Adaptive evolution of rhizobial symbiotic compatibility mediated by co-evolved insertion sequences

ISME Journal

Volumn 12, Issue 1, 2018, Pages 101-111

  Zhao, Ran ^a   Liu, Li Xue ^a   Zhang, Yun Zeng ^a   Jiao, Jian ^a   Cui, Wen Jing ^a   Zhang, Biliang ^a   Wang, Xiao Lin ^a   Li, Meng Lin ^a   Chen, Yi ^a   Xiong, Zhu Qing ^a   Chen, Wen Xin ^a   Tian, Chang Fu ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BACTERIUM; COEVOLUTION; EUKARYOTE; EXPERIMENTAL STUDY; GENE; GENETIC ANALYSIS; GENETICS; GENOME; MUTATION; NITROGEN FIXATION; PHENOTYPE; RHIZOBACTERIUM; SOYBEAN; SYMBIOSIS;

EUKARYOTA; GLYCINE MAX; GLYCINE SOJA; SINORHIZOBIUM;

BACTERIAL PROTEIN;

CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MUTATION; NITROGEN FIXATION; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; PLASMID; SINORHIZOBIUM; SOYBEAN; SYMBIOSIS; TRANSPOSON; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; MUTATION; NITROGEN FIXATION; PHENOTYPE; PHYLOGENY; PLASMIDS; SINORHIZOBIUM; SOYBEANS; SYMBIOSIS; TYPE III SECRETION SYSTEMS;

EID: 85038624442     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2017.136     Document Type: Article

References (62)

1. Agren JA. (2014). Evolutionary transitions in individuality: insights from transposable elements. Trends Ecol Evol 29: 90-96.
2. Anders S, Pyl PT, Huber W. (2015). HTSeq A Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169.
3. Biémont C. (2010). A brief history of the status of transposable elements: From junk DNA to major players in evolution. Genetics 186: 1085-1093.
4. Brookfield JFY. (2005). The ecology of the genome-mobile DNA elements and their hosts. Nat Rev Genet 6: 128-136.
5. Castresana J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
6. Davies EV, James CE, Williams D, O'Brien S, Fothergill JL, Haldenby S et al. (2016). Temperate phages both mediate and drive adaptive evolution in pathogen biofilms. Proc Natl Acad Sci USA 113: 8266-8271.
7. diCenzo GC, Checcucci A, Bazzicalupo M, Mengoni A, Viti C, Dziewit L et al. (2016). Metabolic modelling reveals the specialization of secondary replicons for niche adaptation in Sinorhizobium meliloti. Nat Com-mun 7: 1-10.
8. Epstein B, Branca A, Mudge J, Bharti AK, Briskine R, Farmer AD et al. (2012). Population genomics of the facultatively mutualistic bacteria Sinorhizobium meli-loti and S. medicae. PLoS Genet 8: e1002868.
9. Feiner R, Argov T, Rabinovich L, Sigal N, Borovok I, Herskovits AA. (2015). A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 13: 641-650.
10. Galardini M, Pini F, Bazzicalupo M, Biondi EG, Mengoni A. (2013). Replicon-dependent bacterial genome evolution: the case of Sinorhizobium meliloti. Genome Biol Evol 5: 542-558.
11. Guo HJ, Wang ET, Zhang XX, Li QQ, Zhang YM, Tian CF et al. (2014). Replicon-dependent differentiation of symbiosis-related genes in Sinorhizobium nodulating Glycine max. Appl Environ Microbiol 80: 1245-1255.
12. Harrison E, Brockhurst MA. (2012). Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol 20: 262-267.
13. Harrison PW, Lower RPJ, Kim NKD, Young JPW. (2010). Introducing the bacterial 'chromid': not a chromosome, not a plasmid. Trends Microbiol 18: 141-148.
14. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng J, Richard M et al. (2011). The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43: 476-481.
15. Jiao J, Wu LJ, Zhang B, Hu Y, Li Y, Zhang XX et al. (2016). MucR is required for transcriptional activation of conserved ion transporters to support nitrogen fixation of Sinorhizobium fredii in soybean nodules. Mol Plant-Microbe Interact 29: 352-361.
16. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. (2012). Experimental evolution. Trends Ecol Evol 27: 547-560.
17. Lam H-M, Xu X, Liu X, Chen W, Yang G, Wong F-L et al. (2010). Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42: 1053-1059.
18. Langmead B, Salzberg SL. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
19. Lenski RE. (2017). What is adaptation by natural selection ? Perspectives of an experimental microbiologist. PLoS Genet 13: e1006668.
20. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
21. Li Y-H, Li W, Zhang C, Yang L, Chang R-Z, Gaut BS et al. (2010). Genetic diversity in domesticated soybean (Glycine max) and its wild progenitor (Glycine soja) for simple sequence repeat and single-nucleotide polymorphism loci. New Phytol 188: 242-253.
22. Ling J, Wang H, Wu P, Li T, Tang Y, Naseer N et al. (2016). Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island. Proc Natl Acad Sci USA 113: 13875-13880.
23. Linquist S, Saylor B, Cottenie K, Elliott TA, Kremer SC, Gregory TR. (2013). Distinguishing ecological from evolutionary approaches to transposable elements. Biol Rev 575: 573-584.
24. López-Baena FJ, Monreal JA, Pérez-Montaño F, Guasch-Vidal B, Bellogín RA, Vinardell JM et al. (2009). The absence of Nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams soybean. Mol Plant-Microbe Interact 22: 1445-1454.
25. Losos JB, Arnold SJ, Bejerano G, Brodie ED, Hibbett D, Hoekstra HE et al. (2013). Evolutionary biology for the 21st century. PLoS Biol 11: e1001466.
26. Love MI, Huber W, Anders S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550.
27. Marchetti M, Capela D, Glew M, Cruveiller S, Chane-Woon-Ming B, Gris C et al. (2010). Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol 8: e1000280.
28. Masson-Boivin C, Giraud E, Perret X, Batut J. (2009). Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17: 458-466.
29. Mcclintock B. (2016). Barbara McClintock on defining the unstable genome. Genetics 204: 3-4.
30. McCutcheon JP, Moran NA. (2012). Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10: 13-26.
31. Okazaki S, Kaneko T, Sato S, Saeki K. (2013). Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc Natl Acad Sci USA 110: 17131-17136.
32. Okazaki S, Tittabutr P, Teulet A, Thouin J, Fardoux J, Chaintreuil C et al. (2015). Rhizobium-legume symbiosis in the absence of Nod factors : two possible scenarios with or without the T3SS. ISME J 10: 64-74.
33. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T et al. (2014). The SEED and the rapid annotation of microbial genomes using subsystems Technology (RAST). Nucleic Acids Res 42: 206-214.
34. Pérez-Mendoza D, Sepúlveda E, Pando V, Muñoz S, Nogales J, Olivares J et al. (2005). Identification of the rctA gene, which is required for repression of con-jugative transfer of rhizobial symbiotic megaplasmids. J Bacteriol 187: 7341-7350.
35. Pérez-Montaño F, Jiménez-Guerrero I, Acosta-Jurado S, Navarro-Gómez P, Ollero FJ, Ruiz-Sainz JE et al. (2016). A transcriptomic analysis of the effect of genistein on Sinorhizobium fredii HH103 reveals novel rhizobial genes putatively involved in symbiosis. Sci Rep 6: 31592.
36. Pueppke SG, Bolanos-Vasquez MC, Werner D, Bec-Ferte MP, Prome JC, Krishnan HB. (1998). Release of flavonoids by the soybean cultivars McCall and Peking and their perception as signals by the nitrogen-fixing symbiont Sinorhizobium fredii. Plant Physiol 117: 599-608.
37. Qin J, Wang F, Gu F, Wang J, Chen Q, Zhang M. (2014). A genetic composition analysis of soybean sibling varieties Jidou17 and Ji nf58. Aust J Crop Sci 8: 791-798.
38. Remigi P, Capela D, Clerissi C, Tasse L, Torchet R, Bouchez O et al. (2014). Transient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer. PLOS Biol 12: e1001942.
39. Remigi P, Zhu J, Young JPW, Masson-Boivin C. (2016). Symbiosis within symbiosis: evolving nitrogen-fixing legume symbionts. Trends Microbiol 24: 63-75.
40. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
41. Skorpil P, Saad MM, Boukli NM, Kobayashi H, Ares-Orpel F, Broughton WJ et al. (2005). NopP, a phosphorylated effector of Rhizobium sp strain NGR234, is a major determinant of nodulation of the tropical legumes Flemingia congesta and Tephrosia vogelii. Mol Microbiol 57: 1304-1317.
42. Sprent JI. (2007). Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174: 11-25.
43. Staehelin C, Krishnan HB. (2015). Nodulation outer proteins: double-edged swords of symbiotic rhizobia. Biochem J 470: 263-274.
44. Sullivan JT, Patrick HN, Lowther WL, Scott DB, Ronson CW. (1995). Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc Natl Acad Sci USA 92: 8985-8989.
45. Sullivan JT, Ronson CW. (1998). Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA 95: 5145-5149.
46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
47. Tenaillon O, Barrick JE, Ribeck N, Deatherage DE, Blanchard JL, Dasgupta A et al. (2016). Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536: 165-170.
48. Tian CF, Zhou YJ, Zhang YM, Li QQ, Zhang YZ, Li DF et al. (2012). Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc Natl Acad Sci USA 109: 8629-8634.
49. Toft C, Andersson SGE. (2010). Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11: 465-475.
50. Tsukui T, Eda S, Kaneko T, Sato S, Okazaki S, Kakizaki-chiba K et al. (2013). The type III secretion system of Bradyrhizobium japonicum USDA122 mediates symbiotic incompatibility with Rj2 soybean. Appl Environ Microbiol 79: 1048-1051.
51. 4 genotype soybeans. Appl Environ Microbiol 81: 5812-5819.
52. Udvardi M, Poole PS. (2013). Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64: 781-805.
53. Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. (2011). ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 12: R30.
54. Van de Velde W, Guerra JCP, de Keyser A, de Rycke R, Rombauts S, Maunoury N et al. (2006). Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141: 711-720.
55. Venner S, Feschotte C, Biémont C. (2009). Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet 25: 317-323.
56. Vinardell J-M, Acosta-Jurado S, Zehner S, Göttfert M, Becker A, Baena I et al. (2015). The Sinorhizobium fredii HH103 genome: A comparative analysis with S. fredii strains differing in their symbiotic behavior with soybean. Mol Plant-Microbe Interact 28: 811-824.
57. Vitti JJ, Grossman SR, Sabeti PC. (2013). Detecting natural selection in genomic data. Annu Rev Genet 47: 97-120.
58. Wang D, Wang YC, Wu LJ, Liu JX, Zhang P, Jiao J et al. (2016). Construction and pilot screening of a signature-tagged mutant library of Sinorhizobium fredii. Arch Microbiol 198: 91-99.
59. Wu LJ, Wang HQ, Wang ET, Chen WX, Tian CF, Chen WX. (2011). Genetic diversity of nodulating and non-nodulating rhizobia associated with wild soybean (Glycine soja Sieb. & Zucc.) in different ecoregions of China. FEMS Microbiol Ecol 76: 439-450.
60. Yang S, Tang F, Gao M, Krishnan HB, Zhu H. (2010). R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc Natl Acad Sci USA 107: 18735-18740.
61. Zeyl C, Bell G, Green DM. (1996). Sex and the spread of retrotransposon Ty3 in experimental populations of Saccharomyces cerevisiae. Genetics 143: 1567-1577.
62. Zhang XX, Guo HJ, Jiao J, Zhang P, Xiong HY, Chen WX et al. (2017). Pyrosequencing of rpoB uncovers a significant biogeographical pattern of rhizobial species in soybean rhizosphere. J Biogeogr 44: 1491-1499