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A widespread occurrence of extra open reading frames in plant Ty3/gypsy retrotransposons

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Abstract

Long terminal repeat (LTR) retrotransposons make up substantial parts of most higher plant genomes where they accumulate due to their replicative mode of transposition. Although the transposition is facilitated by proteins encoded within the gag-pol region which is common to all autonomous elements, some LTR retrotransposons were found to potentially carry an additional protein coding capacity represented by extra open reading frames located upstream or downstream of gag-pol. In this study, we performed a comprehensive in silico survey and comparative analysis of these extra open reading frames (ORFs) in the group of Ty3/gypsy LTR retrotransposons as the first step towards our understanding of their origin and function. We found that extra ORFs occur in all three major lineages of plant Ty3/gypsy elements, being the most frequent in the Tat lineage where most (77 %) of identified elements contained extra ORFs. This lineage was also characterized by the highest diversity of extra ORF arrangement (position and orientation) within the elements. On the other hand, all of these ORFs could be classified into only two broad groups based on their mutual similarities or the presence of short conserved motifs in their inferred protein sequences. In the Athila lineage, the extra ORFs were confined to the element 3′ regions but they displayed much higher sequence diversity compared to those found in Tat. In the lineage of Chromoviruses the extra ORFs were relatively rare, occurring only in 5′ regions of a group of elements present in a single plant family (Poaceae). In all three lineages, most extra ORFs lacked sequence similarities to characterized gene sequences or functional protein domains, except for two Athila-like elements with similarities to LOGL4 gene and part of the Chromoviruses extra ORFs that displayed partial similarity to histone H3 gene. Thus, in these cases the extra ORFs most likely originated by transduction or recombination of cellular gene sequences. In addition, the protein domain which is otherwise associated with DNA transposons have been detected in part of the Tat-like extra ORFs, pointing to their origin from an insertion event of a mobile element.

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Acknowledgments

We thank Jasper E. Manning for his help with manuscript preparation. This work was supported by grants AVOZ50510513 from the Academy of Sciences of the Czech Republic, and P501/12/G090 from the Czech Science Foundation.

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Authors and Affiliations

  1. Institute of Plant Molecular Biology, Biology Centre ASCR, Branišovská 31, 37005, Ceske Budejovice, Czech Republic

    Veronika Steinbauerová, Pavel Neumann, Petr Novák & Jiří Macas

  2. Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic

    Veronika Steinbauerová

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  1. Veronika Steinbauerová
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Correspondence to Jiří Macas.

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Steinbauerová, V., Neumann, P., Novák, P. et al. A widespread occurrence of extra open reading frames in plant Ty3/gypsy retrotransposons. Genetica 139, 1543–1555 (2011). https://doi.org/10.1007/s10709-012-9654-9

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  • DOI: https://doi.org/10.1007/s10709-012-9654-9

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