Chapter 12 : The Symbiotic Plasmids of the

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The , with around 18,000 species, is the largest plant family on Earth; its ecological success owes much to the existence of nitrogen-fixing symbioses with prokaryotes. These symbioses occur mainly with members of the family (belonging to the a-proteobacteria). Clearly, research in the molecular biology of rhizobia- legume interactions has illuminated the ways in which bacteria and eukaryotes interact in a symbiotic process. However, this research also showed, almost from the start, the existence of novel forms of genome organization in prokaryotes, such as the finding of multiple large plasmids. Conversely, elimination of the pSym impairs both nodulation and nitrogen fixation of the original bacterial strain. Plasmids p42c, p42e, and p42f influence successful competitiveness between strains for nodulation, while p42f is needed for nitrogen fixation; only the self-conjugative plasmid p42a appears to be dispensable for symbiosis. As everything in biology, the current revolution in genomics has changed the way in which one addresses these problems. On the backbone, genes for nodulation are located in three noncontiguous clusters, which are separate and far apart from three clusters of nitrogen fixation genes. Control by quorum-sensing systems has dominated the study of conjugation in the . However, it must be stressed that conjugative transfer may be modulated by other environmental cues, such as nutritional factors.

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12

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Type III Secretion System
Restriction Fragment Length Polymorphism
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Image of Figure 1
Figure 1

Maps of sequenced pSyms and symbiotic islands. Note that the scale is different between the maps. Abbreviations are defined in the text. Numbers on each map indicate the scale (in kb). References used for each map are as follows: pSymA ( and http://sequence.toulouse.inra.fr/meliloti.html); pNGR234a ( and http://genome.imb-jena.de/other/cfreiber/ pNGR234a2.html); symbiotic island R7A ( and http://sequence.toulouse.inra.fr/msi); symbiotic island MAFF303099 ( and http://www.kazusa.or.jp/rhizobase/). To facilitate comparisons between the symbiotic islands, orientation of the symbiotic island MAFF303099 was reversed from the orientation that appears in the corresponding reference.

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12
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Image of Figure 2
Figure 2

Schematic organization of systems. Direction of transcription is indicated by arrows. The promoter of the operon is marked with an arrowhead labeled P. The positions of the possible centromere-like sequence αand replication origin βin rhizobial systems are indicated by boxes of different shadings. Possible boxes are shown as a stippled box. Proposed regulatory interactions are also indicated; +, activation; − repression.

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12
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Image of Figure 3
Figure 3

Comparison of regions involved in conjugal transfer of pSyms and symbiotic islands. (A) Possible regions providing the Dtr functions in rhizobial systems, compared to the corresponding region in pTiC58. Direction of transcription for each gene is indicated by arrows. Empty boxes mark the location of or/T-like sequences. (B) Possible regions providing the Mpf functions in rhizobial systems, compared to the corresponding region in pTiC58. Symbols are as in (A). Interrupted lines connecting two maps mark genes that are absent. See text for details. References for each region are as follows: pTiC58 (25); pNGR234a ( and http://genome.imb-jena.de/other/cfreiber/pNGR234a2.html); symbiotic island R7A ( and http://sequencc.toulouse.inra.fr/msi); symbiotic island MAFF303099 ( and http://www.kazusa.or.jp/ rhizobase/); pSymA ( and http://sequence.toulouse.inra.fr/meliloti. html); pMLb ( and http://www.kazusa.or.jp/ rhizobase/).

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12
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Image of Figure 4
Figure 4

Location and orientation of identical repeats in sequenced pSyms and symbiotic islands. The sequence of the corresponding pSyms or islands was analyzed using the program Miropeats (86) (available at http://www.jparsons.uklinux.net/bioinf/) running in the intramolecular repeats mode at two different thresholds (300 bp and 1,000 bp, as indicated). All the maps were oriented with the start of the sequence on the left side of the page. Identical repeats are joined by arcs of variable height (lower for direct repeats, higher for inverse repeats). GenBank accession numbers for the sequences analyzed are: pSymA, NC003037; pNGR234a, NC000914; symbiotic island R7A, AL672111. For the symbiotic island MAFF303099, a subfile containing only the sequence of the island was generated from the chromosomal sequence (NC002678); orientation of the subfile was reversed to facilitate comparison with the symbiotic island R7A. Large-scale graphics and analysis tables are available upon request.

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12
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1. Baldani, J. I.,, R. W. Weaver,, M. F. Hynes,, and B. D. Eardly. 1992. Utilization of carbon substrates, electrophoretic enzyme patterns and symbiotic performance of plasmid-cured clover rhizobia. Appl. Environ. Microbiol. 58:23082314.
2. Barnett, M. J.,, R. F. Fisher,, T. Jones,, C. Komp,, A. P. Abola,, F. Barloy-Hubler,, L. Bowser,, D. Capela,, F. Galibert,, J. Gouzy,, M. Gurjal,, A. Hong,, L. Huizar,, R. W. Hyman,, D. Kahn,, M. L. Kahn,, S. Kalman,, D. H. Keating,, C. Palm,, M. C. Peck,, R. Surzycki,, D. H. Wells,, K. C. Yeh,, R. W. Davis,, N. A. Federspiel,, and S. R. Long. 2001. Nucleotide sequence and predicted functions of the entire Sinorbizobium meliloti pSymA megaplasmid. Proc. Natl. Acad. Sci. USA 98:98839888.
3. Barnett, M. J.,, B. G. Rushing,, R. F. Fisher,, and S. R. Long. 1996. Transcription start sites for syrM and nodD3 flank an insertion sequence relic in Rhizobium meliloti. J. Bacteriol. 178:17821787.
4. Baron, C.,, D. O'Callaghan,, and E. Lanka. 2002. Bacterial secrets of secretion: EuroConference on the biology of type IV secretion processes. Mol. Microbiol. 43:13591365.
5. Barran, L. R.,, N. Ritchot,, and E. S. Bromfield. 2001. Sinorbizobium meliloti plasmid pRmll32f replicates by a rolling-circle mechanism. J. Bacteriol. 183:27042708.
6. Bartosik, D.,, J. Baj,, and M. Wlodarczyk. 1998. Molecular and functional analysis of pTAV320, a repABC-type replicon of the Paracoccus versutus composite plasmid pTAVl. Microbiology 144:31493157.
7. Bartosik, D.,, M. Szymanik,, and E. Wysocka. 2001. Identification of the partitioning site within the repABC-type replicon of the composite Paracoccus versutus plasmid pTAVl. J. Bacteriol. 183:62346243.
8. Bever, J. D.,, and E. L. Simms. 2000. Evolution of nitrogen fixation in spatially structured populations of Rhizobium. Heredity 85:366372.
9. Bignell, C.,, and C. M. Thomas. 2001. The bacterial ParA-ParB partitioning proteins. J. Biotechnol. 91:134.
10. Bittinger, M. A.,, J. A. Gross,, J. Widom,, J. Clardy,, and J. Handelsman. 2000. Rhizobium etli CE3 carries vir gene homologs on a self-transmissible plasmid. Mol. Plant- Microbe Interact. 13:10191021.
11. Brewin, N. J.,, J. E. Beringer,, and A. W. B. Johnston. 1980. Plasmid mediated transfer of host-range specificity between two strains of Rhizobium leguminosarum. J. Gen. Microbiol. 120:413420.
12. Brom, S.,, A. Garcia-de los Santos,, L. Cervantes,, R. Palacios,, and D. Romero. 2000. In Rhizobium etli symbiotic plasmid transfer, nodulation competitivity and cellular growth require interaction among different replicons. Plasmid 44:3443.
13. Brom, S.,, A. Garcia de los Santos,, M. L. Girard,, G. Davila,, R. Palacios,, and D. Romero. 1991. High-frequency rearrangements in Rhizobium leguminosarum bv. phaseoli plasmids. J. Bacteriol. 173:13441346.
14. Brom, S.,, A. Garcia de los Santos,, T. Stepkowski,, M. Flores,, G. Davila,, D. Romero and, R. Palacios. 1992. Different plasmids of Rhizobium leguminosarum bv. phaseoli are required for optimal symbiotic performance. J. Bacteriol. 174:51835189.
15. Brom, S.,, L. Girard,, A. Garcia-de los Santos,, J. M. Sanjuan- Pinilla,, J. Olivares,, and J. Sanjuan. 2002. Conservation of plasmid-encoded traits among bean-nodulating Rhizobium species. Appl. Environ. Microbiol. 68:25552561.
16. Cao, T. B.,, and M. H. Saier, Jr. 2001. Conjugal type IV macromolecular transfer systems of gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology 147:32013214.
17. Castillo, M.,, M. Flores,, P. Mavingui,, E. Martinez-Romero,, R. Palacios,, and G. Hernandez. 1999. Increase in alfalfa nodulation, nitrogen fixation and plant growth by specific DNA amplification in Sinorbizobium meliloti. Appl. Environ. Microbiol. 65:27162722.
18. Cevallos, M. A.,, H. Porta,, J. Izquierdo,, C. Tun-Garrido,, A. Garcia-dc-los-Santos,, G. Davila,, and S. Brom. 2002. Rhizobium etli CFN42 contains at least three plasmids of the repABC family: a structural and evolutionary analysis. Plasmid 48:104116.
19. Charles, T. C.,, and T. M. Finan. 1991. Analysis of a 1600- kilobase Rhizobium meliloti megaplasmid using defined deletions generated in vivo. Genetics 127:520.
20. Chen, L.,, Y. Chen,, D. W. Wood, and E, W. Nester. 2002. A new type IV secretion system promotes conjugal transfer in Agrobacterium tumefaciens. J. Bacteriol. 184:48384845.
20.a. Chen, W. M.,, L. Moulin,, C. Bontemps,, P. Vandamme,, G. Bena,, and C. Boivin-Masson. 2003. Legume symbiotic nitrogen fixation by beta-proteobacteria is widespread in nature. J. Bacteriol 185:72667272.
21. Christensen, A. H.,, and K. R. Schubert. 1983. Identification of a Rhizobium trifolii plasmid coding for nitrogen fixation and nodulation genes and its interaction with pJB5JI, a Rhizobium leguminosarum plasmid. J. Bacteriol. 156: 592599.
22. De la Cruz, F.,, and E. Lanka,. 1998. Function of the Ti-plasmid vir proteins: T-complex formation and transfer to the plant cell, p. 282301. In H. P. Spaink,, A. Kondorosi,, and P. J. J. Hooykaas (ed.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Amsterdam, The Netherlands.
23. Denison, R. F., 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156:567576.
24. Falla, T. J., and L. Chopra. 1999. Stabilization of Rhizobium symbiosis plasmids. Microbiology 145:515516.
25. Farrand, S. K., 1998. Conjugal plasmids and their transfer, p. 199233. In H. P. Spaink,, A. Kondorosi,, and P. J. J. Hooykaas (ed.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Amsterdam, The Netherlands.
26. Farrand, S. K.,, I. Hwang,, and D. M. Cook. 1996. The tra region of the nopaline-type Ti plasmid is a chimera with elements related to the transfer systems of RSF1010, RP4 and F. J. Bacteriol. 178:42334247.
27. Farrand, S. K.,, P. B. van Berkum,, and P. Oger, 2003. Agrobacterium is a definable genus of the family Rhizobiaceae. Int. J. Syst. Evol. MicrobioL 53:16811687.
28. Fellay, R.,, X. Perret,, V. Viprey,, W. J. Broughton,, and S. Brenner. 1995. Organization of host-inducible transcripts on the symbiotic plasmid of Rhizobium NGR234. Mol. Microbiol. 16:657667.
29. Finan, T. M.,, S. Weidner,, K. Wong,, J. Buhrmester,, P. Chain,. F. J. Vorholter,, I. Hernandez-Lucas,, A. Becker,, A. Cowie,, J. Gouzy,, B. Golding,, and A. Puhler. 2001. The complete sequence of the 1,683-kb pSymB megaplasmid from the N2- fixing endosymbiont Sinorhizobium meliloti. Proc. Natl. Acad. Sci. USA 98:98899894.
30. Fischer, H. M. 1994. Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev. 58:352386.
31. Flores, M.,, S. Brom,, T. Stepkowski,, M. I. Girard,, G. Davila,, D. Romero,, and R. Palacios. 1993. Gene amplification in Rhizobium: identification and in vivo cloning of discrete amplifiable DNA regions (amplicons) from Rhizobium leguminosarum biovar phaseoli. Proc. Natl. Acad. Sci. USA 90:49324936.
32. Flores, M.,, V. Gonzalez,, S. Brom,, E. Martinez,, D. Piñero,, D. Romero,, G. Davila,, and R. Palacios. 1987. Reiterated DNA sequences in Rhizobium and Agrobacterium. J. Bacteriol. 169:57825788.
33. Flores, M.,, P. Mavingui,, L. Girard,, X. Perret,, W. J. Broughton,, E. Martinez-Romero,, G. Davila,, and R. Palacios. 1998. Three replicons of Rhizobium sp. strain NGR234 harbor symbiotic gene sequences. J. Bacteriol. 180:60526053.
34. Flores, M.,, P. Mavingui,, X. Perret,, W. J. Broughton,, D. Romero,, G. Hernandez,, G. Davila,, and R. Palacios. 2000. Prediction, identification and artificial selection of DNA rearrangements in Rhizobium: toward a natural genomic design. Proc. Natl. Acad. Sci. USA 97:91389146.
35. Freiberg, C.,, R. Fellay,, A. Bairoch,, W. J. Broughton,, A. Rosenthal,, and X. Perret. 1997. Molecular basis of symbiosis between Rhizobium and legumes. Nature 387:394401.
36. Galibert, F.,, T. M. Finan,, S. R. Long,, A. Puhler,, P. Abola,, F. Ampe,, F. Barloy-Hubler,, M. J. Barnett,, A. Becker,, P. Boistard,, G. Bothe,, M. Boutry,, L. Bowser,, J. Buhrmester,, E. Cadieu,, D. Capela,, P. Chain,, A. Cowie,, R. W. Davis,, S. Dreano,, N. A. Federspiel,, R. F. Fisher,, S. Gloux,, T. Godrie,, A. Goffcau,, B. Golding,, J. Gouzy,, M. Gurjal,, I. Hernandez- Lucas,, A. Hong,, L. Huizar,, R. W. Hyman,, T. Jones,, D. Kahn,, M. L. Kahn,, S. Kalman,, D. H. Keating,, E. Kiss,, C. Komp,, V. Lelaure,, D. Masuy,, C. Palm, M. C. Peck,, T. M. Pohl,, D. Portetelle,, B. Purnelle,, U. Ramsperger,, R. Surzycki,, P. Thebault,, M. Vandenbol,, F. J. Vorholter,, S. Weidner,, D. H. Wells,, K. Wong,, K. C. Yeh,, and Je. Batut. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668672.
37. Garcia-de los Santos, A.,, and S. Brom. 1997. Characterization of two plasmid-borne Ipsβ loci of Rhizobium etli required for lipopolysaccharidc synthesis and for optimal interaction with plants. Mol. Plant-Microbe Interact. 10:891902.
38. Garcia-de los Santos, A.,, S. Brom,, and D. Romero. 1996. Rhizobium plasmids in bacteria-legume interactions. World J. Microbiol. Biotechnol. 12:119125.
39. Gcelen, D.,, K. Goethals,, M. Van Montagu,, and M. Holsters. 1995. The nodD locus from Azorhizobium caulinadans is flanked by two repetitive elements. Gene 164:107111.
40. Geniaux, E.,, M. Flores,, R. Palacios,, and E. Martinez. 1995. Presence of megaplasmids in Rhizobium tropici and further evidence of differences between the two R. tropici subtypes. Int. J. Syst. Bacteriol. 45:392394.
41. Gerdes, K.,, S. Ayora,, I. Canosa,, p. Ceglowski,, R. Diaz- Orejas,, T. Franch,, A. P. Gultyaev,, R. B. Jensen,, I. Kobayashi,, C. Macpherson,, D. Summers,, C. M. Thomas,, and U. Zielenkiewiez,. 2000. Plasmid maintenance systems, p. 4985. In C. M. Thomas (ed.), The Horizontal Gene Pool: Bacterial Plasmids and Gene Spread. Harwood Academic Publishers, Amsterdam, The Netherlands.
42. Gerdes, K.,, J. Muller-Jensen,, and R. B. Jensen. 2000. Plasmid and chromosome partitioning: surprises from phylogeny. Mol. Microbiol. 37:455466.
43. Girard, L.,, S. Brom,, A. Davalos,, O. Lopez,, M. Soberon,, and D. Romero. 2000. Differential regulation of fixN reiterated genes in Rhizobium etli by a novel fixL-fixK cascade. Mol. Plant-Microbe Interact. 13:12831292.
44. Girard, L.,, B. Valderrama,, R. Palacios,, D. Romero,, and G. Davila. 1996. Transcriptional activity of the symbiotic plasmid of Rhizobium etli is affected by different environmental conditions. Microbiology 142:28472856.
44.a. Gonzalez, V.,, P. Bustos,, M. A. Ramirez-Romero,, A. Medrano-Soto,, H. Salgado,, I. Hernandez-Gonzalez,, J. C. Hernandez-Celis,, V. Quintero,, G. Moreno-Hagelsieb,, L. Girard,, O. Rodriguez,, M. Flores,, M. A. Cevallos,, J. Collado-Vides,, D. Romero,, and G. Davila. 2003. The mosaic structure of the symbiotic plasmid of Rhizobium etli and its relation with other symbiotic genome compartments. Genome Biol. 4:R36. ( http://genomebiology.eom/2003/4/6/R36).
45. Goodner, B.,, G. Hinkle,, S. Gattung,, N. Miller,, M. Blanchard,, B. Qurollo,, B. S. Goldman,, Y. Cao,, M. Askenazi,, C. Hailing,, L. Mullin,, K. Houmiel,, J. Gordon,, M. Vaudtn,, O. lartchouk,, A. Epp,, F. Liu,, C. Wollam,, M. Allingcr,, D. Doughty,, C. Scott,, C. Lappas,, B. Markelz,, C. Flanagan,, C. Crowcll,, J. Gurson,, C. Lomo,, C. Sear,, G. Strub,, C. Cielo,, and S. Slater. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58, Science 294:23232328.
46. Gottfert, M.,, S. Rothlisberger,, C. Kundig,, C. Beck,, R. Marty,, and H. Hennecke. 2001. Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J. Bacterial. 183:14051412.
46.a. Guo, X.,, M. Flores,, P. Mavingui,, S. I. Fuentes,, G. Hernandez,, G. Davila,, and R. Palacios. 2003. Natural genomic design in Sinorhizobium meliloti: novel genomic architectures. Genome Res. 13:18101817.
47. Gutierrez-Zamora, M. L., and E. Martinez-Romero. 2001. Natural endophytic association between Rhizobium etli and maize (Zea mays L.) .J. Biotechnol. 91:117126.
48.. Hahn, M.,, and H. Hennecke. 1987. Mapping of a Bradyrhizobium japonicum DNA region carrying genes for symbiosis and an asymmetric accumulation of reiterated sequences. Appl. Environ. Microbiol. 53:22472252.
48.a. He, X.,, W. Chang,, D. L. Pierce,, L. O. Seib,, J. Wagner, and C. Fuqua. 2003. Quorum sensing in Rhizobium sp. strain NGR234 regulates conjugal transfer (tra) gene expression and influences growth rate. J. Bacteriol. 185:809822.
49. Herrera-Cervera, J. A.,, J. Olivares,, and J. Sanjuan. 1996. Ammonia inhibition of plasmid pRmeGR4a conjugal transfer between Rhizobium meliloti strains. Appl. Environ. Microbial. 62:11451150.
50. Herrera-Cervera, J. A.,, J. M. Sanjuan-Pinilla,, J. Olivares,, and J. Sanjuan. 1998. Cloning and identification of conjugative transfer origins in the Rhizobium meliloti genome. J. Bacteriol. 180:45834590.
51. Hooykaas, P. J. J.,, H. den Dulk-Ras,, A. J. G. Regensburg- Tuink,, A. A. N, van Brussel, and R, A. Schilperoort. 1985. Expression of a Rhizobium phaseoli Sym plasmid in Rhizobium trifolii and Agrobacterium tumefaciens: income patibility with a Rhizobium trifolii Sym plasmid. Plasmid 14:4752.
52. Hooykaas, P. I. J.,, A. A. N. Van Brussel,, H. Den Dulk-Ras,, G. M. S. Von Slogteren,, and R. A. Schilperoort. 1981. Symplasmid of Rhizobium trifolii expressed in different rhizobial species and in Agrobacterium tumefaciens. Nature 291: 351353.
53. Huguet, T.,, C. Rosenberg,, F. Casse-Delbart,, P. De Lajudie,, L. Jouanin,, J. Batut,, P. Boistard,, J.-S. Julliot,, and J. Denarie,. 1983. Studies on Rhizobium meliloti plasmids and on their role in the control of nodule formation and nitrogen fixation: the pSym megaplasmids and the other large plasmids, p. 3645. In A. Puhler (ed.), Molecular Genetics of the Bacteria- Plant Interaction. Springer-Verlag, Berlin, Germany.
54. Hynes, M. F.,, K. Brucksch,, and U. B. Priefer. 1988. Melanin production encoded by a cryptic plasmid in a Rhizobium leguminosarum strain. Arch. Microbiol. 150:326332.
55. Hynes, M. F.,, and N. F. McGregor. 1990. Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol. Microbiol. 4:567574.
56. Hynes, M. F.,, R. Simon,, and A. Puhler. 1985. The development of plasmid-free strains of Agrobacterium tumefaciens by using incompatibility with a Rhizobium meliloti plasmid to eliminate pAtC58. Plasmid 13:99105.
57. Innes, R. W.,, M. A. Hirose,, and P. L. Kuempel. 1988. Induction of nitrogen-fixing nodules on clover requires only 32 kilobase pairs of DNA from the Rhizobium trifolii symbiosis plasmid. J. Bacteriol. 170:37933802.
58. Jaworski, D. D., and D. B. Clewell. 1995. A functional origin of transfer (oriT) on the conjugative transposon Tn916. J. Bacteriol. 177:66446651.
59. Johnston, A. W. B.,, J. L. Beynon,, A. V. Buchanan-Wollaston,, S. M. Setchell,, P. R. Hirsch,, and J. E. Beringer. 1978. High frequency transfer of of nodulating ability between strains and species of Rhizobium. Nature 276:634636.
60. Johnston, A. W. B.,, G. Hombrecher,, N. J. Brewin,, and M. C. Cooper. 1982. Two transmissible plasmids in Rhizobium leguminosarum strain 300. J. Gen. Microbiol. 128:8593.
61. Kahng, L. S.,, and L. Shapiro. 2001. The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J. Bacteriol. 183:30653075.
61.a. Kahng, L. S.,, and L. Shapiro. 2003. Polar localization of replicon origins in the multipartite genomes of Agrobacterium tumefaciens and Sinorbizobium meliloti. J. Bacteriol. 185:33843391.
62. Kaneko, T.,, Y. Nakamura,, S. Sato,, E. Asamizu,, T. Kato,, S. Sasamoto,, A. Watanabe,, K. Idesawa,, A. Ishikawa,, K. Kawashima,, T. Kimura,, Y. Kishida,, C. Kiyokawa,, M. Kohara,, M. Matsumoto,, A. Matsuno,, Y. Mochizuki,, S. Nakayama,, N. Nakazakt,, S. Shimpo,, M. Sugimoto,, C. Takeucbi,, M. Yamada,, and S. Tabata. 2000. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorbizobium loti. DNA Res. 7:331338.
62.a. Kaneko, T.,, Y. Nakamura,, S. Sato,, K. Minamisawa,, T. Uchiumi,, S. Sasamoto,, A. Watanabe,, K. Idesawa,, M. Iriguchi,, K. Kawashima,, M. Kohara,, M. Matsumoto,, S. Shimpo,, H. Tsuruoka,, T. Wada,, M. Yamada,, and S. Tabata. 2002. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrbizobium japonicum USD A110. DNA Res. 9:189197.
63. Kucey, R. M. N.,, and M. F. Hynes. 1989. Populations of Rhizobium leguminosarum biovars phaseoli and viceae in fields after bean or pea in rotation with nonlegumcs. Can. J. Microbiol. 35:661667.
64. Lai, E.-M.,, and C. I. Kado. 2000. The T-pilus of Agrobacterium tumefaciens. Trends Microbiol. 8:361369.
65. Lamb, J. W.,, G. Hombrecher,, and A. W. B. Johnston. 1982. Plasmid-determined nodulation and nitrogen fixation abilities in Rhizobium phaseoli. Mol. Gen. Genet. 186:449452.
66. Li, P. L.,, and S. K. Farrand. 2000. The replicator of the nopaline-type Ti plasmid pTiC58 is a member of the repABC family and is influenced by the TraR-dependent quorum-sensing regulatory system. J. Bacteriol. 182:179188.
67. Li, P. L.,, H. Hwang,, H. Miyagi,, H. True,, and S. K. Farrand. 1999. Essential components of the Ti plasmid trb system, a type IV macromolecular transporter. J. Bacteriol. 181: 50335041.
68. Lithgow, J. K.,, A. Wilkinson,, A. Hardman,, B. Rodelas,, F. Wisniewski-Dye,, P. Williams,, and J. A. Downie. 2000. The regulatory locus cinRl in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol. Microbiol. 37:8197.
69. Marketon, M. M.,, and J. E. Gonzalez. 2002. Identification of two quorum-sensing systems in Sinorbizobium meliloti. J. Bacteriol. 184:34663475.
70. Martinez, E.,, R. Palacios,, and F. Sanchez. 1987. Nitrogen-fixing nodules induced by Agrobacterium tumefaciens harboring Rhizobium phaseoli plasmids. J. Bacteriol. 169:28282834.
71. Martinez-Romero, E., 2000. Dinitrogen-fixing prokaryotes, p. 112. In A. Balows,, H. G. Truper,, M. Dworkin,, W. Harder,, and K. H. Schleifer (ed.), The Prokaryotes: an Electronic Resource for the Microbiological Community. Springer-Verlag, Berlin, Germany. ( http://link.springer-ny. com/link/service/books/10125/index.htm).
72. Masterson, R. V.,, and A. G. Atherly. 1986. The presence of repeated DNA sequences and partial restriction map of the pSym of Rhizobium fredii USDA193. Plasmid 16:3744.
73. Mavingui, P.,, M. Flores,, X. Guo,, G. Davila,, X. Perret,, W. J. Broughton,, and R. Palacios. 2002. Dynamics of genome architecture in Rhizobium sp. strain NGR234. J. Bacteriol. 184:171176.
74. Mavingui, P.,, M. Flores,, D. Romero,, E. Martinez-Romero,, and R. Palacios. 1997. Generation of Rhizobium strains with improved symbiotic properties by random DNA amplification (RDA). Nature Biotecbnol. 15:564569.
75. Mavingui, P.,, T. Lacremans,, M. Flores,, D. Romero,, E. Martinez-Romero,, and R. Palacios. 1998. Genes essential for Nod factor production and nodulation are located on a symbiotic amplicon (AMPRtr CFN299pc60) in Rhizobium tropici. J. Bacteriol. 180:28662874.
76. Mercado-Blanco, J.,, and J. Olivares. 1993. Stability and transmissibility of the cryptic plasmids of Rhizobium meliloti GR4. Arch. Microbiol. 160:477485.
77.. Mercado-Blanco, J.,, and J. Olivares. 1994. The large non-symbiotic plasmid pRmcGR4a of Rhizobium meliloti GR4 encodes a protein involved in replication that has homology with the RepC protein of Agrobacterium plasmids. Plasmid 32:7579.
78. Mercado-Blanco, J.,, and J. Olivares. 1994. A protein involved in stabilization of a large non-symbiotic plasmid of Rbizobiutn meliloti shows homology to eukaryotic cytoskeletal proteins and DNA-binding proteins. Gene 139: 133134.
79. Mercado-Blanco, J.,, and N. Toro. 1996, Plasmids in Rhizobia: the role of nonsymbiotic plasmids. Mol. Plant- Microbe Interact. 9:535545,
80. Moriguchi, K.,, Y. Maeda,, M. Satou,, N. S. N. Hardayani,, M. Kataoka,, N. Tanaka,, and K. Yoshida. 2001. The complete nucleotide sequence of a plant root-inducing (Ri) plasmid indicates its chimeric structure and evolutionary relationship between tumor-inducing (Ti) and symbiotic (Sym) plasmids in Rbizobiaceae. J. Mol. Biol. 307:771784.
81. Moulin, L.,, A. Munive,, B. Dreyfus,, and C. Boivin-Masson. 2001. Nodulation of legumes by members of the β-subclass of proteobacteria. Nature 411:948950.
82. Nishiguchi, R.,, M. Takanami,, and A. Oka. 1987. Characterization and sequence determination of the hairy root inducing plasmid pRiA4b. Mol. Gen. Genet. 206:18.
83. O'Connell, M. P.,, M. F. Hynes,, and A. Puchler. 1987. Incompatibility between a Rhizobium Sym plasmid and a Ri plasmid of Agrobacterium. Plasmid 18:156163.
84. Oresnik, I. J.,, S. L. Liu,, C. K. Yost,, and M. F. Hynes. 2000. Megaplasmid pRme2011 a of Sinorhizobium meliloti is not required for viability. J. Bacteriol. 182:35823586.
85. Oresnik, I.J.,, L. A. Pacarynuk,, S. A,, P. O'Brien,, C. K. Yost,, and M. F. Hynes. 1998. Plasmid-encoded catabolic genes in Rhizobium leguminosarum bv. trifolii: evidence for a plant-inducible rhamnose locus involved in competition for nodulation. Mol. Plant-Microbe Interact. 11:11751185.
86. Parsons, J.D. 1995. Miropeats: graphical DNA sequence comparisons. Comput. Appl. Biol. Sci. 11:615619.
87. Paulsen, I. T.,, R. Seshadri,, K. E. Nelson,, J. A. Eisen,, J. F. Heidelberg,, T. D. Read,, R. J. Dodson,, L. Umayam,, L. M. Brinkac,, M. J. Beanan,, S. C. Daugherty,, R. T. Deboy,, A. S. Durkin,, J. F. Kolonay,, R. Madupu,, W. C. Nelson,, B. Ayodeji,, M. Kraul,, J. Shetty,, J. Malek,, S. E. Van Aken,, S. RiedmuIIer,, H. Tettelin,, S. R. Gill,, O. White,, S. L. Salzberg,, D. L. Hoover,, L. E. Lindler,, S. M. Hailing,, S. M. Boyle,, and C. M. Fraser. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 99:1314813153.
88. Perret, X.,, C. Freiberg,, A. Rosenthal,, W. J. Broughton,, and R. Fellay. 1999. High-resolution transcriptional analysis of the symbiotic plasmid of Rhizobium NGR234. Mol. Microbiol. 32:415425.
89. Perret, X.,, V. Viprey,, C. Freiberg,, and W. J. Broughton. 1997. Structure and evolution of NGRRS-1, a complex, repeated element in the genome of Rhizobium sp. strain NGR234. J. Bacteriol. 179:74887496.
90. Quintero, V.,, M. A. Cevallos,, and G. Davila. 2002. A site-specific recombinase (RinQ) is required to exert incompatibility towards the symbiotic plasmid of Rhizobium etli. Mol. Microbiol. 46:10231032.
91. Ramirez-Romero, M. A.,, P. Bustos,, M. L. Girard,, O. Rodriguez,, M. A. Cevallos,, and G. Davila. 1997. Sequence, localization and characteristics of the replicator region of the symbiotic plasmid of Rhizobium etli. Microbiology 143: 28252831.
92. Ramirez-Romero, M. A.,, N. Soberon,, A. Perez-Oseguera,, J. Tellez-Sosa,, and M. A. Cevallos. 2000. Structural elements required for replication and incompatibility of the Rhizobium etli symbiotic plasmid. J. Bacterial. 182:31173124.
93. Ramirez-Romero, M. A.,, J. Tellez-Sosa,, H. Barrios,, A. Perez-Oseguera,, V. Rosas,, and M. A. Cevallos. 2001. RepA negatively autoregulates the transcription of the repABC operon of the Rhizobium etli symbiotic plasmid basic replicon. Mol. Microbiol. 42:195204.
94. Rao, J. R.,, M. Fenton,, and B. D. W. Jarvis. 1994. Symbiotic plasmid transfer in Rhizobium leguminosarum bv. trifolii and competition between the inoculant strain ICMP2163 and transconjugant soil bacteria. Soil Biol. Biocbem. 26:339351.
95. Rigottier-Gois, L.,, S. L. Turner,, J. P. W. Young,, and N. Amarger. 1998. Distribution of repC plasmid-replication sequences among plasmids and isolates of Rhizobium leguminosarum bv. viciae from field populations. Microbiology 144:771780.
96. Rivas, R.,, E. Velazquez,, A. Willems,, N. Vizcaino,, N. S. Subba-Rao,, P. F. Matcos,, M. Gillis,. F. B. Dazzo,, and E. Martinez-Molina. 2002. A new species of Devosia that forms a unique nitrogen-fixing root-nodule symbiosis with the aquatic legume Neptunia natans (L.f.) Druce. Appl. Environ. Microbiol. 68:52175222.
97. Rochepeau, P.,, L. B., Selinger,, and M. F. Hynes. 1997. Transposon-like structure of a new plasmid-encoded restriction- modification system in Rhizobium leguminosarum VF39SM. Mol. Gen. Genet. 256:387396.
98. Rodionov, O.,, M. Lobocka,, and M. Yarmolinsky. 1999. Silencing of genes flanking the PI plasmid centromere. Science 283:546549.
99. Rodriguez, C.,, and D. Romero. 1998. Multiple recombination events maintain sequence identity among members of the nitrogenase multigene family in Rhizobium etli. Genetics 149:785794.
100. Romero, D.,, S. Brom,, J. Martinez-Salazar,, M. L. Girard,, R. Palacios,, and G. Davila. 1991. Amplification and deletion of a nod-nif region in the symbiotic plasmid of Rhizobium phaseoli. J. Bacterial. 173:24352441.
101. Romero, D.,, G. Davila,, and R. Palacios,. 1998. The dynamic genome of Rhizobium, p. 153161. In F. J. de Bruijn,, J. R. Lupski,, and G. Weinstock (ed.), Bacterial Genomes: Physical Structure and Analysis. Chapman & Hall, New York, N.Y..
102. Romero, D.,, J. Martinez-Salazar,, L. Girard,, S. Brom,, G. Davila,, R. Palacios,, M. Flores,, and C. Rodriguez. 1995. Discrete amplifiable regions (amplicons) in the symbiotic plasmid of Rhizobium etli CFN42. J. Bacteriol. 177:973980.
103. Romero, D.,, J. Martinez-Salazar,, E. Ortiz,, C. Rodriguez,, and E. Valencia-Morales. 1999. Repeated sequences in bacterial chromosomes and plasmids: a glimpse from sequenced genomes. Res. Microbiol. 150:735743.
104. Romero, D.,, and R. Palacios. 1997. Gene amplification and genomic plasticity in prokaryotes. Ann. Rev. Genet. 31:91111.
105. Schofield, P. R.,, A. H. Gibson,, W. F. Dudman,, and J. M. Watson. 1987. Evidence for genetic exchange and recombination of Rhizobium symbiotic plasmids in a soil population. Appl. Environ. Microbiol. 53:29422947.
106. Schwedock, J.,, and S. R. Long. 1994. An open reading frame downstream of Rhizobium meliloti nodQI shows nucleotide sequence similarity to an Agrobacterium tumefaciens insertion sequence. Mol. Plant-Microbe Interact. 7:151153.
107. Segovia, L.,, J. P. W. Young,, and E. Martinez-Romero. 1993. Reclassification of American Rhizobium leguminosarum biovar phaseoli type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 43:374377.
108. Simms, E. L.,, and J. D. Bever. 1998. Evolutionary dynamics of rhizopine within spatially structured Rhizobium populations. Proc. Roy. Soc. Lond. B 265:17131719.
109. Spaink, H. P. 2000. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54:257288.
110. Squartini, A.,, P. Struffi,, H. Doring,, S. Selenska-Pobell,, E. Tola,, A. Giacomini,, E. Vendramin,, E. Velazquez,, P. F. Mateos,, E. Martinez-Molina,, F. B. Dazzo,, S. Casella,, and M. P. Nuti. 2002. Rhizobium sullae sp. nov. (formerly "Rhizobium hedysari) the root-nodule microsymbiont of Hedysarum coronarium L. Int. J. Syst. Evol. Microbiol. 52:12671276.
111. Sullivan, J. T.,, H. N. Patrick,, W. L. Lowther,, D. B., Scott,, and C. W. Ronson. 1995. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc. Natl. Acad. Sci. USA 92:89858989.
112. Sullivan, J. T.,, and C. W. Ronson. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci. USA 95:51455149.
113. Sullivan, J. T.,, J. R. Trzebiatowski,, R. W. Cruickshank,, J. Gouzy,, S. D. Brown,, R. M. Elliot,, D. J. Fleetwood,, N. G. McCallum,, U. Rossbach,, G. S. Stuart,, J. E. Weaver,, R. J. Webby,, F. J. de Bruijn,, and C. W, Ronson. 2002. Comparative sequence analysis of the symbiosis island of Mesorbizobmm loti strain R7A. J. Bacteriol. 184:30863095.
114. Suzuki, K.,, Y. Hattori,, M. Uraji,, N. Ohta,, K. Iwata,, K. Murata,, A. Katoh,, and K. Yoshida. 2000. Complete nucleotide sequence of a plant tumor-inducing Ti plasmid. Gene 242:331336.
115. Tabata, S.,, P. J. J. Hooykaas,, and A. Oka. 1989. Sequence determination and characterization of the replicator region in the tumor-inducing plasmid pTiB6S3. J. Bacteriol. 171:16651672.
116. Timmers, A. C.,, E. Soupene,, M. C. Auriac,, F. de Billy,, J. Vasse,, P. Boistard,, and G. Truchet. 2000. Saprophytic intracellular rhizobia in alfalfa nodules. Mol. Plant-Microbe Interact. 13:12041213.
117. Tomalsky, M. E.,, S. Colloms,, G. Blakely,, and D.J. Sherratt. 2000. Stability by multimer resolution of pJHCMW1 is due to the Tn 1331 resolvase and not to the Escherichia coli Xer system. Microbiology 146:581589.
118. Tun-Garrido, C.,, P. Bustos,, V. Gonzalez,, and S. Brom. 2003. Conjugative transfer of p42a from Rhizobium etli CFN42, which is required for mobilization of the symbiotic plasmid, is regulated by quorum sensing. J. Bacteriol. 185: 16811692.
119. Turner, S. L.,, L. Rigottier-Gois,, R. S. Power,, N. Amarger,, and J. P. W. Young. 1996. Diversity of repC plasmid-replication sequences in Rhizobium leguminosarum. Microbiology 142:17051713.
120. Turner, S. L.,, and J. P. W. Young. 1995. The replicator region of the Rhizobium leguminosarum cryptic plasmid pRL8JI. FEMS Microbiol. Lett. 133:5358.
121. Turner, S. L.,, and J. P. W. Young. 2001. Evolutionary divergence of the repC family of plasmid replication genes. Plasmid 45:163164.
122. Valdes, A. M.,, and D. Piñero. 1992. Phylogenetic estimation of plasmid exchange in bacteria. Evolution 46:641656.
123. Valencia-Morales, E.,, and D. Romero. 2000. Recombination enhancement by replication (RER) in Rhizobium etli. Genetics 154:971983.
124. Van Berkum, P.,, and B. D. Eardly,. 1998. Molecular evolutionary systematics of the Rhizobiaceae, p. 124. In H. P. Spaink,, A. Kondorosi,, and P. J. J. Hooykaas (ed.), The Rhizobiaceae: Molecular Biology of Model Plant-Associated Bacteria. Kluwer Academic Publishers, Amsterdam, The Netherlands.
125. Van Borm, S.,, A. Buschinger,, J. J. Boomsma,, and J. Billen. 2002. Tetraponera ants have gut symbionts related to nitrogen- fixing root-nodule bacteria. Proc. Roy. Soc. Lond. B 269:20232027.
126. Velazquez, E.,, J. M. Igual,, A. Willems,, M. P. Fernandez,, E. Muñoz,, P. F. Mateos,, A. Abril,, N. Toro,, P. Normand,, E. Cervantes,, M. Gillis,, and E. Martinez-Molina. 2001. Mesorhizobium chacoense sp. nov., a novel species that nodulates Prosopis alba in the Chaco Arido region (Argentina). Int. J. Syst. Evol. Microbiol. 51:10111021.
127. Viprey, V.,, A. Del Greco,, W. Golinowski,, W. J. Broughton,, and X. Perret. 1998. Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28:13811389.
128. Wang, E. T.,, J. Martinez-Romero,, and E. Martinez-Romero. 1999. Genetic diversity of rhizobia from Leucaena leucocephala nodules in Mexican soils. Mol. Ecol. 8:711724.
129. Wang, E. T.,, M. A. Rogel,, A. Garcia-de los Santos,, J. Martinez- Romero,, M. A. Cevallos,, and E. Martinez-Romero. 1999, Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int. J. Syst. Bacteriol. 49:14791491.
130. Wang, E.-T.,, Z. Y. Tan,, A. Willems,, M. Fernandez-Lopez,, B. Reinhold-Hurek,, and E. Martinez-Romero. 2002. Sinorhizobium morelense sp. nov., a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int. J. Syst. Evol. Microbiol. 52:16871693.
131. Wang, E. T.,, P. Van Berkum,, D. Beyene,, X. H. Sui,, O. Dorado,, W. X. Chen,, and E. Martinez-Romero. 1998. Rhizobium huautlense sp. nov., a symbiont of Sesbania herbacea that has a close phylogenetic relationship with Rhizobium galegae. Int. J. Syst. Bacteriol. 48:687699.
132. Wang, E. T.,, P. Van Berkum,, X. H. Sui,, D. Beyene,, W. X. Chen,, and E. Martinez-Romero. 1999. Diversity of rhizobia associated with Amorpha fruticosa isolated from chinese soils and description of Mesorhizohium amorpbae sp. nov. Int. J. Syst. Bacteriol. 49:5165.
133. Wernergreen, J. J.,, and M. A. Riley. 1999. Comparison of the evolutionary dynamics of symbiotic and housekeeping loci: a case for the genetic coherence of rhizobial lineages. Mol. Biol. Evol. 16:98t13.
134. Wilkinson, A.,, V. Danino,, F. Wisniewski-Dye,, J. K. Lithgow,, and J. A. Downie. 2002. N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J. Bacteriol. 184: 45104519.
135. Wood, D. W.,, J. C. Setubal,, R. Kaul,, D. E. Monks,, J. P. Kitajima,, V. K. Okura,, Y. Zhou,, L. Chen,, G. E. Wood,, N. F. Almeida Jr,., L. Woo,, Y. Chen,, I. T. Paulsen,, J. A. Eisen,, P. D. Karp,, D. Bovee Sr.,, P. Chapman,, J. Clendenning,, G. Deatherage,, W. Gillet,, C. Grant,, T. Kutyavin,, R. Levy,, M. J. Li,, E. McClelland,, A. Palmieri,, C. Raymond,, G. Rouse,, C. Saenphimmachak,, Z. Wu,, P. Romero,, D. Gordon,, S. Zhang,, H. Yoo,, Y. Tao,, P. Biddle,, M. Jung,, W. Krespan,, M. Perry,, B. Gordon-Kamm,, L. Liao,, S. Kim,, C. Hendrick,, Z. Y. Zhao,, M. Dolan,, F. Chumley,, S. V. Tingey,, J. F. Tomb,, M. P. Gordon,, M. V. Olson,, and E. W. Nester, 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:23172323.
136. Young, J. M.,, L. D. Kuykendall,, E. Martinez-Romero,, A. Kerr,, and H. Sawada. 2001. A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudic et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int. J. Syst. Evol. MicrobioL 51:89103.
137. Young, J. P. W.,, and M. Wexler. 1988. Sym plasmid and chromosomal genotypes arc correlated in field populations of Rhizobium leguminosarum. J. Gen. Microbiol. 134:27312739.
138. Zechner, E. L.,, F. De la Cruz,, R. Eisenbrandt,, A. M. Grahn,, G. Koraimann,, E. Lanka,, G. Muth,, W. Pansegrau,, C. M. Thomas,, B. M. Wilkins,, and M. Zatyka. 2000. Conjugative DNA transfer processes, p. 87174. In C. M. Thomas (ed.), The Horizontal Gene Pool: Bacterial Plasmids and Gene Spread. Harwood Academic Publishers, Amsterdam, The Netherlands.
139. Zhang, X.-X.,, B. Kosier,, and U. B. Priefer. 2001. Symbiotic plasmid rearrangement in Rhizobium leguminosarum bv. viciae VF39SM. J. Bacteriol. 183:21412144.
140. Zhu, J.,, P. M. Oger,, B. Schrammeijer,, P. J. J. Hooykaas,, S. K. Farrand,, and S. C Winans. 2000. The bases of crown gall tumorigenesis. J. Bacteriol. 182:38853895.


Generic image for table
Table 1

Distribution of symbiotic plasmids (pSyms) in the family

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12
Generic image for table
Table 2

replicons in the family

Citation: Romero D, Brom S. 2004. The Symbiotic Plasmids of the , p 271-290. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch12

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