Razifard Hamid, Visa Sofia, Menda Naama, Mueller Lukas, Tieman Denise, van der Knaap Esther, Caicedo Ana L
Institute for Applied Life Sciences, University of Massachusetts Amherst, Amherst, Massachusetts, USA.
Department of Mathematics and Computer Science, College of Wooster, Wooster, Ohio, USA.
Mol Ecol. 2025 Jul 15:e70024. doi: 10.1111/mec.70024.
Understanding the impact of domestication on deleterious mutations has fascinated evolutionary biologists and breeders alike. A 'cost of domestication' has been reported for some organisms through accumulation of gene disruptions or radical amino acid changes. However, recent evidence paints a more complex picture of this phenomenon in different domesticated species. In this study, we used genomic sequences of 253 tomato accessions to investigate the evolution of deleterious mutations and genomic structural variants (SVs) through tomato domestication history. We apply phylogeny-based methods to identify deleterious mutations in the domesticated tomato as well as its semi-wild and wild relatives. Our results implicate a downward trend throughout domestication in the number of genetic variants, regardless of their functional impact. This suggests that demographic factors have reduced overall genetic diversity, leading to lower deleterious load and SVs as well as loss of some beneficial alleles during tomato domestication. However, we detected an increase in proportions of nonsynonymous and deleterious alleles (relative to synonymous and neutral nonsynonymous alleles, respectively) during the initial stage of tomato domestication in Ecuador. Additionally, deleterious alleles in the commonly cultivated tomato seem to be more frequent than expected under a neutral hypothesis of molecular evolution. Our analyses also revealed frequent deleterious alleles in several well-studied tomato genes, probably involved in response to biotic and abiotic stress as well as fruit development and flavour regulation. To provide a practical guide for breeding experiments, we created TomDel, a public searchable database of 21,162 potentially deleterious alleles identified in this study (hosted on the Solanaceae Genomic Network; https://solgenomics.net/).
了解驯化对有害突变的影响一直吸引着进化生物学家和育种者。对于一些生物，已经报道了通过基因破坏的积累或氨基酸的剧烈变化而产生的“驯化成本”。然而，最近的证据表明，在不同的驯化物种中，这一现象呈现出更为复杂的情况。在本研究中，我们使用了253份番茄种质的基因组序列，以研究有害突变和基因组结构变异（SVs）在番茄驯化历史中的演变。我们应用基于系统发育的方法来识别驯化番茄及其半野生和野生近缘种中的有害突变。我们的结果表明，在整个驯化过程中，无论遗传变异的功能影响如何，其数量都呈下降趋势。这表明人口统计学因素降低了总体遗传多样性，导致番茄驯化过程中有害负荷和SVs降低，以及一些有益等位基因的丢失。然而，我们在厄瓜多尔番茄驯化的初始阶段检测到非同义等位基因和有害等位基因的比例增加（分别相对于同义等位基因和中性非同义等位基因）。此外，在分子进化的中性假设下，常见栽培番茄中的有害等位基因似乎比预期的更为频繁。我们的分析还揭示了几个经过充分研究的番茄基因中频繁出现的有害等位基因，这些基因可能参与了对生物和非生物胁迫的响应以及果实发育和风味调控。为了为育种实验提供实用指南，我们创建了TomDel，这是一个可公开搜索的数据库，包含了本研究中鉴定出的21162个潜在有害等位基因（托管在茄科基因组网络上；https://solgenomics.net/）。
