Spatiotemporal Regulation of a Single Adaptively Evolving<i>Trans</i>-Regulatory Element Contributes to Spermatogenetic Expression Divergence in<i>Drosophila</i>

Huang, Yumei; Su, Rui; Lu, Gendi; Zeng, Weishun; Huang, Chenglong; Zou, Chuangchao; Tang, Tian

doi:10.1093/molbev/msac127

Cited by 3 publications

(2 citation statements)

References 94 publications

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“…The spatiotemporal regulation of miRNAs during development have been widely and precisely studied [30][31][32] . Redundant functions of miRNAs often arises from multiples tissues/organs or different developmental stages 8 .…”

Section: Resultsmentioning

confidence: 99%

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MicroRNA-mediated network redundancy is constrained by purifying selection and contributes to expression robustness

Liufu,

Dai,

Lan

et al. 2024

Preprint

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MicroRNAs (miRNAs) act as trans-acting elements and form composite feedforward circuits (cFFCs) in conjunction with transcription factors (TFs), leading to redundancy in network motifs and influencing gene expression regulation. However, the maintenance of miRNA-mediated regulatory redundancy and its impact on gene expression evolution remain elusive. Using public ChIP-seq/ChIP-chip and ATAC-seq data, we constructed miRNA-mediated cFFCs in Drosophila melanogaster embryos and found that most of predicted miRNA targets are involved in redundant cFFCs. Population genetics analysis revealed that highly redundant cFFCs are subjected to stronger purifying selection than low-redundant or non-redundant cFFCs. This redundancy negatively correlates with expression divergence between D. melanogaster and D. simulans, and is associate with expression stability in D. melanogaster embryos under heat shock. Moreover, highly redundant cFFCs mainly target older genes or young genes with broader expression. Our findings emphasize the biological significance of miRNA-mediated cFFC redundancy in mediating the robustness of gene expression during evolution.

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Section: Resultsmentioning

confidence: 99%

“…The role of miRNA in ne-tuning or buffering gene expression has been extensively investigated 8,11,17,27,32,44 . However, the evolutionary signi cance of miRNA-composed network motifs in gene regulation remains relatively unexplored 25,26 .…”

Section: Discussionmentioning

confidence: 99%

MicroRNA-mediated network redundancy is constrained by purifying selection and contributes to expression robustness

Liufu,

Dai,

Lan

et al. 2024

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

MicroRNA-mediated network redundancy is constrained by purifying selection and contributes to expression robustness in Drosophila melanogaster

Dai,

Lan,

Lyu

et al. 2024

Commun Biol

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MicroRNAs (miRNAs) are post-transcriptional, non-coding regulatory RNAs that function coordinately with transcription factors (TFs) in gene regulatory networks. TFs and their targets are often co-regulated by miRNAs, forming composite feedforward circuits (cFFCs) with varying degrees of redundancy, primarily mediated by miRNAs. However, the maintenance of miRNA-mediated regulatory redundancy and its impact on gene expression evolution remain elusive. By integrating ChIP-seq data from ENCODE and miRNA targeting from TargetScanFly, we quantified miRNA-mediated cFFC redundancy in Drosophila melanogaster embryos and larvae, revealing more than three quarters of miRNA targets are involved in redundant cFFCs. Higher cFFC redundancy, where more miRNAs target the same gene within a cFFC, is correlated with stronger purifying selection, reduced expression divergence between species, and increased expression stability under heat shock stress. Redundant cFFCs primarily regulate older or broadly expressed young genes. These findings highlight the role of miRNA-mediated cFFC redundancy in enhancing gene expression robustness through natural selection.

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Species differences in hormonally mediated gene expression underlie the evolutionary loss of sexually dimorphic coloration inSceloporuslizards

Robinson

Hale

Wittman

et al. 2023

Journal of Heredity

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Phenotypic sexual dimorphism often involves the hormonal regulation of sex-biased expression for underlying genes. However, it is generally unknown whether the evolution of hormonally mediated sexual dimorphism occurs through upstream changes in tissue sensitivity to hormone signals, downstream changes in responsiveness of target genes, or both. Here, we use comparative transcriptomics to explore these possibilities in two species of Sceloporus lizards exhibiting different patterns of sexual dichromatism. Sexually dimorphic S. undulatus develops blue and black ventral coloration in response to testosterone, while sexually monomorphic S. virgatus does not, despite exhibiting similar sex differences in circulating testosterone levels. We administered testosterone implants to juveniles of each species and used RNAseq to quantify gene expression in ventral skin. Transcriptome-wide responses to testosterone were stronger in S. undulatus than in S. virgatus, suggesting species differences in tissue sensitivity to this hormone signal. Species differences in the expression of genes for androgen metabolism and sex hormone binding globulin were consistent with this idea, but expression of the androgen receptor gene was higher in S. virgatus, complicating this interpretation. Downstream of androgen signaling, we found clear species differences in hormonal responsiveness of genes related to melanin synthesis, which were upregulated by testosterone in S. undulatus, but not in S. virgatus. Collectively, our results indicate that hormonal regulation of melanin synthesis pathways contributes to the development of sexual dimorphism in S. undulatus, and that changes in the hormonal responsiveness of these genes in S. virgatus contribute to the evolutionary loss of ventral coloration.

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Spatiotemporal Regulation of a Single Adaptively EvolvingTrans-Regulatory Element Contributes to Spermatogenetic Expression Divergence inDrosophila

Cited by 3 publications

References 94 publications

MicroRNA-mediated network redundancy is constrained by purifying selection and contributes to expression robustness

MicroRNA-mediated network redundancy is constrained by purifying selection and contributes to expression robustness

MicroRNA-mediated network redundancy is constrained by purifying selection and contributes to expression robustness in Drosophila melanogaster

Species differences in hormonally mediated gene expression underlie the evolutionary loss of sexually dimorphic coloration inSceloporuslizards

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