Lawrence Berkeley National Laboratory

Abstract: As atmospheric CO2 rises, increases in photosynthesis and plant growth are routinely documented across ecosystems globally. Although primarily studied in relation to photorespiration, serine metabolism in chloroplasts may play a key role in plant CO2 fertilization responses by linking CO2 assimilation with growth. However, little information is available on the in vivo activity of the plastidic phosphorylated serine pathway. Here, we show that the serine phosphate pathway is part of a ‘photosynthetic C1 pathway’ and demonstrate its high activity in foliage of a C3 tree where it rapidly integrates photosynthesis directly with C1 metabolism contributing to new biomass via methyl transfer reactions and imparting a large natural 13C-depleted signature. Using 13CO2-labelling, we show that leaf serine, the S-methyl group of leaf methionine, pectin methyl esters, and the associated methanol released during cell wall expansion during growth, are directly produced from photosynthetically-linked C1 metabolism, unrelated to photorespiration, within minutes of light exposure. We speculate that the photosynthetic C1 pathway and its key enzyme methionine synthase is highly conserved across the photosynthetic tree of life and may have evolved with oxygenic photosynthesis by providing a mechanism of directly linking carbon assimilation with growth. Although the rise in atmospheric CO2 inhibits major metabolic pathways like photorespiration in C3 plants, our results suggest that the photosynthetic C1 pathway may accelerate and represents a ‘missing link’ between enhanced photosynthesis and growth rates of modern plants and ecosystems during terrestrial CO2 fertilization under a changing climate.