Drivers of Natural Variation in Water-Use Efficiency Under Fluctuating Light Are Promising Targets for Improvement in Sorghum

Improving leaf intrinsic water-use efficiency ( ), the ratio of photosynthetic CO assimilation to stomatal conductance, could decrease crop freshwater consumption. has primarily been studied under steady-state light, but light in crop stands rapidly fluctuates. Leaf responses to these fluctuations substantially affect overall plant performance. Notably, photosynthesis responds faster than stomata to decreases in light intensity: this desynchronization results in substantial loss of . Traits that could improve under fluctuating light, such as faster stomatal movement to better synchronize stomata with photosynthesis, show significant natural diversity in C species. However, C crops have been less closely investigated. Additionally, while modification of photosynthetic or stomatal traits independent of one another will theoretically have a proportionate effect on , in reality these traits are inter-dependent. It is unclear how interactions between photosynthesis and stomata affect natural diversity in , and whether some traits are more tractable drivers to improve . Here, measurements of photosynthesis, stomatal conductance and under steady-state and fluctuating light, along with stomatal patterning, were obtained in 18 field-grown accessions of the C crop sorghum. These traits showed significant natural diversity but were highly correlated, with important implications for improvement of . Some features, such as gradual responses of photosynthesis to decreases in light, appeared promising for improvement of . Other traits showed tradeoffs that negated benefits to , e.g., accessions with faster stomatal responses to decreases in light, expected to benefit , also displayed more abrupt losses in photosynthesis, resulting in overall lower . Genetic engineering might be needed to break these natural tradeoffs and achieve optimal trait combinations, e.g., leaves with fewer, smaller stomata, more sensitive to changes in photosynthesis. Traits describing at steady-state, and the change in following decreases in light, were important contributors to overall under fluctuating light.