Temperature response of Rubisco kinetics in Arabidopsis thaliana: thermal breakpoints and implications for reaction mechanisms

Abstract

Optimization of Rubisco kinetics could improve photosynthetic efficiency, ultimatly 2 1 resulting in increased crop yield. However, imprecise knowledge of the reaction mechanism and 2 2 the individual rate constants limit our ability to optimize the enzyme. Membrane inlet mass Rubisco temperature response and relavance of individual rate constants of the reaction 3 3 mechanisms to potential breakpoints.

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO2 concentrating mechanisms

“…This reaction step is hypothesized to impart selectivity to RuBisCO, based on the degree to which the active site in enzyme‐bound enediol captures the bent CO 2 molecule rather than the linear O 2 (Tcherkez et al , ). This reaction step is inferred to feature a kinetic activation energy barrier to a transition state (Boyd et al , ), which represents the major step in isotopic fractionation by RuBisCO. Carboxylation transition states, which are more specific and similar to the product, correspond to shorter O 2 C–C‐2 bond lengths.…”

“…Few studies of RuBisCO temperature sensitivity report data on K o , and the available data (only for spermatophytes) show contradictory results, with K o showing no thermal sensitivity, while increasing or even decreasing with temperature in other cases (Badger and Collatz, ; Jordan and Ogren, ; Boyd et al , , ). This lack of consistent trend might be related to the difficulty of directly measuring this parameter, because K o is usually calculated indirectly from the inhibition of the carboxylase activity at different O 2 concentrations, and this approach might lead to less reliable data.…”

“…Additionally, the existence of thermal breakpoints in the temperature response of RuBisCO kinetic traits has been proposed on the basis of a biphasic Arrhenius temperature response mainly in k cat c (Sage, ; Kubien et al , ; Perdomo et al , ; Sharwood et al , ), but also in K cat o , K c and/or S c/o (Badger and Collatz, ; Boyd et al , ) of plant RuBisCOs, leading to E a values that differ between temperature ranges. Different explanations for these thermal breakpoints have been proposed, such as changes in the rate‐limiting step of the reaction mechanism caused by changes in enzyme conformation (Badger and Collatz, ), deactivation of RuBisCO at low temperatures (Sage, ; Kubien et al , ), or differences in the thermal responses of the elementary rate constants proposed by Farquhar () that describe the reaction mechanism of RuBisCO (Boyd et al , ). It is unknown if these thermal breakpoints are universal to all RuBisCOs, as most of the data of thermal dependence of RuBisCO kinetic traits to date was obtained in studies where only three or four temperatures were analyzed (Haslam et al , ; Galmés et al , ; Hermida‐Carrera et al , ; Orr et al , ).…”

“…More notably, a positive relationship between DH a for S c/o and DH a for k cat c indicated that the widely assumed trade-offs between these RuBisCO catalytic traits at 25°C (Figure 3c) vary with temperature, and that contrasting relationships within spermatophytes are in principle possible. Few studies of RuBisCO temperature sensitivity report data on K o , and the available data (only for spermatophytes) show contradictory results, with K o showing no thermal sensitivity, while increasing or even decreasing with temperature in other cases (Badger and Collatz, 1977;Jordan and Ogren, 1984;Boyd et al, 2015Boyd et al, , 2019. This lack of consistent trend might be related to the difficulty of directly measuring this parameter, because K o is usually calculated indirectly from the inhibition of the carboxylase activity at different O 2 concentrations, and this approach might lead to less reliable data.…”

Revisiting tradeoffs in Rubisco kinetic parameters

“…Data was filtered as described in SI. k cat,O is usually not measured directly, 29 but is rather inferred as k cat,O = (k cat,C /K C ) / (S C/O /K O ). We assumed that experimental error is normally distributed and used 10 4 -fold bootstrapping to estimate 199 k cat,O values and 95% confidence intervals thereof.…”