Jardine, Kolby J.Gallo, LuizaRoth, MelissaUpadhyaya, ShivaniNorthen, TrentKosina, SuzanneTcherkez, GuillaumeEudes, AymerickDomigues, TomasGreule, MarkusSom, SumanKeppler, Frank2025-05-232025-05-23PubMed:39516667http://www.scopus.com/inward/record.url?scp=85209476000&partnerID=8YFLogxKhttps://hdl.handle.net/1885/733751726Although 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. (Figure presented.) (Figure presented.)The authors would like to thank Christina Wistrom for maintaining optimal growth conditions of poplar trees in the UC Berkeley Oxford Tract greenhouse and facilitating the integration of a real-time volatile metabolomics laboratory. We would also like to thank Christina Procopiou for the assistance with the C1 photosynthesis animation development and helpful discussions with Alister Rogers on AdoMet recycling mechanisms, and Dan Feldman on methanol remote sensing. This research was supported by the DOE Office of Science, Office of Biological and Environmental Research (BER), Early Career Research Project (ECRP) grant no. FP00007421 and the DOE Joint BioEnergy Institute (http://www.jbei.org) supported by contract DE-AC02-05CH11231. Additional DOE funding for the research came from the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) through contract no. DE-AC02-05CH11231 as part of DOE\u2019s Terrestrial Ecosystem Science Program. The metabolomics analysis was supported by m-CAFEs Microbial Community Analysis & Functional Evaluation in Soils, (m-CAFEs@lbl.gov) a Science Focus Area at Lawrence Berkeley National Laboratory funded by the U.S. Department of Energy, Office of Science, Office of Biological & Environmental Research DE-AC02-05CH11231. TFD received financial support from the Brazilian National Council for Scientific and Technological Development (CNPq) grant 312589/2022-0 (Bolsa de produtividade em Pesquisa). LBG received financial support from AUSPIN Edital 001/2022 \u2013 Programa de Bolsas de Interc\u00E2mbio Internacional. The authors would like to thank Christina Wistrom for maintaining optimal growth conditions of poplar trees in the UC Berkeley Oxford Tract greenhouse and facilitating the integration of a real-time volatile metabolomics laboratory. We would also like to thank Christina Procopiou for the assistance with the C photosynthesis animation development and helpful discussions with Alister Rogers on AdoMet recycling mechanisms, and Dan Feldman on methanol remote sensing. This research was supported by the DOE Office of Science, Office of Biological and Environmental Research (BER), Early Career Research Project (ECRP) grant no. FP00007421 and the DOE Joint BioEnergy Institute ( http://www.jbei.org ) supported by contract DE-AC02-05CH11231. Additional DOE funding for the research came from the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) through contract no. DE-AC02-05CH11231 as part of DOE\u2019s Terrestrial Ecosystem Science Program. The metabolomics analysis was supported by m-CAFEs Microbial Community Analysis & Functional Evaluation in Soils, (m-CAFEs@lbl.gov) a Science Focus Area at Lawrence Berkeley National Laboratory funded by the U.S. Department of Energy, Office of Science, Office of Biological & Environmental Research DE-AC02-05CH11231. TFD received financial support from the Brazilian National Council for Scientific and Technological Development (CNPq) grant 312589/2022-0 (Bolsa de produtividade em Pesquisa). LBG received financial support from AUSPIN Edital 001/2022 \u2013 Programa de Bolsas de Interc\u00E2mbio Internacional. 1enPublisher Copyright: © The Author(s) 2024.202410.1038/s42003-024-07142-085209476000