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The mode of expression divergence in Drosophila fat body is infection-specific

ABSTRACT: Transcription is controlled by the interactions of cis-acting DNA elements with diffusible trans-acting factors. Changes in cis or trans factors can drive expression divergence within and between species, and the relative prevalence of each can reveal the evolutionary path to variation. Previous work delineating the mode of expression divergence in animals has largely used whole body expression measurements in a single condition. Since cis-acting elements often drive expression in a subset of cell types or conditions, these measurements may not capture the complete contribution of cis-acting changes. Here, we quantify the mode of expression divergence in the Drosophila fat body, the primary immune organ, in several conditions. We performed allele-specific expression analysis using two geographically distinct lines of D. melanogaster and their F1 hybrids. We performed separate infections with Gram-negative S. marcescens or Gram-positive E. faecalis bacteria, which trigger the two primary signaling pathways in the Drosophila innate immune response. The mode of expression divergence strongly depends on the condition, with trans-acting effects dominating in response to Gram-positive infection and cis-acting effects dominating in Gram-negative and pre-infection conditions. Expression divergence in several receptor proteins may underlie the infection-specific trans effects. Before infection, when the fat body has a metabolic role, there are many compensatory effects, changes in cis and trans that counteract each other to maintain expression levels. This work demonstrates that within a single tissue, the mode of expression divergence varies between conditions and suggests that these differences reflect the diverse evolutionary histories of host-pathogen interactions.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE155033 | GEO | 2021/03/23

REPOSITORIES: GEO

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Project description:Both cis- and trans-regulatory mutations contribute to gene expression divergence within and between species. To estimate their relative contributions, we examined two yeast strains, BY4741 (a laboratory strain) and RM11-1a (a wild strain), for their gene expression divergence first by microarray. By incorporating the obtained array data with ChIP-chip data, we generated a set of single-regulator-regulated genes that showed expression divergence between BY4741 and RM11-1a. We randomly selected 50 of these genes for further study. We found substantial variations in the DNA sequences of the promoter regions of these genes and in their regulators between the two strains, which are potential sources of expression divergence. We then developed a step-by-step approach to assess the relative contributions of cis- and trans-variations to expression divergence by using pyrosequencing to quantify the mRNA levels of the two alleles of BY4741 and RM11-1a in co-cultures and in hybrid diploids. Among the 50 genes studied, 4 genes showed no significant expression difference when the two strains were grown in separate cultures or in the same culture (co-culture) and 6 genes showed significant expression difference in separate cultures but not in co-culture. The remaining 40 genes showed expression divergence between the two strains in co-culture. Among these 40 genes, pyrosequencing of diploids showed that 18 cases of expression divergence (45%=18/40) can be attributed to differences in trans-acting factors alone, 7 cases (17.5%) mainly to trans-variations, 8 cases (20%) to both cis- and trans-acting factors, 3 cases (7.5%) mainly to cis-variations, and 4 cases (10%) to cis-acting factors alone. In addition, we replaced the BY promoter by the RM promoter in each of 10 BY genes that were found from our microarray data to have expression divergence between BY and RM, and in each case our quantitative PCR analysis revealed the cis effect of the promoter replacement on gene expression. In summary, our study suggests that trans-acting factors play the major role in expression evolution between yeast strains, but the role of cis variation is also important. Keywords: comparative gene expression between strains

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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The mode of expression divergence in Drosophila fat body is infection-specific

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