Evolution of Symbiosis Genes: Vertical and Horizontal Gene Transfer

  • Chang Fu TianEmail author
  • J. Peter W. Young


Conserved nitrogen fixation genes nifHDK and nifENB have been found in 14 phyla from either bacteria or archaea (Dos Santos et al. 2012), while nodulation function is restricted to Alphaproteobacteria and Betaproteobacteria. Consequently, nitrogen fixation is proposed to predate nodulation function. Although nif genes can be co-transferred with nod genes among rhizobia (Sullivan et al. 1995; Sullivan and Ronson 1998), the symbiosis-specific nif genes can have a close relationship with homologues from non-symbiotic loci or non-rhizobial strains of the same genus (Bontemps et al. 2010; Okubo et al. 2016), indicating potential replacement of transferred nif genes by indigenous ones. Moreover, the flavonoid-induced transfer of a symbiosis island harbouring nod but not nif genes from Azorhizobium caulinodans to other rhizobia has been reported (Ling et al. 2016). Therefore, the evolutionary history of nitrogen fixation genes can be disassociated from that of nodulation genes (Fig. 6.1).


  1. Amadou C, Pascal G, Mangenot S, et al. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 2008;18:1472–83. gr.076448.108 [pii]10.1101/gr.076448.108CrossRefGoogle Scholar
  2. Aoki S, Ito M, Iwasaki W. From β- to α-proteobacteria: the origin and evolution of rhizobial nodulation genes nodIJ. Mol Biol Evol. 2013;30:2494–508. Scholar
  3. Barcellos FG, Menna P, Batista JSD, et al. Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil. Appl Environ Microbiol. 2007;73:2635–43. Scholar
  4. Bontemps C, Elliott GN, Simon MF, et al. Burkholderia species are ancient symbionts of legumes. Mol Ecol. 2010;19:44–52. MEC4458 [pii] 10.1111/j.1365-294X.2009.04458.xCrossRefGoogle Scholar
  5. Brockwell J, Bottomley PJ. Recent advances in inoculant technology and prospects for the future. Soil Biol Biochem. 1995;27:683–97.CrossRefGoogle Scholar
  6. Capela D, Marchetti M, Clérissi C, et al. Recruitment of a lineage-specific virulence regulatory pathway promotes intracellular infection by a plant pathogen experimentally evolved into a legume symbiont. Mol Biol Evol. 2017;34:2503–21. Scholar
  7. Dos Santos PC, Fang Z, Mason SW, et al. Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes. BMC Genomics. 2012;13:1–12. Scholar
  8. Gonzalez JE, Reuhs BL, Walker GC. Low molecular weight EPS II of Rhizobium meliloti allows nodule invasion in Medicago sativa. Proc Natl Acad Sci U S A. 1996;93:8636–41.CrossRefGoogle Scholar
  9. Guan SH, Gris C, Cruveiller S, et al. Experimental evolution of nodule intracellular infection in legume symbionts. ISME J. 2013;7:1367–77. Scholar
  10. Guo HJ, Wang ET, Zhang XX, et al. Replicon-dependent differentiation of symbiosis-related genes in Sinorhizobium nodulating Glycine max. Appl Environ Microbiol. 2014;80:1245–55. Scholar
  11. Hu Y, Jiao J, Liu LX, et al. Evidence for phosphate starvation of rhizobia without terminal differentiation in legume nodules. Mol Plant-Microbe Interact. 2018;31:1060–8. Scholar
  12. Jiao J, Ni M, Zhang B, et al. Coordinated regulation of core and accessory genes in the multipartite genome of Sinorhizobium fredii. PLoS Genet. 2018;14:e1007428. Scholar
  13. Jimenez-Guerrero I, Francisco P, Monreal A, et al. The Sinorhizobium (Ensifer) fredii HH103 type 3 secretion system suppresses early defense responses to effectively nodulate soybean. Mol Plant-Microbe Interact. 2015;28:790–9. Scholar
  14. Ktari A, Nouioui I, Furnholm T, et al. Permanent draft genome sequence of Frankia sp. NRRL B-16219 reveals the presence of canonical nod genes, which are highly homologous to those detected in Candidatus Frankia Dg1 genome. Stand Genomic Sci. 2017;12:1–10. Scholar
  15. Kumar N, Lad G, Giuntini E, et al. Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium leguminosarum. Open Biol. 2015;5:140133. Scholar
  16. Leigh JA. Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A. 1985;82:6231–5. Scholar
  17. Lindeberg M, Cunnac S, Collmer A. Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol. 2012;20:199–208. Scholar
  18. Ling J, Wang H, Wu P, et al. Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island. Proc Natl Acad Sci U S A. 2016;113:13875–80. Scholar
  19. Liu LX, Li QQ, Zhang YZ, et al. The nitrate-reduction gene cluster components exert lineage-dependent contributions to optimization of Sinorhizobium symbiosis with soybeans. Environ Microbiol. 2017;19:4926–38. Scholar
  20. Lodwig EM, Hosie AH, Bourdes A, et al. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature. 2003;422:722–6. nature01527 [pii]CrossRefPubMedGoogle Scholar
  21. Mao C, Qiu J, Wang C, et al. NodMutDB: a database for genes and mutants involved in symbiosis. Bioinformatics. 2005;21:2927–9. bti427 [pii]10.1093/bioinformatics/bti427CrossRefGoogle Scholar
  22. Marchetti M, Capela D, Glew M, et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 2010;8:e1000280. Scholar
  23. Masson-Boivin C, Giraud E, Perret X, Batut J. Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol. 2009;17:458–66. S0966-842X(09)00164-4 [pii]10.1016/j.tim.2009.07.004CrossRefGoogle Scholar
  24. Okazaki S, Kaneko T, Sato S, Saeki K. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc Natl Acad Sci U S A. 2013;110:17131–6. Scholar
  25. Okubo T, Piromyou P, Tittabutr P, et al. Origin and evolution of nitrogen fixation genes on symbiosis islands and plasmid in Bradyrhizobium. Microbes Environ. 2016;31:260–7. Scholar
  26. Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ. Bacterial associations with legumes. Crit Rev Plant Sci. 2015;34:17–42. Scholar
  27. Persson T, Battenberg K, Demina IV, et al. Candidatus Frankia datiscae Dg1, the Actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS One. 2015;10:e0127630. Scholar
  28. Prell J, White JP, Bourdes A, et al. Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci U S A. 2009;106:12477–82. Scholar
  29. Prell J, Bourdes A, Kumar S, et al. Role of symbiotic auxotrophy in the Rhizobium-legume symbioses. PLoS One. 2010;5:e13933. Scholar
  30. Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol. 2016;24:63–75. Scholar
  31. Sugawara M, Epstein B, Badgley BD, et al. Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies. Genome Biol. 2013;14:R17. Scholar
  32. Sugawara M, Takahashi S, Umehara Y, et al. Variation in bradyrhizobial NopP effector determines symbiotic incompatibility with Rj2-soybeans via effector-triggered immunity. Nat Commun. 2018;9:6–10. Scholar
  33. Sullivan JT, Ronson CW. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci U S A. 1998;95:5145–9.CrossRefGoogle Scholar
  34. Sullivan JT, Patrick HN, Lowther WL, et al. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci U S A. 1995;92:8985–9. Scholar
  35. Tian CF, Young JPW, Wang ET, et al. Population mixing of Rhizobium leguminosarum bv. viciae nodulating Vicia faba: the role of recombination and lateral gene transfer. FEMS Microbiol Ecol. 2010;73:563–76. Scholar
  36. Tian CF, Zhou YJ, Zhang YM, et al. Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc Natl Acad Sci U S A. 2012;109:8629–34. Scholar
  37. Van Nguyen T, Wibberg D, Battenberg K, et al. An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genomics. 2016;17:796. Scholar
  38. Xiong HY, Zhang XX, Guo HJ, et al. The epidemicity of facultative microsymbionts in faba bean rhizosphere soils. Soil Biol Biochem. 2017;115:243–52. Scholar
  39. Young JPW. Bacteria are smartphones and mobile genes are apps. Trends Microbiol. 2016;24:931–2. Scholar
  40. Yuan ZC, Zaheer R, Finan TM. Regulation and properties of PstSCAB, a high-affinity, high-velocity phosphate transport system of Sinorhizobium meliloti. J Bacteriol. 2006;188:1089–102. Scholar
  41. Zhang XX, Guo HJ, Wang R, et al. Genetic divergence of Bradyrhizobium nodulating soybeans as revealed by multilocus sequence analysis of genes inside and outside the symbiosis island. Appl Environ Microbiol. 2014;80:3181–90. Scholar
  42. Zhao R, Liu LX, Zhang YZ, et al. Adaptive evolution of rhizobial symbiotic compatibility mediated by co-evolved insertion sequences. ISME J. 2018;12:101–11. Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.State Key Laboratory of AgrobiotechnologyBeijingChina
  2. 2.College of Biological Sciences andRhizobium Research CenterChina Agricultural UniversityBeijingChina
  3. 3.Department of BiologyUniversity of YorkYorkUK

Personalised recommendations