Author response: Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution

AbstractThe evolution of sex chromosomes is usually considered to be driven by sexually antagonistic selection in the diploid phase. However, selection during the haploid gametic phase of the lifecycle has recently received theoretical attention as possibly playing a central role in sex chromosome evolution, especially in plants where gene expression in the haploid phase is extensive. In particular, male-specific haploid selection might favour the linkage of pollen beneficial alleles to male sex determining regions on incipient Y chromosomes. This linkage might then allow such alleles to further specialise for the haploid phase. Purifying haploid selection is also expected to slow the degeneration of Y-linked genes expressed in the haploid phase. Here, we examine the evolution of gene expression in flower buds and pollen of two species of Rumex to test for signatures of haploid selection acting during plant sex chromosome evolution. We find that genes with high ancestral pollen expression bias occur more often on sex chromosomes than autosomes and that genes on the Y chromosome are more likely to become enriched for pollen expression bias. We also find that genes with low expression in pollen are more likely to be lost from the Y chromosome. Our results suggest that sex-specific haploid selection during the gametophytic stage of the lifecycle may be a major contributor to several features of plant sex chromosome evolution.

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Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution

eLife ◽

10.7554/elife.17365 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 14

Author(s):

Bayly S Wheeler ◽

Erika Anderson ◽

Christian Frøkjær-Jensen ◽

Qian Bian ◽

Erik Jorgensen ◽

...

Keyword(s):

Gene Expression ◽

X Chromosome ◽

Dosage Compensation ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Nuclear Periphery ◽

Single Copy ◽

Dosage Compensation Complex ◽

Gene Dose ◽

Caenorhabditis Elegans Genome

Changes in chromosome number impair fitness by disrupting the balance of gene expression. Here we analyze mechanisms to compensate for changes in gene dose that accompanied the evolution of sex chromosomes from autosomes. Using single-copy transgenes integrated throughout the Caenorhabditis elegans genome, we show that expression of all X-linked transgenes is balanced between XX hermaphrodites and XO males. However, proximity of a dosage compensation complex (DCC) binding site (rex site) is neither necessary to repress X-linked transgenes nor sufficient to repress transgenes on autosomes. Thus, X is broadly permissive for dosage compensation, and the DCC acts via a chromosome-wide mechanism to balance transcription between sexes. In contrast, no analogous X-chromosome-wide mechanism balances transcription between X and autosomes: expression of compensated hermaphrodite X-linked transgenes is half that of autosomal transgenes. Furthermore, our results argue against an X-chromosome dosage compensation model contingent upon rex-directed positioning of X relative to the nuclear periphery.

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Transcriptional regulation of dosage compensation in Carica papaya

Scientific Reports ◽

10.1038/s41598-021-85480-3 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Juan Liu ◽

Jennifer Han ◽

Anupma Sharma ◽

Ching Man Wai ◽

Ray Ming ◽

...

Keyword(s):

Gene Expression ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Expression Patterns ◽

Global Gene Expression ◽

Sex Chromosome Evolution ◽

Global Gene Expression Profiling ◽

Heterogametic Sex

AbstractSex chromosome evolution results in the disparity in gene content between heterogametic sex chromosomes and creates the need for dosage compensation to counteract the effects of gene dose imbalance of sex chromosomes in males and females. It is not known at which stage of sex chromosome evolution dosage compensation would evolve. We used global gene expression profiling in male and female papayas to assess gene expression patterns of sex-linked genes on the papaya sex chromosomes. By analyzing expression ratios of sex-linked genes to autosomal genes and sex-linked genes in males relative to females, our results showed that dosage compensation was regulated on a gene-by-gene level rather than whole sex-linked region in papaya. Seven genes on the papaya X chromosome exhibited dosage compensation. We further compared gene expression ratios in the two evolutionary strata. Y alleles in the older evolutionary stratum showed reduced expression compared to X alleles, while Y alleles in the younger evolutionary stratum showed elevated expression compared to X alleles. Reduced expression of Y alleles in the older evolutionary stratum might be caused by accumulation of deleterious mutations in regulatory regions or transposable element-mediated methylation spreading. Most X-hemizygous genes exhibited either no or very low expression, suggesting that gene silencing might play a role in maintaining transcriptional balance between females and males.

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