The evolution of the angiosperm plastid genome

Thesis

Plastids originated from the endosymbiosis of a cyanobacterium by a eukaryotic cell approximately 1.5 billion years ago. Since then, their genome has undergone substantial reduction, with present day plastids retaining less than 5% of genes found in their cyanobacterial ancestor. Many of these remaining genes are essential for photosynthesis, including components of the photosystems, NAD(P)H dehydrogenase-like complex, cytochrome b6f complex and rubisco. While previous comparative analyses have shown that the plastid genome has evolved exceptionally slowly, it is unknown why this slow evolution occurs and whether adaptation has occurred given this constraint. This thesis seeks to address both of these questions through an investigation of the constraints on plastid gene evolution and a search for hallmarks of adaptive evolution that may have been previously overlooked. I reveal that there is significant variation in the rate of molecular evolution between the plastid-encoded genes, with those involved in energy production evolving notably slower than those involved in information processing (i.e., transcription and translation). Additionally, I discover that three key factors – gene position, level of gene expression and the encoded protein’s composition – collectively account for >50% of the variation in the rate of sequence evolution. Thus, contrary to expectations, factors unrelated to the molecular function of a gene are the major determinants its evolvability. A novel computational approach, herein named RECUR, was subsequently developed to identify hallmarks of adaptive evolution in the plastid genome. In combination with conventional methods for detecting selection, I identified evidence of adaptive evolution at 7% of the residues in genes encoding components of the photosystems. Through the use of various in silico approaches, I predicted the impact of these evolutionary changes on the photosystems and revealed that evolution has repeatedly influenced the interaction between photosystem II and its D1 subunit, potentially reducing the energetic barrier for D1 turnover and enhancing photosystem II repair. In conclusion, this thesis has leveraged millions of years of natural selection experiments to identify plausible engineering targets for enhancing photosynthesis. Moreover, the development of RECUR enables the broader scientific community to explore recurrent evolution, facilitating new discoveries and aiding evolutionary guided protein engineering.

Authors: Robbins, E

• DOI: 10.5287/ora-yrw8yqxna
• Type of award: DPhil
• Level of award: Doctoral
• Awarding institution: University of Oxford
• Language: English
• Keywords: photosystems; chloroplast; adaptive evolution; plastid genome
• Subjects: Bioinformatics; Molecular evolution; Adaptive radiation (Evolution); Biology; Plant diversity