Interannual variation of stomatal traits in tree crops and its impact on environmental resilience

Climate change is driving an increased demand for freshwater in agriculture and this highlights an important need to enhance crop water-use efficiency. Making these improvements in perennial crops, such as fruit trees, can be particularly challenging because of long generation cycles and difficulties in genetic transformation. Nonetheless, tree crops play critical roles in global food security and strategies for climate adaptation are strongly needed. Stomata are fundamental gatekeepers of plant-water relations and represent promising targets for crop improvement. Here, we investigated stomatal density (SD) and function in four consecutive years from 2019 to 2022 in a genetically diverse population of 269 apple accessions from across the globe (Malus × domestica Borkh.). Apples are the third most valuable fruit crop worldwide and physiologically representative of many temperate tree crops. SD exhibited a normal distribution within the population, showing significant differences among accessions that remained consistent across 2019, 2020, and 2021. From this population, we identified two subsets of 20 accessions with contrasting SD: the highest stomatal density (HSD) ranging from 370 mm-2 to 500 mm-2, and the lowest stomatal density (LSD) ranging from 192 mm-2 to 316 mm-2. These SD groups were used to compare stomatal function, leaf physiology, and crop productivity across two seasons in 2021 and 2022. While SD defined consistent differences in stomatal conductance (gs) and instantaneous water-use efficiency (iWUE) between groups, seasonal conditions defined the operational values. LSD had lower gs and greater iWUE in both years. However, in 2022, characterized by hotter conditions and a nearly double VPD compared to the previous year, LSD reduced gs to rates that constrained photosynthesis and ultimately reduced fruit yield compared with 2021. HSD experienced an equivalent gs decline in 2022, but photosynthesis and fruit yield were unaffected compared with 2021. Our results demonstrate a clear trade-off between water savings (LSD) and tree productivity (HSD) as driven by stomatal traits. Moreover, the consistency of SD across years makes it a reliable functional trait for predicting plant performance amidst environmental responses. Finally, in contrast to the prevailing literature that suggests LSD would be the preferred ideotype for climate adaptation in crops, HSD plants may actually provide greater resilience to climate variability in managed orchards and other agricultural systems.