Ty3, a Position-specific Retrotransposon in Budding Yeast

Abstract

Long terminal repeat (LTR) retrotransposons constitute significant fractions of many eukaryotic genomes. Two ancient families are Ty1/Copia (Pseudoviridae) and Ty3/Gypsy (Metaviridae). The Ty3/Gypsy family probably gave rise to retroviruses based on the domain order, similarity of sequences, and the envelopes encoded by some members. The Ty3 element of Saccharomyces cerevisiae is one of the most completely characterized elements at the molecular level. Ty3 is induced in mating cells by pheromone stimulation of the mitogen-activated protein kinase pathway as cells accumulate in G1. The two Ty3 open reading frames are translated into Gag3 and Gag3-Pol3 polyprotein precursors. In haploid mating cells Gag3 and Gag3-Pol3 are assembled together with Ty3 genomic RNA into immature virus-like particles in cellular foci containing RNA processing body proteins. Virus-like particle Gag3 is then processed by Ty3 protease into capsid, spacer, and nucleocapsid, and Gag3-Pol3 into those proteins and additionally, protease, reverse transcriptase, and integrase. After haploid cells mate and become diploid, genomic RNA is reverse transcribed into cDNA. Ty3 integration complexes interact with components of the RNA polymerase III transcription complex resulting in Ty3 integration precisely at the transcription start site. Ty3 activation during mating enables proliferation of Ty3 between genomes and has intriguing parallels with metazoan retrotransposon activation in germ cell lineages. Identification of nuclear pore, DNA replication, transcription, and repair host factors that affect retrotransposition has provided insights into how hosts and retrotransposons interact to balance genome stability and plasticity.

Sequence Assembly of Yarrowia lipolytica Strain W29/CLIB89 Shows Transposable Element Diversity

“…These elements are similar to retroviruses in that the upstream LTR contains the promoter for transcription of genomic RNA and the downstream LTR specifies transcription termination and polyadenylation [42, 43]. Retrotransposons typically contain two ORFs.…”

“…Members of the Ty1/Copy and Ty3/Gypsy LTR retrotransposon classes display patterns of targeting by integrase to genomic histone marks (chromodomain class) or RNAP3 genes [42, 54, 55]. A subset of Ty3/Gypsy elements, including the eponymous Ty3, exclusively target RNAP3 transcription start sites [42].…”

“…A subset of Ty3/Gypsy elements, including the eponymous Ty3, exclusively target RNAP3 transcription start sites [42]. Because tDNA are transcribed into pre-tRNAs which have an approximately 10-nt pre-sequence, the insertion of a 5-bp target site duplication positions retrotransposon sequence 15 to 17 bp upstream of mature tRNA-coding sequence.…”

Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination

“…Retrotransposons are mobile genetic elements that transpose via an RNA intermediate and impact genome size, structure, function and molecular evolution in diverse eukaryotic lineages [1,2]. The budding yeast Saccharomyces cerevisiae is a powerful model organism for studying retrovirus-like long terminal repeat (LTR) retrotransposons, with many fundamental aspects of retrotransposon biology initially characterized in this species [3][4][5]. The complete sequencing of the yeast genome provided the first insight into organization and evolution of retrotransposons at the genomic scale [6][7][8][9][10].…”

Reverse Transcription in the Saccharomyces cerevisiae Long-Terminal Repeat Retrotransposon Ty3

“…Minus (−) strand DNA synthesis in Ty3 is primed by host tRNA i Met , the same species utilized by the distantly-related Ty1 and Ty5 retrotransposons [11]. Interestingly, while Ty3 and Ty1 prime from the native 3′-end of the tRNA, Ty5 RT initiates from a 3′-end produced by host cell RNase P-mediated internal cleavage within the anticodon loop [12,13,14].…”