Rubisco Evolution in C4 Eudicots: An Analysis of Amaranthaceae Sensu Lato

Background: Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) catalyses the key reaction in the photosynthetic assimilation of CO2. In C-4 plants CO2 is supplied to Rubisco by an auxiliary CO2-concentrating pathway that helps to maximize the carboxylase activity of the enzyme while suppressing its oxygenase activity. As a consequence, C-4 Rubisco exhibits a higher maximum velocity but lower substrate specificity compared with the C-3 enzyme. Specific amino-acids in Rubisco are associated with C-4 photosynthesis in monocots, but it is not known whether selection has acted on Rubisco in a similar way in eudicots. Methodology/Principal Findings: We investigated Rubisco evolution in Amaranthaceae sensu lato (including Chenopodiaceae), the third-largest family of C-4 plants, using phylogeny-based maximum likelihood and Bayesian methods to detect Darwinian selection on the chloroplast rbcL gene in a sample of 179 species. Two Rubisco residues, 281 and 309, were found to be under positive selection in C-4 Amaranthaceae with multiple parallel replacements of alanine by serine at position 281 and methionine by isoleucine at position 309. Remarkably, both amino-acids have been detected in other C-4 plant groups, such as C-4 monocots, illustrating a striking parallelism in molecular evolution. Conclusions/Significance: Our findings illustrate how simple genetic changes can contribute to the evolution of photosynthesis and strengthen the hypothesis that parallel amino-acid replacements are associated with adaptive changes in Rubisco. Citation: Kapralov MV, Smith JAC, Filatov DA (2012) Rubisco Evolution in C-4 Eudicots: An Analysis of Amaranthaceae Sensu Lato. PLoS ONE 7(12): e52974. doi:10.1371/journal.pone.0052974