Nitrogen demand, supply, and acquisition strategy control plant responses to elevated CO2 at different scales

Abstract

Plants respond to elevated atmospheric CO2 concentrations by reducing leaf nitrogen content and photosynthetic capacity - patterns that correspond with increased net photosynthesis rates, total leaf area, and total biomass. Nitrogen supply has been hypothesized to be the primary factor controlling these responses, as nitrogen availability limits net primary productivity globally. Recent work using evo-evolutionary optimality theory suggests that leaf photosynthetic responses to elevated CO2 are independent of nitrogen supply and are instead driven by leaf nitrogen demand to build and maintain photosynthetic enzymes, which optimizes resource allocation to photosynthetic capacity and maximizes allocation to growth. Here, Glycine max L. (Merr) seedlings were grown under two CO2 concentrations, with and without inoculation with Bradyrhizobium japonicum, and across nine soil nitrogen fertilization treatments in a full-factorial growth chamber experiment to reconcile the role of nitrogen supply and demand on leaf and whole-plant responses to elevated CO2. After seven weeks, elevated CO2 increased net photosynthesis rates despite reduced leaf nitrogen content and maximum rates of Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco) carboxylation and electron transport for RuBP regeneration. Effects of elevated CO2 on net photosynthesis and indices of photosynthetic capacity were independent of nitrogen fertilization and inoculation. However, increasing nitrogen fertilization enhanced positive effects of elevated CO2 on total leaf area and total biomass due to increased nitrogen uptake and reduced carbon costs to acquire nitrogen. Whole-plant responses to elevated CO2 were not modified by inoculation across the nitrogen fertilization gradient, as plant investment toward symbiotic nitrogen fixation was similar between CO2 treatments. These results indicate that leaf nitrogen demand to build and maintain photosynthetic enzymes drives leaf photosynthetic responses to elevated CO2, while nitrogen supply regulates whole-plant responses. Our findings build on previous work suggesting that terrestrial biosphere models may improve simulations of photosynthetic processes under future novel environments by adopting optimality principles.