro RA, Delamuta JRM, Ormeno-Orrillo E, Rogel MA, Andrade DS, Martinez-Romero E, Hungria M (2014) Rhizobium paranaense sp. nov., an effective N2-fixing symbiont of common bean (Phaseolus vulgaris L.) with broad geographical distribution in Brazil. Int J Syst Evol Microbiol 64:3222–3229
Dall'Agnol RF, Bournaud C, de Faria SM, Béna G, Moulin L, Hungria M (2017) Genetic diversity of symbiotic Paraburkholderia species isolated from nodules of Mimosa pudica (L.) and Phaseolus vulgaris (L.) grown in soils of the Brazilian Atlantic Forest (Mata Atlântica). FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fix027
Dangeard PA (1926) Recherches sur les tubercles radicaux des Légumineuses. Botaniste 16:1–275
da Silva K, Florentino LA, da Silva KB, de Brandt E, Vandamme P, de Souza Moreire FM (2012) Cupriavidus necator isolates are able to fix nitrogen in symbiosis with different legume species. Syst Appl Microbiol 35:175–182
de Lajudie P, Laurent-Fulele E, Willems A, Torck U, Coopman R, Collins MD, Kersters K, Dreyfus B, Gillis M (1998) Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int J Syst Bacteriol 48:1277–1290
De Ron A, Papa R, Bitocchi E, González AM, Debouck DG, Brick MA, Fourie D, Marsolais F, Beaver J, Geffroy V, McClean P, Santalla M, Lozano R, Yuste-Lisbona FJ, Casquero PA (2015) Common bean. In: De Ron A (ed) Grain legumes. Handbook of plant breeding. Springer, New York, NY10
del Cerro P, Ayala-García P, Jiménez-Guerrero I, López-Baena FJ, Vinardell JM, Megías M, Hungria M, Gil-Serrano AM, Pérez-Montaño F, Ollero FJ (2019) The non-flavonoid inducible nodA3 and the flavonoid regulated nodA1 genes of Rhizobium tropici CIAT 899 guarantee nod factor production and nodulation of different host legumes. Plant Soil 440:185–200
Díaz-Alcántara CA, Ramírez-Bahena MH, Mulas D, García-Fraile P, Gómez-Moriano A, Peix A, Velázquez E, González-Andrés F (2014) Analysis of rhizobial strains nodulating Phaseolus vulgaris from Hispaniola Island, a geographic bridge between Meso and South America and the first historical link with Europe. Syst Appl Microbiol 37:149–156
Diouf A, de Lajudie P, Neyra M, Kersters K, Gillis M, Martinez-Romero E, Gueye M (2000) Polyphasic characterization of rhizobia that nodulate Phaseolus vulgaris in West Africa (Senegal and Gambia). Int J Syst Evol Microbiol 50:159–170
Elbanna K, Elbadry M, Gamal-Eldin H (2009) Genotypic and phenotypic characterization of rhizobia that nodulates snap bean (Phaseolus vulgaris L.) in Egyptian soils. Syst Appl Microbiol 32:522–530
Faghire M, Mandri B, Oufdou K, Bargaz A, Ghoulam C, Ramírez-Bahena MH, Velázquez E, Peix A (2012) 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. Syst Appl Microbiol 35:156–164
Ferguson BJ, Mens C, Hastwell AH, Zhang M, Su H, Jones CH, Chu X, Gresshoff PM (2019) Legume nodulation: the host controls the party. Plant Cell Environ 42:41–51
Flores-Félix JD, Sánchez-Juanes F, García-Fraile P, Valverde A, Mateos PF, Gónzalez-Buitrago JM, Velázquez E, Rivas R (2019) Phaseolus vulgaris is nodulated by the symbiovar viciae of several genospecies of Rhizobium laguerreae complex in a Spanish region where Lens culinaris is the traditionally cultivated legume. Syst Appl Microbiol 42:240–247
Food and Agricultural organization of United Nations (FAO) (2018) https://fao.org/faostat/en/#data/QC
García-Fraile P, Mulas-García D, Peix A, Rivas R, González-Andrés F, Velázquez E (2010) 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 56:566–657
Geniaux E, Laguerre G, Amarger N (1993) Comparison of geographically distant populations of Rhizobium isolated from root nodules of Phaseolus vulgaris. Mol Ecol 2:295–302
Gepts P, Bliss FA (1988) Dissemination pathways of common bean (Phaseolus vulgaris, Fabaceae) deduced from phaseolin electrophoretic variability. II. Eur Afr Econ Bot 42:86–104
Gepts P, Debouck D (1991) Origin, domestication, and evolution of the common bean (Phaseolus vulgaris L.). In: van Schoonhoven A, Voysest O (eds) Common beans: research for crop improvement. CAB International and CIAT, Wallingford, pp 7–54
Gomes Basso Los F, Ferreira Zielinski AA, Wojeicchowski JP, Nogueira A, Mottin Demiate I (2018) Beans (Phaseolus vulgaris L.): whole seeds with complex chemical composition. Curr Opin Food Sci 19:63–71
Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36:1389–1398
Gunnabo AH, Geurts R, Wolde-Meskel E, Degefu T, Giller KE, van Heerwaarden J (2019) Genetic interaction studies reveal superior performance of Rhizobium tropici CIAT899 on a range of diverse east African common bean (Phaseolus vulgaris L.) genotypes. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01763-19
Gurkanli CT, Ozkoc I, Gunduz I (2013) Genetic diversity of rhizobia nodulating common bean (Phaseolus vulgaris L.) in the Central Black Sea region of Turkey. Ann Microbiol 63:971–987
Gwyn AB, Handelsman J (1993) Evaluation of a strategy for identifying nodulation competitiveness genes in Rhizobium leguminosavum biovar phaseoli. J Gene Microbiol 139:529–538
Herrera-Cervera JA, Jb C-M, Laguerre G, Tichy HV, Requena N, Amarger N, Martinez-Romero E, Olivares J, Sanjuan J (1999) At least five rhizobial species nodulate Phaseolus vulgaris in a Spanish soil. FEMS Microbiol Ecol 30:87–97
Huo Y, Tong W, Wang J, Wang F, Bai W, Wang E, Shi P, Chen W, Wei G (2019) Rhizobium chutanense sp. nov., isolated from root nodules of Phaseolus vulgaris in China. Int J Syst Evol Microbiol 69:2049–2056
Jordan DC (1984) Family III Rhizobiaceae. In: Krieg NR, Holt JG (eds) Bergeys manual of systematic bacteriology, vol I. Williams and Wilkins Co., Baltimore, pp 234–242
Junier P, Alfaro M, Guevara R, Witzel KP, Caru M (2014) Genetic diversity of Rhizobium present in nodules of Phaseolus vulgaris L. cultivated in two soils of the central region in Chile. Appl Soil Ecol 80:60–66
Karanja NK, Wood M (1988) Selecting Rhizobium phaseoli strains for use with beans (Phaseolus vulgaris L.) in Kenya: ineffectiveness and tolerance of acidity and aluminium. Plant Soil 112:7–13
Kawaka F, Makonde H, Dida M, Opala P, Ombori O, Maingi J, Muoma J (2018) Genetic diversity of symbiotic bacteria nodulating common bean (Phaseolus vulgaris) in western Kenya. PLoS ONE. https://doi.org/10.1371/journal.pone.0207403
Koskey G, Mburu SW, Njeru EM, Kimiti JM, Ombori O, Maingi JM (2017) Potential of native rhizobia in enhancing nitrogen fixation and yields of climbing beans (Phaseolus vulgaris L.) in contrasting environments of Eastern Kenya. Front Plant Sci 8:443
Laguerre G, Fernandez MP, Edel V, Normand P, Amarger N (1993a) Genomic heterogeneity among French Rhizobium strains isolated from Phaseolus vulgaris L. Int J Syst Bacteriol 43:761–767
Laguerre G, Geniaux E, Mazurier SI, Rodriguez-Casartelli R, Amarger N (1993b) Conformity and diversity among field isolates of Rhizobium leguminosarum bv. viciae, bv. trifolii, bv. phaseoli revealed by DNA hybridization using chromosome and plasmid probes. Can J Microbiol 39:412–419
Li X, Tong W, Wang L, Rahman SU, Wei G, Tao S (2018) A novel strategy for detecting recent horizontal gene transfer and its application to Rhizobium strains. Front Microbiol 9:973
Litalien A, Zeeb B (2020) Curing the earth: a review of anthropogenic soil salinization and plant based strategies for sustainable mitigation. Sci Total Environ 698:134235
López-Guerrero MG, Ormeño-Orrillo E, Velázquez E, Rogel MA, Acosta JL, Gónzalez V, Martínez J, Martínez-Romero E (2012) Rhizobium etli taxonomy revised with novel genomic data and analyses. Syst Appl Microbiol 35:353–358
López-López A, Rogel-Hernández MA, Barois I, Ortiz-Ceballos AL, Martínez J, Ormeno-Orrillo E, Martinez-Romero E (2012) Rhizobium grahamii sp. nov. from nodules of Dalea termatea, Leucocephala and clitoria termatea and Rhizobium mesoamericanum sp. nov. from nodules of Phaseolus vulgaris, Siratro, cowpea and Mimosa pundica. Int J Syst Evol Microbiol 62:2264–2271
Lopez-Lopez AS, Negrete-Yankelevich S, Rogel MR, Ormeno-Orrillo E, Martinez J, Martinez-Romero E (2013) Native bradyrhizobia from Los Tuxtlas in Mexico are symbionts of Phaseolus lunatus (Lima bean). Syst Appl Microbiol 36:33–38
Martínez-Aguilar L, Salazar-Salazar C, Méndez RD, Caballero-Mellado J, Hirsch AM, Vásquez-Murrieta MS, Estrada-de los Santos P (2013) Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris. Anton van Leeuwen 104:1063–1071
Martínez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Syst Bacteriol 41:417–426
Martinez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252:11–23
Matsubara M, Zuniga-Davila D (2015) Phenotypic and molecular differences among rhizobia that nodulate Phaseolus lunatus in the Supe valley in Peru. Ann Microbiol 65:1803–1808
Mhamdi R, Jebara M, Aouani ME, Ghrir R, Mars M (1999) Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. Biol Fertil Soils 28:313–320
Mhamdi R, Laguerre G, Aouani ME, Mars M, Amarger N (2002) Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. FEMS Microbiol Ecol 41:77–84
Michiels J, Dombrecht B, Vermeiren N, Xi C, Luyten E, Vanderleyden J (1998) Phaseolus vulgaris is a non-selective host for nodulation. FEMS Microbiol Ecol 26:193–205
Mnasri B, Aouani ME, Mhamdi R (2007) Nodulation and growth of common bean (Phaseolus vulgaris) under water deficiency. Soil Biol Biochem 39:1744–1750
Mnasri B, Saidi S, Chihaoui SA, Mhamdi R (2012) Sinorhizobium americanum symbiovar mediterranense is a predominant symbiont that nodulates and fixes nitrogen with common bean (Phaseolus vulgaris L.) in a Northern Tunisian field. Syst Appl Microbiol 35:263–269
Mnsari B, Liu TY, Saidi S, Chen WF, Chen XW, Zhang XX, Mahmdi R (2014) Rhizobium azibense sp. nov., a nitrogen fixing bacterium isolated from root-nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 64:1501–1506
Morad M, Sara S, Alireza E, Reza CM, Mohammad D (2013) Effects of seed inoculation by Rhizobium strains on yield and yield components in common bean cultivars (Phaseolus vulgaris L.). Int J Biosci 3:134–141
Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K (2015) Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 38:84–90
Mrabet M, Mhamdi R, Tajini F, Tiwari R, Trabelsi M, Aouani ME (2005) Competitiveness and symbiotic effectiveness of a R. gallicum strain isolated from root nodules of Phaseolus vulgaris. Europ J Agron 22:209–216
Mulas D, García-Fraile P, Carro L, Ramírez-Bahena MH, Casquero P, Velázquez E, González-Andrés F (2011) 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 43:2283–2293
Mwenda GM, O'Hara GW, De Meyer SE, Howieson JG, Terpolilli JJ (2018) Genetic diversity and symbiotic effectiveness of Phaseolus vulgaris-nodulating rhizobia in Kenya. Syst Appl Microbiol 41:291–299
Oliveira-Santos J, Antunes JEL, Araujo ASF, Pereira-Lyra MCC, Gomes RLF, Lopes ACA, Figueiredo MVB (2011) Genetic diversity amonmg native isolates of rhizobia from Phaseolus lunatus. Ann Microbiol 61:437–444
Ormeño-Orrillo E, Vinuesa P, Zuniga-Davilla D, Martinez-Romero E (2006) Molecular diversity of native bradyrhizobia isolated from Lima bean (Phaseolus lunatus L.) in Preu. Syst Appl Microbiol 29:253–262
Ormeño-Orrillo E, Menna P, Almeida LG, Ollero FJ, Nicolás MF, Pains Rodrigues E, Shigueyoshi Nakatani A, Silva Batista JS, Oliveira Chueire LM, Souza RC, Ribeiro Vasconcelos AT, Megías M, Hungria M, Martínez-Romero E (2012) Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp PRF 81 which are used in inoculants for common bean (Phaseolus vulgaris L.). BMC Genom 13:735
Pastor-Bueis R, Sánchez-Cañizares C, James EK, González-Andrés F (2019) Formulation of a highly effective inoculant for common bean based on an autochthonous elite strain of Rhizobium leguminosarum bv. phaseoli, and genomic-based insights into its agronomic performance. Front Microbiol 10:2724
Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42
Pereira EG, Lacerda AM, Lima AS, Moreira FMS, Carvalho D, Siqueira JQ (2002) Genotypic, phenotypic and symbiotic diversity amongst rhizobia isolates from Phaseolus vulgaris L. growing in the Amazon region. In: Pedrosa FO, Hungria M, Yates G, Newton WE (eds) Nitrogen fixation: from molecules to crop productivity. Current plant science and biotechnology in agriculture. Springer, Dordrecht38
Pérez-Ramírez NO, Rogel MA, Wang E, Castellanos JZ, Martínez-Romero E (1998) Seeds of Phaseolus vulgaris bean carry Rhizobium etli. FEMS Microbiol Ecol 26:289–296
Rahman MH, Khatun S, Ali SR, Yasmin S, Kamruzzaman M, Rashid MH (2018) Morpho-physiological diversity of root nodule rhizobia from Mimosa (Mimosa pudica L.) and water Mimosa (Neptunia oleracea L.). J Bacteriol Mycol 5:1061
Rajnovic I, Ramírez-Bahena MH, Sánchez-Juanes F, González-Buitrago JM, Kajic S, Peix Á, Velázquez E, Sikora S (2019) Phylogenetic diversity of rhizobia nodulating Phaseolus vulgaris in Croatia and definition of the symbiovar phaseoli within the species Rhizobium pisi. Syst Appl Microbiol 42:126019
Ramírez-Bahena MH, García-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martínez-Molina E, Velázquez E (2008) Revision of the taxonomic status of the species Rhizobium leguminosarum (Frank 1879) Frank 1889AL, Rhizobium phaseoli Dangeard 1926AL and Rhizobium trifolii Dangeard 1926AL. R. trifolii is a later synonym of R. leguminosarum. Reclassification of the strain R. leguminosarum DSM 30132 (=NCIMB 11478) as Rhizobium pisi sp. nov. Int J Syst Evol Microbiol 58(11):2484–2490
Ramírez-Puebla ST, Hernández MAR, Guerrero Ruiz G, Ormeño-Orrillo E, Martinez-Romero JC, Servín-Garcidueñas LE, Núñez-de la Mora A, Amescua-Villela G, Negrete-Yankelevich S, Martínez-Romero E (2019) Nodule bacteria from the cultured legume Phaseolus dumosus (belonging to the Phaseolus vulgaris cross-inoculation group) with common tropici phenotypic characteristics and symbiovar but distinctive phylogenomic position and chromid. Syst Appl Microbiol 42:373–382
Ren B, Wang X, Duan J, Ma J (2019) Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation. Science 365:919–922
Ribeiro RA, Rogel MA, Lopez-Lopez A, Ormeno-Orrillo E, Barcellos FG, Martinez J, Thompson FL, Martinez-Romero E, Hungria M (2012) Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol 62:1179–1184
Ribeiro RA, Martins TB, Ormeño-Orrillo E, Marçon Delamuta JR, Rogel MA, Martínez-Romero E, Hungria M (2015) Rhizobium ecuadorense sp. nov., an indigenous N2-fixing symbiont of the Ecuadorian common bean (Phaseolus vulgaris L.) genetic pool. Int J Syst Evol Microbiol 65:3162–3169
Rípodas C, Castaingts M, Clúa J, Villafañe J, Blanco FA, Zanetti ME (2019) The PvNF-YA1 and PvNF-YB7 subunits of the heterotrimeric NF-Y transcription factor influence strain preference in the Phaseolus vulgaris-Rhizobium etli symbiosis. Front Plant Sci 10:221
Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) druce. Appl Environ Microbiol 68:5217–5222
Rivas R, Suba WA, Rao NS, Mateos PF, Dazzo FB, Kroppenste RM, Martinez-Molina E, Gillis M, Velazques E (2003) Description of Devosia neputunia sp. novel that nodulates and fixes nitrogen in symbiosis with Neptunia natans, an aquatic legume from India. Syst Appl Micrbiol 24:47–53
Román-Ponce B, Zhang YJ, Vásquez-Murrieta MS, Sui XH, Chen WF, Padilla JCA, Guo XW, Gao JL, Yan J, Wei Ge H, Wang ET (2016) Rhizobium acidisoli sp. nov., isolated from 1 root nodules of Phaseolus vulgaris in acid 2 soils in Mexico. Int J Syst Evol Microbiol 66:398–406
Rouhrazi K, Khodakaramian G, Velázquez E (2016) Phylogenetic diversity of rhizobial species and symbiovars nodulating Phaseolus vulgaris in Iran. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnw024
Samago TY, Anniye EW, Dakora FD (2018) Grain yield of common bean (Phaseolus vulgaris L.) varieties is markedly increased by rhizobial inoculation and phosphorus application in Ethiopia. Symbiosis 75:245–255
Segovia L, Young JPW, Martínez-Romero E (1993) Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Bacteriol 43:374–377
Shamseldin A (2007) Use of DNA markers to select well adapted Phaseolus-symbionts under acid and high temperature conditions. Biotechno Lett 29:37–44
Shamseldin A, Werner D (2004) Selection of competitive strains of Rhizobium nodulating Phaseolus vulgaris and adapted to environmental conditions in Egypt, using the gus-reporter gene technique. World J Microbiol Biotechnol 20:377–382
Shamseldin A, Werner D (2005) High salt and high pH tolerance of new isolated Rhizobium etli strains from Egyptian soils. Curr Microbiol 50:11–16
Shamseldin A, Werner D (2007) Presence of Rhizobium etli bv. phaseoli and Rhizobium gallicum bv. gallicum in Egyptian soils. World J Microbiol Biotechnol 23:285–289
Shamseldin A, Vinuesa P, Thierfelder H, Werner D (2005) Rhizobium etli and Rhizobium gallicum nodulate Phaseolus vulgaris in Egyptian soils and display cultivar-dependent symbiotic efficiency. Symbiosis 38:145–161
Silva C, Vinuesa P, Eguiarte LE, Martínez-Romero E, Souza V (2003) 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 69:884–893
Souza V, Eguiarte L, Avila G, Cappello R, Gallardo C, Montoya J, Piñero D (1994) Genetic structure of Rhizobium etli biovar phaseoli associated with wild and cultivated bean plants (Phaseolus vulgaris and Phaseolus coccineus) in Morelos. Mexico Appl Environ Microbiol 60:1260–1268
Talbi C, Delgado MJ, Girard L, Ramírez-Trujillo A, Caballero-Mellado J, Bedmar EJ (2010) Burkholderia phymatum strains capable of nodulating Phaseolus vulgaris are present in Moroccan soils. Appl Environ Microbiol 76:4587–4591
Tamimi SM, Young JPW (2004) Rhizobium etli is the dominant common bean nodulating rhizobia in cultivated soils from different locations in Jordan. Appl Soil Ecol 26:193–200
Tong W, Li X, Wang E, Cao Y, Chen W, Tao S, Wei G (2020) Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts. BMC Genom 21:186
Valverde A, Igual JM, Peix A, Cervantes E, Velazquez E (2006) Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol 56:2631–2637
Valverde A, Velázquez E, Cervantes E, Igual JM, van Berkum P (2011) Evidence of an American origin for symbiosis-related genes in Rhizobium lusitanum. Appl Environ Microbiol 77:5665–5670
Velázquez E, Martínez-Romero E, Rodríguez-Navarro DN, Trujillo ME, Daza A, Mateos PF, Martínez-Molina E, van Berkum P (2001) Characterization of rhizobial isolates of Phaseolus vulgaris by staircase electrophoresis of low-molecular-weight RNA. Appl Environ Microbiol 67:1008–1010
Verástegui-Valdés MM, Zhang YJ, Rivera-Orduna FN, Cheng HP, Sui XH, Wang ET (2014) Microsymbionts of Phaseolus vulgaris in acid and alkaline soils of Mexico. Syst Appl Microbiol 37:605–612
Wang TE, Chen WX (2004) Estimation of biotic and a biotic factors that affect migration of Rhizobia. In: Werner D (ed) Biological resources and migration. Springer, Berlin
Wang ET, Martinez-Romero E (2000) Sesbania herbacea-Rhizobium huautlense nodulation in floded soils and comparative characterization of S. herbacea-nodulating Rhizobium in different environments. Microbiol Ecol 40:25–32
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14
Wang F, Wang TE, Wu LJ, Sui XH Jr, Ying L, Chen WX (2011) Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int J Syst Evol Microbiol 61:2582–2588
Wang L, Cao Y, Wang ET, Ya J, Qiao S, Jiao ZS, Liu ZL, Wei GH (2016) Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi Province. Syst Appl Microbiol 39:211–219
Yan J, Yan H, Liu LX, Chen WF, Zhang XX, Verástegui-Valdés MM, Wang ET, Han XZ (2017) Rhizobium hidalgonense sp. nov., a nodule endophytic bacterium of Phaseolus vulgaris in acid soil. Arch Microbiol 199:97–104
Zhang X, Blair MW, Wang S (2008) Genetic diversity of Chinese common bean (Phaseolus vulgaris L.) landraces assessed with simple sequence repeat markers. Theor Appl Gen 117:629–640
Zinga MK, Jaiswal SK, Dakora FD (2017) Presence of diverse rhizobial communities responsible for nodulation of common bean (Phaseolus vulgaris) in South African and Mozambican soils. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw236
Zurdo-Piñeiro JL, Velázquez E, Lorite MJ, Brelles-Mariño G, Schröder EC, Bedmar EJ, Mateos PF, Martínez-Molina E (2004) Identification of fast-growing rhizobia nodulating tropical legumes from Puerto Rico as Rhizobium gallicum and Rhizobium tropici. Syst Appl Microbiol 27:469–477
Zurdo-Piñeiro JL, García-Fraile P, Rivas R, Peix A, León-Barrios M, Willems A, Mateos PF, Martínez-Molina E, Velázquez E, Van Berkum P (2009) Rhizobia from Lanzarote, the Canary Islands, that nodulate Phaseolus vulgaris have characteristics in common with Sinorhizobium meliloti isolates from main land Spain. Appl Environ Microbiol 75:2354–2359
Acknowledgements
This review article was funded under the financial project STDF1268 from the Academy of Scientific Research and Technology Applications, Cairo, Egypt. Special thanks should be given by authors to the reviewers who gave important notes that contributed significantly to strength our manuscript.
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Shamseldin, A., Velázquez, E. The promiscuity of Phaseolus vulgaris L. (common bean) for nodulation with rhizobia: a review. World J Microbiol Biotechnol 36, 63 (2020). https://doi.org/10.1007/s11274-020-02839-w
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DOI: https://doi.org/10.1007/s11274-020-02839-w