Sulfate Metabolism in C Species Is Controlled by the Root and Connected to Serine Biosynthesis.

The evolution of C photosynthesis led to an increase in carbon assimilation rates and plant growth compared to C photosynthetic plants. This enhanced plant growth, in turn, affects the requirement for soil-derived mineral nutrients. However, mineral plant nutrition has scarcely been considered in connection with C photosynthesis. Sulfur is crucial for plant growth and development, and preliminary studies in the genus suggested metabolic differences in sulfate assimilation along the C evolutionary trajectory. Here, we show that in controlled conditions, foliar accumulation of the reduced sulfur compounds Cys and glutathione (GSH) increased with progressing establishment of the C photosynthetic cycle in different species. An enhanced demand for reduced sulfur in C species is reflected in high rates of [S]sulfate incorporation into GSH upon sulfate deprivation and increased GSH turnover as a reaction to the inhibition of GSH synthesis. Expression analyses indicate that the γ-glutamyl cycle is crucial for the recycling of GSH in C species. Sulfate reduction and GSH synthesis seems to be preferentially localized in the roots of C species, which might be linked to its colocalization with the phosphorylated pathway of Ser biosynthesis. Interspecies grafting experiments of (C) and (C) revealed that the root system primarily controls sulfate acquisition, GSH synthesis, and sulfate and metabolite allocation in C and C plants. This study thus shows that evolution of C photosynthesis resulted in a wide range of adaptations of sulfur metabolism and points out the need for broader studies on importance of mineral nutrition for C plants.