Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms

Abstract

Nuclear and plastid (chloroplast) genomes experience different mutation rates, levels of selection, and transmission modes, yet key cellular functions depend on coordinated interactions between proteins encoded in both genomes. Functionally related proteins often show correlated changes in rates of sequence evolution across a phylogeny (evolutionary rate covariation or ERC), offering a means to detect previously unidentified suites of coevolving and cofunctional genes. We performed phylogenomic analyses across angiosperm diversity, scanning the nuclear genome for genes that exhibit ERC with plastid genes. As expected, the strongest hits are highly enriched for plastid-targeted proteins, providing evidence that cytonuclear interactions affect rates of molecular evolution at genome-wide scales. Many identified nuclear genes function in post-transcriptional regulation and the maintenance of protein homeostasis (proteostasis), including protein translation (in both the plastid and cytosol), import, quality control and turnover. We also identified nuclear genes that exhibit strong signatures of coevolution with the plastid genome but lack organellar-targeting annotations, making them candidates for having previously undescribed roles in plastids. In sum, our genome-wide analyses reveal that plastid- nuclear coevolution extends beyond the intimate molecular interactions within chloroplast enzyme complexes and may be driven by frequent rewiring of the machinery responsible for maintenance of plastid proteostasis in angiosperms.

Rapid sequence evolution is associated with genetic incompatibilities in the plastid Clp complex

“…Numerous studies have identified correlated rates of sequence evolution between genes in cytoplasmic and nuclear genomes and interpreted those as evidence of coevolution to maintain functional interactions (Osada and Akashi 2012;Pett and Lavrov 2015;Zhang, et al 2015;Adrion, et al 2016;Rockenbach, et al 2016;Zhang, et al 2016;Yan, et al 2019;Forsythe, et al 2021). Rarely, however, have such phylogenetic studies been coupled with functional tests for genetic incompatibilities.…”

“…In angiosperms with highly divergent copies of clpP1, there are also correlated increases in the rate of protein sequence evolution in nuclear-encoded Clp subunits Forsythe, et al 2021) and signatures of positive selection on these nuclear genes based on both population genetic and phylogenetic data (Rockenbach, et al 2016). The apparent action of positive selection on interacting proteins encoded in two different genomes is reminiscent of antagonistic molecular coevolution that can occur between hosts and pathogens (Hughes and Nei 1988;Aguileta, et al 2009).…”

Molecular evolution following allopolyploidization in Gossypium

“…The plastid genomes of B. oleracea and B. rapa have very few differences, and a recent analysis did not detect extensive incompatibilities with nuclear subgenomes . By contrast, elevated rates of protein-sequence evolution and ω values in organelle-interacting genes have been detected repeatedly in lineages with rapidly evolving cytoplasmic genomes (Osada and Akashi 2011;Barreto and Burton 2013b;Sloan et al 2014;Havird et al 2015;Rockenbach et al 2016;Weng et al 2016b;Havird et al 2017;Barreto et al 2018;Yan et al 2019;Forsythe et al 2020). Therefore, genome-wide analyses of evolutionary rates appear to be sensitive enough to detect cytonuclear incompatibilities when their effects are strong.…”