Avelino Camila C, Mendonca Carolina A, Goldstein Gabriel, Bruno Henry Bonilla, Carvalho Antonio Bernardo, Vibranovski Maria D
Department of Genetics and Evolutionary Biology, Institute of Biosciences, University of São Paulo, São Paulo, São Paulo, Brazil.
School of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil.
PLoS Genet. 2025 Sep 11;21(9):e1011511. doi: 10.1371/journal.pgen.1011511. eCollection 2025 Sep.
The inherent differences between sex chromosomes in males and females create conflicts in gene expression, driving the evolution of regulatory mechanisms such as Meiotic Sex Chromosome Inactivation (MSCI), a process that transcriptionally silences the sex chromosomes during male meiosis. In this study, we explore the evolutionary dynamics of MSCI within the Drosophila genus by analyzing transcriptomes across different stages of spermatogenesis in D. melanogaster and its progressively more distant relatives, D. simulans, D. willistoni, and D. mojavensis. Stage-enriched bulk RNA sequencing, showing a strong correlation in spermatogenic gene expression patterns among these species, revealed that MSCI dates back to the early evolution of the Drosophila genus, impacting the regulation of both coding and long non-coding RNAs. Notably, for newly evolved genes, X-linked genes show higher expression levels than autosomal genes during mitosis and meiosis, indicating that MSCI predominantly regulates older genes. In contrast, newly evolved autosomal genes exhibit a gradual increase in expression throughout spermatogenesis, reaching their peak in the post-meiotic phase. During this phase, the expression of X-linked new genes decreases, eventually aligning with that of autosomal genes. This expression pattern suggests that haploid selection plays a crucial role in the regulation of new genes, with monoallelic expression of the X chromosome providing an advantage across all stages of germline development, while autosomal gene expression gains a selective edge primarily in the post-meiotic phase. Together, these findings provide new insights into the evolution of sex chromosomes and highlight the critical role of MSCI in shaping gene expression profiles in Drosophila.
雄性和雌性性染色体之间的固有差异导致了基因表达上的冲突，推动了诸如减数分裂性染色体失活（MSCI）等调控机制的进化，MSCI是一个在雄性减数分裂过程中转录沉默性染色体的过程。在本研究中，我们通过分析黑腹果蝇及其亲缘关系逐渐疏远的近亲拟果蝇、威氏果蝇和莫哈韦果蝇精子发生不同阶段的转录组，探索果蝇属内MSCI的进化动态。阶段富集的大量RNA测序显示这些物种间精子发生基因表达模式有很强的相关性，结果表明MSCI可追溯到果蝇属的早期进化，影响着编码RNA和长链非编码RNA的调控。值得注意的是，对于新进化的基因，在有丝分裂和减数分裂期间，X连锁基因的表达水平高于常染色体基因，这表明MSCI主要调控较古老的基因。相反，新进化的常染色体基因在整个精子发生过程中表达逐渐增加，在减数分裂后阶段达到峰值。在此阶段，X连锁新基因的表达下降，最终与常染色体基因的表达趋于一致。这种表达模式表明单倍体选择在新基因的调控中起关键作用，X染色体的单等位基因表达在生殖系发育的所有阶段都具有优势，而常染色体基因表达主要在减数分裂后阶段获得选择优势。总之，这些发现为性染色体的进化提供了新的见解，并突出了MSCI在塑造果蝇基因表达谱中的关键作用。
