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Lacoste, E.

Publications and source records attributed to Lacoste, E..

3 recordsLinked to original sources

Scenarios for the emergence of new miRNA genes in the plant Arabidopsis halleri

MicroRNAs (miRNAs) are central players of the regulation of gene expression in Eukaryotes. The repertoires of miRNA genes vary drastically even among closely related species, indicating that they are evolutionarily labile. However, the processes by which they originate over the course of evolution and the nature of their progenitors across the genome remain poorly understood. Here we analyzed miRNA genes in Arabidopsis halleri, a plant species where we recently documented a large number of species-specific miRNA genes, likely to represent recent events of emergence. Analysis of sequence homology across the genome indicates that a diversity of sources contributes to the emergence of new miRNA genes, including inverted duplications from protein-coding genes, rearrangements of transposable element sequences and duplications of preexisting miRNA genes. Our observations indicate that the origin from protein-coding genes was less common than was previously considered. In contrast, we estimate that almost half of the new miRNA genes likely emerged from transposable elements. Miniature inverted transposable elements (MITE) seem to be particularly important contributors to new miRNA genes, with the Harbinger and Mariner transposable element superfamilies representing disproportionate sources for their emergence. We further analyzed the recent expansion of a miRNA family derived from MuDR elements, and the duplication of miRNA genes formed by two hAT transposons. Overall, our results illustrate the rapid pace at which new regulatory elements can arise from the modification of preexisting sequences in a genome, and highlight the central role of certain categories of transposable elements in this process.

evolutionary biology↗

The evolutionary history and functional specialization of microRNA genes in Arabidopsis halleri and A. lyrata

MicroRNAs (miRNAs) are a class of small non-coding RNAs that play important regulatory roles in plant genomes. While some miRNA genes are deeply conserved, the majority appear to be species-specific, raising the question of how they emerge and integrate into cellular regulatory networks. To better understand this, we first performed a detailed annotation of miRNA genes in the closely related plants Arabidopsis halleri and A. lyrata and evaluated their phylogenetic conservation across 87 plant species. We then characterized the process by which newly emerged miRNA genes progressively acquire the properties of "canonical" miRNA genes, in terms of size and stability of the hairpin precursor, loading of their cleavage products into Argonaute proteins, and potential to regulate downstream target genes. Nucleotide polymorphism was lower in the mature miRNA sequence than in the other parts of the hairpin (stem, terminal loop), and the regions of coding sequences targeted by miRNAs also had reduced diversity as compared to their neighboring regions along the genes. These patterns were less pronounced for recently emerged than for evolutionarily conserved miRNA genes, suggesting a weaker selective constraint on the most recent miRNA genes. Our results illustrate the rapid birth-and-death of miRNA genes in plant genomes, and provide a detailed picture of the evolutionary processes by which a small fraction of them eventually integrate into "core" biological processes.

evolutionary biology↗

Modifiers of genetic dominance at the Arabidopsis self-incompatibility locus retain proto-miRNA features and act through non-canonical gene silencing pathways

Self-incompatibility in flowering plants is a common mechanism that prevents self-fertilization and promotes outcrossing. In Brassicaceae, the self-incompatibility locus is highly diverse, with many alleles arranged in a complex dominance hierarchy and exhibiting monoallelic expression in heterozygote individuals. Monoallelic expression of the pollen self-incompatibility gene is achieved through the action of sRNA precursors that resemble miRNAs, although the underlying molecular mechanisms remain elusive. Here, we engineered Arabidopsis thaliana lines expressing components of the Arabidopsis halleri self-incompatibility system, and used a reverse genetics approach to pinpoint the pathways underlying the function of these sRNA precursors. We showed that they trigger a robust decrease in transcript abundance of the recessive self-incompatibility genes, but not through the canonical transcriptional or post-transcriptional gene silencing pathways. Furthermore, we observed that single sRNA precursors are typically processed into hundreds of sRNA molecules with a variety of sizes, abundance levels and ARGONAUTE loading preferences. Our results suggest that these seemingly arbitrary processing characteristics are essential for establishing the self-incompatibility dominance hierarchy, as they enable a single sRNA precursor from a dominant allele to effectively repress multiple recessive alleles, thus providing a unique example of how small RNAs mediate gene silencing within a highly complex regulatory network. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=80 SRC="FIGDIR/small/591913v3_ufig1.gif" ALT="Figure 1"> View larger version (24K): org.highwire.dtl.DTLVardef@b32c02org.highwire.dtl.DTLVardef@10e65d3org.highwire.dtl.DTLVardef@3f14b3org.highwire.dtl.DTLVardef@1682d57_HPS_FORMAT_FIGEXP M_FIG C_FIG

plant biology↗