Huang Yuheng, Gao Zita Y, Ly Kayla, Lin Leila, Lambooij Jan-Paul, King Elizabeth G, Janssen Aniek, Wei Kevin H-C, Lee Yuh Chwen G
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697.
Center for Molecular Medicine, University Medical Center Utrecht, Utrecht 3584 CG, The Netherlands.
Proc Natl Acad Sci U S A. 2025 Mar 25;122(12):e2427312122. doi: 10.1073/pnas.2427312122. Epub 2025 Mar 18.
Meiotic recombination is a prominent force shaping genome evolution, and understanding why recombination rates vary within and between species has remained a central, though challenging, question. Variation in recombination is widely thought to influence the efficacy of selection in purging transposable elements (TEs), prevalent selfish genetic elements, leading to widely observed negative correlations between TE abundance and recombination rates across taxa. However, accumulating evidence suggests that TEs could instead be the cause rather than the consequence of this relationship. To test this prediction, we formally investigated the influence of polymorphic, putatively active TEs on recombination rates. We developed and benchmarked an approach that uses PacBio long-read sequencing to efficiently, accurately, and cost-effectively identify crossovers (COs), a key recombination product, among large numbers of pooled recombinant individuals. By applying this approach to Drosophila strains with distinct TE insertion profiles, we found that polymorphic TEs, especially RNA-based TEs and TEs with local enrichment of repressive marks, reduce the occurrence of COs. Such an effect leads to different CO frequencies between homologous sequences with and without TEs, contributing to varying CO maps between individuals. The suppressive effect of TEs on CO is further supported by two orthogonal approaches-analyzing the distributions of COs in panels of recombinant inbred lines in relation to TE polymorphism and applying marker-assisted estimations of CO frequencies to isogenic strains with and without transgenically inserted TEs. Our investigations reveal how the constantly changing TE landscape can actively modify recombination, shaping genome evolution within and between species.
减数分裂重组是塑造基因组进化的重要力量，理解物种内部和物种之间重组率为何不同一直是一个核心问题，尽管颇具挑战性。人们普遍认为重组的变化会影响清除转座元件（TEs）（普遍存在的自私遗传元件）的选择效率，从而导致在不同分类群中广泛观察到TE丰度与重组率之间的负相关。然而，越来越多的证据表明，TEs反而可能是这种关系的原因而非结果。为了验证这一预测，我们正式研究了多态性的、假定活跃的TEs对重组率的影响。我们开发并验证了一种方法，该方法使用PacBio长读长测序，在大量混合的重组个体中高效、准确且经济地识别交叉（COs）（一种关键的重组产物）。通过将这种方法应用于具有不同TE插入图谱的果蝇品系，我们发现多态性TEs，尤其是基于RNA的TEs和具有局部抑制标记富集的TEs，会减少COs的发生。这种效应导致有TEs和没有TEs的同源序列之间的CO频率不同，从而造成个体间CO图谱的差异。TEs对CO的抑制作用还得到了两种正交方法的进一步支持——分析重组自交系群体中COs相对于TE多态性的分布，以及将CO频率的标记辅助估计应用于有和没有转基因插入TEs的近交系。我们的研究揭示了不断变化的TE景观如何能够积极地改变重组，塑造物种内部和物种之间的基因组进化。
