Biased gene introgression and adaptation in face of chloroplast capture in Aquilegia

<p><span>Chloroplast capture</span><span>, a phenomenon that can occur through interspecific hybridization and introgression, has been frequently suggested as an explanation for cytonuclear discordance in plants. In theory, the captured donor chloroplasts may not cooperate with the recipient nuclear genome, especially chloroplast-targeted nuclear genes. However, relatively few studies have documented the mechanisms of cytonuclear coevolution and its potential species differentiation and possible functional differences in the face of chloroplast capture. To explore this crucial question, we chose the <em>Aquilegia</em> genus, which is known for having minimal sterility among the species, and we inferred that <em>A</em>. <em>amurensis</em> captured the plastome of <em>A</em>. <em>parviflora</em> based on cytonuclear discordance and gene flow between these two species. We focused on the introgression region and its differentiation with closely related species, especially its composition in a chloroplast capture scenario. We found that nuclear genes encoding cytonuclear enzyme complexes or organelle localized (CECs) were significantly enriched in the introgression regions, indicating that the CEC genes of chloroplast donor species were selectively retained and displaced the original CEC genes in chloroplast receptor species due to cytonuclear interactions during introgression. Notably, the intrinsic factor of cytonuclear compatibility may have a higher degree of evolutionary distance for the introgressed CEC genes between <em>A</em>. <em>amurensis</em> and <em>A</em>. <em>parviflora</em>. Introgression from <em>A</em>. <em>parviflora</em> promotes the differentiation of <em>A</em>. <em>amurensis</em> and <em>A</em>. <em>japonica</em>. Furthermore, we found that one of the overrepresented gene ontology terms in these introgressed genes was terpene synthase activity (GO: 0010333) in which more than one-third of the genes were CEC genes, showing that <em>A</em>. <em>amurensis</em> had similar release patterns for terpenes in flowers of <em>A</em>. <em>parviflora</em> when compared with <em>A</em>. <em>japonica</em>.</span> <span>Altogether, this study helps to clarify the mechanisms of cytonuclear coevolution, species differentiation and functional differences in face of chloroplast capture and highlights a critical role of chloroplast capture in adaptation.</span></p>