Sequence-variable mosaics: Composites of recurrent transposition characterizing the genomes of phylogenetically diverse phytoplasmas

Phytoplasmas are cell wall-less prokaryotes characterized by small, AT-rich genomes that encode capabilities for obligate, transkingdom parasitism and pathogenicity in plants and insect vectors. Inability to isolate and characterize phytoplasmas in pure culture has led to adoption of the 'Candidatus species' convention to refer to distinct phytoplasma lineages. In this study, we provide evidence that multiple, sequence-variable mosaics (SVMs) of clustered genes and repetitive extragenic palindromes are characteristic features of phytoplasma genome architecture in phylogenetically diverse species. The findings suggest that the origin of SVMs was an ancient event in evolution of the phytoplasma clade, while current forms of SVMs are results of dramatic and more recent events. Sequence diversity of hypervariable regions indicated rapid evolution possibly involving capture of mobile elements recurrently targeted to SVMs. Multiple events of targeted mobile element attack, recombination, and rearrangement conceivably account for the composite structure of SVMs. Proteins encoded by the highly variable region included a lysophospholipase and other putatively secreted and/or transmembrane, cell surface-interacting proteins potentially significant in phytoplasma-host interactions.