Analysis of durum wheat photosynthetic organs during grain filling reveals the ear as a water stress-tolerant organ and the peduncle as the largest pool of primary metabolites

The pool of carbon- and nitrogen-rich metabolites is quantitatively relevant in non-foliar photosynthetic organs during grain filling, which have a better response to water limitation than flag leaves. The response of durum wheat to contrasting water regimes has been extensively studied at leaf and agronomic level in previous studies, but the water stress effects on source-sink dynamics, particularly non-foliar photosynthetic organs, is more limited. Our study aims to investigate the response of different photosynthetic organs to water stress and to quantify the pool of carbon and nitrogen metabolites available for grain filling. Five durum wheat varieties were grown in field trials in the Spanish region of Castile and León under irrigated and rainfed conditions. Water stress led to a significant decrease in yield, biomass, and carbon and nitrogen assimilation, improved water use efficiency, and modified grain quality traits in the five varieties. The pool of carbon (glucose, glucose-6-phosphate, fructose, sucrose, starch, and malate) and nitrogen (glutamate, amino acids, proteins and chlorophylls) metabolites in leaf blades and sheaths, peduncles, awns, glumes and lemmas were also analysed. The results showed that the metabolism of the blades and peduncles was the most susceptible to water stress, while ear metabolism showed higher stability, particularly at mid-grain filling. Interestingly, the total metabolite content per organ highlighted that a large source of nutrients, which may be directly involved in grain filling, are found outside the blades, with the peduncles being quantitatively the most relevant. We conclude that yield improvements in our Mediterranean agro-ecosystem are highly linked to the success of shoots in producing ears and a higher number of grains, while grain filling is highly dependent on the capacity of non-foliar organs to fix CO₂ and N. The ear organs show higher stress resilience than other organs, which deserves our attention in future breeding programmes.