Satisfying leaf nitrogen demand under drought is determined by soil nitrogen availability and drought severity

Plants balance water and nitrogen acquisition to optimize carbon gain, particularly under resource-limited conditions. These tradeoffs can be predicted from the photosynthetic least-cost theory, but its applicability under severe drought and nitrogen limitation within a single species remains untested. We examined how soil water stress and nitrogen limitation shape leaf-level water and nitrogen economics and the associated plant carbon costs of soil resource acquisition in common sunflower (Helianthus annuus L.) grown under two nitrogen levels and three soil water availability scenarios. Contrary to photosynthetic least-cost theory, increasing drought severity reduced leaf nitrogen content (Narea) under low nitrogen, likely due to impaired nitrogen uptake via transpiration-driven mass flow. Likewise, the maximum Ribulose-1,5-Biphosphate Carboxylase/Oxygenase (RuBisCO) carboxylation rate (Vcmax) and net photosynthetic rate (Anet) decreased over time as drought progressed under low soil nitrogen. However, under high nitrogen, and in line with least-cost theory, Narea, Vcmax and Anet remained stable, with Narea increasing over time, enhancing leaf water-use efficiency. Total leaf area and biomass increased with soil nitrogen availability, but this effect weakened under severe drought. Notably, carbon costs of nitrogen acquisition increased with drought severity only under low nitrogen, indicating water stress impedes nitrogen uptake. These findings highlight the need to integrate soil resource demand and availability into photosynthesis models, especially under extreme drought and nitrogen limitation.