To understand the effect of heat and drought on three major cereal crops, the physiological and biochemical (i.e., metabolic) factors affecting photosynthesis were examined in rice, wheat, and maize plants grown under long-term water deficit (WD), high temperature (HT) and the combination of both stresses (HT-WD). Diffusional limitations to photosynthesis prevailed under WD for the C3 species, rice and wheat. Conversely, biochemical limitations prevailed under WD for the C4 species, maize, under HT for all three species, and under HT-WD in rice and maize. These biochemical limitations to photosynthesis were associated with Rubisco activity that was highly impaired at HT and under HT-WD in the three species. Decreases in Rubisco activation were unrelated to the amount of Rubisco and Rubisco activase (Rca), but were probably caused by inhibition of Rca activity, as suggested by the mutual decrease and positive correlation between Rubisco activation state and the rate of electron transport. Decreased Rubisco activation at HT was associated with biochemical limitation of net CO2 assimilation rate (AN). Overall, the results highlight the importance of Rubisco as a target for improving the photosynthetic performance of these C3 (wheat and rice) and C4 (maize) cereal crops under increasingly variable and warmer climates.

Summary RuBisCO‐catalyzed CO2 fixation is the main source of organic carbon in the biosphere. This enzyme is present in all domains of life in different forms (III, II, and I) and its origin goes back to 3500 Mya, when the atmosphere was anoxygenic. However, the RuBisCO active site also catalyzes oxygenation of ribulose 1,5‐bisphosphate, therefore, the development of oxygenic photosynthesis and the subsequent oxygen‐rich atmosphere promoted the appearance of CO2 concentrating mechanisms (CCMs) and/or the evolution of a more CO2‐specific RuBisCO enzyme. The wide variability in RuBisCO kinetic traits of extant organisms reveals a history of adaptation to the prevailing CO2/O2 concentrations and the thermal environment throughout evolution. Notable differences in the kinetic parameters are found among the different forms of RuBisCO, but the differences are also associated with the presence and type of CCMs within each form, indicative of co‐evolution of RuBisCO and CCMs. Trade‐offs between RuBisCO kinetic traits vary among the RuBisCO forms and also among phylogenetic groups within the same form. These results suggest that different biochemical and structural constraints have operated on each type of RuBisCO during evolution, probably reflecting different environmental selective pressures. In a similar way, variations in carbon isotopic fractionation of the enzyme point to significant differences in its relationship to the CO2 specificity among different RuBisCO forms. A deeper knowledge of the natural variability of RuBisCO catalytic traits and the chemical mechanism of RuBisCO carboxylation and oxygenation reactions raises the possibility of finding unrevealed landscapes in RuBisCO evolution.

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The CO2-fixing enzyme Ribulose bisphosphate carboxylase-oxygenase (Rubisco) links the inorganic and organic phases of the global carbon cycle. In aquatic systems, the catalytic adaptation of algae Rubiscos has been more expansive and followed an evolutionary pathway that appears distinct to terrestrial plant Rubisco. Here, we extend this survey to differing seagrass species of the genus Posidonia to reveal how their disjunctive geographical distribution and diverged phylogeny, along with their CO2 concentrating mechanisms (CCMs) effectiveness, have impacted their Rubisco kinetic properties. The Rubisco from Posidonia species showed lower carboxylation efficiencies and lower sensitivity to O2 inhibition than those measured for terrestrial C3 and C4-plant Rubiscos. Compared to the Australian Posidonia species, Rubisco from the Mediterranean P. oceanica had 1.5-2–fold lower carboxylation and oxygenation efficiencies, coinciding with effective CCMs and five Rubisco large subunit (RbcL) amino acid substitutions. Among the Australian Posidonia species, CCM effectiveness was higher in P. sinuosa and lower in the deep-living P. angustifolia, likely related to the 20–35% lower Rubisco carboxylation efficiency in P. sinuosa and the 2–fold higher Rubisco content in P. angustifolia. Our results suggest that the catalytic evolution of Posidonia Rubisco has been impacted by the low CO2 availability and gas exchange properties of marine environments, but with contrasting Rubisco kinetics according to the time of diversification among the species. As a result, the relationships between maximum carboxylation rate and CO2- and O2-affinities of Posidonia Rubiscos follow an alternative path to that characteristic of terrestrial angiosperm Rubiscos.

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Summary Seaweeds have a wide ecophysiological and phylogenetic diversity with species expressing different Rubisco forms that frequently coexist with biophysical CO2 concentrating mechanisms (CCMs), an adaptation that overcomes the low CO2 availability and gas diffusion in seawater. Here, we assess the possible coevolution between the Rubisco catalysis and the type and effectiveness of CCMs present in six upper subtidal macroalgal species belonging to three phylogenetic groups of seaweeds. A wide diversity in the Rubisco kinetic traits was found across the analyzed species, although the specificity factor was the only parameter explained by the expressed Rubisco form. Differences in the catalytic trade‐offs were found between Rubisco forms, indicating that ID Rubiscos could be better adapted to the intracellular O2 : CO2 ratio found in marine organisms during steady‐state photosynthesis. The biophysical components of the CCMs also differed among macroalgal species, resulting in different effectiveness to concentrate CO2 around Rubisco active sites. Interestingly, an inverse relationship was found between the effectiveness of CCMs and the in vitro Rubisco carboxylation efficiency, which possibly led to a similar carboxylation potential across the analyzed macroalgal species. Our results demonstrate a coevolution between Rubisco kinetics and CCMs across phylogenetically distant marine macroalgal species sharing the same environment.

Background and Aims Carnivorous plants can enhance photosynthetic efficiency in response to prey nutrient uptake, but the underlying mechanisms of increased photosynthesis are largely unknown. Here we investigated photosynthesis in the pitcher plant Nepenthes × ventrata in response to different prey-derived and root mineral nutrition to reveal photosynthetic constrains. Methods Nutrient-stressed plants were irrigated with full inorganic solution or fed with four different insects: wasps, ants, beetles or flies. Full dissection of photosynthetic traits was achieved by means of gas exchange, chlorophyll fluorescence and immunodetection of photosynthesis-related proteins. Leaf biochemical and anatomical parameters together with mineral composition, nitrogen and carbon isotopic discrimination of leaves and insects were also analysed. Key Results Mesophyll diffusion was the major photosynthetic limitation for nutrient-stressed Nepenthes × ventrata, while biochemistry was the major photosynthetic limitation after nutrient application. The better nutrient status of insect-fed and root-fertilized treatments increased chlorophyll, pigment–protein complexes and Rubisco content. As a result, both photochemical and carboxylation potential were enhanced, increasing carbon assimilation. Different nutrient application affected growth, and root-fertilized treatment led to the investment of more biomass in leaves instead of pitchers. Conclusions The study resolved a 35-year-old hypothesis that carnivorous plants increase photosynthetic assimilation via the investment of prey-derived nitrogen in the photosynthetic apparatus. The equilibrium between biochemical and mesophyll limitations of photosynthesis is strongly affected by the nutrient treatment.