Abstract

BackgroundRetrotransposons comprise a ubiquitous and abundant class of eukaryotic transposable elements. All members of this class rely on reverse transcriptase activity to produce a DNA copy of the element from the RNA template. However, other activities of the retrotransposon-encoded polyprotein may differ between diverse retrotransposons. The polyprotein domains corresponding to each of these activities may have their own evolutionary history independent from that of the reverse transcriptase, thus underlying the modular view on the evolution of retrotransposons. Furthermore, some transposable elements can independently evolve similar domain architectures by acquiring functionally similar but phylogenetically distinct modules. This convergent evolution of retrotransposons may ultimately suggest similar regulatory pathways underlying the lifecycle of the elements.ResultsHere, we provide new examples of the convergent evolution of retrotransposons of species from two unrelated taxa: green plants and parasitic protozoan oomycetes. In the present study we first analyzed the available genomic sequences of oomycete species and characterized two groups of Ty3/Gypsy long terminal repeat retrotransposons, namely Chronos and Archon, and a subgroup of L1 non-long terminal repeat retrotransposons. The results demonstrated that the retroelements from these three groups each have independently acquired plant-related ribonuclease H domains. This process closely resembles the evolution of retrotransposons in the genomes of green plants. In addition, we showed that Chronos elements captured a chromodomain, mimicking the process of chromodomain acquisition by Chromoviruses, another group of Ty3/Gypsy retrotransposons of plants, fungi, and vertebrates.ConclusionsRepeated and strikingly similar acquisitions of ribonuclease H domains and chromodomains by different retrotransposon groups from unrelated taxa indicate similar selection pressure acting on these elements. Thus, there are some major trends in the evolution of the structural composition of retrotransposons, and characterizing these trends may enhance the current understanding of the retrotransposon life cycle.

Highlights

  • Retrotransposons comprise a ubiquitous and abundant class of eukaryotic transposable elements

  • Diversity of Archaea-like ribonuclease H (RNH) (aRNH)-containing retrotransposons in oomycete genomes aRNH is a subgroup of the type I RNH, which includes Fungi/Metazoa-like RNHs and long terminal repeat retrotransposons (LTR-reverse transcriptase (RT)) RNH

  • While Fungi/Metazoa-like RNHs (fmRNH) and aRNHs are characterized by the presence of histidine or arginine residues respectively in the active site, LTR-RTs RNHs lack any conserved residues in that position [4, 16]. aRNHs were originally described in the archaeal genomes and were identified as cellular genes in the genomes of plants and some bacteria [20]

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Summary

Introduction

Retrotransposons comprise a ubiquitous and abundant class of eukaryotic transposable elements All members of this class rely on reverse transcriptase activity to produce a DNA copy of the element from the RNA template. Some transposable elements can independently evolve similar domain architectures by acquiring functionally similar but phylogenetically distinct modules This convergent evolution of retrotransposons may suggest similar regulatory pathways underlying the lifecycle of the elements. Non-LTR-RTs often rely on host genome-encoded RNH activity, as the reverse transcription of these transposons occurs directly in the nucleus where the host cellular RNH enzyme is naturally present [4, 15]. Some nonLTR-RTs of oomycetes and plants have acquired RNH closely related to the Archaea-like RNHs (aRNH) These two groups of non-LTR-RTs independently acquired aRNHs [6, 11]. Similar to retroviruses, the Tat LTR-RTs of green plants have acquired an additional RNH domain, aRNH, indicating structural and functional convergence between plant Tat LTR-RTs and vertebrate retroviruses [5]

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