Scaling nitrogen and carbon interactions: what are the consequences of biological buffering?

Understanding the consequences of elevated CO2 (eCO2; 800 ppm) on terrestrial ecosystems is a central theme in global change biology, but relatively little is known about how altered plant C and N metabolism influences higher levels of biological organization. Here, we investigate the consequences of C and N interactions by genetically modifying the N-assimilation pathway in Arabidopsis and initiating growth chamber and mesocosm competition studies at current CO2 (cCO2; 400 ppm) and eCO2 over multiple generations. Using a suite of ecological, physiological, and molecular genomic tools, we show that a single-gene mutant of a key enzyme (nia2) elicited a highly orchestrated buffering response starting with a fivefold increase in the expression of a gene paralog (nia1) and a 63% increase in the expression of gene network module enriched for N-assimilation genes. The genetic perturbation reduced amino acids, protein, and TCA-cycle intermediate concentrations in the nia2 mutant compared to the wild-type, while eCO2 mainly increased carbohydrate concentrations. The mutant had reduced net photosynthetic rates due to a 27% decrease in carboxylation capacity and an 18% decrease in electron transport rates. The expression of these buffering mechanisms resulted in a penalty that negatively correlated with fitness and population dynamics yet showed only minor alterations in our estimates of population function, including total per unit area biomass, ground cover, and leaf area index. This study provides insight into the consequences of buffering mechanisms that occur post-genetic perturbations in the N pathway and the associated outcomes these buffering systems have on plant populations relative to eCO2.