The ‘Photosynthetic C1 pathway’ links carbon assimilation and growth in plants

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.