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In this work we study the proliferation of transposable elements (TEs) and the epigenetic response of plants during the process of polyploidization. Through a deterministic model, expanding on our previous work on TE proliferation under epigenetic regulation, we study the long-term TE distribution and TE stability in the subgenomes of both autopolyploids and allopolyploids. We also explore different small-interfering RNA (siRNA) action modes on the subgenomes, including a model where siRNAs are not directed to specific genomes and one where siRNAs are directed - i.e. more active - in subgenomes with higher TE loads. In the autopolyploid case, we find long-term stable equilbria that tend to equilibrate the number of active TEs between subgenomes. In the allopolyploid case, directed siRNA action is fundamental to avoid a "winner takes all" outcome of the competition between the TEs in the different subgenomes. We also show that decaying oscillations in the number of TEs occur naturally in all cases, perhaps explaining some of the observed features of 'genomic shock' after hybridization events, and that the balance in the dynamics of the different types of siRNA is determinant for the synchronization of these oscillations., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

RNA molecules carry information in their primary sequence and also their secondary structure. Secondary structure can confer important functional information, but it is also a signal for an RNAi-like host epigenetic response mediated by small RNAs (smRNAs). In this study, we used two bioinformatic methods to predict local secondary structures across features of the maize genome, focusing on small regions that had similar folding properties to pre-miRNA loci. We found miRNA-like secondary structures to be common in genes and most, but not all, superfamilies of RNA and DNA transposable elements (TEs). The miRNA-like regions map to a higher diversity of smRNAs than regions without miRNA-like structure, explaining up to 27% of variation in smRNA mapping for some TE superfamilies. This mapping bias is more pronounced among putatively autonomous TEs relative to nonautonomous TEs. Genome-wide, miRNA-like regions are also associated with elevated methylation levels, particularly in the CHH context. Among genes, those with miRNA-like secondary structure are 1.5-fold more highly expressed, on average, than other genes. However, these genes are also more variably expressed across the 26 nested association mapping founder lines, and this variability positively correlates with the number of mapping smRNAs. We conclude that local miRNA-like structures are a nearly ubiquitous feature of expressed regions of the maize genome, that they correlate with higher smRNA mapping and methylation, and that they may represent a trade-off between functional requirements and the potentially negative consequences of smRNA production., (© 2023 Martin et al.; Published by Cold Spring Harbor Laboratory Press.)

Methylated CHH (mCHH) islands are peaks of CHH methylation that occur primarily upstream to genes. These regions are actively targeted by the methylation machinery, occur at boundaries between heterochromatin and euchromatin, and tend to be near highly expressed genes. Here we took an evolutionary perspective by studying upstream mCHH islands across a sample of eight grass species. Using a statistical approach to define mCHH islands as regions that differ from genome-wide background CHH methylation levels, we demonstrated that mCHH islands are common and associate with 39% of genes, on average. We hypothesized that islands should be more frequent in genomes of large size, because they have more heterochromatin and hence more need for defined boundaries. We found, however, that smaller genomes tended to have a higher proportion of genes associated with 5' mCHH islands. Consistent with previous work suggesting that islands reflect the silencing of the edge of transposable elements (TEs), genes with nearby TEs were more likely to have mCHH islands. However, the presence of mCHH islands was not a function solely of TEs, both because the underlying sequences of islands were often not homologous to TEs and because genic properties also predicted the presence of 5' mCHH islands. These genic properties included length and gene-body methylation (gbM); in fact, in three of eight species, the absence of gbM was a stronger predictor of a 5' mCHH island than TE proximity. In contrast, gene expression level was a positive but weak predictor of the presence of an island. Finally, we assessed whether mCHH islands were evolutionarily conserved by focusing on a set of 2,720 orthologs across the eight species. They were generally not conserved across evolutionary time. Overall, our data establish additional genic properties that are associated with mCHH islands and suggest that they are not just a consequence of the TE silencing machinery., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Transposable elements (TEs) regularly capture fragments of genes. When the host silences these TEs, siRNAs homologous to the captured regions may also target the genes. This epigenetic crosstalk establishes an intragenomic conflict: silencing the TEs has the cost of silencing the genes. If genes are important, however, natural selection may maintain function by moderating the silencing response, which may also advantage the TEs. In this study, we examined this model by focusing on Helitrons, Pack-MULEs, and Sirevirus LTR retrotransposons in the maize genome. We documented 1263 TEs containing exon fragments from 1629 donor genes. Consistent with epigenetic conflict, donor genes mapped more siRNAs and were more methylated than genes with no evidence of capture. However, these patterns differed between syntelog versus translocated donor genes. Syntelogs appeared to maintain function, as measured by gene expression, consistent with moderation of silencing for functionally important genes. Epigenetic marks did not spread beyond their captured regions and 24nt crosstalk siRNAs were linked with CHH methylation. Translocated genes, in contrast, bore the signature of silencing. They were highly methylated and less expressed, but also overrepresented among donor genes and located away from chromosomal arms, which suggests a link between capture and gene movement. Splitting genes into potential functional categories based on evolutionary constraint supported the synteny-based findings. TE families captured genes in different ways, but the evidence for their advantage was generally less obvious; nevertheless, TEs with captured fragments were older, mapped fewer siRNAs, and were slightly less methylated than TEs without captured fragments. Collectively, our results argue that TE capture triggers an intragenomic conflict that may not affect the function of important genes but may lead to the pseudogenization of less-constrained genes., (Copyright © 2020 The Author. Published by Elsevier Inc. All rights reserved.)

Background: Several studies have mined short-read RNA sequencing datasets to identify long non-coding RNAs (lncRNAs), and others have focused on the function of individual lncRNAs in abiotic stress response. However, our understanding of the complement, function and origin of lncRNAs - and especially transposon derived lncRNAs (TE-lncRNAs) - in response to abiotic stress is still in its infancy., Results: We utilized a dataset of 127 RNA sequencing samples that included total RNA datasets and PacBio fl-cDNA data to discover lncRNAs in maize. Overall, we identified 23,309 candidate lncRNAs from polyA+ and total RNA samples, with a strong discovery bias within total RNA. The majority (65%) of the 23,309 lncRNAs had sequence similarity to transposable elements (TEs). Most had similarity to long-terminal-repeat retrotransposons from the Copia and Gypsy superfamilies, reflecting a high proportion of these elements in the genome. However, DNA transposons were enriched for lncRNAs relative to their genomic representation by ~ 2-fold. By assessing the fraction of lncRNAs that respond to abiotic stresses like heat, cold, salt and drought, we identified 1077 differentially expressed lncRNA transcripts, including 509 TE-lncRNAs. In general, the expression of these lncRNAs was significantly correlated with their nearest gene. By inferring co-expression networks across our large dataset, we found that 39 lncRNAs are as major hubs in co-expression networks that respond to abiotic stress, and 18 appear to be derived from TEs., Conclusions: Our results show that lncRNAs are enriched in total RNA samples, that most (65%) are derived from TEs, that at least 1077 are differentially expressed during abiotic stress, and that 39 are hubs in co-expression networks, including a small number that are evolutionary conserved. These results suggest that lncRNAs, including TE-lncRNAs, may play key regulatory roles in moderating abiotic responses.

Transposable elements (TEs) compose the majority of angiosperm DNA. Plants counteract TE activity by silencing them epigenetically. One form of epigenetic silencing requires 21-22 nt small interfering RNAs that act to degrade TE mRNA and may also trigger DNA methylation. DNA methylation is reinforced by a second mechanism, the RNA-dependent DNA methylation (RdDM) pathway. RdDM relies on 24 nt small interfering RNAs and ultimately establishes TEs in a quiescent state. These host factors interact at a systems level, but there have been no system level analyses of their interactions. Here, we define a deterministic model that represents the propagation of active TEs, aspects of the host response and the accumulation of silenced TEs. We describe general properties of the model and also fit it to biological data in order to explore two questions. The first is why two overlapping pathways are maintained, given that both are likely energetically expensive. Under our model, RdDM silenced TEs effectively even when the initiation of silencing was weak. This relationship implies that only a small amount of RNAi is needed to initiate TE silencing, but reinforcement by RdDM is necessary to efficiently counter TE propagation. Second, we investigated the reliance of the host response on rates of TE deletion. The model predicted that low levels of deletion lead to few active TEs, suggesting that silencing is most efficient when methylated TEs are retained in the genome, thereby providing one explanation for the large size of plant genomes.

Transposable elements (TEs) constitute the majority of plant genomes, but most are epigenetically inactivated by their host. Research over the last decade has elucidated many of the molecular components that are required for TE silencing. In contrast, the evolutionary dynamics between TEs and silencing pathways are less clear. Here, we discuss current information about these dynamics from both mechanistic and evolutionary perspectives. We highlight new evidence that palindromic sequences within TEs may act as signals for host recognition and that cis-regulatory regions of TEs may be sites of ongoing arms races with host defenses. We also discuss patterns of TE aging after they are silenced; while there is not yet a consensus, it appears that TEs are removed more rapidly near genes, such that older TE insertions tend to be farther from genes. We conclude by discussing the energetic costs for maintaining silencing pathways, which appear to be substantive. The maintenance of silencing pathways across many species suggests that epigenetic emergencies are frequent., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Most angiosperm nuclear DNA is repetitive and derived from silenced transposable elements (TEs). TE silencing requires substantial resources from the plant host, including the production of small interfering RNAs (siRNAs). Thus, the interaction between TEs and siRNAs is a critical aspect of both the function and the evolution of plant genomes. Yet the co-evolutionary dynamics between these two entities remain poorly characterized. Here we studied the organization of TEs within the maize (Zea mays ssp mays) genome, documenting that TEs fall within three groups based on the class and copy numbers. These groups included DNA elements, low copy RNA elements and higher copy RNA elements. The three groups varied statistically in characteristics that included length, location, age, siRNA expression and 24:22 nucleotide (nt) siRNA targeting ratios. In addition, the low copy retroelements encompassed a set of TEs that had previously been shown to decrease expression within a 24 nt siRNA biogenesis mutant (mop1). To investigate the evolutionary dynamics of the three groups, we estimated their abundance in two landraces, one with a genome similar in size to that of the maize reference and the other with a 30% larger genome. For all three accessions, we assessed TE abundance as well as 22 nt and 24 nt siRNA content within leaves. The high copy number retroelements are under targeted similarly by siRNAs among accessions, appear to be born of a rapid bust of activity, and may be currently transpositionally dead or limited. In contrast, the lower copy number group of retrolements are targeted more dynamically and have had a long and ongoing history of transposition in the maize genome.

Transposable elements (TEs) are often the primary determinant of genome size differences among eukaryotes. In plants, the proliferation of TEs is countered through epigenetic silencing mechanisms that prevent mobility. Recent studies using the model plant Arabidopsis thaliana have revealed that methylated TE insertions are often associated with reduced expression of nearby genes, and these insertions may be subject to purifying selection due to this effect. Less is known about the genome-wide patterns of epigenetic silencing of TEs in other plant species. Here, we compare the 24-nt siRNA complement from A. thaliana and a closely related congener with a two- to threefold higher TE copy number, Arabidopsis lyrata. We show that TEs--particularly siRNA-targeted TEs--are associated with reduced gene expression within both species and also with gene expression differences between orthologs. In addition, A. lyrata TEs are targeted by a lower fraction of uniquely matching siRNAs, which are associated with more effective silencing of TE expression. Our results suggest that the efficacy of RNA-directed DNA methylation silencing is lower in A. lyrata, a finding that may shed light on the causes of differential TE proliferation among species.

The genome of maize (Zea mays ssp. mays) consists mostly of transposable elements (TEs) and varies in size among lines. This variation extends to other species in the genus Zea: although maize and Zea luxurians diverged only ∼140,000 years ago, their genomes differ in size by ∼50%. We used paired-end Illumina sequencing to evaluate the potential contribution of TEs to the genome size difference between these two species. We aligned the reads both to a filtered gene set and to an exemplar database of unique repeats representing 1,514 TE families; ∼85% of reads mapped against TE repeats in both species. The relative contribution of TE families to the B73 genome was highly correlated with previous estimates, suggesting that reliable estimates of TE content can be obtained from short high-throughput sequencing reads, even at low coverage. Because we used paired-end reads, we could assess whether a TE was near a gene by determining if one paired read mapped to a TE and the second read mapped to a gene. Using this method, Class 2 DNA elements were found significantly more often in genic regions than Class 1 RNA elements, but Class 1 elements were found more often near other TEs. Overall, we found that both Class 1 and 2 TE families account for ∼70% of the genome size difference between B73 and luxurians. Interestingly, the relative abundance of TE families was conserved between species (r = 0.97), suggesting genome-wide control of TE content rather than family-specific effects.

Transposable elements (TEs) constitute the majority of angiosperm DNA, but the processes that govern their accumulation remain mysterious. Here we discuss the three major forces that govern the accumulation of TEs, corresponding to the three panels of a triptych. The first force, transposition, creates new copies of TEs, but is regulated by both host- and TE-specific mechanisms. The second force, deletion of TE DNA, is capable of removing vast swaths of genomic regions via recombinational processes, but we still have very little insight into how deletion varies across species and even among TE types. Finally, we focus on the often-ignored third panel of our triptych - the population processes that determine the ultimate evolutionary fate of TE insertions., (2010 Elsevier Ltd. All rights reserved.)

Background: Transposable Elements (TEs) make up the majority of plant genomes, and thus understanding TE evolutionary dynamics is key to understanding plant genome evolution. Plant reproductive systems are diverse and mating type variation is one factor among many hypothesized to influence TE evolutionary dynamics. Here, we collected a large TE-display data set in self-fertilizing Arabidopsis thaliana, and compared it to data gathered in outcrossing Arabidopsis lyrata. We analyzed seven TE families in four natural populations of each species to tease apart the effects of mating system, demography, transposition, and selection in determining patterns of TE diversity., Results: Measures of TE band differentiation were largely consistent across TE families. However, patterns of diversity in A. thaliana Ac elements differed significantly from that other TEs, perhaps signaling a lack of recent transposition. Across TE families, we estimated higher allele frequencies and lower selection coefficients on A. thaliana TE insertions relative to A. lyrata TE insertions., Conclusions: The differences in TE distributions between the two Arabidopsis species represents a synthesis of evolutionary forces that include the transposition dynamics of individual TE families and the demographic histories of populations. There are also species-specific differences that could be attributed to the effects of mating system, including higher overall allele frequencies in the selfing lineage and a greater proportion of among population TE diversity in the outcrossing lineage.

Transposable elements (TEs) are ubiquitous genomic parasites. The deleterious consequences of the presence and activity of TEs have fueled debate about the evolutionary forces countering their expansion. Purifying selection is thought to purge TE insertions from the genome, and TE sequences are targeted by hosts for epigenetic silencing. However, the interplay between epigenetic and evolutionary forces countering TE expansion remains unexplored. Here we analyze genomic, epigenetic, and population genetic data from Arabidopsis thaliana to yield three observations. First, gene expression is negatively correlated with the density of methylated TEs. Second, the signature of purifying selection is detectable for methylated TEs near genes but not for unmethylated TEs or for TEs far from genes. Third, TE insertions are distributed by age and methylation status, such that older, methylated TEs are farther from genes. Based on these observations, we present a model in which host silencing of TEs near genes has deleterious effects on neighboring gene expression, resulting in the preferential loss of methylated TEs from gene-rich chromosomal regions. This mechanism implies an evolutionary tradeoff in which the benefit of TE silencing imposes a fitness cost via deleterious effects on the expression of nearby genes.

The goal of this study was to assess the extent to which transposable elements (TEs) have contributed to protein-coding regions in Arabidopsis thaliana. To do this, we first characterized the extent of chimeric TE-gene constructs. We compared a genome-wide TE database to genomic sequences, annotated coding regions, and EST data. The comparison revealed that 7.8% of expressed genes contained a region with close similarity to a known TE sequence. Some groups of TEs, such as helitrons, were underrepresented in exons relative to their genome-wide distribution; in contrast, Copia-like and En/Spm-like sequences were overrepresented in exons. These 7.8% percent of genes were enriched for some GO-based functions, particularly kinase activity, and lacking in other functions, notably structural molecule activity. We also examined gene family evolution for these genes. Gene family information helped clarify whether the sequence similarity between TE and gene was due to a TE contributing to the gene or, instead, the TE co-opting a portion of the gene. Most (66%) of these genes were not easily assigned to a gene family, and for these we could not infer the direction of the relationship between TE and gene. For the remainder, where appropriate, we built phylogenetic trees to infer the direction of the TE-gene relationship by parsimony. By this method, we verified examples where TEs contributed to expressed proteins. Our results are undoubtedly conservative but suggest that TEs may have contributed small protein segments to as many as 1.2% of all expressed, annotated A. thaliana genes.

Background: Helitrons are DNA transposable elements that are proposed to replicate via a rolling circle mechanism. Non-autonomous helitron elements have captured gene fragments from many genes in maize (Zea mays ssp. mays) but only a handful of genes in Arabidopsis (Arabidopsis thaliana). This observation suggests very different histories for helitrons in these two species, but it is unclear which species contains helitrons that are more typical of plants., Results: We performed computational searches to identify helitrons in maize and rice genomic sequence data. Using 12 previously identified helitrons as a seed set, we identified 23 helitrons in maize, five of which were polymorphic among a sample of inbred lines. Our total sample of maize helitrons contained fragments of 44 captured genes. Twenty-one of 35 of these helitrons did not cluster with other elements into closely related groups, suggesting substantial diversity in the maize element complement. We identified over 552 helitrons in the japonica rice genome. More than 70% of these were found in a collinear location in the indica rice genome, and 508 clustered as a single large subfamily. The japonica rice elements contained fragments of only 11 genes, a number similar to that in Arabidopsis. Given differences in gene capture between maize and rice, we examined sequence properties that could contribute to differences in capture rates, focusing on 3' palindromes that are hypothesized to play a role in transposition termination. The free energy of folding for maize helitrons were significantly lower than those in rice, but the direction of the difference differed from our prediction., Conclusion: Maize helitrons are clearly unique relative to those of rice and Arabidopsis in the prevalence of gene capture, but the reasons for this difference remain elusive. Maize helitrons do not seem to be more polymorphic among individuals than those of Arabidopsis; they do not appear to be substantially older or younger than the helitrons in either species; and our analyses provided little evidence that the 3' hairpin plays a role.

Transposable elements (TEs) are the major component of most plant genomes, and characterizing their population dynamics is key to understanding plant genome complexity. Yet there have been few studies of TE population genetics in plant systems. To study the roles of selection, transposition, and demography in shaping TE population diversity, we generated a polymorphism dataset for six TE families in four populations of the flowering plant Arabidopsis lyrata. The TE data indicated significant differentiation among populations, and maximum likelihood procedures suggested weak selection. For strongly bottlenecked populations, the observed TE band-frequency spectra fit data simulated under neutral demographic models constructed from nucleotide polymorphism data. Overall, we propose that TEs are subjected to weak selection, the efficacy of which varies as a function of demographic factors. Thus, demographic effects could be a major factor driving distributions of TEs among plant lineages.

Helitrons, a recently discovered superfamily of DNA transposons that capture host gene fragments, constitute up to 2% of the Arabidopsis thaliana genome. In this study, we identified 565 insertions of a family of nonautonomous Helitrons, known as Basho elements. We aligned subsets of these elements, estimated their phylogenetic relationships, and used branch lengths to yield insight into the age of each Basho insertion. The age distribution suggests that 87% of Bashos inserted within 5 Myr, subsequent to the divergence between A. thaliana and its sister species Arabidopsis lyrata. We screened 278 of these insertions for their presence or absence in a sample of 47 A. thaliana accessions. With both phylogenetic and population frequency data, we investigated the effects of gene density, recombination rate, and element length on Basho persistence. Our analyses suggested that longer Basho copies are less likely to persist in the genome, consistent with selection against the deleterious effects of ectopic recombination between Basho elements. Furthermore, we determined that 39% of Basho elements contain fragments of expressed protein-coding genes, but all of these fragments were explained by only 5 gene-capture events. Overall, the picture of A. thaliana Helitron evolution is one of rapid expansion, relatively few gene-capture events, and weak selection correlated with element length.