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Slow molecular evolution of rubisco limits adaptive improvement of CO2 assimilation

View ORCID ProfileJacques W. Bouvier, View ORCID ProfileDavid M. Emms, View ORCID ProfileSteven Kelly
doi: https://doi.org/10.1101/2022.07.06.498985
Jacques W. Bouvier
1Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, United Kingdom
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David M. Emms
1Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, United Kingdom
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Steven Kelly
1Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, United Kingdom
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  • For correspondence: steven.kelly@plants.ox.ac.uk
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Abstract

Rubisco assimilates CO2 to form the sugars that fuel life on Earth. Although rubisco is the source of most carbon in the biosphere, it is a surprisingly inefficient catalyst with a modest carboxylase turnover rate and a competing oxygenase activity which results in the loss of fixed CO2. These apparent shortcomings of rubisco present a puzzling evolutionary paradox: why does the enzyme appear well suited to the high CO2 low O2 conditions of its origin, rather than the low CO2 high O2 conditions of the present day? To help answer this question, we perform a phylogenetically resolved analysis of the molecular and kinetic evolution of Form I rubisco. We discover that rubisco is among the slowest evolving genes on Earth. Specifically, we find that the rubisco catalytic large subunit evolves substantially slower than its cognate small subunit, and is slower than >98% of all other genes and enzymes across the tree of life. Next, through simultaneous analysis of rubisco molecular and kinetic evolution in C3 angiosperms, we demonstrate that despite its slow molecular evolution, rubisco kinetics have evolved, and are continuing to evolve, to improve CO2/O2 specificity, carboxylase turnover and overall carboxylation efficiency. Thus, slow molecular evolution has severely limited rubisco kinetic optimisation, resulting in the present enzyme that is poorly adapted for current conditions.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted July 06, 2022.
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Slow molecular evolution of rubisco limits adaptive improvement of CO2 assimilation
Jacques W. Bouvier, David M. Emms, Steven Kelly
bioRxiv 2022.07.06.498985; doi: https://doi.org/10.1101/2022.07.06.498985
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Slow molecular evolution of rubisco limits adaptive improvement of CO2 assimilation
Jacques W. Bouvier, David M. Emms, Steven Kelly
bioRxiv 2022.07.06.498985; doi: https://doi.org/10.1101/2022.07.06.498985

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