Moaine El Baidouri

Widespread and frequent horizontal transfers of transposable elements in plants

Vertical, transgenerational transmission of genetic material occurs through reproduction of living organisms. In addition to vertical inheritance, horizontal gene transfer between reproductively isolated species has recently been shown to be an important, if not dominant, mechanism in the evolution of prokaryotic genomes. In contrast, only a few horizontal transfer (HT) events have been characterized so far in eukaryotes and mainly concern transposable elements (TEs). Whether these are frequent and have a significant impact on genome evolution remains largely unknown. We performed a computational search for highly conserved LTR retrotransposons among 40 sequenced eukaryotic genomes representing the major plant families. We found that 26 genomes (65%) harbor at least one case of horizontal TE transfer (HTT). These transfers concern species as distantly related as palm and grapevine, tomato and bean, or poplar and peach. In total, we identified 32 cases of HTTs, which could translate into more than 2 million among the 13,551 monocot and dicot genera. Moreover, we show that these TEs have remained functional after their transfer, occasionally causing a transpositional burst. This suggests that plants can frequently exchange genetic material through horizontal transfers and that this mechanism may be important in TE-driven genome evolution.

Comparative Genomic Paleontology across Plant Kingdom Reveals the Dynamics of TE-Driven Genome Evolution

Long terminal repeat-retrotransposons (LTR-RTs) are the most abundant class of transposable elements (TEs) in plants. They strongly impact the structure, function, and evolution of their host genome, and, in particular, their role in genome size variation has been clearly established. However, the dynamics of the process through which LTR-RTs have differentially shaped plant genomes is still poorly understood because of a lack of comparative studies. Using a new robust and automated family classification procedure, we exhaustively characterized the LTR-RTs in eight plant genomes for which a high-quality sequence is available (i.e., Arabidopsis thaliana, A. lyrata, grapevine, soybean, rice, Brachypodium dystachion, sorghum, and maize). This allowed us to perform a comparative genome-wide study of the retrotranspositional landscape in these eight plant lineages from both monocots and dicots. We show that retrotransposition has recurrently occurred in all plant genomes investigated, regardless their size, and through bursts, rather than a continuous process. Moreover, in each genome, only one or few LTR-RT families have been active in the recent past, and the difference in genome size among the species studied could thus mostly be accounted for by the extent of the latest transpositional burst(s). Following these bursts, LTR-RTs are efficiently eliminated from their host genomes through recombination and deletion, but we show that the removal rate is not lineage specific. These new findings lead us to propose a new model of TE-driven genome evolution in plants.

A comparative epigenomic analysis of polyploidy-derived genes in soybean and common bean

Reference methylomes provide insights into the evolutionary role of DNA methylation in paleopolyploid genomes. Soybean (Glycine max) and common bean (Phaseolus vulgaris) share a paleopolyploidy (whole-genome duplication [WGD]) event, approximately 56.5 million years ago, followed by a genus Glycine-specific polyploidy, approximately 10 million years ago. Cytosine methylation is an epigenetic mark that plays an important role in the regulation of genes and transposable elements (TEs); however, the role of DNA methylation in the fate/evolution of genes following polyploidy and speciation has not been fully explored. Whole-genome bisulfite sequencing was used to produce nucleotide resolution methylomes for soybean and common bean. We found that, in soybean, CG body-methylated genes were abundant in WGD genes, which were, on average, more highly expressed than single-copy genes and had slower evolutionary rates than unmethylated genes, suggesting that WGD genes evolve more slowly than single-copy genes. CG body-methylated genes were also enriched in shared single-copy genes (single copy in both species) that may be responsible for the broad and high expression patterns of this class of genes. In addition, diverged methylation patterns in non-CG contexts between paralogs were due mostly to TEs in or near genes, suggesting a role for TEs and non-CG methylation in regulating gene expression post polyploidy. Reference methylomes for both soybean and common bean were constructed, providing resources for investigating epigenetic variation in legume crops. Also, the analysis of methylation patterns of duplicated and single-copy genes has provided insights into the functional consequences of polyploidy and epigenetic regulation in plant genomes.

Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

The genus Oryza is a model system for the study of molecular evolution over time scales ranging from a few thousand to 15 million years. Using 13 reference genomes spanning the Oryza species tree, we show that despite few large-scale chromosomal rearrangements rapid species diversification is mirrored by lineage-specific emergence and turnover of many novel elements, including transposons, and potential new coding and noncoding genes. Our study resolves controversial areas of the Oryza phylogeny, showing a complex history of introgression among different chromosomes in the young ‘AA’ subclade containing the two domesticated species. This study highlights the prevalence of functionally coupled disease resistance genes and identifies many new haplotypes of potential use for future crop protection. Finally, this study marks a milestone in modern rice research with the release of a complete long-read assembly of IR 8 ‘Miracle Rice’, which relieved famine and drove the Green Revolution in Asia 50 years ago.Genome assemblies of 13 domesticated and wild rice relatives reveal salient features of genome evolution across the genus Oryza, especially rapid species diversification and turnover of transposons. This study also releases a complete long-read assembly of IR 8 ‘Miracle Rice’.

Comprehensive Definition of Genome Features in Spirodela polyrhiza by High-Depth Physical Mapping and Short-Read DNA Sequencing Strategies

&NA; Spirodela polyrhiza is a fast‐growing aquatic monocot with highly reduced morphology, genome size and number of protein‐coding genes. Considering these biological features of Spirodela and its basal position in the monocot lineage, understanding its genome architecture could shed light on plant adaptation and genome evolution. Like many draft genomes, however, the 158‐Mb Spirodela genome sequence has not been resolved to chromosomes, and important genome characteristics have not been defined. Here we deployed rapid genome‐wide physical maps combined with high‐coverage short‐read sequencing to resolve the 20 chromosomes of Spirodela and to empirically delineate its genome features. Our data revealed a dramatic reduction in the number of the rDNA repeat units in Spirodela to fewer than 100, which is even fewer than that reported for yeast. Consistent with its unique phylogenetic position, small RNA sequencing revealed 29 Spirodela‐specific microRNA, with only two being shared with Elaeis guineensis (oil palm) and Musa balbisiana (banana). Combining DNA methylation data and small RNA sequencing enabled the accurate prediction of 20.5% long terminal repeats (LTRs) that doubled the previous estimate, and revealed a high Solo:Intact LTR ratio of 8.2. Interestingly, we found that Spirodela has the lowest global DNA methylation levels (9%) of any plant species tested. Taken together our results reveal a genome that has undergone reduction, likely through eliminating non‐essential protein coding genes, rDNA and LTRs. In addition to delineating the genome features of this unique plant, the methodologies described and large‐scale genome resources from this work will enable future evolutionary and functional studies of this basal monocot family. Significance statement Spirodela polyrhiza is a fast‐growing aquatic and basal monocot with a small genome, so understanding its genome architecture should inform plant adaptation strategies and genome evolution. However, long repetitive regions are formidable challenges for the proper assembly, annotation and closure of genome projects. Here we overcame this bottleneck by combining high‐throughput sequencing and genome mapping technologies to generate a validated sequence map of the 20 Spirodela polyrhiza chromosomes. Genome‐wide profiling data revealed a genome in a cycle of reduction with very low global DNA methylation and a reduced ribosomal DNA as well as gene content.

A new approach for annotation of transposable elements using small RNA mapping

Transposable elements (TEs) are mobile genomic DNA sequences found in most organisms. They so densely populate the genomes of many eukaryotic species that they are often the major constituents. With the rapid generation of many plant genome sequencing projects over the past few decades, there is an urgent need for improved TE annotation as a prerequisite for genome-wide studies. Analogous to the use of RNA-seq for gene annotation, we propose a new method for de novo TE annotation that uses as a guide 24 nt-siRNAs that are a part of TE silencing pathways. We use this new approach, called TASR (for Transposon Annotation using Small RNAs), for de novo annotation of TEs in Arabidopsis, rice and soybean and demonstrate that this strategy can be successfully applied for de novo TE annotation in plants. Executable PERL is available for download from: http://tasr-pipeline.sourceforge.net/

Horizontal Transfers and the New Model of TE-Driven Genome Evolution in Eukaryotes

In this chapter, we present a new model of TE-driven genome evolution in eukaryotes. This model is based on the recent discovery of the propensity of transposable elements to be transferred horizontally among plant and animal species. We propose that the horizontal transfer of transposable elements (HTTs) is a key mechanism of long-term survival of TEs in eukaryotic genomes, by allowing TEs to escape from the silencing machinery of their host genome. We provide a description of the most recent discoveries of HTTs among plants and animals, an up-to-date description of the TE silencing pathways in eukaryotes, and some characteristics of TE biology in terms of functional impact and of response to environmental stress.

Publisher Correction: Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza

This article was not made open access when initially published online, which was corrected before print publication. In addition, ORCID links were missing for 12 authors and have been added to the HTML and PDF versions of the article.

Genic C-Methylation in Soybean Is Associated with Gene Paralogs Relocated to Transposable Element-Rich Pericentromeres

Most plants are polyploid due to whole-genome duplications (WGD) and can thus have duplicated genes. Following a WGD, paralogs are often fractionated (lost) and few duplicate pairs remain. Little attention has been paid to the role of DNA methylation in the functional divergence of paralogous genes. Using high-resolution methylation maps of accessions of domesticated and wild soybean, we show that in soybean, a recent paleopolyploid with many paralogs, DNA methylation likely contributed to the elimination of genetic redundancy of polyploidy-derived gene paralogs. Transcriptionally silenced paralogs exhibit particular genomic features as they are often associated with proximal transposable elements (TEs) and are preferentially located in pericentromeres, likely due to gene movement during evolution. Additionally, we provide evidence that gene methylation associated with proximal TEs is implicated in the divergence of expression profiles between orthologous genes of wild and domesticated soybean, and within populations.