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Biased Gene Introgression and Adaptation in the Face of Chloroplast Capture in Aquilegia amurensis
Systematic Biology ( IF 6.1 ) Pub Date : 2024-07-13 , DOI: 10.1093/sysbio/syae039 Huaying Wang 1 , Wei Zhang 1, 2 , Yanan Yu 1 , Xiaoxue Fang 1 , Tengjiao Zhang 1 , Luyuan Xu 1 , Lei Gong 1 , Hongxing Xiao 1
Systematic Biology ( IF 6.1 ) Pub Date : 2024-07-13 , DOI: 10.1093/sysbio/syae039 Huaying Wang 1 , Wei Zhang 1, 2 , Yanan Yu 1 , Xiaoxue Fang 1 , Tengjiao Zhang 1 , Luyuan Xu 1 , Lei Gong 1 , Hongxing Xiao 1
Affiliation
—Chloroplast capture, a phenomenon that can occur through interspecific hybridization and introgression, is frequently invoked to explain cytonuclear discordance in plants. However, relatively few studies have documented the mechanisms of cytonuclear coevolution and its potential for driving species differentiation and possible functional differences in the context of chloroplast capture. To address this crucial question, we chose the Aquilegia genus, which is known for having minimal sterility among species, and inferred that A. amurensis captured the plastome of A. parviflora based on cytonuclear discordance and gene flow between the 2 species. We focused on the introgression region and its differentiation from corresponding regions in closely related species, especially its composition in a chloroplast capture scenario. We found that nuclear genes encoding cytonuclear enzyme complexes (CECs; i.e., organelle-targeted genes) of chloroplast donor species were selectively retained and displaced the original CEC genes in chloroplast-receiving species due to cytonuclear interactions during introgression. Notably, the intrinsic correlation of CEC introgression was a greater degree of evolutionary distance for these CECs between A. amurensis and A. parviflora. Terpene synthase activity genes (GO: 0010333) were overrepresented among the introgressed genes, and more than 30% of these genes were CEC genes. These findings support our observations that floral terpene release pattern is similar between A. amurensis and A. parviflora compared with A. japonica. Our study clarifies the mechanisms of cytonuclear coevolution, species differentiation, and functional differences in the context of chloroplast capture and highlights the potential role of chloroplast capture in adaptation.
中文翻译:
Aquilegia amurensis 叶绿体捕获的偏向基因渗入和适应
—叶绿体捕获是一种可以通过种间杂交和渗入发生的现象,经常被用来解释植物中的细胞核不一致。然而,相对较少的研究记录了细胞核协同进化的机制及其在叶绿体捕获背景下驱动物种分化和可能的功能差异的潜力。为了回答这个关键问题,我们选择了以物种间不育性最小而闻名的 Aquilegia 属,并根据细胞核不一致和两个物种之间的基因流动推断 A. amurensis 捕获了 A. parviflora 的质体组。我们专注于渗入区域及其与密切相关物种中相应区域的分化,尤其是它在叶绿体捕获情景中的组成。我们发现,由于渗入过程中的细胞核相互作用,编码叶绿体供体物种的细胞核酶复合物 (CEC;即细胞器靶向基因) 的核基因被选择性保留并取代了叶绿体受体物种中的原始 CEC 基因。值得注意的是,CEC 渗入的内在相关性是这些 CECs 在 A. amurensis 和 A. parviflora 之间的更大程度的进化距离。萜烯合酶活性基因 (GO: 0010333) 在渗入基因中代表性过高,其中超过 30% 的基因是 CEC 基因。这些发现支持我们的观察,即 A. amurensis 和 A. parviflora 与 A. japonica 之间的花萜烯释放模式相似。我们的研究阐明了叶绿体捕获背景下细胞核协同进化、物种分化和功能差异的机制,并强调了叶绿体捕获在适应中的潜在作用。
更新日期:2024-07-13
中文翻译:
Aquilegia amurensis 叶绿体捕获的偏向基因渗入和适应
—叶绿体捕获是一种可以通过种间杂交和渗入发生的现象,经常被用来解释植物中的细胞核不一致。然而,相对较少的研究记录了细胞核协同进化的机制及其在叶绿体捕获背景下驱动物种分化和可能的功能差异的潜力。为了回答这个关键问题,我们选择了以物种间不育性最小而闻名的 Aquilegia 属,并根据细胞核不一致和两个物种之间的基因流动推断 A. amurensis 捕获了 A. parviflora 的质体组。我们专注于渗入区域及其与密切相关物种中相应区域的分化,尤其是它在叶绿体捕获情景中的组成。我们发现,由于渗入过程中的细胞核相互作用,编码叶绿体供体物种的细胞核酶复合物 (CEC;即细胞器靶向基因) 的核基因被选择性保留并取代了叶绿体受体物种中的原始 CEC 基因。值得注意的是,CEC 渗入的内在相关性是这些 CECs 在 A. amurensis 和 A. parviflora 之间的更大程度的进化距离。萜烯合酶活性基因 (GO: 0010333) 在渗入基因中代表性过高,其中超过 30% 的基因是 CEC 基因。这些发现支持我们的观察,即 A. amurensis 和 A. parviflora 与 A. japonica 之间的花萜烯释放模式相似。我们的研究阐明了叶绿体捕获背景下细胞核协同进化、物种分化和功能差异的机制,并强调了叶绿体捕获在适应中的潜在作用。