Phylogenetic Analysis of Ribonuclease H Domains Suggests a Late, Chimeric Origin of LTR Retrotransposable Elements and Retroviruses

Abstract

We have conducted a phylogenetic analysis of the Ribonuclease HI (RNH) domains present in Eubacteria, Eukarya, all long-term repeat (LTR)-bearing retrotransposons, and several late-branching clades of non-LTR retrotransposons. Analysis of this simple yet highly conserved enzymatic domain from these disparate sources provides surprising insights into the evolution of eukaryotic retrotransposons. First, it indicates that the lineage of elements leading to vertebrate retroviruses acquired a new RNH domain either from non-LTR retrotransposons or from a eukaryotic host genome. The preexisting retroviral RNH domain degenerated to become the tether (connection) domain of the reverse transcriptase (RT)-RNH complex. Second, it indicates that all LTR retrotransposons arose in eukaryotes well after the origin of the non-LTR retrotransposons. Because of the younger age of the LTR retrotransposons, their complex structure, and the absence of any prokaryotic precursors, we propose that the LTR retrotransposons originated as a fusion between a DNA-mediated transposon and a non-LTR retrotransposon. The resulting two-step mechanism of LTR retrotransposition, in which RNA is reverse transcribed away from the chromosomal target site, rather than directly onto the target site, was probably an adaptation to the uncoupling of transcription and translation in eukaryotic cells.

Sustained retrotransposition is mediated by nucleotide deletions and interelement recombinations

“…nized as a pivotal event in the evolution of the vertebrate retroviral lineage from retrotransposons (21), but the selective advantage of the new RH in that lineage is also as yet unknown. A region of the Ty1 RH that had been shown in mutagenesis experiments to have a large effect on retrotransposition rate because the defective RH is unable to remove the polypurine tract primer from the cDNA during retrotransposition (22), is identical in RH A and RH B .…”

Review Article: ISTR, a Retrotransposons-Based Marker to Assess Plant Genome Variability with Special Emphasis in the Genera <i>Zea</i> and <i>Agave</i>

“…Transposable elements are segments of DNA with the ability to move between different sites in chromosome and they moves directly as DNA in a "copy and paste" or "cut and paste" fashion, whereas retrotransposons expand via reverse transcription of an mRNA intermediate transcribed from the mobile element [12,13]. Retrotransposons have been found in every type of organism, are ubiquitous, dynamic and abundant in eukaryotic genomes [8,14]. They are categorized into two large groups, long-terminal-repeat (LTR) and non-LTR retrotransposons also known as LINE elements, on the basis of their overall structures.…”

Factors that Affect the Horizontal Transfer of Transposable Elements

“…Non-LTR elements seem to be an ancient, monophyletic lineage that predates the diversification of eukaryotes (Malik et al, 1999) and may have originated from group II introns (Zimmerly et al, 1995;Dai and Zimmerly, 2002). The LTR retrotransposons seem to be much younger, and may have originated from the fusion of a non-LTR retrotransposon with a Class II TE, the former providing the machinery for reverse transcription and the latter the integrase activity (Capy et al, 1996;Malik and Eickbush, 2001). Vertebrate retroviruses, in turn, form a clade within the LTR retrotransposons, and are closely related to the retrotransposon superfamily Ty3-gypsy (Xiong and Eickbush, 1990;Pélisson et al, 1997;Malik and Eickbush, 2001).…”

“…The LTR retrotransposons seem to be much younger, and may have originated from the fusion of a non-LTR retrotransposon with a Class II TE, the former providing the machinery for reverse transcription and the latter the integrase activity (Capy et al, 1996;Malik and Eickbush, 2001). Vertebrate retroviruses, in turn, form a clade within the LTR retrotransposons, and are closely related to the retrotransposon superfamily Ty3-gypsy (Xiong and Eickbush, 1990;Pélisson et al, 1997;Malik and Eickbush, 2001). The common ancestry of the integrase of LTR retrotransposons and the transposase of some Class II elements establishes an evolutionary link between the two Classes (Capy et al, 1996).…”

“…The common ancestry of the integrase of LTR retrotransposons and the transposase of some Class II elements establishes an evolutionary link between the two Classes (Capy et al, 1996). The emerging picture is one of a modular evolution of TEs whereby new TE families are formed when an existing TE acquires structural features perfected by another (Ivics et al, 1996;Lerat et al, 1999;Malik and Eickbush, 2001). In spite of being a characteristic feature of these TEs, the transposases of different Class II families apparently have independent origins (Capy et al, 1996).…”