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Journal of Bacteriology, April 2009, p. 2501-2511, Vol. 191, No. 8
0021-9193/09/$08.00+0     doi:10.1128/JB.01779-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Genome Sequences of Three Agrobacterium Biovars Help Elucidate the Evolution of Multichromosome Genomes in Bacteria ^,

Steven C. Slater,¹ Barry S. Goldman,² Brad Goodner,³ João C. Setubal,^4,5* Stephen K. Farrand,⁶ Eugene W. Nester,⁷ Thomas J. Burr,⁸ Lois Banta,⁹ Allan W. Dickerman,⁵ Ian Paulsen,¹⁰ Leon Otten,¹¹ Garret Suen,^12, Roy Welch,¹² Nalvo F. Almeida,^5,13 Frank Arnold,³ Oliver T. Burton,⁹ Zijin Du,² Adam Ewing,³ Eric Godsy,² Sara Heisel,² Kathryn L. Houmiel,^14,15 Jinal Jhaveri,^5, Jing Lu,² Nancy M. Miller,² Stacie Norton,² Qiang Chen,¹⁴ Waranyoo Phoolcharoen,¹⁴ Victoria Ohlin,³ Dan Ondrusek,³ Nicole Pride,³ Shawn L. Stricklin,² Jian Sun,^5,¶ Cathy Wheeler,^3,|| Lindsey Wilson,³ Huijun Zhu,² and Derek W. Wood^7,15

Great Lakes Bioenergy Research Center, 1550 Linden Dr., University of Wisconsin, Madison, Wisconsin 53706,¹ Monsanto Company, 800 North Lindbergh Boulevard, St. Louis, Missouri 63167,² Department of Biology, Hiram College, Hiram, Ohio 44234,³ Department of Computer Science, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24060,⁴ Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24060,⁵ Department of Microbiology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801,⁶ Department of Microbiology, University of Washington, Seattle, Washington 98195,⁷ Department of Plant Pathology, Cornell University, NYSAES, Geneva, New York 14456,⁸ Department of Biology, Williams College, Williamstown, Massachusetts 01267,⁹ Department of Chemistry and Biomolecular Sciences, Macquarie University, North Ryde, New South Wales NSW2109, Australia,¹⁰ Institute of Plant Molecular Biology, Strasbourg 67084, France,¹¹ Department of Biology, Syracuse University, Syracuse, New York 13244,¹² Department of Computing and Statistics, Federal University of Mato Grosso do Sul, Campo Grande, Brazil,¹³ The Biodesign Institute, Arizona State University, 1001 S. McAllister Ave., Tempe, Arizona, 85287,¹⁴ Department of Biology, Seattle Pacific University, Seattle, Washington 98119,¹⁵

Received 18 December 2008/ Accepted 10 February 2009

The family Rhizobiaceae contains plant-associated bacteria with critical roles in ecology and agriculture. Within this family, many Rhizobium and Sinorhizobium strains are nitrogen-fixing plant mutualists, while many strains designated as Agrobacterium are plant pathogens. These contrasting lifestyles are primarily dependent on the transmissible plasmids each strain harbors. Members of the Rhizobiaceae also have diverse genome architectures that include single chromosomes, multiple chromosomes, and plasmids of various sizes. Agrobacterium strains have been divided into three biovars, based on physiological and biochemical properties. The genome of a biovar I strain, A. tumefaciens C58, has been previously sequenced. In this study, the genomes of the biovar II strain A. radiobacter K84, a commercially available biological control strain that inhibits certain pathogenic agrobacteria, and the biovar III strain A. vitis S4, a narrow-host-range strain that infects grapes and invokes a hypersensitive response on nonhost plants, were fully sequenced and annotated. Comparison with other sequenced members of the Alphaproteobacteria provides new data on the evolution of multipartite bacterial genomes. Primary chromosomes show extensive conservation of both gene content and order. In contrast, secondary chromosomes share smaller percentages of genes, and conserved gene order is restricted to short blocks. We propose that secondary chromosomes originated from an ancestral plasmid to which genes have been transferred from a progenitor primary chromosome. Similar patterns are observed in select Beta- and Gammaproteobacteria species. Together, these results define the evolution of chromosome architecture and gene content among the Rhizobiaceae and support a generalized mechanism for second-chromosome formation among bacteria.

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* Corresponding author. Mailing address: Virginia Bioinformatics Institute, Washington St., MC 0477, Blacksburg, VA 24060. Phone: (540) 231-9464. Fax: (540) 231-2606. E-mail: setubal{at}vt.edu

Published ahead of print on 27 February 2009.

Supplemental material for this article may be found at http://jb.asm.org/.

Present address: Great Lakes Bioenergy Research Center, University of Wisconsin—Madison, Madison, WI 53706-1521.

Present address: Weather Bill, San Francisco, CA 94108.

^¶ Present address: La Jolla Institute for Allergy & Immunology, La Jolla, CA 92037.

^|| Present address: Department of Biology, John Carroll University, Cleveland, OH 44118.

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Journal of Bacteriology, April 2009, p. 2501-2511, Vol. 191, No. 8
0021-9193/09/$08.00+0     doi:10.1128/JB.01779-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

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