Abstract
The term ‘Rhizobium-legume symbiosis’ refers to numerous plant-bacterial interrelationships. Typically, from an evolutionary perspective, these symbioses can be considered as species-to-species interactions, however, such plant-bacterial symbiosis may also be viewed as a low-scale environmental interplay between individual plants and the local microbial population. Rhizobium-legume interactions are therefore highly important in terms of microbial diversity and environmental adaptation thereby shaping the evolution of plant-bacterial symbiotic systems. Herein, the mechanisms underlying and modulating the diversity of rhizobial populations are presented. The roles of several factors impacting successful persistence of strains in rhizobial populations are discussed, shedding light on the complexity of rhizobial-legume interactions.
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Vance C.P., Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources, Plant Physiol., 2001, 127, 390–397
Herridge D.F., Peoples M.B., Boddey R.M., Global inputs of biological nitrogen fixation in agricultural systems, Plant Soil, 2008, 311, 1–18
Unkovich M.J., Baldock J., Peoples M.B., Prospects and problems of simple linear models for estimating symbiotic N2 fixation by crop and pasture legumes, Plant Soil, 2010, 329, 75–89
Peoples M.B., Brockwell J., Herridge D.F., Rochester I.J., Alves B.J.R., Urquiaga S., et al., The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems, Symbiosis, 2009, 48, 1–17
Willems A., The taxonomy of rhizobia: an overview, Plant Soil, 2006, 287, 3–14
Franche C., Lindström K., Elmerich C., Nitrogenfixing bacteria associated with leguminous and non-leguminous plants, Plant Soil, 2009, 321, 35–59
Masson-Boivin C., Giraud E., Perret X., Batut J., Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?, Trends Microbiol., 2009, 17, 458–466
Gyaneshwar P., Hirsch A.M., Moulin L., Wen-Ming Ch., Elliott G.N., Bontemps C., et al., Legumenodulating Betaproteobacteria: diversity, host range, and future prospects, Mol. Plant-Microbe Interact., 2011, 24, 1276–1288
Perret X., Staehelin C., Broughton W.J., Molecular basis of symbiotic promiscuity, Microbiol Mol. Biol. Rev., 2000, 64, 180–201
Ramirez-Bahena M.H., Garcia-Fraile P., Peix A., Valverde A., Rivas R., Igual J.M., et al., Revision of 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 DSM30132 (=NCIMB 11478) as Rhizobium pisi sp. nov., Int. J. Syst. Evol. Microbiol., 2008, 58, 2484–2490
Tian Ch.F., Young J.P.W., Wang E.T., Tamimi S.M., Chen W.X., Population mixing of Rhizobium leguminosarum bv. viciae nodulating Vicia faba: the role of recombination and lateral gene transfer, FEMS Microbiol. Ecol., 2009, 73, 563–576
Doyle J.J., Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria, Trends Plant Sci., 1998, 3, 473–478
Lee A., Hirsch A.M., Choreographing the complex interaction between legumes and α- and β-rhizobia, Plant Signal Behav., 2006, 1, 161–168
Jones K.M., Kobayashi H., Davies B.W., Taga M.E., Walker G.C., How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model, Nat. Rev. Microbiol., 2007, 5, 619–633
den Herder G., Parniske M, The unbearable naivety of legumes in symbiosis, Curr. Opin. Plant Biol. 2009, 12, 491–499
Timmers A.C., Soupene E., Auriac M.C., de Billy F., Vasse J., Boistard P., et al., Saprophytic intracellular rhizobia in alfalfa nodules, Mol. Plant-Microbe Interact., 2000, 13, 1204–1213
Galibert F., Finan T.M., Long S.R., Pühler A., Abola P., Ampe F., et al., The composite genome of the legume symbiont Sinorhizobium meliloti, Science, 2001, 293, 668–672
Gonzalez V., Santamaria R.I., Bustos P., Hernandez-Gonzalez I.L., Medrano-Soto A., Moreno-Hagelsieb G., et al., The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons, Proc. Natl. Acad. Sci. USA, 2006, 103, 3834–3839
Young J.P., Crossman L.C., Johnston A.W., Thomson N.R., Ghazoui Z.F., Hull K.H., et al., The genome of Rhizobium leguminosarum has recognizable core and accessory components, Genome Biol., 2006, 7, R34
Palacios R., Newton W.E. (Eds.), Genomes and genomics of nitrogen-fixing organisms, Springer Netherlands, Dordrecht, 2005
Guo X., Flores M., Mavingui P., Fuentes S.I., Hernandez G., Davila G., et al., Natural genomic design in Sinorhizobium meliloti: novel genomic architectures, Genome Res., 2003, 13, 1810–1817
Król J., Mazur A., Marczak M., Skorupska A., Syntenic arrangements of the surface polysaccharide biosynthesis genes in Rhizobium leguminosarum, Genomics, 2007, 89, 237–247
Konstantinidis K.T., Tjedje J.M., Genomic insights that advance the species definition for prokaryotes, Proc. Natl. Acad. Sci. USA, 2004, 102, 2567–2572
Slater F.R., Bailey M.J., Tett A.J., Turner S.L., Progress towards understanding the fate of plasmids in bacterial communities, FEMS Microbiol. Ecol., 2008, 66, 3–13
Castillo-Ramirez S., Vazques-Castellanos J.F., Gonzalez V., Cevallos M.A., Horizontal gene transfer and diverse functional constrains within a common replication-partitioning system in Alphaproteobacteria: the repABC operon, BMC Genomics, 2009, 10, 536
Mazur A., Majewska B., Stasiak G., Wielbo J., Skorupska A., repABC-based replication systems of Rhizobium leguminosarum bv. trifolii TA1 plasmids: incompatibility and evolutionary analyses, Plasmid, 2011, 66, 53–66
Cervantes-Riviera R., Pedraza-Lopez F., Perez-Segura G., Cevallos M.A., The replication origin of repABC plasmid, BMC Microbiol., 2011, 11, 158
Landeta C., Davalos A., Cevallos M.A., Geiger O., Brom S., Romero D., Plasmids with chromosomelike role in rhizobia, J. Bacteriol., 2011, 193, 1317–1326
Harrison P.W., Lower R.J.P., Kim N.K.D., Young J.P.W., Introducing the bacterial “chromid”: not a chromosome, not a plasmid, Trends Microbiol., 2010, 18, 141–148
Gonzalez V., Acosta J.L., Santamaria R.I., Bustos P., Fernandez J.L., Hernandez-Gonzalez I.L., et al., Conserved symbiotic plasmid DNA sequences in the multireplicon pangenomic structure of Rhizobium etli, Appl. Environ. Microbiol., 2010, 76, 1604–1614
Bentley S., Sequencing the species pan-genome, Nat. Rev. Microbiol., 2009, 7, 258–259
Mazur A., Stasiak G., Wielbo J., Kubik-Komar A., Marek-Kozaczuk M., Skorupska A., Intragenomic diversity of Rhizobium leguminosarum bv. trifolii clover nodule isolates, BMC Microbiol., 2011, 11, 123
Crossmann L.C., Castillo-Ramirez S., McAnnula C., Lozano L., Vernikos G.S., Acosta J.L., et al., A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen fixing bacteria, PLoS One, 2008, 3, e2567
Brom S., Garcia-de los Santos A., de Lourdes-Girard M., Davilla G., Palacios R., Romero D., High-frequency rearrangements in Rhizobium leguminosarum bv. phaseoli plasmids, J. Bacteriol., 1991, 173, 1344–1346
Brom S., Garcia-de los Santos A., Cervantes L., Palacios R., Romero D., In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons, Plasmid, 2000, 44, 34–43
Brom S., Girard L., Tun-Garrido C., Garcia-de los Santos A., Bustos P., Gonzalez V., et al., Transfer of symbiotic plasmid of Rhizobium etli CFN42 requires cointegration with p42a, which may be mediated by site-specific recombination, J. Bacteriol., 2004, 186, 7538–7548
Broughton W.J., Samrey U., Stanley J., Ecological genetics of Rhizobium meliloti: symbiotic plasmid transfer in the Medicago sativa rhizosphere, FEMS Microbiol. Lett., 1987, 40, 251–255
Wernegreen J.J., Harding E.E., Riley M.A., Rhizobium gone native: unexpected plasmid stability of indigenous Rhizobium leguminosarum, Proc. Natl. Acad. Sci. USA, 1997, 94, 5483–5488
Bailly X., Olivieri I., Brunel B., Cleyet-Marel J.-C., Bena G., Horizontal gene transfer and homologous recombination drive the evolution of the nitrogenfixing symbionts of Medicago species, J. Bacteriol., 2007, 189, 5223–5236
Ding H., Hynes M.F., Plasmid transfer systems in the rhizobia, Can. J. Microbiol., 2009, 55, 917–927
Giuntini E., Mengoni A., de Filippo C., Cavalieri D., Aubin-Horth N., Landry C.R., et al., Largescale genetic variation of the symbiosis-required megaplasmid pSymA revealed by comparative genomic analysis of Sinorhizobium meliloti natural strains, BMC Genomics, 2005, 6, 158
Cervantes L., Bustos P., Girard L., Santamaria R.I., Davila G., Vinuesa P., et al., The conjugative plasmid of a bean-nodulating Sinorhizobium fredii strain is assembled from sequences of two Rhizobium plasmids and the chromosome of a Sinorhizobium strain, BMC Microbiol., 2011, 11, 149
Zhang X.-X., Kosier B., Priefer U.B., Symbiotic plasmid rearrangement in Rhizobium leguminosarum bv. viciae VF39SM, J. Bacteriol., 2001, 183, 2141–2144
Fondi M., Bacci G., Brilli M., Papaleo M.C., Mengoni A., Vaneechoutte M., et al., Exploring the evolutionary dynamics of plasmids: the Acinetobacter pan-plasmidome, BMC Evol. Biol., 2010, 10, 59
Pistorio M., Giusti M.A., del Papa M.F., Draghi W.O., Lozano M.J., Tejerizo G.T., et al., Conjugal properties of the Sinorhizobium meliloti plasmid mobilome, FEMS Microbiol. Ecol., 2008, 65, 372–382
Martyniuk S., Oron J., Martyniuk M., Diversity and numbers of root-nodule bacteria (rhizobia) in Polish soils, Acta Soc. Bot. Polon., 2005, 74, 83–86
Drew E.A., Ballard R.A., Improving N2 fixation from the plant down: compatibility of Trifolium subterraneum L. cultivars with soil rhizobia can influence symbiotic performance, Plant Soil, 2010, 327, 261–277
Ballard R.A., Charman N., McInnes A., Davidson J.A., Size, symbiotic effectiveness and genetic diversity of field pea rhizobia (Rhizobium leguminosarum bv. viciae) populations in South Australian soils, Soil Biol. Biochem., 2010, 36, 1347–1355
Silva C., Kan F.L., Martinez-Romero E., Population genetic structure of Sinorhizobium meliloti and S. medicae isolated from nodules of Medicago spp. in Mexico, FEMS Microbiol. Ecol., 2007, 60, 477–489
Depret G., Laguerre G., Plant phenology and genetic variability on root and nodule development strongly influence genetic structuring of Rhizobium leguminosarum biovar viciae populations nodulating pea, New Phytol., 2008, 179, 224–235
Sachs J.L., Kembel S.W., Lau A.H., Simms E.L., In situ phylogenetic structure and diversity of wild Bradyrhizobium communities, Appl. Environ. Microbiol., 2009, 75, 4727–4735
Wielbo J., Marek-Kozaczuk M., Mazur A., Kubik-Komar A., Skorupska A., Genetic and metabolic divergence within a Rhizobium leguminosarum bv. trifolii population recovered from clover nodules, Appl. Environ. Microbiol., 2010, 76, 4593–4600
Wielbo J., Marek-Kozaczuk M., Mazur A., Kubik-Komar A., Skorupska A., The structure and metabolic diversity of population of pea microsymbionts isolated from root nodules, British Microbiology Research Journal, 2011, 1, 55–69
Lakzian A., Murphy P., Turner A., Beynon J.L., Giller K.E., Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance, Soil Biol. Biochem., 2002, 34, 519–529
Castro I.V., Ferreira E.M., McGrath S.P., Survival and plasmid stability of rhizobia introduced into a contaminated soil, Soil Biol. Biochem., 2003, 35, 49–54
Lakzian A., Murphy P., Giller K.E., Transfer and loss of naturally-occurring plasmids among isolates of Rhizobium leguminosarum bv. viciae in heavy metal contaminated soils, Soil Biol. Biochem., 2007, 39, 1066–1077
Laguerre G., Courde L., Nouaim R., Lamy I., Revellin C., Breuil M.C., et al., Response of rhizobial populations to moderate copper stress applied to an agricultural soil, Microbiol. Ecol., 2006, 52, 426–435
Denison R.F., Kiers E.T., Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis, FEMS Microbiol. Lett., 2004, 237, 187–193
Denison R.F., Kiers E.T., Why are most rhizobia beneficial to their plant hosts, rather than parasitic?, Microbes Infect., 2004, 6, 1235–1239
Simms E.L., Taylor D.L., Partner choice in nitrogenfixation mutualism of legumes and rhizobia, Integr. Comp. Biol., 2002, 42, 369–380
Oono R., Denison R.F., Kiers E.T., Controlling the reproductive fate of rhizobia: how universal are legume sanctions?, New Phytol., 2009, 183, 967–979
Stuurman N., Bras C.P., Schlaman H.R.M., Wijfjes A.H.M., Bloemberg G., Spaink H.P., Use of green fluorescent protein color variants expressed on stable broad-host-range vectors to visualize rhizobia interacting with plants, Mol. Plant Microbe Interact., 2000, 13, 1163–1169
Gage D.J., Infection and invasion of roots by symbiotic nitrogen-fixing rhizobia during nodulation of temperate legumes, Microbiol. Mol. Biol. Rev., 2004, 68, 280–300
Wielbo J., Kuske J., Marek-Kozaczuk M., Skorupska A., The competition between Rhizobium leguminosarum bv. viciae strains progresses until late stages of symbiosis, Plant Soil, 2010, 337, 125–135
Wielbo J., Marek-Kozaczuk M., Kidaj D., Skorupska A., Competitiveness of Rhizobium leguminosarum bv. trifolii strains in mixed inoculation of clover (Trifolium pratense), Pol. J. Microbiol., 2011, 60, 43–49
McInnes A., Thies J.E., Abbott L.K., Howieson J.G., Structure and diversity among rhizobial strains, populations and communities - a review, Soil Biol. Biochem., 2004, 36, 1295–1308
Vlassak K.M., Vanderleyden J., Factors influencing nodule occupancy by inoculant rhizobia, Crit. Rev. Plant Sci., 1997, 16, 163–229
Robleto E.A., Kmiecik K., Oplinger E.S., Nienhuis J., Triplett E.W., Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions, Appl. Environ. Microbiol., 1998, 64, 2630–2633
Wilson R.A., Handley B.A., Beringer J.E., Bacteriocin production and resistance in a field population of Rhizobium leguminosarum bv. viciae, Soil Biol. Biochem., 1998, 30, 413–417
Oresnik I.J., Twelker S., Hynes M.F., Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins, Appl. Environ. Microbiol., 1999, 65, 2833–2840
Hynes M.F., O’Connel M.P. Host plant effect on competition among strains of Rhizobium leguminosarum, Can. J. Microbiol., 1990, 36, 864–869
Yost C.K., Rath A.M., Noel T.C., Hynes M.F., Characterization of genes involved in erythritol catabolism in Rhizobium leguminosarum bv. viciae, Microbiology, 2006, 152, 2061–2074
Kohler P.R.A., Zheng J.Y., Schoffers E., Rossbach S., Inositol catabolism, a key pathway in Sinorhizobium meliloti for competitive host nodulation, Appl. Environ. Microbiol., 2010, 76, 7972–7980
Wielbo J., Marek-Kozaczuk M., Kubik-Komar A., Skorupska A., Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness, Can. J. Microbiol., 2007, 53, 957–967
Ramachandran V.K., East A.K., Karunakaran R., Downie A., Poole P.S., Adaptation of Rhizobium leguminosarum to pea, alfalfa and sugar beet rhizospheres investigated by comparative transcriptomics, Genome Biol. 2011, 12, R106
Gaworzewska E.T., Carlile M.J., Positive chemotaxis of Rhizobium leguminosarum and other bacteria towards root exudates from legumes and other plants, J. Gen. Microbiol., 1982, 128, 1179–1188
Bertin C., Yang X., Weston L.A., The role of root exudates and allelochemicals in the rhizosphere, Plant Soil, 2003, 256, 67–83
Prell J., Poole P., Metabolic changes of rhizobia in legume nodules, Trends Microbiol., 2006, 14, 161–168
White J., Prell J., James E.K., Poole P., Nutrient sharing between symbionts, Plant Physiol., 2007, 144, 604–614
Mellor H.Y., Glenn A.R., Dilworth M.J., Symbiotic and competitive properties of motility mutants of Rhizobium trifolii TA1, Arch. Microbiol., 1987, 148, 34–39
Miller L.D., Yost C.K., Hynes M.F., Alexandre G., The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol. Microbiol., 2007, 63, 348–362
Mabood F., Jung W.J., Smith D.L., Signals in the underground: microbial signaling and plant productivity, In: Nautiyal C.S., Dion P.E., Chopra V.L. (Eds.), Molecular mechanisms of plant and microbe coexistence, Springer-Verlag Berlin, Heidelberg, 2008
Maj D., Wielbo J., Marek-Kozaczuk M., Skorupska A., Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum, Microbiol. Res., 2010, 165, 50–60
Mongiardini E.J., Ausmees N., Perez-Gimenez J., Althabegoiti M.J., Quelas J.I., Lopez-Garcia S.L., et al., The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation, FEMS Microbiol. Ecol., 2008, 65, 279–288
Mongiardini E.J., Perez-Gimenez J., Althabegoiti M.J., Covelli J., Quelas J.I., Lopez-Garcia S.L., et al., Overproduction of the rhizobial adhesion RapA1 increases competitiveness for nodulation, Soil. Biol. Biochem., 2009, 41, 2017–2020
Moënne-Loccoz Y., Weaver R.W., Involvement of plasmids in saprophytic performance and sodium chloride tolerance of clover rhizobia W14-2 in vitro, Appl. Soil Ecol., 1996, 3, 137–148
Vinuesa P., Neumann-Silkow F., Pacios-Bras C., Spaink H.P., Martinez-Romero E., Werner D., Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness, Mol. Plant-Microbe Interact., 2003, 16, 159–168
Streeter J.G., Effect of trehalose on survival of Bradyrhizobium japonicum during desiccation, J. Appl. Microbiol., 2003, 95, 484–491
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
Wielbo J., Kidaj D., Koper P., Kubik-Komar A., Skorupska A., The effect of biotic and physical factors on the competitive ability of Rhizobium leguminosarum, Cent. Eur. J. Biol., 2012, 7, 13–24
Duodu S., Bhuvaneswari T.V., Gudmundsson J., Svenning M.M., Symbiotic and saprophytic survival of three unmarked Rhizobium leguminosarum biovar trifolii strains introduced into the field, Environ. Microbiol., 2005, 7, 1049–1058
Jensen E.S., Sorensen L.H., Survival of Rhizobium leguminosarum in soil after addition as inoculants, FEMS Microbiol. Ecol., 1987, 45, 221–226
Svenning M.M., Gudmundsson J., Fagerli I.L., Leinonen P., Competition for nodule occupancy between introduced strains of Rhizobium leguminosarum bv. trifolii and its influence on plant production, Ann. Bot., 2001, 88, 781–787
Martyniuk S., Wozniakowska A., Martyniuk M., Effect of agricultural practices on populations of Rhizobium in some field experiments, Bot. Lithuanica, 1999, suppl. 3, 99–102
Palmer K.M., Young J.P.W., Higher diversity of Rhizobium leguminosarum biovar viciae populations in arable soils than in grassland soils, Appl. Environ. Microbiol., 2000, 66, 2445–2450
Rangin C., Brunel B., Cleyet-Marel J.-C., Perrineau M.-M., Bena G., Effects of Medicago truncatula genetic diversity, rhizobial competition, and strain effectiveness on the diversity of a natural Sinorhizobium species community, Appl. Environ. Microbiol., 2008, 74, 5653–5661
Ikeda S., Okubo T., Anda M., Nakashita H., Yasuda M., Sato S., et al., Community- and genomebased views of plant-associated bacteria: plantbacterial interactions in soybean and rice, Plant Cell Physiol., 2010, 51, 1398–1410
Gubry-Rangin C., Garcia M., Bena G., Partner choice in Medicago truncatula-Sinorhizobium symbiosis, Proc. R. Soc. B., 2010, 277, 1947–1951
Laguerre G., Depret G., Bourion V., Duc G., Rhizobium leguminosarum bv. viciae genotypes interact with pea plants in developmental responses of nodules, roots and shoots, New Phytol., 2007, 176, 680–690
Barcellos F.G., Menna P., da Silva Batista J.S., Hungria M., Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in Brazilian savannah soil, Appl. Environ. Microbiol., 2007, 73, 2635–2643
Steenkamp E.T., Stępkowski T., Przymusiak A., Botha W.J., Law I.J., Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harboring nodulation genes that belong to the large pantropical clade common in Africa, Mol. Phylogenet. Evol., 2008, 48, 1131–1144
Estrella M.J., Munoz S., Soto M.J., Ruiz O., Sanjuan J., Genetic diversity and host range of rhizobia nodulating Lotus tenuis in typical soils of the Salado River basin (Argentina), Appl. Environ. Microbiol., 2009, 75, 1088–1098
Aoki S., Kondo T., Prevost D., Nakata S., Kajita T., Ito M., Genotypic and phenotypic diversity of rhizobia isolated from Lathyrus japonicus indigenous to Japan, Syst. Appl. Microbiol., 2010, 33, 383–397
Alvarez-Martinez E.R., Valverde A., Ramirez-Bahena M.H., Garcia-Fraile P., Tejedor C., Mateos P.F., et al., The analysis of core and symbiotic genes reveals their common phylogenetic origin and suggests the distribution of Rhizobium leguminosarum strains together with Vicia seeds, Arch. Microbiol., 2009, 191, 659–668
Han T.X, Tian Ch.F., Wang E.T., Chen W.X., Associations among rhizobial chromosomal background, nod genes and host plants based on the analysis of symbiosis of indigenous rhizobia and wild legumes native to Xinjiang, Microb. Ecol., 2010, 59, 311–323
Stępkowski T., Moulin L., Krzyżanska A., McInnes A., Law I.J., Howieson J., European origin of Bradyrhizobium populations infecting lupins and serradella in soils of Western Australia and South Africa, Appl. Environ. Microbiol., 2005, 71, 7041–7052
Stępkowski T., Hughes C.E., Law I.J., Markiewicz Ł., Gurda D., Chlebicka A., et al., Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees, Appl. Environ. Microbiol., 2007, 73, 3254–3264
de Meyer S.E., van Hoorde K., Vekeman B., Braeckman T., Willems A., Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium), Soil Biol. Biochem., 2011, 43, 2384–2396
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. USA, 2004, 101, 13548–13553
Martinez-Romero E., Coevolution in Rhizobiumlegume symbiosis?, DNA Cell Biol., 2009, 28, 361–370
Doyle J.J., Phylogenetic perspectives on the origins of nodulation, Mol. Plant-Microbe Interact., 2011, 24, 1289–1295
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Wielbo, J. Rhizobial communities in symbiosis with legumes: genetic diversity, competition and interactions with host plants. cent.eur.j.biol. 7, 363–372 (2012). https://doi.org/10.2478/s11535-012-0032-5
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DOI: https://doi.org/10.2478/s11535-012-0032-5