GSE51809
Heterochronic meiotic misexpression in an interspecific yeast hybrid
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. Overall design: 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.