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Heterochronic meiotic misexpression in an interspecific yeast hybrid

ABSTRACT: Changes in gene regulation rapidly accumulate between species and may contribute to reproductive isolation through misexpression of genes in interspecific hybrids. Hybrid misexpression, defined by expression levels outside the range of both parental species, is thought to be a result of cis- and trans-acting regulatory changes that interact in the hybrid, or arise from changes in the relative abundance of various tissues or cell types due to defects in developmental. Here, we show that misexpressed genes in a sterile interspecific Saccharomyces yeast hybrid result from a heterochronic shift in the timing of the normal meiotic gene expression program. By tracking nuclear divisions, we find that S. cerevisiae initiates meiosis earlier than its closest known relative, S. paradoxus, yet both species complete meiosis at the same time. Although the hybrid up- and down-regulates genes in a similar manner to both parents, the hybrid meiotic program occurs earlier than both parents. The timing shift results in a heterochronic pattern of misexpression throughout meiosis I and the beginning of meiosis II. Coincident with the timing of misexpression, we find an increase in the relative abundance of opposing cis and trans-acting changes and compensatory changes, as well as a transition from predominantly trans-acting to cis-acting expression divergence over the course of meiosis. However, misexpression does not appear to be a direct consequence of cis- and trans-acting regulatory divergence. Our results demonstrate that hybrid misexpression in yeast results from a heterochronic shift in the meiotic gene expression program.

ORGANISM(S): Saccharomyces cerevisiae Saccharomyces cerevisiae x Saccharomyces paradoxus Saccharomyces paradoxus

PROVIDER: GSE51809 | GEO | 2013/10/31

SECONDARY ACCESSION(S): PRJNA225473

REPOSITORIES: GEO

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Project description:Changes in gene regulation rapidly accumulate between species and may contribute to reproductive isolation through misexpression of genes in interspecific hybrids. Hybrid misexpression, defined by expression levels outside the range of both parental species, is thought to be a result of cis- and trans-acting regulatory changes that interact in the hybrid, or arise from changes in the relative abundance of various tissues or cell types due to defects in developmental. Here, we show that misexpressed genes in a sterile interspecific Saccharomyces yeast hybrid result from a heterochronic shift in the timing of the normal meiotic gene expression program. By tracking nuclear divisions, we find that S. cerevisiae initiates meiosis earlier than its closest known relative, S. paradoxus, yet both species complete meiosis at the same time. Although the hybrid up- and down-regulates genes in a similar manner to both parents, the hybrid meiotic program occurs earlier than both parents. The timing shift results in a heterochronic pattern of misexpression throughout meiosis I and the beginning of meiosis II. Coincident with the timing of misexpression, we find an increase in the relative abundance of opposing cis and trans-acting changes and compensatory changes, as well as a transition from predominantly trans-acting to cis-acting expression divergence over the course of meiosis. However, misexpression does not appear to be a direct consequence of cis- and trans-acting regulatory divergence. Our results demonstrate that hybrid misexpression in yeast results from a heterochronic shift in the meiotic gene expression program. We analyzed three biological replicates of the parental yeast strains, S. cerevisiae and S. paradoxus, and four replicates of their hybrid over four developmental time points. Two hybrid replicates contain MATa from S. cerevisiae and MATalpha from S. paradoxus. The other two hybrid replicates are reciprocal crosses. The developmental time points are T0, which serves as a control, and is the moment cells enter sporulation media. M1 is the beginning of meiosis I. M1/M2 is the overlap of the end of meiosis I and the beginning of meiosis II. M2 is the end of meiosis II.

Project description:The X chromosome has a large effect on hybrid dysfunction, particularly hybrid male sterility. Although the evidence for this so-called large-X effect is clear, its molecular causes are not yet fully understood. One possibility is that, under certain conditions, evolution proceeds faster in X-linked loci than in their autosomal counterparts due to both natural selection and their hemizygosity in males (i.e. Faster-X effect), an effect that is expected to be greatest in genes with male-biased expression. Here I studied variation in transcript abundance within and between species in Drosophila yakuba, D. santomea and their hybrid males to evaluate both the faster-X and large-X effects at the level of genome-wide gene expression. I found that expression in X-linked male-biased genes evolves faster than in their autosomal counterparts, an effect that is accompanied by a unique reduction in gene expression polymorphism. Although we do not know the precise relationship between nucleotide and gene expression changes, elevated divergence to polymorphism ratios are consistent with Darwinian selection driving expression differences between species in X-linked male-biased genes, likely enhanced by male hemizygosity. Abundant changes in both cis- and trans-regulatory elements underlie regulatory gene expression divergence in the majority of the genes analyzed despite the recent split of the two sister species. I detected a large-X effect on regulation of expression in hybrid males, affecting mostly male-biased genes but also, to a lesser degree, nonsex-biased genes. Interestingly this misexpression is concentrated mostly in autosomal genes, likely facilitated by the rapid evolution of sex-linked trans-acting factors. I conclude that the faster evolution of X-linked male-biased genes, at both protein and expression levels, can contribute to explain the large effect of the X chromosome on hybrid male sterility, possibly mediating autosomal misexpression through cis-trans interactions.

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Heterochronic meiotic misexpression in an interspecific yeast hybrid

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