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

Chloroplast capture, 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 Aquilegia genus, which is known for having minimal sterility
among the species, and we inferred that A. amurensis captured the plastome
of A. parviflora 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 A. amurensis
and A. parviflora. Introgression from A. parviflora promotes the
differentiation of A. amurensis and A. japonica. 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 A. amurensis had
similar release patterns for terpenes in flowers of A. parviflora when
compared with A. japonica. 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.