Epigenetics drive the evolution of sex chromosomes in animals and plants

Epigenetics is the study of changes in gene activity that can be transmitted through cell divisions but cannot be explained by changes in the DNA sequence. Epigenetic mechanisms are central to gene regulation, phenotypic plasticity, development and the preservation of genome integrity. Epigenetic mechanisms are often held to make a minor contribution to evolutionary change because epigenetic states are typically erased and reset at every generation, and are therefore, not heritable. Nonetheless, there is growing appreciation that epigenetic variation makes direct and indirect contributions to evolutionary processes. First, some epigenetic states are transmitted intergenerationally and affect the phenotype of offspring. Moreover, bona fide heritable ‘epialleles' exist and are quite common in plants. Such epialleles could, therefore, be subject to natural selection in the same way as conventional DNA sequence-based alleles. Second, epigenetic variation enhances phenotypic plasticity and phenotypic variance and thus can modulate the effect of natural selection on sequence-based genetic variation. Third, given that phenotypic plasticity is central to the adaptability of organisms, epigenetic mechanisms that generate plasticity and acclimation are important to consider in evolutionary theory. Fourth, some genes are under selection to be ‘imprinted' identifying the sex of the parent from which they were derived, leading to parent-of-origin-dependent gene expression and effects. These effects can generate hybrid disfunction and contribute to speciation. Finally, epigenetic processes, particularly DNA methylation, contribute directly to DNA sequence evolution, because they act as mutagens on the one hand and modulate genome stability on the other by keeping transposable elements in check. This article is part of the theme issue ‘How does epigenetics influence the course of evolution?'

Section: Direct Effects Of Epigenetics On Genome Evolutionmentioning

confidence: 99%

How does epigenetics influence the course of evolution?

Ashe

Colot

Oldroyd

2021

“…Ohno [9] hypothesized that X upregulation first evolved to compensate for Y degeneration and that X inactivation evolved afterwards to re-establish ancestral expression levels in females. However, a demonstration of the order of events is still lacking [18] and an alternative scenario is discussed later in this review [19]. In adult tissues of placental mammals, X-inactivation is random, affecting the paternal or maternal X with equal probability and the inactive X varies from cell to cell.…”

Section: Introductionmentioning

confidence: 99%

Dosage compensation evolution in plants: theories, controversies and mechanisms

Muyle

Marais

Bačovský

et al. 2022

Self Cite

In a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation (DC), a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species, we lack the data to differentiate between global and gene-by-gene DC. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.

“…[5]). Sexually labile individuals might help in this enterprise by allowing the identification of mutations, differences in gene expression, or epigenetic mechanisms [100]. In the case of trioecy with a genetic basis, monoclinous or monoecious individuals can easily be selected and maintained artificially, as is the case for some crop species ( C. sativa , V. vinifera , C. papaya ).…”

Section: Discussionmentioning

confidence: 99%

Labile sex expression in angiosperm species with sex chromosomes

Käfer

Méndez

Mousset

2022

Here, we review the literature on sexual lability in dioecious angiosperm species with well-studied sex chromosomes. We distinguish three types of departures from strict dioecy, concerning either a minority of flowers in some individuals (leakiness) or the entire individual, which can constantly be bisexual or change sex. We found that for only four of the 22 species studied, reports of lability are lacking. The occurrence of lability is only weakly related to sex chromosome characteristics (number of sex-linked genes, age of the non-recombining region). These results contradict the naive idea that lability is an indication of the absence or the recent evolution of sex chromosomes, and thereby contribute to a growing consensus that sex chromosomes do not necessarily fix sex determination once and for all. We discuss some implications of these findings for the evolution of sex chromosomes, and suggest that more species with well-characterized lability should be studied with genomic data and tools. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.