Brassicaceae display diverse photorespiratory carbon recapturing mechanisms

Abstract

AbstractCarbon concentrating mechanisms enhance the carboxylase efficiency of the central photosynthetic enzyme rubisco by providing supra-atmospheric concentrations of CO2in its surrounding. In the C4photosynthesis pathway, this is achieved by combinatory changes to leaf biochemistry and anatomy. Carbon concentration by the photorespiratory glycine shuttle requires fewer and less complex modifications. It could represent an early step during evolution from C3to C4photosynthesis and an inspiration for engineering approaches. Plants displaying CO2compensation points between 10 to 40 ppm are therefore often termed ‘C3–C4intermediates’. In the present study, we perform a physiological, biochemical and anatomical survey of a large number of Brassicaceae species to better understand the C3-C4intermediate phenotype. Our phylogenetic analysis suggested that C3-C4metabolism evolved up to five times independently in the Brassicaceae. The efficiency of the pathways showed considerable variation between the species but also within species. Centripetal accumulation of organelles in the bundle sheath was consistently observed in all C3-C4classified accessions indicating a crucial role of anatomical features for CO2concentrating pathways. Leaf metabolite patterns were strongly influenced by the individual plant accessions, but accumulation of photorespiratory shuttle metabolites glycine and serine was generally observed. Analysis of PEPC activities suggests that C4-like shuttles have not evolve in the investigated Brassicaceae.HighlightOur physiological, biochemical and anatomical survey of Brassicaceae revels multiple evolution of C3-C4intermediacy connected to variation in photorespiratory carbon recapturing efficiency and a distinct C3-C4bundle sheath anatomy.