Diverse transposable element landscapes in pathogenic and nonpathogenic yeast models: the value of a comparative perspective

Abstract

Genomics and other large-scale analyses have drawn increasing attention to the potential impacts of transposable elements (TEs) on their host genomes. However, it remains challenging to transition from identifying potential roles to clearly demonstrating the level of impact TEs have on genome evolution and possible functions that they contribute to their host organisms. I summarize TE content and distribution in four well-characterized yeast model systems in this review: the pathogens Candida albicans and Cryptococcus neoformans, and the nonpathogenic species Saccharomyces cerevisiae and Schizosaccharomyces pombe. I compare and contrast their TE landscapes to their lifecycles, genomic features, as well as the presence and nature of RNA interference pathways in each species to highlight the valuable diversity represented by these models for functional studies of TEs. I then review the regulation and impacts of the Ty1 and Ty3 retrotransposons from Saccharomyces cerevisiae and Tf1 and Tf2 retrotransposons from Schizosaccharomyces pombe to emphasize parallels and distinctions between these wellstudied elements. I propose that further characterization of TEs in the pathogenic yeasts would enable this set of four yeast species to become an excellent set of models for comparative functional studies to address outstanding questions about TE-host relationships.

A nuclear pore sub-complex restricts the propagation of Ty retrotransposons by limiting their transcription

“…Indeed, mechanismwise, the common phenotypic signatures of Nup84 complex and ulp1 mutants, as well as our epistasis analysis, support the view that the Nup84 complex represses Ty1 transcription by controlling the activity of the SUMO-deconjugating enzyme Ulp1 (Fig 3, 4), which is itself sensitive to environmental conditions, alike Ty1 (e.g. chemical stresses, [75][76][77]). In this context, the regulation of Ty1 transcription through the Nup84 complex/Ulp1 axis echoes the previously reported impact of the nuclear basket in the repression of GAL genes [78].…”

Transposable Elements Contribute to Genome Dynamics and Gene Expression Variation in the Fungal Plant PathogenVerticillium dahliae

“…Modifications in suppression patterns induced by changes in the environment could imply a trade-off between the functional TE derepression and increased probability of TE expansions and TE mobilization on nearby genes, or even changes in the genome structure ( Seidl et al 2016 ). In Schizosaccharomyces pombe , for instance, changes in temperature and nutrient availability induce TE insertions in promoters of stress-dependent genes, and these insertions have been associated with higher expression of the targeted genes ( Feng et al 2013 ; Maxwell 2020 ). In the plant-pathogen Z. tritici , changes in nutrient composition led to increased TE expression, and a TE insertion in proximity of an effector gene contribute to reduced expression and virulence ( Fouche et al 2020 ).…”

“…This observation raises the possibility that polymorphic TEs form part of the regulation of genes in the vicinity as cis-regulatory sequences or as a consequence of changes in the chromatin conformation ( Le Rouzic et al 2007 ; Hollister and Gaut 2009 ; Huang et al 2012 ; Szitenberg et al 2016 ; Choi and Lee 2020 ). For instance, TEs and TE-derived sequences can be co-opted in promoter sequences and contribute to the control of gene expression ( Sundaram and Wysocka 2020 ; Cosby et al 2021 ), as for example, Tf1 retrotransposon insertions in S. pombe occur in promoters and induce consistently higher expression of neighboring genes ( Leem et al 2008 ; Guo and Levin 2010 ; Maxwell 2020 ). Furthermore, this could explain the maintenance of polymorphic TEs in V. dahliae , as the TE suppression of these elements could negatively affect the expression levels of neighboring genes, favoring their colocalization.…”

The genome of the CTG(Ser1) yeast Scheffersomyces stipitisis plastic

“…Indeed, recent sequence analyses demonstrate that the C. albicans genome contains fewer than initial predicted full-length transposable elements. Different types of repeats with no homology to transposon drive genomic diversity (47,73,(77)(78)(79).…”