Zakerzade Rana, Chang Ching-Ho, Chatla Kamalakar, Krishnapura Ananya, Appiah Samuel P, Zhang Jacki, Unckless Robert L, Blumenstiel Justin P, Bachtrog Doris, Wei Kevin H-C
Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada.
Life Sciences Institute, University of British Columbia, Vancouver British Columbia, Canada.
PLoS Genet. 2025 Jan 13;21(1):e1011549. doi: 10.1371/journal.pgen.1011549. eCollection 2025 Jan.
The synaptonemal complex (SC) is a protein-rich structure essential for meiotic recombination and faithful chromosome segregation. Acting like a zipper to paired homologous chromosomes during early prophase I, the complex is a symmetrical structure where central elements are connected on two sides by the transverse filaments to the chromatin-anchoring lateral elements. Despite being found in most major eukaryotic taxa implying a deeply conserved evolutionary origin, several components of the complex exhibit unusually high rates of sequence turnover. This is puzzlingly exemplified by the SC of Drosophila, where the central elements and transverse filaments display no identifiable homologs outside of the genus. Here, we exhaustively examine the evolutionary history of the SC in Drosophila taking a comparative phylogenomic approach with high species density to circumvent obscured homology due to rapid sequence evolution. Contrasting starkly against other genes involved in meiotic chromosome pairing, SC genes show significantly elevated rates of coding evolution due to a combination of relaxed constraint and recurrent, widespread positive selection. In particular, the central element cona and transverse filament c(3)G have diversified through tandem and retro-duplications, repeatedly generating paralogs with novel germline activity. In a striking case of molecular convergence, c(3)G paralogs that independently arose in distant lineages evolved under positive selection to have convergent truncations to the protein termini and elevated testes expression. Surprisingly, the expression of SC genes in the germline is prone to change suggesting recurrent regulatory evolution which, in many species, resulted in high testes expression even though Drosophila males are achiasmic. Overall, our study recapitulates the poor conservation of SC components, and further uncovers that the lack of conservation extends to other modalities including copy number, genomic locale, and germline regulation. Considering the elevated testes expression in many Drosophila species and the common ancestor, we suggest that the activity of SC genes in the male germline, while still poorly understood, may be a prime target of constant evolutionary pressures driving repeated adaptations and innovations.
联会复合体（SC）是一种富含蛋白质的结构，对减数分裂重组和忠实的染色体分离至关重要。在减数分裂前期I早期，该复合体就像拉链一样作用于配对的同源染色体，它是一种对称结构，其中央元件通过横向细丝在两侧与锚定染色质的侧向元件相连。尽管在大多数主要的真核生物类群中都发现了它，这意味着其具有深度保守的进化起源，但该复合体的几个组成部分却表现出异常高的序列更替率。果蝇的SC就是一个令人费解的例子，其中央元件和横向细丝在果蝇属之外没有可识别的同源物。在这里，我们采用具有高物种密度的比较系统基因组学方法，详尽地研究了果蝇中SC的进化历史，以规避由于快速序列进化导致的同源性模糊问题。与参与减数分裂染色体配对的其他基因形成鲜明对比的是，由于宽松的限制和反复出现的广泛正选择相结合，SC基因显示出显著提高的编码进化速率。特别是，中央元件cona和横向细丝c(3)G通过串联和逆转录复制而多样化，反复产生具有新的生殖系活性的旁系同源物。在一个引人注目的分子趋同案例中，在遥远谱系中独立出现的c(3)G旁系同源物在正选择下进化，使其蛋白质末端具有趋同的截短并提高了睾丸表达。令人惊讶的是，SC基因在生殖系中的表达容易发生变化，这表明存在反复的调控进化，在许多物种中，即使果蝇雄性没有交叉互换，也导致了睾丸中的高表达。总体而言，我们的研究概括了SC组件的保守性较差的情况，并进一步发现这种缺乏保守性还延伸到其他方面，包括拷贝数、基因组位置和生殖系调控。考虑到许多果蝇物种及其共同祖先中睾丸表达的升高，我们认为，虽然对雄性生殖系中SC基因的活性仍知之甚少，但它可能是持续进化压力的主要目标，驱动着反复的适应和创新。
