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

Charles P Pignon,Andrew D B Leakey,Johannes Kromdijk,Stephen P Long

doi:10.3389/fpls.2021.627432

Abstract

Improving leaf intrinsic water-use efficiency (iWUE), the ratio of photosynthetic CO2 assimilation to stomatal conductance, could decrease crop freshwater consumption. iWUE 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 iWUE. Traits that could improve iWUE under fluctuating light, such as faster stomatal movement to better synchronize stomata with photosynthesis, show significant natural diversity in C3 species. However, C4 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 iWUE, in reality these traits are inter-dependent. It is unclear how interactions between photosynthesis and stomata affect natural diversity in iWUE, and whether some traits are more tractable drivers to improve iWUE. Here, measurements of photosynthesis, stomatal conductance and iWUE under steady-state and fluctuating light, along with stomatal patterning, were obtained in 18 field-grown accessions of the C4 crop sorghum. These traits showed significant natural diversity but were highly correlated, with important implications for improvement of iWUE. Some features, such as gradual responses of photosynthesis to decreases in light, appeared promising for improvement of iWUE. Other traits showed tradeoffs that negated benefits to iWUE, e.g., accessions with faster stomatal responses to decreases in light, expected to benefit iWUE, also displayed more abrupt losses in photosynthesis, resulting in overall lower iWUE. 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 iWUE at steady-state, and the change in iWUE following decreases in light, were important contributors to overall iWUE under fluctuating light.

Highlights

Water is the primary abiotic factor limiting crop productivity (Boyer, 1982), with agriculture consuming up to 85% of freshwater withdrawals (WWAP, 2015; D’Odorico et al, 2020)
Because increases in photosynthetic photon flux density (PPFD) are typically less impactful to intrinsic water-use efficiency (iWUE) than decreases in PPFD, this study focused on extracting nonsteady-state traits following decreases in PPFD
This study shows significant variation among sorghum accessions in steadystate and non-steady-state A and gs and stomatal density and size, reveals how variation in these traits drives variation in iWUE, and discusses how tradeoffs between these should shape strategies for decreasing crop water use

Summary

Introduction

Water is the primary abiotic factor limiting crop productivity (Boyer, 1982), with agriculture consuming up to 85% of freshwater withdrawals (WWAP, 2015; D’Odorico et al, 2020). Breeding has almost tripled productivity of major crops over the last 60 years, without parallel improvement in the amount of water required to produce a ton of crop biomass (Sinclair et al, 1984; Ort and Long, 2014). Improving crop water-use efficiency is important to achieve the crop productivity required to meet global demand (Bonsch et al, 2016; Flexas, 2016; FAO et al, 2018; Leakey et al, 2019). The ratio of A to gs gives leaf intrinsic water-use efficiency (iWUE) (Leakey et al, 2019). Most inter- and intra-specific surveys of A, gs and iWUE, and analyses of their limitations have concerned steady-state conditions (Galmes et al, 2007; Giuliani et al, 2013; Driever et al, 2014; Jahan et al, 2014; Sollenberger et al, 2014; Viswanathan et al, 2014; Tomeo and Rosenthal, 2017; Yabiku and Ueno, 2017; Leakey et al, 2019)

Methods

Results

Discussion

Conclusion