Rubisco evolution in C₄ eudicots: an analysis of Amaranthaceae sensu lato

• Published in: PloS one 2012-12, Vol.7 (12), p.e52974-e52974
• Main Authors: Kapralov, Maxim V, Smith, J Andrew C, Filatov, Dmitry A
• Format: Article
• Language: English
• Subjects: Acids; Adaptation; Alanine; Amaranthaceae; Amaranthaceae - enzymology; Amaranthaceae - genetics; Amino acids; Anatomy & physiology; Aquatic plants; Base Sequence; Bayesian analysis; Biological evolution; Biology; Carbon dioxide; Chenopodiaceae; Cyperaceae; Enzymes; Evolution; Evolution & development; Evolution, Molecular; Flowers & plants; Genes, Plant - physiology; Isoleucine; Methionine; Molecular biology; Molecular evolution; Molecular Sequence Data; Oxygenase; Photosynthesis; Photosynthesis - genetics; Phylogenetics; Phylogeny; Physiology; Plant sciences; Poaceae; Positive selection; Proteins; RbcL gene; Ribulose-1,5-bisphosphate; Ribulose-bisphosphate carboxylase; Ribulose-Bisphosphate Carboxylase - genetics; Ribulosephosphates - metabolism; Selection, Genetic; Serine; Sorghum; Substrate specificity; Substrates; Temperature
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0052974

Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) catalyses the key reaction in the photosynthetic assimilation of CO₂. In C₄ 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, C₄ Rubisco exhibits a higher maximum velocity but lower substrate specificity compared with the C₃ enzyme. Specific amino-acids in Rubisco are associated with C₄ photosynthesis in monocots, but it is not known whether selection has acted on Rubisco in a similar way in eudicots. We investigated Rubisco evolution in Amaranthaceae sensu lato (including Chenopodiaceae), the third-largest family of C₄ 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 C₄ 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 C₄ plant groups, such as C₄ monocots, illustrating a striking parallelism in molecular evolution. 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.