Experimental evolution of nodule intracellular infection in legume symbionts

ISME Journal

Volumn 7, Issue 7, 2013, Pages 1367-1377

  Guan, Su Hua ^a   Gris, Carine ^a   Cruveiller, Stéphane ^b   Pouzet, Cécile ^c,d   Tasse, Lena ^a   Leru, Aurélie ^c,d   Maillard, Aline ^a   Médigue, Claudine ^b   Batut, Jacques ^a   Masson Boivin, Catherine ^a   Capela, Delphine ^a  

^a LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

^b DIF   (France)

^c CNRS   (France)

^d CNRS 5546   (France)

Author keywords

experimental evolution; genomics; infection; rhizobium; symbiosis

Indexed keywords

VIRULENCE FACTOR;

ADAPTIVE RADIATION; BACTERIUM; ENDOSYMBIONT; GENOMICS; INFECTIVITY; LEGUME; MUTATION; MUTUALISM; NITROGEN FIXATION; NODULATION; PATHOGEN; PLANT DEFENSE; RHIZOBACTERIUM; SECRETION; SOIL MICROORGANISM;

ARTICLE; BACTERIAL SECRETION SYSTEM; EVOLUTION; FABACEAE; GENETICS; MICROBIOLOGY; MUTATION; PATHOGENICITY; PLANT ROOT; RHIZOBIUM; SYMBIOSIS;

BACTERIAL SECRETION SYSTEMS; BIOLOGICAL EVOLUTION; FABACEAE; MUTATION; PLANT ROOTS; RHIZOBIUM; SYMBIOSIS; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); RALSTONIA SOLANACEARUM; RHIZOBIACEAE; RHIZOBIUM;

EID: 84880920733     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.24     Document Type: Article

References (52)

1. Aldon D, Brito B, Boucher C, Genin S. (2000). A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. Embo J 19: 2304-2314
2. Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C, Capela D et al. (2008). Genome sequence of the betarhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18: 1472-1483
3. Bontemps C, Elliott GN, Simon MF, Dos Reis Junior FB, Gross E, Lawton RC et al. (2010). Burkholderia species are ancient symbionts of legumes. Mol Ecol 19: 44-52
4. Boucher CA, Barberis PA, Trigalet AP, Demery DA. (1985). Transposon mutagenesis of Pseudomonas solanacearum-isolation of Tn5 induced avirulent mutants. J Gen Microbiol 131: 2449-2457
5. Brito B, Marenda M, Barberis P, Boucher C, Genin S. (1999). prhJ and hrpG, two new components of the plant signal-dependent regulatory cascade controlled by PrhA in Ralstonia solanacearum. Mol Microbiol 31: 237-251
6. Brockhurst MA, Colegrave N, Rozen DE. (2011). Nextgeneration sequencing as a tool to study microbial evolution. Mol Ecol 20: 972-980
7. Buckling A, Maclean RC, Brockhurst MA, Colegrave N. (2009). The Beagle in a bottle. Nature 457: 824-829
8. Capoen W, Goormachtig S, De Rycke R, Schroeyers K, Holsters M. (2005). SrSymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci USA 102: 10369-10374
9. Chatterjee A, Balatti PA, Gibbons W, Pueppke SG. (1990). Interaction of Rhizobium fredii USDA257 and nodulation mutants derived from it with the agronomically improved soybean cultivar McCall. Planta 180: 301-311
10. Chen WM, James EK, Prescott AR, Kierans M, Sprent JI. (2003). Nodulation of Mimosa spp. by the betaproteobacterium Ralstonia taiwanensis. Mol Plant Microbe Interact 16: 1051-1061
11. Crook MB, Lindsay DP, Biggs MB, Bentley JS, Price JC, Clement SC et al. (2012). Rhizobial plasmids that cause impaired symbiotic nitrogen fixation and enhanced host invasion. Mol Plant Microbe Interact 25: 1026-1033
12. Dagan T, Martin W. (2007). Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution. Proc Natl Acad Sci USA 104: 870-875
13. Deakin WJ, Broughton WJ. (2009). Symbiotic use of pathogenic strategies: Rhizobial protein secretion systems. Nature Rev Microbiol 7: 312-320
14. Gage DJ. (2002). Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184: 7042-7046
15. Gage DJ. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68: 280-300
16. Genin S. (2010). Molecular traits controlling host range and adaptation to plants in Ralstonia solanacearum. New Phytol 187: 920-928
17. Genin S, Gough CL, Zischek C, Boucher CA. (1992). Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol Microbiol 6: 3065-3076
18. Gibson KE, Kobayashi H, Walker GC. (2008). Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42: 413-441
19. Gough C, Cullimore J. (2011). Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol Plant Microbe Interact 24: 867-878
20. Huang JZ, Carney BF, Denny TP, Weissinger AK, Schell MA. (1995). A complex network regulates expression of eps and other virulence genes of Pseudomonas solanacearum. J Bacteriol 177: 1259-1267
21. Hubber A, Vergunst AC, Sullivan JT, Hooykaas PJJ, Ronson CW. (2004). Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol Microbiol 54: 561-574
22. Ivanov S, Fedorova E, Bisseling T. (2010). Intracellular plant microbe associations: Secretory pathways and the formation of perimicrobial compartments. Curr Opin Plant Biol 13: 372-377
23. Limpens E, Mirabella R, Fedorova E, Franken C, Franssen H, Bisseling T et al. (2005). Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc Natl Acad Sci USA 102: 10375-10380
24. L. H. Madsen, L. Tirichine, A. Jurkiewicz, J. T. Sullivan, A. B. Heckmann, A. S. Bek et al., Nat Commun 1, 10 (2010)
25. M. Marchetti, D. Capela, M. Glew, S. Cruveiller, B. Chane-Woon-Ming, C. Gris et al., PLoS Biol. 8, e1000280 (2010)
26. Marchetti M, Catrice O, Batut J, Masson-Boivin C. (2011). Cupriavidus taiwanensis bacteroids in Mimosa pudica indeterminate nodules are not terminally differentiated. Appl Environ Microbiol 77: 2161-2164
27. 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
28. Meng FH, Yao J, Allen C. (2011). A motN mutant of Ralstonia solanacearum is hypermotile and has reduced virulence. J Bacteriol 193: 2477-2486
29. Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O et al. (2006). Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobiumlegume symbiosis. Proc Natl Acad Sci USA 103: 5230-5235
30. Momeni B, Chen C-C, Hillesland KL, Waite A, Shou W. (2011). Using artificial systems to explore the ecology and evolution of symbioses. Cell Mol Life Sci 68: 1353-1368
31. Moran NA. (2006). Symbiosis. Curr Biol 16: R866-R871
32. Ochman H, Moran N. (2001). Genes lost and genes found: Evolution of bacterial pathogenesis and symbiosis. Science 292: 1096-1099
33. Oldroyd GED, Murray JD, S.Poole P, Downie JA. (2011). The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45: 119-144
34. Ovchinnikova E, Journet E-P, Chabaud M, Cosson V, Ratet P, Duc G et al. (2011). IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago spp. Mol Plant Microbe Interact 24: 1333-1344
35. Pelosi L, Kühn L, Guetta D, Garin J, Geiselmann J, Lenski RE et al. (2006). Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173: 1851-1869
36. Plener L, Manfredi P, Valls M, Genin S. (2010). PrhG, a transcriptional regulator responding to growth conditions, is involved in the control of the type III secretion system regulon in Ralstonia solanacearum. J Bacteriol 192: 1011-1019
37. Popa O, Dagan T. (2011). Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 14: 615-623
38. Poueymiro M, Genin S. (2009). Secreted proteins from Ralstonia solanacearum: A hundred tricks to kill a plant. Curr Opin Microbiol 12: 44-52
39. Ramsay JP, Sullivan JT, Jambari N, Ortori CA, Heeb S, Williams P et al. (2009). A LuxRI-family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes. Mol Microbiol 73: 1141-1155
40. Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, Ronson CW. (2006). Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol 62: 723-734
41. Rogel M, Hernández-Lucas I, Kuykendall L, Balkwill D, Martinez-Romero E. (2001). Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl Environ Microbiol 67: 3264-3268
42. Sachs JL, Skophammer RG, Regus JU. (2011). Evolutionary transitions in bacterial symbiosis. Proc Natl Acad Sci USA 108: 10800-10807
43. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, Arlat M et al. (2002). Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415: 497-502
44. Schell MA, Denny TP, Huang JZ. (1994). VsrA, a second two-component sensor regulating virulence genes of Pseudomonas solanacearum. Mol Microbiol 11: 489-500
45. Schneider P, Jacobs JM, Neres J, Aldrich CC, Allen C, Nett M et al. (2009). The global virulence regulators VsrAD and PhcA control secondary metabolism in the plant pathogen Ralstonia solanacearum. Chembiochem 10: 2730-2732
46. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ. (2011). Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480: 241-244
47. J. I. Sprent, Nodulation in Legumes (Royal Botanic gardens, Kew, UK, 2001)
48. Sprent JI. (2007). Evolving ideas of legume evolution and diversity: A taxonomic perspective on the occurrence of nodulation. New Phytol 174: 11-25
49. Sullivan J, Ronson C. (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
50. Turner SL, Young JPW. (2000). The glutamine synthetases of rhizobia: Phylogenetics and evolutionary implications. Mol Biol Evol 17: 309-319
51. Valls M, Genin S, Boucher C. (2006). Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. Plos Pathog 2: 798-807
52. Yang SM, Tang F, Gao MQ, Krishnan HB, Zhu HY. (2010). R gene-controlled host specificity in the legumerhizobia symbiosis. Proc Natl Acad Sci USA 107: 18735-18740