Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off

Journal article

Rubisco assimilates CO₂ to form the sugars that fuel life on earth. Correlations between rubisco kinetic traits across species have led to the proposition that rubisco adaptation is highly constrained by catalytic trade-offs. However, these analyses did not consider the phylogenetic context of the enzymes that were analyzed. Thus, it is possible that the correlations observed were an artefact of the presence of phylogenetic signal in rubisco kinetics and the phylogenetic relationship between the species that were sampled. Here, we conducted a phylogenetically resolved analysis of rubisco kinetics and show that there is a significant phylogenetic signal in rubisco kinetic traits. We re-evaluated the extent of catalytic trade-offs accounting for this phylogenetic signal and found that all were attenuated. Following phylogenetic correction, the largest catalytic trade-offs were observed between the Michaelis constant for CO₂ and carboxylase turnover (∼21–37%), and between the Michaelis constants for CO₂ and O₂ (∼9–19%), respectively. All other catalytic trade-offs were substantially attenuated such that they were marginal (<9%) or non-significant. This phylogenetically resolved analysis of rubisco kinetic evolution also identified kinetic changes that occur concomitant with the evolution of C₄ photosynthesis. Finally, we show that phylogenetic constraints have played a larger role than catalytic trade-offs in limiting the evolution of rubisco kinetics. Thus, although there is strong evidence for some catalytic trade-offs, rubisco adaptation has been more limited by phylogenetic constraint than by the combined action of all catalytic trade-offs.

Authors: Bouvier, JW; Emms, DM; Rhodes, T; Bolton, JS; Brasnett, A

• Publication status: Published
• Peer review status: Peer reviewed
• Publisher: Oxford University Press
• Journal: Molecular Biology and Evolution
• Volume: 38
• Issue: 7
• Pages: 2880–2896
• Publication date: 2021-03-19
• Acceptance date: 2021-03-11
• DOI: 10.1093/molbev/msab079
• EISSN: 1537-1719
• ISSN: 0737-4038
• Language: English
• Keywords: phylogenetic constraint; catalytic constraint; evolution; rubisco; C4 photosynthesis