Evolutionary and functional relationships between plant and microbial C1 metabolism in terrestrial ecosystems.

One-carbon (C1) metabolism, centered on the universal methyl donor S-adenosyl methionine (SAM), plays critical roles in biosynthesis, redox regulation, and stress responses across plants and microbes. A recently proposed photosynthetic C1 pathway links SAM methyl groups directly to RuBisCO-mediated CO2 assimilation and integrates with nitrogen and sulfur metabolism. Light-dependent SAM synthesis may regulate the methylation of biopolymers and specialized metabolites and help mitigate photorespiratory stress under elevated temperature and drought. Phylogenetic analysis of two core enzymes suggests evolutionary continuity from methylotrophic microbes to land plants, supporting microbial origins via endosymbiotic gene transfer. Beyond intracellular roles, C1 metabolism drives biosphere-atmosphere exchange via gases such as methane, methanol, formic acid, and formaldehyde, and numerous specialized volatiles synthesized through SAM methylation. S-methylmethionine, a mobile C1 metabolite, may mediate phloem transport of reduced sulfur, nitrogen, and methyl groups, linking above- and belowground C1 cycling in plants. Advances in real-time gas sensing now allow the high-frequency quantification of C1 fluxes from leaves, stems, and soils, highlighting C1 metabolism as a critical and underrecognized component of terrestrial carbon and nutrient cycling. Given its microbial ancestry and the production of diverse volatile biosignatures, C1 metabolism may also offer unique insights into life's origins and biosignature detection on exoplanets.