Metabolic adaptation of a photosynthetic angiosperm to extreme CO2 levels in Yellowstone: living on the edge

Abstract

Abstract How do plants adapt to elevated CO2 levels? This much-studied question has returned ambiguous answers. CO2 is the carbon nutrient for all photosynthesis, underlying global biomass productivity. Small increases in CO2 levels may boost photosynthetic efficiency in the short term, but at higher levels it inhibits biomass production and increases susceptibility to stress. Whether photosynthesis can favorably adapt to extreme CO2 over prolonged periods of time remains yet unknown. Here, we investigate changes in photosynthetic metabolism in a C3 plant growing along a natural CO2 gradient in Yellowstone NP over many decades. We find that plants adapted to grow near high CO2 sources (~ 6000 ppm) require similarly high CO2 to open Linear Electron Flow (LEF) for NADPH reoxidation. Cyclic Electron Flow (CEF) for ATP generation is upregulated and photogenerated ATP is shorter-lived in high CO2-Adapted plants where it is more rapidly lost in the dark. We attribute the shift in regulation away from LEF to higher CEF to the low chloroplast ATP levels caused by the stressful growth conditions, as revealed by stunted biomass and leaf chlorosis.