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Diverse Transposable Element Landscapes in Pathogenic and Nonpathogenic Yeast Models: the Value of a Comparative Perspective Patrick H

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Diverse Transposable Element Landscapes in Pathogenic and Nonpathogenic Yeast Models: the Value of a Comparative Perspective Patrick H Maxwell Mobile DNA (2020) 11:16 https://doi.org/10.1186/s13100-020-00215-x REVIEW Open Access Diverse transposable element landscapes in pathogenic and nonpathogenic yeast models: the value of a comparative perspective Patrick H. Maxwell 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 well- studied 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. Keywords: Candida albicans, Cryptococcus neoformans, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Retrotransposon, Transposable element, Tf1, Tf2, Ty1, Ty3 Background genomic site, which is referred to as a “copy-and-paste” Transposable elements (TEs) are a diverse set of genetic el- mechanism (Fig. 1). Two example subclasses are long ements that can move to new sites in genomes and sub- terminal repeat (LTR) retrotransposons, with the four stantially contribute to genotypic and phenotypic variation. superfamilies Ty1/copia (Pseudoviridae), Ty3/gypsy (Meta- They are divided into two main classes, followed by sub- viridae), BEL, and endogenous retroviruses, and non-LTR classes, superfamilies, and families based on their sequence retrotransposons, with approximately 30 superfamilies, structures and mechanisms of mobility, or transposition such as CRE, I, jockey,L1,andR2[1]. LTR retrotranspo- [1]. Mobility of Class 1 elements, known as retrotranspo- sons reverse transcribe cDNA prior to integration by DDE- sons, occurs through reverse transcriptionofanRNAinto type integrases, while non-LTR retrotransposons nick tar- a complementary DNA (cDNA) that is inserted at a new get sites using endonuclease domains to initiate reverse transcription (Fig. 1)[1, 2]. Mobility of Class 2 elements, known as DNA transposons, involves DDE transposase Correspondence: [email protected] proteins that excise DNA copies of elements from donor Biology Department, Siena College, Loudonville, NY, USA © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Maxwell Mobile DNA (2020) 11:16 Page 2 of 26 Fig. 1 Comparison of transposition cycles of four subclasses of transposable elements (TEs). Simplified representations of major steps in the transposition cycles of two subclasses of DNA transposons (cut-and-paste and peel-and-paste) and two subclasses of retrotransposons (long terminal repeat (LTR) and non-LTR) are shown. Light gray and lavender lines represent donor and target genomic sites, respectively. Boxed arrowheads indicate terminal inverted repeats (cut-and-paste) or LTRs. Curved black arrows indicate repair of the donor site after transposon excision, small purple or blue arrows represent new DNA synthesis, and wavy lines represent RNA. TP- transposase (DDE-type for cut-and-paste or HUH nuclease/helicase-type for peel-and-paste), RT- reverse transcriptase, IN- integrase, EN- endonuclease domain. sites and integrate them at new genomic sites, a “cut-and- cycles [2]. It has long been discussed that activation of TEs paste” mechanism, for approximately 20 superfamilies, such by stress could produce random genetic variation that gives as EnSpm, Harbinger, Mariner/Tc1, and MULE (Mutator- rise to occasional genotypes better adapted to the relevant like elements) (Fig. 1)[1, 2]. Mobility of the Crypton super- stress. Many TEs are activated by particular stresses, and family involves tyrosine recombinases and possible circular thereissomeevidencethattheirtranscriptionortranspos- DNA intermediates, while Helitron mobility involves trans- ition can produce beneficial mutations or changes in gene posases with HUH nuclease and helicase activities that nick expression for adaptation to stress [5]. An increasing num- and unwind one transposon strand, which is replicated to ber of studies, particularly large-scale genomic, transcrip- form a double-stranded circular DNA that is used to inte- tomic, and epigenomic studies, are providing evidence that grateacopyatanewsite(“peel-and-paste”,Fig.1)[2–4]. TEs dispersed throughout genomes provide cis-regulatory TEs are widely known for causing mutations when they sequences and transcriptional start sites for expression of are mobile, but they also contribute to chromosomal rear- neighboring genes [6]. There are also observations consist- rangements, and have transcriptional control sequences ent with particular groups of TEs with common cis- that can affect expression of neighboring genes [2]. Unre- regulatory sequences dispersed at various genomic sites stricted activity of a mutagenic agent is typically deleterious, contributing to the evolution of gene regulatory networks so organisms have many layers of defense that restrict TE coordinately controlling large numbers of genes [6]. TEs mobility at various stages of their complex transposition are also now being analyzed on a massive scale. For Maxwell Mobile DNA (2020) 11:16 Page 3 of 26 instance, a recent study of DNA transposons in 1730 fungal Genomic features of the four yeasts genomes shows that DNA transposon content is correlated Yeasts in general have small gene-dense genomes with with fungal lifestyles (such as soil-living, associated with relatively low TE content that can facilitate manipulation plants or animals), and increased numbers of DNA trans- and evaluation of a large proportion of the total TEs in a posons but fewer functional copies are present in species genome. Genomic features data are shown for reference with RNA interference defense systems [7]. A second study genomes for two major varieties of Cryptococcus neofor- of total TE content in 625 fungal genomes by the same mans, var. grubii, also called serotype A, and var. neofor- group reports that the number of TEs in genes is correlated mans, also called serotype D (Table 1). It was proposed with fungal lifestyles, and differences in clustering of TEs in that these varieties be given different species names [10], genomic regions is correlated with their potential for being but a large international group more recently proposed active elements [8]. using the term “Cryptococcus neoformans species com- The types of studies just discussed are very important plex” until variations between a large number of strains and exciting, and are leading to increased interest in are more thoroughly analyzed [11]. I will refer to the studying TEs. However, they must be thoughtfully con- species complex as simply C. neoformans and indicate if sidered and presented, because they raise exciting possi- particular information is relevant to only one serotype in bilities, but in many cases additional functional studies this review. Cryptococcus neoformans has the largest and are needed to verify these possibilities [2, 5, 6]. For in- most metazoan-like haploid genome of the four yeasts, stance, TEs differ in whether they are activated or inhib- with introns in virtually all genes (typically multiple per ited by particular stresses, how they affect expression of gene) and relatively large regional centromeres that all neighboring genes, and evidence of negative impacts of include retrotransposon sequences (Table 1)[12–14]. TEs during stress have been reported [5]. Biochemical Candida albicans has the next largest haploid reference activities consistent with cellular functions for TEs do genome, with several hundred fewer open reading not guarantee that TEs have those relevant functions, frames (ORFs),
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