Department of Plant and Microbial Biology, University of Minnesota, St. Paul, MN 55108;
Department of Biology, The Pennsylvania State University, University Park, PA 16802.
Proc Natl Acad Sci U S A. 2021 Aug 31;118(35). doi: 10.1073/pnas.2102914118.
Genomic structural variants (SVs) can play important roles in adaptation and speciation. Yet the overall fitness effects of SVs are poorly understood, partly because accurate population-level identification of SVs requires multiple high-quality genome assemblies. Here, we use 31 chromosome-scale, haplotype-resolved genome assemblies of an outcrossing, long-lived tree species that is the source of chocolate-to investigate the fitness consequences of SVs in natural populations. Among the 31 accessions, we find over 160,000 SVs, which together cover eight times more of the genome than single-nucleotide polymorphisms and short indels (125 versus 15 Mb). Our results indicate that a vast majority of these SVs are deleterious: they segregate at low frequencies and are depleted from functional regions of the genome. We show that SVs influence gene expression, which likely impairs gene function and contributes to the detrimental effects of SVs. We also provide empirical support for a theoretical prediction that SVs, particularly inversions, increase genetic load through the accumulation of deleterious nucleotide variants as a result of suppressed recombination. Despite the overall detrimental effects, we identify individual SVs bearing signatures of local adaptation, several of which are associated with genes differentially expressed between populations. Genes involved in pathogen resistance are strongly enriched among these candidates, highlighting the contribution of SVs to this important local adaptation trait. Beyond revealing empirical evidence for the evolutionary importance of SVs, these 31 de novo assemblies provide a valuable resource for genetic and breeding studies in .
基因组结构变异（SVs）在适应和物种形成中起着重要作用。然而，SVs 的整体适应度效应仍知之甚少，部分原因是准确识别 SVs 需要多个高质量的基因组组装。在这里，我们使用 31 个染色体规模的、单倍型解析的基因组组装，这些组装来自一种异交的、长寿的树种，是巧克力的来源，用于研究 SVs 在自然种群中的适应度后果。在这 31 个品系中，我们发现了超过 160000 个 SVs，它们共同覆盖了基因组的 8 倍以上，而单核苷酸多态性和短插入缺失（125 对 15 Mb）。我们的结果表明，这些 SVs 绝大多数是有害的：它们以低频率分离，并从基因组的功能区域中缺失。我们表明，SVs 影响基因表达，这可能损害基因功能，并导致 SVs 的有害影响。我们还为一个理论预测提供了经验支持，即 SVs，特别是倒位，通过抑制重组导致有害核苷酸变异的积累而增加遗传负荷。尽管总体上具有不利影响，但我们鉴定了具有局部适应特征的个体 SVs，其中几个与种群之间差异表达的基因有关。在这些候选基因中，参与病原体抗性的基因强烈富集，突出了 SVs 对这一重要的局部适应特征的贡献。除了揭示 SVs 在进化中的重要性的经验证据外，这 31 个从头组装还为 中的遗传和育种研究提供了宝贵的资源。
