Plastid-nuclear coevolution of ribosomal protein genes in papilionoid legumes.

Abstract

In plants, cellular function is orchestrated by three distinct genomes located within the nucleus, mitochondrion, and plastid. These genomes are interdependent, requiring tightly coordinated maintenance and expression. Plastids host several multisubunit protein complexes encoded by both the plastid and nuclear genomes. To investigate plastid-nuclear coevolution, this study focused on plastid ribosomal protein genes that are encoded by both plastid and nuclear genomes from 50 taxa across 15 of the 22 early branching major clades of the legume subfamily Papilionoideae. Comparative analysis of substitution rates was conducted across five gene sets: nuclear-encoded plastid-targeted ribosomal protein genes (NuCpRP), nuclear-encoded cytosol-targeted ribosomal genes (NuCyRP), other nuclear-encoded plastid-targeted genes that are not involved in ribosomes (NuCpOT), plastid-encoded ribosomal protein genes (CpRP) and plastid-encoded photosynthesis genes (CpPS).¹ Elevated nonsynonymous substitution rates (d_N) and ratios of nonsynonymous to synonymous substitution rates (d_N/d_S; ω) were observed in both CpRP and NuCpRP compared to the other gene sets. Significant differences in d_N for CpRP and NuCpRP were found between the papilionoid 50-kb inversion clade and other legumes. Using coevolution statistics and evolutionary rate covariation, strong signals of cytonuclear coevolution were identified, where nonsynonymous substitutions in CpRP and NuCpRP genes co-occur along the same branches of the Papilionoideae phylogeny. Increased ω in a few CpRP genes was due to intensified positive selection whereas most of the CpRP and NuCpRP increased ω was caused by relaxed purifying selection. This pattern not only underscores the role of cytonuclear incompatibility in driving speciation but also highlights its constraints on the genetic enhancement of papilionoid crop species.