The evolutionary constraints on angiosperm chloroplast adaptation

Abstract

The chloroplast (plastid) arose via the endosymbiosis of a photosynthetic cyanobacterium by a non-photosynthetic eukaryotic cell approximately 1.5 billion years ago. Although the plastid underwent rapid evolution by genome reduction, its genome organisation is highly conserved and the rate of molecular evolution of its genes is low. Here, we investigate the factors that have constrained the rate of molecular evolution of protein coding genes in the plastid genome. Through phylogenomic analysis of 773 angiosperm plastid genomes we show that there is substantial variation in the rate of molecular evolution between genes. We demonstrate that the distance of a plastid gene from the origin of replication influences the rate at which it has evolved, consistent with time and distance-dependent nucleotide mutation gradients. We further show that the amino acid composition of a gene product constraints its substitution tolerance, limiting its mutation landscape and its corresponding rate of molecular evolution. Finally, we demonstrate that the mRNA abundance of a gene is a critical factor in determining its rate of molecular evolution, suggesting the presence of transcription mediated DNA repair in the plastid. Collectively, we show that the location, composition, and expression of a gene account for ~50% of the variation in its rate of molecular evolution. Thus, these three factors are a major limitation on the capacity for adaptive evolution of plastid genes, and ultimately constrain the evolvability of the chloroplast.

Response to Tcherkez and Farquhar: Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off

“…In summary, therefore, although rubisco catalytic trade-offs exist as determined by chemistry, these represent a less serious constraint on rubisco kinetic adaptation compared to previous assumptions. Instead, phylogenetic constraints, likely caused by slow molecular evolution in rubisco (Bouvier et al, 2022) and more general constraints on the molecular evolution of chloroplast encoded genes (Robbins and Kelly, 2022), have presented a more significant barrier to improved rubisco catalytic efficiency.…”

“…Thus, rubisco evolution is only weakly constrained by catalytic trade-offs and is instead more limited by phylogenetic constraint. We propose that this phylogenetic constraint arises from a combination of a high degree of purifying selection (Robbins and Kelly, 2022), the requirement for high levels of transcript and protein abundance (Kelly, 2018; Robbins and Kelly, 2022; Seward and Kelly, 2018), the requirement for maintaining complementarity to a wide array of molecular chaperones which assist in protein folding and assembly (e.g., Raf1, Raf2, RbcX, BSD2, Cpn60/Cpn20) and metabolic regulation (e.g., rubisco activase) (Aigner et al, 2017; Carmo-Silva et al, 2015), and finally, the need to preserve overall protein stability within the molecular activity-stability trade-offs (Cummins et al, 2018; Duraõ et al, 2015; Studer et al, 2014). These factors combined contribute to the exceedingly slow rate of molecular evolution in rbcL (Bouvier et al, 2022) which presents a major barrier on rubisco optimisation.…”

Rubisco is evolving for improved catalytic efficiency and CO2assimilation in plants

“…Although dissecting the factors which constrain the rate of rbcL evolution is beyond the scope of the current study, the slow pace of rbcL molecular evolution is most likely a consequence of several synergistic factors 90 including constraints imposed by expression [91][92][93][94][95] , selection to preserve protein function [96][97][98][99][100] , and the requirements for protein-protein interactions in vivo [101][102][103][104] . These factors would be particularly pertinent for rubisco given that it is the most abundant protein in organisms in which it is found 68,70 , it is subject to catalytic trade-offs 21,22,80,81 and molecular activity-stability trade-offs [105][106][107][108] , and given that it relies on multiple interacting partners and chaperones for folding, assembly and metabolic regulation 68,109 .…”

Widespread adaptive evolution in the photosystems of angiosperms provides new insight into the evolution of photosystem II repair

“…The plastid genome dataset and phylogenetic tree used in this study was the same as in (Robbins and Kelly 2023). In brief, the full set of sequenced plastid genomes was downloaded from the National Center of Biotechnology and Information (NCBI) in July 2021.…”

“…As the cyanobacterium evolved into the semi-autonomous organelle known as the plastid, its genome underwent a substantial reduction, such that it now harbours <5% of the genes found in its cyanobacterial ancestor (Blanchard and Schmidt 1995; Martin, et al 2002; Kelly 2021). Despite this large reduction, the gene content and organisation has been highly conserved across the angiosperm lineage (Palmer and Thompson 1982; Jansen, et al 2007; Zhu, et al 2016; Robbins and Kelly 2023). Among the ∼80 protein-coding genes that have remained in the plastid genome many encode core photosystem reaction centre proteins.…”