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Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

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Bouvier, Jacques W, Emms, David M, Rhodes, Timothy, Bolton, Jai S, Brasnett, Amelia, Eddershaw, Alice, Nielsen, Jochem R, Unitt, Anastasia +2 more·2021·Molecular Biology and Evolution
DOI 10.1093/molbev/msab079PMC PMC8233502

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Abstract

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.

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  • The problem of species not being independent can be exacerbated by additional levels of non-independence, including genes within genomes and genomes of the same or closely related species.

    “In genomic datasets, data points can correspond to genomes or even individual genes, meaning the problem of species not being independent can be exacerbated by additional levels of non-independence, including genes within genomes, such as those carried on the same replicon, and genomes of the same or closely related species16,19,21–26.”

    From A phylogenetic approach to comparative genomics (2025) · cites this paper as [26]

    The Introduction explains that Rubisco measurements from closely related species are non-independent because of shared ancestry. The paper does not address the claimed additional levels of non-independence among genes within a genome or among multiple genomes of the same species; the Materials and Methods discuss species-level phylogenetic correction instead. Page numbers were not available in our copy. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • The problem of non-independence can be exacerbated when examining genomes or genes.

    “This problem of non-independence can be exacerbated when examining genomes or genes.”

    From A phylogenetic approach to comparative genomics (2025) · cites this paper as [26]

    The Introduction explains that rubisco genes share ancestry, making measurements from closely related species non-independent. The Results confirm this for carboxylase-related kinetic traits in angiosperms, but the paper does not establish that non-independence is generally exacerbated when examining genomes or genes. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

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Authors
Bouvier, J. W., Emms, D. M., Rhodes, T., Bolton, J. S., Brasnett, A., Eddershaw, A., Nielsen, J. R., Unitt, A., Whitney, S. M., & Kelly, S.
Affiliations
  • University of Oxford (GB)
  • Australian National University (AU)
Corresponding author
Kelly, Steven
ORCID
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Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2021-03-19
Volume
38
Issue
7
Pages
2880-2896
ISSN
  • 0737-4038 (ISSN-L)
  • 1537-1719
DOI
10.1093/molbev/msab079
PMC
PMC8233502
OpenAlex
W3137932374
Cited by
65
References
1
Citations by year
2026: 13 · 2025: 6 · 2024: 12 · 2023: 14 · 2022: 14 · 2021: 5 · 2020: 1
FWCI
3.53
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Biology and Evolution (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ANU Open Research (Australian National University) (submittedVersion, cc-by)
  • Oxford University Research Archive (ORA) (University of Oxford) (submittedVersion, cc-by)
Funders
  • Royal Society and the European Union’s Horizon 2020 research and innovation program (637765)
  • Biotechnology and Biological Sciences Research Council (BB/M011224/1, BB/P003117/1)
  • Australian Government through the Australian Research Council Centre of Excellence for Translational Photosynthesis (CE140100015)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Physical Sciences › Environmental Science › Global and Planetary Change › Plant Water Relations and Carbon Dynamics
Keywords
Rubisco, phylogenetic constraints, enzyme kinetics, C4 photosynthesis, phylogenetic signal, evolution of photosynthesis, Rubisco activase
MeSH terms
Adaptation, Biological, Kinetics, Photosynthesis, Phylogeny, Ribulose-Bisphosphate Carboxylase, Triticum, Evolution, Molecular

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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