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Open Access Research article

Transposable elements in phytopathogenic Verticillium spp.: insights into genome evolution and inter- and intra-specific diversification

Stefan G Amyotte1, Xiaoping Tan2, Kayla Pennerman2, Maria del Mar Jimenez-Gasco3, Steven J Klosterman4, Li-Jun Ma5, Katherine F Dobinson16* and Paola Veronese2*

Author affiliations

1 University of Western Ontario, London, ON, Canada

2 Department of Plant Pathology, North Carolina State University, Raleigh, NC, USA

3 Department of Plant Pathology, Penn State University, University Park, PA, USA

4 USDA-ARS, Salinas, CA, USA

5 University of Massachusetts, Amherst, MA, USA

6 Agriculture and Agri-Food Canada, London, ON, Canada

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Citation and License

BMC Genomics 2012, 13:314  doi:10.1186/1471-2164-13-314

Published: 16 July 2012

Abstract

Background

Verticillium dahliae (Vd) and Verticillium albo-atrum (Va) are cosmopolitan soil fungi causing very disruptive vascular diseases on a wide range of crop plants. To date, no sexual stage has been identified in either microorganism suggesting that somatic mutation is a major force in generating genetic diversity. Whole genome comparative analysis of the recently sequenced strains VdLs.17 and VaMs.102 revealed that non-random insertions of transposable elements (TEs) have contributed to the generation of four lineage-specific (LS) regions in VdLs.17.

Results

We present here a detailed analysis of Class I retrotransposons and Class II “cut-and-paste” DNA elements detected in the sequenced Verticillium genomes. We report also of their distribution in other Vd and Va isolates from various geographic origins. In VdLs.17, we identified and characterized 56 complete retrotransposons of the Gypsy-, Copia- and LINE-like types, as well as 34 full-length elements of the “cut-and-paste” superfamilies Tc1/mariner, Activator and Mutator. While Copia and Tc1/mariner were present in multiple identical copies, Activator and Mutator sequences were highly divergent. Most elements comprised complete ORFs, had matching ESTs and showed active transcription in response to stress treatment. Noticeably, we found evidences of repeat-induced point mutation (RIP) only in some of the Gypsy retroelements. While Copia-, Gypsy- and Tc1/mariner-like transposons were prominent, a large variation in presence of the other types of mobile elements was detected in the other Verticillium spp. strains surveyed. In particular, neither complete nor defective “cut-and-paste” TEs were found in VaMs.102.

Conclusions

Copia-, Gypsy- and Tc1/mariner-like transposons are the most wide-spread TEs in the phytopathogens V. dahliae and V. albo-atrum. In VdLs.17, we identified several retroelements and “cut-and-paste” transposons still potentially active. Some of these elements have undergone diversification and subsequent selective amplification after introgression into the fungal genome. Others, such as the ripped Copias, have been potentially acquired by horizontal transfer. The observed biased TE insertion in gene-rich regions within an individual genome (VdLs.17) and the “patchy” distribution among different strains point to the mobile elements as major generators of Verticillium intra- and inter-specific genomic variation.

Keywords:
Transposable elements; Verticillium spp.; Retrotransposons; DNA transposons; Repeat-induced point mutation (RIP); TE domestication; Genome evolution