Brassicaceae display variation in efficiency of photorespiratory carbon-recapturing mechanisms

Carbon-concentrating mechanisms enhance the carboxylase efficiency of Rubisco by providing supra-atmospheric concentrations of CO(2) in its surroundings. Beside the C(4) photosynthesis pathway, carbon concentration can also be achieved by the photorespiratory glycine shuttle which requires fewer and less complex modifications. Plants displaying CO(2) compensation points between 10 ppm and 40 ppm are often considered to utilize such a photorespiratory shuttle and are termed ‘C(3)–C(4) intermediates’. In the present study, we perform a physiological, biochemical, and anatomical survey of a large number of Brassicaceae species to better understand the C(3)–C(4) intermediate phenotype, including its basic components and its plasticity. Our phylogenetic analysis suggested that C(3)–C(4) metabolism evolved up to five times independently in the Brassicaceae. The efficiency of the pathway showed considerable variation. Centripetal accumulation of organelles in the bundle sheath was consistently observed in all C(3)–C(4)-classified taxa, indicating a crucial role for anatomical features in CO(2)-concentrating pathways. Leaf metabolite patterns were strongly influenced by the individual species, but accumulation of photorespiratory shuttle metabolites glycine and serine was generally observed. Analysis of phosphoenolpyruvate carboxylase activities suggested that C(4)-like shuttles have not evolved in the investigated Brassicaceae. Convergent evolution of the photorespiratory shuttle indicates that it represents a distinct photosynthesis type that is beneficial in some environments.