Phylogenomic analysis reveals genome-wide purifying selection on TBE transposons in the ciliate Oxytricha.

Xiao Chen,Laura F. Landweber

doi:10.1186/s13100-016-0057-9

Abstract

BackgroundTransposable elements are a major player contributing to genetic variation and shaping genome evolution. Multiple independent transposon domestication events have occurred in ciliates, recruiting transposases to key roles in cellular processes. In the ciliate Oxytricha trifallax, the telomere-bearing elements (TBE), a Tc1/mariner transposon, occupy a significant portion of the germline genome and are involved in programmed genome rearrangements that produce a transcriptionally active somatic nucleus from a copy of the germline nucleus during development.ResultsHere we provide a thorough characterization of the distribution and sequences of TBE transposons in the Oxytricha germline genome. We annotate more than 10,000 complete and 24,000 partial TBE sequences. TBEs cluster into four major families and display a preference for either insertion into DNA segments that are retained in the somatic genome or their maintenance at such sites. The three TBE-encoded genes in all four families display dN/dS ratios much lower than 1, suggesting genome-wide purifying selection. We also identify TBE homologs in other ciliate species for phylogenomic analysis.ConclusionsThis paper provides genome-wide characterization of a major class of ciliate transposons. Phylogenomic analysis reveals selective constraints on transposon-encoded genes, shedding light on the evolution and domesticated functions of these transposons.Electronic supplementary materialThe online version of this article (doi:10.1186/s13100-016-0057-9) contains supplementary material, which is available to authorized users.

Highlights

Transposable elements are a major player contributing to genetic variation and shaping genome evolution
We infer the levels of selective constraints acting on the three transposon-encoded Open reading frame (ORF), and we discovered homologs of telomere-bearing elements (TBE) transposons in other ciliate genomes
Phylogenetic analysis confirms that the TBE2.1 and TBE2.2 42kD and 22kD genes do not form separate monophyletic clades (Fig. 1b and c), whereas the 57kD genes are clearly distinguishable between TBE2.1 and TBE2.2 (Fig. 1d)

Summary

Introduction

Transposable elements are a major player contributing to genetic variation and shaping genome evolution. In the ciliate Oxytricha trifallax, the telomere-bearing elements (TBE), a Tc1/mariner transposon, occupy a significant portion of the germline genome and are involved in programmed genome rearrangements that produce a transcriptionally active somatic nucleus from a copy of the germline nucleus during development. TEs play important roles in shaping the genome and facilitating genome evolution by processes that can promote genome rearrangements, contribute to the origin of new genes and alter gene expression [1,2,3,4]. Ciliates provide novel model systems to study transposable elements because multiple TEs, especially the transposases they encode, have been recruited to provide important cellular functions for somatic development [8, 9]. The terminal sequences of Paramecium IESs resemble the terminal inverted repeats of Tec elements in Euplotes [12, 15] and the ends of Tc1/mariner transposons [16], leading to the hypothesis that many IESs are remnants of TE insertions [17]

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