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Living with Genome Instability: the Adaptation of Phytoplasmas to Diverse Environments of Their Insect and Plant Hosts

Xiaodong Bai,¹ Jianhua Zhang,^1,2, Adam Ewing,^1, Sally A. Miller,² Agnes Jancso Radek,^3, Dmitriy V. Shevchenko,³ Kiryl Tsukerman,³ Theresa Walunas,³ Alla Lapidus,^3,¶ John W. Campbell,^3,|| and Saskia A. Hogenhout^1*

Department of Entomology,¹ Department of Plant Pathology, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, Ohio 44691,² Integrated Genomics, Chicago, Illinois 60612³

Received 30 September 2005/ Accepted 23 January 2006

Phytoplasmas ("Candidatus Phytoplasma," class Mollicutes) cause disease in hundreds of economically important plants and are obligately transmitted by sap-feeding insects of the order Hemiptera, mainly leafhoppers and psyllids. The 706,569-bp chromosome and four plasmids of aster yellows phytoplasma strain witches' broom (AY-WB) were sequenced and compared to the onion yellows phytoplasma strain M (OY-M) genome. The phytoplasmas have small repeat-rich genomes. This comparative analysis revealed that the repeated DNAs are organized into large clusters of potential mobile units (PMUs), which contain tra5 insertion sequences (ISs) and genes for specialized sigma factors and membrane proteins. So far, these PMUs appear to be unique to phytoplasmas. Compared to mycoplasmas, phytoplasmas lack several recombination and DNA modification functions, and therefore, phytoplasmas may use different mechanisms of recombination, likely involving PMUs, for the creation of variability, allowing phytoplasmas to adjust to the diverse environments of plants and insects. The irregular GC skews and the presence of ISs and large repeated sequences in the AY-WB and OY-M genomes are indicative of high genomic plasticity. Nevertheless, segments of 250 kb located between the lplA and glnQ genes are syntenic between the two phytoplasmas and contain the majority of the metabolic genes and no ISs. AY-WB appears to be further along in the reductive evolution process than OY-M. The AY-WB genome is 154 kb smaller than the OY-M genome, primarily as a result of fewer multicopy sequences, including PMUs. Furthermore, AY-WB lacks genes that are truncated and are part of incomplete pathways in OY-M.

Authors' contributions: X.B., performance of the majority of the bioinformatics analysis (annotation, comparative genome analyses, defining metabolic pathways of AY-WB, and submission of sequences to GenBank), and writing of manuscript; J.Z., development of DNA isolation method, DNA isolation, gap closure, and annotation of selected sequences; A.E., annotation of selected sequences and characterization of PMUs; S.A.M., project initiation, project support, and providing materials and resources; A.J.R., sequencing and gap closure; D.V.S., construction of AY-WB genomic libraries, sequencing, and gap closure; K.T., bioinformatics (sequence assembly and gap closure); T.W., bioinformatics (maintenance of annotation database and automated annotation); A.L., project manager for construction of AY-WB genomic libraries, sequencing, and gap closure; J.W.C., project manager for bioinformatics (sequence assemply, gap closure, maintenance of annotation database, and assembly); S.A.H., project initiation, overall project management (experimental work, annotation, and all other bioinformatics analyses), and writing of manuscript.

Present address: Potato Research Center, Agriculture and Agri-Food Canada, Fredericton, NB E3B 4Z7, Canada.

Present address: GCB Graduate Group, University of Pennsylvania, Philadelphia, PA 19104.

Present address: Epicentre Technologies Corp., Madison, WI 53713.

^¶ Present address: Microbial Genomics, DOE Joint Genome Institute, Walnut Creek, CA 94598.

^|| Present address: Scarab Genomics, LLC, Madison, WI 53713.

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