Epigenetic effects of polymorphic Y chromosomes modulate chromatin components, immune response, and sexual conflict

Abstract

Genetic conflicts between sexes and generations provide a foundation for understanding the functional evolution of sex chromosomes and sexually dimorphic phenotypes. Y chromosomes of Drosophila contain multi-megabase stretches of satellite DNA repeats and a handful of protein-coding genes that are monomorphic within species. Nevertheless, polymorphic variation in heterochromatic Y chromosomes of Drosophila result in genome-wide gene expression variation. Here we show that such naturally occurring Y-linked regulatory variation (YRV) can be detected in somatic tissues and contributes to the epigenetic balance of heterochromatin/ euchromatin at three distinct loci showing position-effect variegation (PEV). Moreover, polymorphic Y chromosomes differentially affect the expression of thousands of genes in XXY female genotypes in which Y-linked protein-coding genes are not transcribed. The data show a disproportionate influence of YRV on the variable expression of genes whose protein products localize to the nucleus, have nucleic-acid binding activity, and are involved in transcription, chromosome organization, and chromatin assembly. These include key components such as HP1, Trithorax-like (GAGA factor), Su(var)3-9, Brahma, MCM2, ORC2, and inner centromere protein. Furthermore, mitochondria-related genes, immune response genes, and transposable elements are also disproportionally affected by Y chromosome polymorphism. These functional clusterings may arise as a consequence of the involvement of Y-linked heterochromatin in the origin and resolution of genetic conflicts between males and females. Taken together, our results indicate that Y chromosome heterochromatin serves as a major source of epigenetic variation in natural populations that interacts with chromatin components to modulate the expression of biologically relevant phenotypic variation.evolution | heterochromatin | position-effect variegation | regulatory

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

“…gambiae strain in 2014 is transcriptionally active and has been stably integrated ever since, establishing that the Y chromosome is amenable to the molecular manipulation required for Y-linked genetic vector control strategies (68). The high level of satellite DNA polymorphism within species could have important phenotypic consequences for fitness-related traits (8,9). Moreover, the dramatic degree of satellite DNA turnover on the Y between closely related species has been implicated in hybrid incompatibility in Drosophila (69-71).…”

“…In animals with morphologically distinct (heterogametic) sex chromosomes, the Y has ceased crossing over with the X across some or all of its length and the nonrecombining region is transmitted clonally by males (4,5). The absence of recombination initiates progressive genetic decaygene loss and accumulation of repetitive sequences-but there is increasing recognition that even relatively old and otherwise highly degenerate Y chromosomes retain functional importance not only for sexual reproduction but for their contributions to global gene regulation, affecting health and survival (6)(7)(8)(9)(10). Notwithstanding these critical roles, the Y chromosome remains one of the most recalcitrant and poorly characterized portions of any genome more than a decade into the postgenomic era, with current knowledge resting largely on only two animal groups: mammals and Drosophila (2,11).…”

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

“…Genome-wide gene expression in genotypes differing only in Y chromosome origin revealed cryptic Y chromosome diversity (Lemos et al, 2008;Lemos et al, 2010;Jiang et al, 2010;Branco et al, 2013a). These include changes in the expression level of genes involved with functions as varied as metabolism, cell division, immune response and chromatin structure.…”

Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans

“…These could involve, for instance, differential recruitment of chromatin-modifying proteins to rDNA arrays with variable CN. Disproportional binding to rDNA locus might result in altered concentrations throughout the rest of the genome, thereby effecting genome-wide chromatin environments and transcription rates 8,[51][52][53] . The observation that rDNA dosage is correlated with the expression of several proteins that modify the chromatin (Fig.…”