The ‘photosynthetic C1 pathway’ links carbon assimilation and growth in California poplar

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. Here, we show that the phosphorylated serine pathway is part of a 'photosynthetic C₁ pathway' and demonstrate its high activity in foliage of a C₃ tree where it rapidly integrates photosynthesis and C₁ metabolism contributing to new biomass via methyl transfer reactions, 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, within minutes of light exposure. We speculate that the photosynthetic C₁ pathway is highly conserved across the photosynthetic tree of life, is responsible for synthesis of the greenhouse gas methane, and may have evolved with oxygenic photosynthesis by providing a mechanism of directly linking carbon and ammonia assimilation with growth. Although the rise in atmospheric CO₂ inhibits major metabolic pathways like photorespiration, our results suggest that the photosynthetic C₁ pathway may accelerate and represents a missing link between enhanced photosynthesis and plant growth rates during CO₂ fertilization under a changing climate.