Transposable elements contribute to fungal genes and impact fungal lifestyle

Abstract

The last decade brought a still growing experimental evidence of mobilome impact on host’s gene expression. We systematically analysed genomic location of transposable elements (TEs) in 625 publicly available fungal genomes from the NCBI database in order to explore their potential roles in genome evolution and correlation with species’ lifestyle. We found that non-autonomous TEs and remnant copies are evenly distributed across genomes. In consequence, they also massively overlap with regions annotated as genes, which suggests a great contribution of TE-derived sequences to host’s coding genome. Younger and potentially active TEs cluster with one another away from genic regions. This non-randomness is a sign of either selection against insertion of TEs in gene proximity or target site preference among some types of TEs. Proteins encoded by genes with old transposable elements insertions have significantly less repeat and protein-protein interaction motifs but are richer in enzymatic domains. However, genes only proximal to TEs do not display any functional enrichment. Our findings show that adaptive cases of TE insertion remain a marginal phenomenon, and the overwhelming majority of TEs are evolving neutrally. Eventually, animal-related and pathogenic fungi have more TEs inserted into genes than fungi with other lifestyles. This is the first systematic, kingdom-wide study concerning mobile elements and their genomic neighbourhood. The obtained results should inspire further research concerning the roles TEs played in evolution and how they shape the life we know today.

Transposable Elements are an evolutionary force shaping genomic plasticity in the parthenogenetic root-knot nematode Meloidogyne incognita

“…The lack of evident correlation between the phylogenetic signal regardless whether it is TE-based or SNV-based and the biological traits under consideration suggests most of the variations follow the drift between isolates and are not necessarily adaptive, which is not surprising. A similar conclusion was also drawn recently by analyzing 625 fungal genomes and observing that most TE movements were presumably neutral and adaptive ones being marginal (Muszewska et al 2019). On another note, as explained in the first section of the discussion, TE activity is possibly very recent in M. incognita and this might contribute to the current lack of evidence for association between TE activity, including invasion or decay across populations and adaptive traits.…”

Austropuccinia psidii, causing myrtle rust, has a gigabase-sized genome shaped by transposable elements

“…In fungi TEs have been implicated in genome compartmentalization in a subset of plant pathogens (Frantzeskakis et al 2020), regulation of gene expression (Castanera et al 2016), and evolution of avirulence effectors (Zhong et al 2017; Salcedo et al 2017). In addition, TEs themselves appear to be regulated by stress conditions (Lanciano & Mirouze 2018; Muszewska et al 2019) such as during plant infection in the case of Zymoseptoria tritici (Fouché et al 2020). This stress dependent TE expression might explain why many plants and fungi have highly variable TE insertion site landscapes at the population level were many loci are unfixed, as shown for Arabidopsis thaliana (L.) Heynh (Stuart et al 2016; Quadrana et al 2016) and Z. tritici (Lorrain et al 2020; Oggenfuss et al 2020).…”

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

“…For instance, a recent study of DNA transposons in 1730 fungal genomes shows that DNA transposon content is correlated with fungal lifestyles (such as soil-living, associated with plants or animals), and increased numbers of DNA transposons but fewer functional copies are present in species with RNA interference defense systems [7]. A second study of total TE content in 625 fungal genomes by the same group reports that the number of TEs in genes is correlated with fungal lifestyles, and differences in clustering of TEs in genomic regions is correlated with their potential for being active elements [8].…”

“…For example, functional analyses of TE enhancer sequences expected to regulate gene expression in mouse embryonic stem cells based on transcriptomic and epigenomic data show that only a small subset of the enhancers tested had substantial effects on gene expression [9]. Furthermore, one of the large-scale studies of fungi mentioned earlier shows that nearly all TEs analyzed are likely to be experiencing neutral evolution [8]. Overall, there is a growing discussion of the need to experimentally examine the potentially significant impacts of TEs on their hosts [2,5,6].…”