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Bouvier, J. W.

Publications and source records attributed to Bouvier, J. W..

3 recordsLinked to original sources

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

Rubisco is the primary entry point for carbon into the biosphere. It has been widely proposed that rubisco is highly constrained by catalytic trade-offs due to correlations between the enzymes kinetic traits across species. In previous work, we have shown that these correlations, and thus the strength of catalytic trade-offs, have been over-estimated due to the presence of phylogenetic signal in the kinetic trait data (Bouvier et al., 2021). We demonstrated that only canonical trade-offs between the Michaelis constant for CO2 and carboxylase turnover, and between the Michaelis constants for CO2 and O2 were robust to phylogenetic effects. We further demonstrated that phylogenetic constraints have limited rubisco adaptation to a greater extent than the combined action of catalytic trade-offs. Recently, however, our claims have been contested by Tcherkez and Farquhar (2021), who have argued that the phylogenetic signal we detect in rubisco kinetic traits is an artefact of species sampling, the use of rbcL-based trees for phylogenetic inference, laboratory-to-laboratory variability in kinetic measurements, and homoplasy of the C4 trait. In the present article, we respond to these criticisms on a point-by-point basis and conclusively show that all are either incorrect or invalid. As such, we stand by our original conclusions. Specifically, the magnitude of rubisco catalytic trade-offs have been overestimated in previous analyses due to phylogenetic biases, and rubisco kinetic evolution has in fact been more limited by phylogenetic constraint.

evolutionary biology↗

Brassicaceae display diverse photorespiratory carbon recapturing mechanisms

Carbon concentrating mechanisms enhance the carboxylase efficiency of the central photosynthetic enzyme rubisco by providing supra-atmospheric concentrations of CO2 in its surrounding. In the C4 photosynthesis pathway, this is achieved by combinatory changes to leaf biochemistry and anatomy. Carbon concentration by the photorespiratory glycine shuttle requires fewer and less complex modifications. It could represent an early step during evolution from C3 to C4 photosynthesis and an inspiration for engineering approaches. Plants displaying CO2 compensation points between 10 to 40 ppm are therefore often termed C3-C4 intermediates. In the present study, we perform a physiological, biochemical and anatomical survey of a large number of Brassicaceae species to better understand the C3-C4 intermediate phenotype. Our phylogenetic analysis suggested that C3-C4 metabolism evolved up to five times independently in the Brassicaceae. The efficiency of the pathways showed considerable variation between the species but also within species. Centripetal accumulation of organelles in the bundle sheath was consistently observed in all C3-C4 classified accessions indicating a crucial role of anatomical features for CO2 concentrating pathways. Leaf metabolite patterns were strongly influenced by the individual plant accessions, but accumulation of photorespiratory shuttle metabolites glycine and serine was generally observed. Analysis of PEPC activities suggests that C4-like shuttles have not evolve in the investigated Brassicaceae. HighlightOur physiological, biochemical and anatomical survey of Brassicaceae revels multiple evolution of C3-C4 intermediacy connected to variation in photorespiratory carbon recapturing efficiency and a distinct C3-C4 bundle sheath anatomy.

plant biology↗

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

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 analysed. 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 (most likely caused by a slow rate of molecular evolution) 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 such trade-offs.

plant biology↗