Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends

Abstract

The present study characterizes the kinetic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) from 28 terrestrial plant species, representing different phylogenetic lineages, environmental adaptations and photosynthetic mechanisms. Our findings confirm that past atmospheric CO(2)/O(2) ratio changes and present environmental pressures have influenced Rubisco kinetics. One evolutionary adaptation to a decreasing atmospheric CO(2)/O(2) ratio has been an increase in the affinity of Rubisco for CO(2) (Kc falling), and a consequent decrease in the velocity of carboxylation (kcat (c)), which in turn has been ameliorated by an increase in the proportion of leaf protein accounted by Rubisco. The trade-off between K(c) and k(cat)(c) was not universal among the species studied and deviations from this relationship occur in extant forms of Rubisco. In species adapted to particular environments, including carnivorous plants, crassulacean acid metabolism species and C(3) plants from aquatic and arid habitats, Rubisco has evolved towards increased efficiency, as demonstrated by a higher k(cat)(c)/K(c) ratio. This variability in kinetics was related to the amino acid sequence of the Rubisco large subunit. Phylogenetic analysis identified 13 residues under positive selection during evolution towards specific Rubisco kinetic parameters. This crucial information provides candidate amino acid replacements, which could be implemented to optimize crop photosynthesis under a range of environmental conditions.

Surveying Rubisco diversity and temperature response to improve crop photosynthetic efficiency

“…C 3 plants surveyed ranged in S C/O from 111 to 91. Catalytic values generally agreed with previously reported ranges (Ishikawa et al, 2011;Galmés et al, 2014b;Occhialini et al, 2016).…”

“…This provides important new insights on the response of Rubisco catalysis to temperature and its consistency across diverse species, while further highlighting the diversity of catalysis. It is important to note that a number of plant groups such as trees and basal angiosperms remain either underrepresented in biochemical data sets or have only just begun to be surveyed (Galmés et al, 2014b) and provide potential areas where additional valuable information can be gleamed from characterization. Data are also lacking for crop species, with few represented in the literature and often with incomplete characterization.…”

“…The software MODELTEST 3.7 (Posada and Crandall, 1998;Posada and Buckley, 2004) was used to check for the best model before running the phylogenetic analyses using maximum-likelihood inference conducted with RAxML version 7.2.6 (Stamatakis, 2006). Rubisco amino acid residues under positive selection associated with particular kinetic traits were identified using codon-based substitution models in comparative analysis of protein-coding DNA sequences within the phylogenetic framework using branch-site tests of positive selection along prespecified foreground branches in the PAML v.4.7 package (Yang, 2007) as described (Kapralov et al, , 2012Galmés et al, 2014b). Branches leading to species with high or low K c air , k cat c , K o , k cat o , and S C/O at 25°C were marked as foreground branches.…”

“…Previous characterization of Rubisco from a limited number of species has not only demonstrated significant differences in the underlying catalytic parameters, but also suggests that further undiscovered diversity exists in nature and that the properties of some of these enzymes could be beneficial if present in crop plants (Carmo-Silva et al, 2015). Recent studies clearly illustrate the variation possible among even closely related species (Galmés et al, 2005(Galmés et al, , 2014b(Galmés et al, , 2014cKubien et al, 2008;Andralojc et al, 2014;Prins et al, 2016).…”

Rubisco Catalytic Properties and Temperature Response in Crops

“…These data revealed the existence of significant variability in the main Rubisco kinetic parameters both among C 3 species (Yeoh et al, 1980(Yeoh et al, , 1981Bird et al, 1982;Jordan and Ogren, 1983;Parry et al, 1987;Castrillo, 1995;Delgado et al, 1995;Kent and Tomany, 1995;Balaguer et al, 1996;Bota et al, 2002;Galmés et al, 2005Galmés et al, , 2014aGalmés et al, , 2014cGhannoum et al, 2005;Ishikawa et al, 2009) and between C 3 and C 4 species (Kane et al, 1994;Sage, 2002;Kubien et al, 2008;Perdomo et al, 2015b). The existence of Rubiscos with different catalytic traits implies that the success, in terms of photosynthetic improvement, of Rubisco engineering approaches in crops will depend on the specific performance of the native enzyme from each crop species.…”