Evolutionary Dynamics of hAT DNA Transposon Families in Saccharomycetaceae

Abstract

Transposable elements (TEs) are widespread in eukaryotes but uncommon in yeasts of the Saccharomycotina subphylum, in terms of both host species and genome fraction. The class II elements are especially scarce, but the hAT element Rover is a noteworthy exception that deserves further investigation.Here, we conducted a genome-wide analysis of hAT elements in 40 ascomycota. A novel family, Roamer, was found in three species, whereas Rover was detected in 15 preduplicated species from Kluyveromyces, Eremothecium, and Lachancea genera, with up to 41 copies per genome. Rover acquisition seems to have occurred by horizontal transfer in a common ancestor of these genera. The detection of remote Rover copies in Naumovozyma dairenensis and in the sole Saccharomyces cerevisiae strain AWRI1631, without synteny, suggests that two additional independent horizontal transfers took place toward these genomes. Such patchy distribution of elements prevents any anticipation of TE presence in incoming sequenced genomes, even closely related ones.The presence of both putative autonomous and defective Rover copies, as well as their diversification into five families, indicate particular dynamics of Rover elements in the Lachancea genus. Especially, we discovered the first miniature inverted-repeat transposable elements (MITEs) to be described in yeasts, together with their parental autonomous copies. Evidence of MITE insertion polymorphism among Lachancea waltii strains suggests their recent activity. Moreover, 40% of Rover copies appeared to be involved in chromosome rearrangements, showing the large structural impact of TEs on yeast genome and opening the door to further investigations to understand their functional and evolutionary consequences.

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

“…1A), similar to most Saccharomycotina sequenced genomes ). Finally, we found a small number of Class I retrotransposons (from one to 17) in all species except in L. cidri and L. meyersii, while Class II elements are more widespread, with at least one copy in L. cidri and Lachancea fermentati and up to 41 copies in L. fantastica (Supplemental Table S2; Sarilar et al 2014).…”

“…We identified complete and partial transposable elements as well as solo-LTRs using BLAST against known transposable elements of Ty1/Copia, Ty3/Gypsy, and class-II superfamilies. Elements of the Rover and Roamer families are described elsewhere (Sarilar et al 2014). The position of centromeres in the seven newly sequenced Lachancea genomes and in L. waltii was inferred from synteny conservation with already annotated centromeres in L. thermotolerans, L. kluyveri, and Zygosaccharomyces rouxii (Souciet et al 2009).…”

Naumovozyma castellii: an alternative model for budding yeast molecular biology

“…(). It was later identified as a novel hAT DNA transposon family named Roamer (Sarilar et al ., ; reviewed in Wolfe et al ., ). Most Roamer copies are located at a synteny breakpoint with the closest relative N .…”

Horizontal transfer and proliferation of Tsu4 in Saccharomyces paradoxus

“…Since the initial discovery of horizontal transfer of the P element from Drosophila willistoni to D. melanogaster [4], a large number of cases of horizontal TE transfer (HTT) have been reported, especially among animals species (data compiled in [5]). However, surprisingly few cases of HTT have been reported in fungi [6,7,8,9,10,11,12], despite an abundance of genomic resources in this taxonomic group. Advances in long-read whole genome shotgun sequencing now allow comprehensive analysis of TE sequences in high-quality genome assemblies, and may therefore provide new opportunities for detecting HTT events in fungi and other organisms.…”