Symbiosis Genes: Organisation and Diversity

Wang, En Tao; Young, J. Peter W.

doi:10.1007/978-981-32-9555-1_5

En Tao Wang⁶ &
J. Peter W. Young⁷

756 Accesses
2 Citations

Abstract

With only specific exceptions, almost all the symbiotic rhizobia have a set of symbiosis genes that include nodulation- and N₂-fixing-related genes. Organisation of the symbiosis genes and their roles in the synthesis of Nod factors (LCOs) and nitrogen fixation are first illustrated and compared. Then the diversity and phylogeny of the nodulation gene nodC are discussed in detail in various rhizobia with narrow or broad host ranges. The relationship between the nodC phylogeny and the rhizobial host range is explored in detail.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Chapter: USD 29.95; Price excludes VAT (USA)

eBook: USD 129.00; Price excludes VAT (USA)

Softcover Book: USD 169.99; Price excludes VAT (USA)

Hardcover Book: USD 169.99; Price excludes VAT (USA)

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

Aguilar OM, 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;101:13548–53.
Article CAS Google Scholar
Amarger N, Bours M, Revoy F, Allard MR, Laguerre G. Rhizobium tropici nodulates field-grown Phaseolus vulgaris in France. Plant Soil. 1994;161(2):147–56. https://doi.org/10.1007/BF00046386.
Article CAS Google Scholar
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.
Article CAS Google Scholar
Andrews M, Andrews ME. Specificity in legume-rhizobia symbioses. Int J Mol Sci. 2017;18(4):705.
Article Google Scholar
Bec-Ferte M-P, Krishnan HB, Prome D, Savagnac A, Pueppke SG, Prome J-C. Structures of nodulation factors from the nitrogen-fixing soybean symbiont Rhizobium fredii USDA257. Biochemistry. 1994;33(39):11782–8. https://doi.org/10.1021/bi00205a014.
Article CAS PubMed Google Scholar
Cao Y, Wang E-T, Zhao L, Chen W-M, Wei G-H. Diversity and distribution of rhizobia nodulated with Phaseolus vulgaris in two ecoregions of China. Soil Biol Biochem. 2014;78:128–37. https://doi.org/10.1016/j.soilbio.2014.07.026.
Article CAS Google Scholar
Chang YL, Wang JY, Wang ET, Liu HC, Sui XH, Chen WX. Bradyrhizobium lablabi sp. nov., isolated from effective nodules of Lablab purpureus and Arachis hypogaea. Int J Syst Evol Microbiol. 2011;61(10):2496–502. https://doi.org/10.1099/ijs.0.027110-0.
Article PubMed Google Scholar
Chen WF, Guan SH, Zhao CT, Yan XR, Man CX, Wang ET, Chen WX. Different Mesorhizobium species associated with Caragana carry similar symbiotic genes and have common host ranges. FEMS Microbiol Lett. 2008;283(2):203–9. https://doi.org/10.1111/j.1574-6968.2008.01167.x.
Article CAS PubMed Google Scholar
Chen J, Hu M, Ma H, Wang Y, Wang ET, Zhou Z, Gu J. Genetic diversity and distribution of bradyrhizobia nodulating peanut in acid-neutral soils in Guangdong Province. Syst Appl Microbiol. 2016;39(6):418–27. https://doi.org/10.1016/j.syapm.2016.06.002.
Article PubMed Google Scholar
D’Haeze W, Holsters M. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology. 2002;12(6):79R–105R. https://doi.org/10.1093/glycob/12.6.79R.
Article PubMed Google Scholar
Dall’Agnol RF, Ribeiro RA, Delamuta JRM, Ormeno-Orrillo E, Rogel MA, Andrade DS, Martinez-Romero E, Hungria M. 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. 2014;64:3222–9. https://doi.org/10.1099/ijs.0.064543-0.
Article PubMed Google Scholar
Estrella MJ, Muñoz S, Soto MJ, Ruiz O, Sanjuán 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(4):1088–98. https://doi.org/10.1128/aem.02405-08.
Article CAS PubMed Google Scholar
Faruque OM, Miwa H, Yasuda M, Fujii Y, Kaneko T, Sato S, Okazaki S. Identification of Bradyrhizobium elkanii genes involved in incompatibility with soybean plants carrying the Rj4 allele. Appl Environ Microbiol. 2015;81(19):6710–7. https://doi.org/10.1128/AEM.01942-15.
Article CAS PubMed PubMed Central Google Scholar
Fischer H-M. Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev. 1994;58(3):352–86.
CAS PubMed PubMed Central Google Scholar
Flores-Félix JD, Carro L, Velázquez E, Valverde A, Cerda-Castillo E, Garcia-Fraile P, Rivas R. Phyllobacterium endophyticum sp. nov. isolated from nodules of Phaseolus vulgaris in Northern Spain. Int J Syst Evol Microbiol. 2012;63:821–6. https://doi.org/10.1099/ijs.0.038497-0.
Article CAS PubMed Google Scholar
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;56:657–66.
Article Google Scholar
Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Vermeglio A, Medigue C, Sadowsky M. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science. 2007;316(5829):1307–12. https://doi.org/10.1126/science.1139548.
Article PubMed Google Scholar
Hageman RV, Burris RH. Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle. Proc Natl Acad Sci U S A. 1978;75(6):2699–702.
Article CAS Google Scholar
Jarvis BDW, Van Berkum P, Chen WX, Nour SM, Fernandez MP, Cleyet-Marel JC, Gillis M. Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol. 1997;47(3):895–8. https://doi.org/10.1099/00207713-47-3-895.
Article Google Scholar
Ji Z, Yan H, Cui Q, Wang E, Chen W, Chen W. Genetic divergence and gene flow among Mesorhizobium strains nodulating the shrub legume Caragana. Syst Appl Microbiol. 2015;38(3):176–83. https://doi.org/10.1016/j.syapm.2015.02.007.
Article CAS PubMed Google Scholar
Jiao YS, Liu YH, Yan H, Wang ET, Tian CF, Chen WX, Guo BL, Chen WF. Rhizobial diversity and nodulation characteristics of the extremely promiscuous legume Sophora flavescens. Mol Plant-Microbe Interact. 2015a;28(12):1338–52. https://doi.org/10.1094/mpmi-06-15-0141-r.
Article CAS PubMed Google Scholar
Jiao YS, Yan H, Ji ZJ, Liu YH, Sui XH, Wang ET, Guo BL, Chen WX, Chen WF. Rhizobium sophorae sp. nov. and Rhizobium sophoriradicis sp. nov., nitrogen-fixing rhizobial symbionts of the medicinal legume Sophora flavescens. Int J Syst Evol Microbiol. 2015b;65(2):497–503. https://doi.org/10.1099/ijs.0.068916-0.
Article CAS PubMed Google Scholar
Jiao J, Wu LJ, Zhang B, Hu Y, Li Y, Zhang XX, Guo HJ, Liu LX, Chen WX, Zhang Z, Tian CF. MucR is required for transcriptional activation of conserved ion transporters to support nitrogen fixation of Sinorhizobium fredii in soybean nodules. Mol Plant-Microbe Interact. 2016;29(5):352–61. https://doi.org/10.1094/MPMI-01-16-0019-R.
Article CAS PubMed Google Scholar
Jimenez-Guerrero I, Acosta-Jurado S, Del Cerro P, Navarro-Gomez P, Lopez-Baena FJ, Ollero FJ, Vinardell JM, Perez-Montano F. Transcriptomic studies of the effect of nod gene-inducing molecules in rhizobia: different weapons, one purpose. Genes (Basel). 2017;9(1):E1. https://doi.org/10.3390/genes9010001.
Article CAS Google Scholar
Kneip C, Lockhart P, Voss C, Maier UG. Nitrogen fixation in eukaryotes – new models for symbiosis. BMC Evol Biol. 2007;7:55. https://doi.org/10.1186/1471-2148-7-55.
Article CAS PubMed PubMed Central Google Scholar
Laguerre G, Nour SM, 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(Pt 4):981–93. https://doi.org/10.1099/00221287-147-4-981.
Article CAS PubMed Google Scholar
Laranjo M, Young JPW, Oliveira S. Multilocus sequence analysis reveals multiple symbiovars within Mesorhizobium species. Syst Appl Microbiol. 2012;35(6):359–67.
Article CAS Google Scholar
Leigh JA, Signer ER, Walker GC. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A. 1985;82(18):6231–5. https://doi.org/10.1073/pnas.82.18.6231.
Article CAS PubMed PubMed Central Google Scholar
Lewin A, Cervantes E, Chee-Hoong W, Broughton WJ. nodSU, two new nod genes of the broad host range Rhizobium strain NGR234 encode host-specific nodulation of the tropical tree Leucaena leucocephala. Mol Plant-Microbe Interact. 1990;3(5):317–26.
Article CAS Google Scholar
Li M, Li Y, Chen WF, Sui XH, Li Y, Li Y, Wang ET, Chen WX. Genetic diversity, community structure and distribution of rhizobia in the root nodules of Caragana spp. from arid and semi-arid alkaline deserts, in the north of China. Syst Appl Microbiol. 2012;35(4):239–45. https://doi.org/10.1016/j.syapm.2012.02.004.
Article PubMed Google Scholar
Li YH, Wang R, Zhang XX, Young JPW, Wang ET, Sui XH, Chen WX. Bradyrhizobium guangdongense sp. nov. and Bradyrhizobium guangxiense sp. nov., isolated from effective nodules of peanut. Int J Syst Evol Microbiol. 2015;65(12):4655–61. https://doi.org/10.1099/ijsem.0.000629.
Article CAS PubMed Google Scholar
Liu YH, Jiao YS, Liu LX, Wang D, Tian CF, Wang ET, Wang L, Chen WX, Wu SY, Guo BL, Guan ZG, Poinsot V, Chen WF. Nonspecific symbiosis between Sophora flavescens and different rhizobia. Mol Plant-Microbe Interact. 2018a;31(2):224–32. https://doi.org/10.1094/mpmi-05-17-0117-r.
Article CAS PubMed Google Scholar
Liu YH, Wang ET, Jiao YS, Tian CF, Wang L, Wang ZJ, Guan JJ, Singh RP, Chen WX, Chen WF. Symbiotic characteristics of Bradyrhizobium diazoefficiens USDA 110 mutants associated with shrubby sophora (Sophora flavescens) and soybean (Glycine max). Microbiol Res. 2018b;214:19–27. https://doi.org/10.1016/j.micres.2018.05.012.
Article CAS PubMed Google Scholar
Long SR. Rhizobium symbiosis: nod factors in perspective. Plant Cell. 1996;8(10):1885–98. https://doi.org/10.1105/tpc.8.10.1885.
Article CAS PubMed PubMed Central Google Scholar
Lorite MJ, Estrella MJ, Escaray FJ, Sannazzaro A, Videira e Castro IM, Monza J, Sanjuán J, León-Barrios M. The rhizobia-Lotus symbioses: deeply specific and widely diverse. Front Microbiol. 2018;9:2055. https://doi.org/10.3389/fmicb.2018.02055.
Article PubMed PubMed Central Google Scholar
Lu YL, Chen WF, Wang ET, Guan SH, Yan XR, Chen WX. Genetic diversity and biogeography of rhizobia associated with Caragana species in three ecological regions of China. Syst Appl Microbiol. 2009;32(5):351–61. https://doi.org/10.1016/j.syapm.2008.10.004.
Article CAS PubMed Google Scholar
Marie C, Broughton WJ, Deakin WJ. Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol. 2001;4(4):336–42. https://doi.org/10.1016/S1369-5266(00)00182-5.
Article CAS PubMed Google Scholar
Martinez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris l. beans and Leucaena sp. trees. Int J Syst Bacteriol. 1991;41(3):417–26.
Article CAS Google Scholar
Mulas D, García-Fraile P, Carro L, Ramírez-Bahena MH, 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;43:2283–93.
Article CAS Google Scholar
Nelson MS, Sadowsky MJ. Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes. Front Plant Sci. 2015;6:491. https://doi.org/10.3389/fpls.2015.00491.
Article PubMed PubMed Central Google Scholar
Nguyen TD, Heenan PB, De Meyer SE, James TK, Chen W-M, Morton JD, Andrews M. Genetic diversity and nitrogen fixation of mesorhizobia symbionts of New Zealand endemic Sophora species. N Z J Bot. 2017;55(4):466–78. https://doi.org/10.1080/0028825X.2017.1376689.
Article Google Scholar
Nour SM, Fernandez MP, Normand P, Cleyet-Marel JC. Rhizobium ciceri sp. nov., consisting of strains that nodulate chickpeas (Cicer arietinum L.). Int J Syst Bacteriol. 1994;44(3):511–22.
Article CAS Google Scholar
Nour SM, Cleyet-Marel JC, Normand P, Fernandez MP. Genomic heterogeneity of strains nodulating chickpeas (Cicer arietinum L.) and description of Rhizobium mediterraneum sp. nov. Int J Syst Bacteriol. 1995;45(4):640–8.
Article CAS Google Scholar
Ormeño-Orrillo E, Aguilar-Cuba Y, ZúñigaDávila D. Draft genome sequence of Rhizobium sophoriradicis H4, a nitrogen-fixing bacterium associated with the leguminous plant Phaseolus vulgaris on the coast of Peru. Genome Announc. 2018;6(21):e00241–18.
Article Google Scholar
Ramírez-Bahena MH, García-Fraile P, Peix A, Valverde A, Rivas R, Igual JM, Mateos PF, Martínez-Molina E, Velázquez E. 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. 2008;58(11):2484–90. https://doi.org/10.1099/ijs.0.65621-0.
Article CAS PubMed Google Scholar
Ramírez-Bahena M-H, Chahboune R, Velázquez E, Gómez-Moriano A, Mora E, Peix A, Toro M. Centrosema is a promiscuous legume nodulated by several new putative species and symbiovars of Bradyrhizobium in various American countries. Syst Appl Microbiol. 2013;36(6):392–400. https://doi.org/10.1016/j.syapm.2013.03.007.
Article CAS PubMed Google Scholar
Ribeiro RA, Rogel MA, López-López A, Ormeño-Orrillo E, Barcellos FG, Martínez J, Thompson FL, Martínez-Romero E, Hungria M. Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol. 2012;62(5):1179–84. https://doi.org/10.1099/ijs.0.032912-0.
Article PubMed Google Scholar
Rivas R, Laranjo M, Mateos PF, Oliveira S, Martínez-Molina E, Velázquez E. Strains of Mesorhizobium amorphae and Mesorhizobium tianshanense, carrying symbiotic genes of common chickpea endosymbiotic species, constitute a novel biovar (ciceri) capable of nodulating Cicer arietinum. Lett Appl Microbiol. 2007;44(4):412–8.
Article CAS Google Scholar
Sanjuan J, Carlson RW, Spaink HP, Bhat UR, Barbour WM, Glushka J, Stacey G. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc Natl Acad Sci U S A. 1992;89(18):8789–93. https://doi.org/10.1073/pnas.89.18.8789.
Article CAS PubMed PubMed Central Google Scholar
Santos JWM, Silva JF, Ferreira TDS, Dias MAM, Fraiz ACR, Escobar IEC, Santos RC, Lima LM, Morgante CV, Fernandes-Júnior PI. Molecular and symbiotic characterization of peanut bradyrhizobia from the semi-arid region of Brazil. Appl Soil Ecol. 2017;121:177–84. https://doi.org/10.1016/j.apsoil.2017.09.033.
Article Google Scholar
Segovia L, Young JPW, Martínez-Romero E. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int J Syst Bacteriol. 1993;43(2):374–7.
Article CAS Google Scholar
Shamseldin A. The role of different genes involoved in symbiotic nitrogen fixation – review. Glob J Biotechnol Biochem. 2013;8(4):84–94.
CAS Google Scholar
Sugawara M, Epstein B, Badgley BD, Unno T, Xu L, Reese J, Gyaneshwar P, Denny R, Mudge J, Bharti AK, Farmer AD, May GD, Woodward JE, Médigue C, Vallenet D, Lajus A, Rouy Z, Martinez-Vaz B, Tiffin P, Young ND, Sadowsky MJ. Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies. Genome Biol. 2013;14(2):R17. https://doi.org/10.1186/gb-2013-14-2-r17.
Article CAS PubMed PubMed Central Google Scholar
Sullivan JT, Eardly BD, van Berkum P, Ronson CW. Four unnamed species of nonsymbiotic rhizobial isolated from the rhizosphere of Lotus corniculatus. Appl Environ Microbiol. 1996;62:2818–25.
CAS PubMed PubMed Central Google Scholar
Tian CF, Zhou YJ, Zhang YM, Li QQ, Zhang YZ, Li DF, Wang S, Wang J, Gilbert LB, Li YR, Chen WX. Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc Natl Acad Sci U S A. 2012;109(22):8629–34. https://doi.org/10.1073/pnas.1120436109.
Article PubMed PubMed Central Google Scholar
Valverde A, Igual JM, Peix A, Cervantes E, Velázquez E. Rhizobium lusitanum sp. nov. a bacterium that nodulates Phaseolus vulgaris. Int J Syst Evol Microbiol. 2006;56:2631–7.
Article CAS Google Scholar
Wang ET, van Berkum P, Sui XH, Beyene D, Chen WX, Martinez-Romero E. Diversity of rhizobia associated with Amorpha fruticosa isolated from Chinese soils and description of Mesorhizobium amorphae sp. nov. Int J Syst Bacteriol. 1999;49(Pt 1):51–65. https://doi.org/10.1099/00207713-49-1-51.
Article PubMed Google Scholar
Wang ET, Rogel MA, Sui XH, Chen WX, Martinez-Romero E, van Berkum P. Mesorhizobium amorphae, a rhizobial species that nodulates Amorpha fruticosa, is native to American soils. Arch Microbiol. 2002;178(4):301–5. https://doi.org/10.1007/s00203-002-0448-9.
Article CAS PubMed Google Scholar
Wang F, Wang ET, Wu LJ, Sui XH, Li Y, Chen WX. Rhizobium vallis sp. nov., isolated from nodules of three leguminous species. Int J Syst Evol Microbiol. 2011;61(11):2582–8. https://doi.org/10.1099/ijs.0.026484-0.
Article PubMed Google Scholar
Wang D, Xue H, Wang Y, Yin R, Xie F, Luo L. The Sinorhizobium meliloti ntrX gene is involved in succinoglycan production, motility, and symbiotic nodulation on alfalfa. Appl Environ Microbiol. 2013a;79(23):7150–9. https://doi.org/10.1128/aem.02225-13.
Article CAS PubMed PubMed Central Google Scholar
Wang R, Chang YL, Zheng WT, Zhang D, Zhang XX, Sui XH, Wang ET, Hu JQ, Zhang LY, Chen WX. Bradyrhizobium arachidis sp. nov., isolated from effective nodules of Arachis hypogaea grown in China. Syst Appl Microbiol. 2013b;36(2):101–5. https://doi.org/10.1016/j.syapm.2012.10.009.
Article CAS PubMed Google Scholar
Wang L, Cao Y, Wang ET, Qiao YJ, Jiao S, Liu ZS, Zhao L, Wei GH. Biodiversity and biogeography of rhizobia associated with common bean (Phaseolus vulgaris L.) in Shaanxi Province. Syst Appl Microbiol. 2016;39(3):211–9. https://doi.org/10.1016/j.syapm.2016.02.001.
Article PubMed Google Scholar
Wang D, Couderc F, Tian CF, Gu WJ, Xue LL, Poinsot V. Conserved composition of nod factors and exopolysaccharides produced by different phylogenetic lineage Sinorhizobium strains nodulating soybean. Front Microbiol. 2018;9:2852.
Article Google Scholar
Wu LJ, Wang HQ, Wang ET, Chen WX, Tian CF. Genetic diversity of nodulating and non-nodulating rhizobia associated with wild soybean (Glycine soja Sieb. & Zucc.) in different ecoregions of China. FEMS Microbiol Ecol. 2011;76(3):439–50. https://doi.org/10.1111/j.1574-6941.2011.01064.x.
Article CAS PubMed Google Scholar
Yan H, Xie JB, Ji ZJ, Yuan N, Tian CF, Ji SK, Wu ZY, Zhong L, Chen WX, Du ZL, Wang ET, Chen WF. Evolutionarily conserved nodE, nodO, T1SS, and hydrogenase system in rhizobia of Astragalus membranaceus and Caragana intermedia. Front Microbiol. 2017;8:2282. https://doi.org/10.3389/fmicb.2017.02282.
Article PubMed PubMed Central Google Scholar
Zhang YM, Li Y Jr, Chen WF, Wang ET, Tian CF, Li QQ, Zhang YZ, Sui XH, Chen WX. Biodiversity and biogeography of rhizobia associated with soybean plants grown in the North China Plain. Appl Environ Microbiol. 2011;77(18):6331–42. https://doi.org/10.1128/aem.00542-11.
Article CAS PubMed PubMed Central Google Scholar
Zhang JJ, Liu TY, Chen WF, Wang ET, Sui XH, Zhang XX, Li Y, Li Y, Chen WX. Mesorhizobium muleiense sp. nov., nodulating with Cicer arietinum L. Int J Syst Evol Microbiol. 2012;62(11):2737–42. https://doi.org/10.1099/ijs.0.038265-0.
Article CAS PubMed Google Scholar
Zhang J, Guo C, Chen W, de Lajudie P, Zhang Z, Shang Y, Wang ET. Mesorhizobium wenxiniae sp. nov., isolated from chickpea (Cicer arietinum L.) in China. Int J Syst Evol Microbiol. 2018a;68(6):1930–6. https://doi.org/10.1099/ijsem.0.002770.
Article CAS PubMed Google Scholar
Zhang J, Shang Y, Wang E, Chen W, de Lajudie P, Li B, Guo C, Yang X, Zheng J, Liu C. Mesorhizobium jarvisii sv. astragali as predominant microsymbiont for Astragalus sinicus L. in acidic soils, Xinyang, China. Plant Soil. 2018b;433(1):201–12. https://doi.org/10.1007/s11104-018-3830-3.
Article CAS Google Scholar
Zhao CT, Wang ET, Chen WF, Chen WX. Diverse genomic species and evidences of symbiotic gene lateral transfer detected among the rhizobia associated with Astragalus species grown in the temperate regions of China. FEMS Microbiol Lett. 2008;286(2):263–73. https://doi.org/10.1111/j.1574-6968.2008.01282.x.
Article CAS PubMed Google Scholar
Zhao L, Deng Z, Yang W, Cao Y, Wang E, Wei G. Diverse rhizobia associated with Sophora alopecuroides grown in different regions of Loess Plateau in China. Syst Appl Microbiol. 2010;33(8):468–77. https://doi.org/10.1016/j.syapm.2010.08.004.
Article CAS PubMed Google Scholar

Download references

Author information

Authors and Affiliations

Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad de Mexico, Mexico
En Tao Wang
Department of Biology, University of York, York, UK
J. Peter W. Young

Authors

En Tao Wang
View author publications
You can also search for this author in PubMed Google Scholar
J. Peter W. Young
View author publications
You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

About this chapter

Cite this chapter

Wang, E.T., Young, J.P.W. (2019). Symbiosis Genes: Organisation and Diversity. In: Ecology and Evolution of Rhizobia. Springer, Singapore. https://doi.org/10.1007/978-981-32-9555-1_5

Download citation

DOI: https://doi.org/10.1007/978-981-32-9555-1_5
Published: 20 November 2019
Publisher Name: Springer, Singapore
Print ISBN: 978-981-32-9554-4
Online ISBN: 978-981-32-9555-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)

Publish with us

Policies and ethics