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Heterochronic meiotic misexpression in an interspecific yeast hybrid.

ABSTRACT: Regulatory changes rapidly accumulate between species, and interspecific hybrids often misexpress genes. Hybrid misexpression, expression levels outside the range of both parental species, can result from cis- and trans-acting regulatory changes that interact abnormally in hybrids. Thus, misexpressed genes may contribute to hybrid sterility. However, in the context of a whole organism, misexpression may not result directly from cis-trans interactions but rather indirectly from differences between hybrid and parental abundance of cell types. Here we eliminate the confounding effects of cell types by examining gene expression in a sterile interspecific yeast hybrid during meiosis. We investigated gene expression of the yeasts Saccharomyces cerevisiae, S. paradoxus, and their hybrid at multiple meiotic stages. Although the hybrid and parents exhibit similar changes in expression levels across meiosis, the hybrid meiotic program occurs earlier than either parent. The timing change produces a heterochronic pattern of misexpression during midmeiosis. Coincident with the timing of misexpression, we find a transition from predominantly trans-acting to cis-acting expression divergence and an increase in the number of opposing cis-trans changes. However, we find no direct relationship between opposing cis-trans changes and misexpression. Contrary to the notion that cis-trans interactions cause misexpression, a heterochronic shift in the normal meiotic gene expression program produces patterns of misexpression in an yeast hybrid. Our results imply that temporal dynamics of single cell types is important to understanding hybrid misexpression and its relationship to cis-trans interactions.

SUBMITTER: Swain Lenz D

PROVIDER: S-EPMC4032130 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Heterochronic meiotic misexpression in an interspecific yeast hybrid.

Swain Lenz Devjanee D Riles Linda L Fay Justin C JC

Molecular biology and evolution 20140307 6

Regulatory changes rapidly accumulate between species, and interspecific hybrids often misexpress genes. Hybrid misexpression, expression levels outside the range of both parental species, can result from cis- and trans-acting regulatory changes that interact abnormally in hybrids. Thus, misexpressed genes may contribute to hybrid sterility. However, in the context of a whole organism, misexpression may not result directly from cis-trans interactions but rather indirectly from differences betwee ...[more]

PMID: 24608322

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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.

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Heterochronic meiotic misexpression in an interspecific yeast hybrid.

Publications

Heterochronic meiotic misexpression in an interspecific yeast hybrid.

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