Biology subjects

Muyle, A.

Publications and source records attributed to Muyle, A..

12 recordsLinked to original sources

bioRxiv2023

Evolution of sex-biased gene expression during transitions to separate sexes in the Silene genus

Sexual dimorphism is widespread among species with separate sexes and its extent is thought to be governed by the differential expression of thousands of genes between males and females (known as Sex-Biased Genes, hereafter SBGs). SBGs have been studied in numerous species, but rarely in a comparative way, which curtails our understanding of their evolution, especially during multiple independent transitions to separate sexes. We sequenced the transcriptomes of nine dioecious species, two gynodioecious species (separate females and hermaphrodites) and two hermaphrodite species from the Silene genus. Our dataset provides access to three independent transitions to dioecy (dating from less than 1 Myo to about 11 Myo). We demonstrated that male-biased expression emerges first during a transition to separate sexes, later followed by female-biased genes. Furthermore, we showed that, despite a mixture of selective regimes, positive selection significantly affects the evolution of some SBGs. Overall, this study provides new insights on the causes of SBG evolution during transitions to separate sexes. TeaserThis study describes the evolution of sex-biased gene expression during a transition to separate sexes in plants.

evolutionary biology↗

bioRxiv2023

The Silene latifolia genome and its giant Y chromosome

In some species, the Y is a tiny chromosome but the dioecious plant Silene latifolia has a giant [~]550 Mb Y chromosome, which has remained unsequenced so far. Here we used a hybrid approach to obtain a high-quality male S. latifolia genome. Using mutants for sexual phenotype, we identified candidate sex-determining genes on the Y. Comparative analysis of the sex chromosomes with outgroups showed the Y is surprisingly rearranged and degenerated for a [~]11 MY-old system. Recombination suppression between X and Y extended in a stepwise process, and triggered a massive accumulation of repeats on the Y, as well as in the non-recombining pericentromeric region of the X, leading to giant sex chromosomes. One-Sentence SummaryThis work uncovers the structure, function, and evolution of one of the largest giant Y chromosomes, that of the model plant Silene latifolia, which is almost 10 times larger than the human Y, despite similar genome sizes.

genomics↗

bioRxiv2022

Diverse patterns of secondary structure across genes and transposable elements are associated with siRNA production and epigenetic fate

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 potential signal for an RNAi-like host epigenetic response mediated by small interfering RNAs (siRNAs). In this study, we predicted local secondary structures in features of the maize genome, focusing on small regions that had folding energies similar to pre-miRNA loci. We found secondary structures to be common in retrotransposons, in Helitrons, and in genes. These structured regions mapped higher diversities of siRNAs than regions without structure, explaining up to 24% of variation of the siRNA distribution across some TE types. Among genes, those with secondary structure were 1.5-fold more highly expressed, on average, than genes without secondary structure. However, these genes were also more variably expressed across the 26 NAM lines, and this variability correlated with the number of mapping siRNAs. We conclude that local stem-loop structures are a nearly ubiquitous feature of expressed regions of the maize genome, that they correlate with higher siRNA mapping, and that they can represent a trade-off between functional need and the potentially negative consequences of siRNA production.

genomics↗

bioRxiv2020

Chromosome-scale assembly of the genome of Salix dunnii reveals a male-heterogametic sex determination system on chromosome 7

Sex determination systems in plants can involve either female or male heterogamety (ZW or XY, respectively). Here we used Illumina short reads, Oxford Nanopore Technologies (ONT) long reads, and Hi-C reads to assemble the first chromosome-scale genome of a female willow tree (Salix dunnii), and to predict genes using transcriptome sequences and available databases. The final genome sequence of 328 Mb in total was assembled in 29 contigs, and includes 31,501 genes. We inferred a male heterogametic sex determining factor on chromosome 7, suggesting that, unlike the female heterogamety of most species in the genus Salix, male heterogamety evolved in the subgenus Salix. The S. dunnii X-linked region occupies about 3.21 Mb of chromosome 7, and is probably in a pericentromeric region. Our data suggest that this region is enriched for transposable element insertions, and about one third of its 124 protein-coding genes were gained via duplications from other genome regions. We detect purifying selection on the genes that were ancestrally present in the region, though some have been lost. Transcriptome data from female and male individuals show more male- than female-biased genes in catkin and leaf tissues, and indicate enrichment for male-biased genes in the pseudo-autosomal regions. Our study provides valuable genomic resources for studying sex chromosome evolution in Salicaceae family.

genomics↗

bioRxiv2020

Gene body methylation is under selection in Arabidopsis thaliana

In plants, mammals and insects, some genes are methylated in the CG dinucleotide context, a phenomenon called gene body methylation. It has been controversial whether this phenomenon has any functional role. Here, we took advantage of the availability of 876 leaf methylomes in Arabidopsis thaliana to characterize the population frequency of methylation at the gene level and estimated the site-frequency spectrum of allelic states (epialleles). Using a population genetics model specifically designed for epigenetic data, we found that genes with ancestral gene body methylation are under significant selection to remain methylated. Conversely, all genes taken together were inferred to be under selection to be unmethylated. The estimated selection coefficients were small, similar to the magnitude of selection acting on codon usage. We also estimated that A. thaliana is losing gene body methylation three-fold more rapidly than gaining it, which could be due to a recent reduction in the efficacy of selection after a switch to selfing. Finally, we investigated the potential function of gene body methylation through its link with gene expression level. Across genes with polymorphic methylation states, the expression of gene body methylated alleles was consistently and significantly higher than unmethylated alleles. Although it is difficult to disentangle genetic from epigenetic effects, our work suggests that gbM has a small but measurable effect on fitness, perhaps due to its association to a phenotype like gene expression.

genetics↗

bioRxiv2020

Evidence for dosage compensation in Coccinia grandis, a plant with a highly heteromorphic XY system

Some ~15.000 angiosperms are dioecious, but mechanisms of sex determination in plants remain poorly understood. In particular, how Y chromosomes evolve and degenerate, and whether dosage compensation evolves as a response, are matters of debate. Here we focus on Coccinia grandis, a dioecious cucurbit with the highest level of X/Y heteromorphy recorded so far. We identified sex-linked genes using RNA sequences from a cross and a model-based method termed SEX-DETector. Parents and F1 individuals were genotyped and the transmission patterns of SNPs then analysed. In the >1300 sex-linked genes studied, X-Y divergence was 0.13 - 0.17, and substantial Y degeneration is implied by an average Y/X expression ratio of 0.63 and an inferred gene loss on the Y of ~40%. We also found reduced Y gene expression being compensated by elevated expression of corresponding genes on the X and an excess of sex-biased genes on the sex chromosomes. Molecular evolution of sex-linked genes in C. grandis is thus comparable to that in Silene latifolia, another dioecious plant with a strongly heteromorphic XY system, and cucurbits are the fourth plant family in which dosage compensation is described, suggesting it might be common in plants.

plant biology↗

bioRxiv2019

The genetic basis of sex determination in grapevines (Vitis spp.)

Sex determination in grapevine evolved through a complex succession of switches in sexual systems. Phased genomes built with single molecule real-time sequencing reads were assembled for eleven accessions of cultivated hermaphrodite grapevines and dioecious males and females, including the ancestor of domesticated grapevine and other related wild species. By comparing the phased sex haplotypes, we defined the sex locus of the Vitis genus and identified polymorphisms spanning regulatory and coding sequences that are in perfect association with each sex-type throughout the genus. These findings identified a novel male-fertility candidate gene, INP1, and significantly refined the model of sex determination in Vitis and its evolution.

evolutionary biology↗

bioRxiv2019

Gene capture by transposable elements leads to epigenetic conflict

Plant 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 cross-talk 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. Here, we examined this model by focusing on three TE families in maize: Helitrons, Pack-MULEs and Sirevirus LTR retrotransposons. We documented 1,263 TEs containing exon fragments from 1,629 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 vs. 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 cross-talk siRNAs were linked with CHH methylation. Translocated genes, in contrast, bore the signature of silencing by being highly methylated and less expressed. They were also overrepresented among donor genes, suggesting a link between capture and gene movement. The evidence for an advantage to TEs was less obvious. TEs with captured fragments were older, mapped fewer siRNAs and were slightly less methylated than TEs without captured fragments but showed no evidence of increased copy numbers. Altogether, our results demonstrate that TE capture triggers an epigenetic conflict for important genes, but it may lead to pseudogenization for less constrained genes.

genomics↗

bioRxiv2019

The Genomics of Selfing in Maize (Zea mays ssp. mays): Catching Purging in the Act

In plants, self-fertilization is both an important reproductive strategy and a valuable genetic tool. In theory, selfing increases homozygosity at a rate of 0.50 per generation. Increased homozygosity can uncover recessive deleterious variants and lead to inbreeding depression, unless it is countered by the loss of these variants by genetic purging. Here we investigated the dynamics of purging on genomic scale by testing three predictions. The first was that heterozygous, putatively deleterious SNPs were preferentially lost from the genome during continued selfing. The second was that the loss of deleterious SNPs varied as a function of recombination rate, because recombination increases the efficacy of selection by uncoupling linked variants. Finally, we predicted that genome size (GS) decreases during selfing, due to the purging of deleterious transposable element (TE) insertions. We tested these three predictions by following GS and SNP variants in a series of selfed maize (Zea mays ssp. mays) lines over six generations. In these lines, putatively deleterious alleles were purged, and purging was more pronounced in highly recombining regions. Homozygosity increased more slowly than expected; instead of increasing by 50% each generation, it increased by 35% to 40%. Finally, three lines showed dramatic decreases in GS, losing an average of 398 Mb from their genomes over the short timeframe of our experiment. TEs were the principal component of loss, and GS loss was more likely for lineages that began with more TE and more chromosomal knob repeats. Overall, this study documented remarkable GS loss - as much DNA as three Arabidopsis thaliana genomes, on average - in only a few generations of selfing.

genomics↗

bioRxiv2018

Dioecy in plants: an evolutionary dead end? Insights from a population genomics study in the Silene genus

About 15,000 angiosperm species ([~]6%) have separate sexes, a phenomenon known as dioecy. Early work reported a lower species richness in dioecious compared to non-dioecious sister clades, which was taken to suggest that dioecy might be an evolutionary dead end. More recently, phylogenetic analyses using different methodologies have challenged this conclusion. Here, we used a population genomics approach to look for evidence of evolutionary handicaps of dioecy in the Silene genus at the molecular level. We obtained RNA-seq data of individuals from several populations in 13 closely related species with different breeding systems: seven dioecious, three hermaphroditic and three gynodioecious species. We show that dioecy is associated with increased genetic diversity and a higher selection efficacy both against deleterious and for beneficial mutations while controlling for differences in population size. We conclude that, in the Silene genus, dioecious species bear no sign of mutational burden or upcoming extinction. On the contrary, dioecious species harbor a higher potential for adaptation than their non-dioecious relatives. Our results do not support the evolutionary dead end hypothesis and re-open the question why dioecy is rare in angiosperms.\n\nSignificance statementDioecy (=separate sexes) is much rarer in flowering plants compared to animals and other organisms. The \"dead-end hypothesis\" states that dioecious plant populations might experience evolutionary handicaps such as low seed dispersal (as only 50% of the individuals, the females, contribute), which might cause high genetic drift, low adaptation and ultimately extinction. Here we tested this hypothesis by focusing on the genus Silene and by comparing the population genetics of 13 dioecious and non-dioecious species. We found that dioecious Silene species exhibit lower genetic drift and more adaptation compared to their non-dioecious relatives. Our results thus reject the dead-end hypothesis and re-open the question of why dioecy is rare in flowering plants.

evolutionary biology↗

bioRxiv2017

Maternal X chromosome upregulation in both sexes initiates dosage compensation evolution

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044).\n\nSex chromosomes have repeatedly evolved from a pair of autosomes1. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals2-4. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants5. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals.

evolutionary biology↗

bioRxiv2017

Hallmarks of early sex-chromosome evolution in the dioecious plant Mercurialis annua revealed by de novo genome assembly, genetic mapping and transcriptome analysis

Suppressed recombination around a sex-determining locus allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. Both genetic mapping and exome resequencing of individuals across the species range independently identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about a third of the Y chromosome has ceased recombining, a region containing 568 transcripts and spanning 22.3 cM in the corresponding female map. Patterns of gene expression hint at the possible role of sexually antagonistic selection in having favored suppressed recombination. In total, the genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. There was limited evidence of Y-chromosome degeneration in terms of gene loss and pseudogenization, but sequence divergence between the X and Y copies of many sex-linked genes was higher than between M. annua and its dioecious sister species M. huetii with which it shares a sex-determining region. The Mendelian inheritance of sex in interspecific crosses, combined with the other observed pattern, suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining about one million years ago. Article summaryPlants that evolved separate sexes (dioecy) recently are ideal models for studying the early stages of sex-chromosome evolution. Here, we use karyological, whole genome and transcriptome data to characterize the homomorphic sex chromosomes of the annual dioecious plant Mercurialis annua. Our analysis reveals many typical hallmarks of dioecy and sex-chromosome evolution, including sex-biased gene expression and high X/Y sequence divergence, yet few premature stop codons in Y-linked genes and very little outright gene loss, despite 1/3 of the sex chromosome having ceased recombination in males. Our results confirm that the M. annua species complex is a fertile system for probing early stages in the evolution of sex chromosomes.

genomics↗