Enhanced photorespiratory and TCA pathways by elevated CO2 to manage ammonium nutrition in tomato leaves

Plants grown under exclusive ammonium (NH₄⁺) nutrition have high carbon (C) demand to sustain proper nitrogen (N) assimilation and energy required for plant growth, generally impaired when compared to nitrate (NO₃⁻) nutrition. Thereby, the increment of the atmospheric carbon dioxide (CO₂) concentration, in the context of climate change, will potentially allow plants to better face ammonium nutrition. In this work, tomato (Solanum lycopersicum L.) plants were grown under ammonium or nitrate nutrition in conditions of ambient (aCO₂, 400 ppm) or elevated CO₂ (eCO_2, 800 ppm) atmosphere. Elevated CO₂ increased photosynthesis rate and tomato shoot growth regardless of the N source. In the case of NH₄⁺-fed leaves the positive effect of elevated CO₂ occurred despite of the high tissue NH₄⁺ accumulation. Under eCO₂ ammonium nutrition triggered, among others, the modulation of genes related to C provision pathways (including carbonic anhydrase and glyoxylate cycle), antioxidant response and cell membranes protection. The enhanced photosynthate production at eCO₂ facilitated C skeleton provision through the TCA cycle and anaplerotic pathways to promote amino acid synthesis. Moreover, photorespiratory activity was stimulated by eCO₂ and contributed to yield serine as additional sink for NH₄⁺ excess. Overall, these changes denote a connection between the respiratory and the photorespiratory pathways linked to ammonium nutrition. This metabolic strategy may allow crops to grow efficiently using ammonium as fertilizer in a future climate change scenario, while mitigating N losses.