Diurnal stomatal apertures and density ratios affect whole-canopy stomatal conductance, water-use efficiency and yield

Key physiological traits of crop plants, such as transpiration, stomatal conductance, and photosynthesis are highly related to plant productivity. However, these traits are typically studied under steady-state conditions or modeled using only a few measured data points which do not reflect the dynamic behavior of the plant in response to field conditions. In this work, we hypothesized that the plastic behavior of whole-plant water balance regulation, as previously observed in tomato WT, was partially lost in the breeding process due to selective pressure towards productivity. We also hypothesized that this plastic behavior would be observed in some members of the tomato introgression lines (ILs) population, which was created by crossing the WT and M82 lines, particularly in ILs that demonstrate improved drought response. To overcome the steady-state bottleneck, and to test our hypothesis we used a gravimetric functional-phenotyping platform and a reverse-phenotyping method to examine the dynamic whole-plant water-regulation responses of tomato ILs and compared those responses with several years of yield performance in commercial fields. Indeed, our study enabled us to identify high plasticity in a few ideotypic ILs. We found that ideotype lines with highly plastic stomatal conductance and high abaxial-adaxial stomatal density ratios had stomatal apertures that peaked early in the day, even under water-deficit conditions. These traits resulted in dynamic daily water-use efficiency, along with rapid recovery of transpiration when irrigation was resumed after a period of imposed drought. Abaxial stomatal density was also found to be strongly correlated with the expression of the stomatal-development genes SPCH and ZEP. This study demonstrates how a reverse functional phenotyping approach based on field yield data, continuous and simultaneous whole-plant water-balance measurements and anatomical examination of individual leaves can help us to understand and identify dynamic and complex yield-related physiological traits.