Natural variation in stomatal dynamics drives divergence in heat stress tolerance and contributes to seasonal intrinsic water-use efficiency in Vitis vinifera (subsp. sativa and sylvestris)

Abstract

Stomata control CO2 uptake for photosynthesis and water loss through transpiration, thus playing a key role in leaf thermoregulation, water-use efficiency (iWUE) and plant productivity. In this work, we investigated the relationship between several leaf traits and hypothesized that stomatal behavior to fast (i.e. minutes) environmental changes co-determines along with steady-state traits the physiological response of grapevine to the surrounding fluctuating environment over the growing season. No relationship between iWUE, heat stress (HS) tolerance and stomatal traits was observed in field grown grapevine, suggesting that other physiological mechanisms are involved in determining leaf evaporative cooling capacity and the seasonal ratio of CO2 uptake (A) to stomatal conductance (gs). Indeed, cultivars that in the field had an unexpected combination of high iWUE but low sensitivity to thermal stress, displayed a quick stomatal closure to light, but a sluggish closure to increased vapor pressure deficit (VPD) levels. This strategy aiming both at conserving water under a high-to-low light transition and in prioritizing evaporative cooling under a low-to-high VPD transition, was mainly observed in Regina and Syrah. Moreover, cultivars with different known responses to soil moisture deficit or high air VPD (isohydric vs anisohydric) had opposite behavior under fluctuating environments, with the isohydric cultivar showing slow stomatal closure to reduced light intensity but quick temporal responses to VPD manipulation. We propose that stomatal behavior to fast environmental fluctuations can play a critical role on leaf thermoregulation and water conservation under natural field conditions in grapevine.

VvEPFL9-1 Knock-Out via CRISPR/Cas9 Reduces Stomatal Density in Grapevine

“…Furthermore, the conditions of dynamic light intensity such as those present in the greenhouse, may have contributed to accentuate the water saving behavior of the lines with lower stomatal density. Indeed, reducing stomatal density can limit stomatal clustering ( Harrison et al, 2020 ) and therefore increase stomatal responsiveness to environmental cues ( Faralli et al, 2021 ). Important differences for g s were also observed between Experiments 1 and 3, suggesting that plant age and pot-effect significantly influences operating g s , although the g s values are inside the ranges shown by Lavoie-Lamoureux et al (2017) for pot-grown grapevine.…”

“…In drought-stressed grapevine, stomatal closure is triggered by hydraulic signals and maintained by abscisic acid following re-watering ( Lovisolo et al, 2010 ; Tombesi et al, 2015 ). Genotypic variation for stomatal sensitivity to reduced water availability has been shown to exist in grapevine ( Schultz, 2003 ; Soar et al, 2006 ; Bota et al, 2016 ; Villalobos-González et al, 2019 ; Faralli et al, 2021 ).…”

Genetic variation in photosynthesis: many variants make light work

“…It should therefore be no surprise that genetic variation in photosynthetic traits in response to abiotic stress is strongly represented in the current issue. Faralli et al (2022) present variation between stomatal dynamics across a range of Vitis vinifera (grapevine) genotypes, which contributed significantly to differentiation in heat tolerance and water use efficiency. Ortiz and Salas-Fernandez (2022) analyse the genetic control of photosynthesis in response to drought stress in Sorghum bicolor , identifying several genomic regions associated with variation in gas exchange and chlorophyll fluorescence traits, which might be used to further enhance already substantial drought tolerance of this C 4 food, feed, and bioenergy crop.…”

Water Stress Impacts on Grapevines (Vitis vinifera L.) in Hot Environments: Physiological and Spectral Responses

“…On 13 March 2020, the vines were moved from the glasshouse to the CER to allow them to acclimate. During acclimation (13)(14)(15)(16)(17), the average temperature, relative humidity (RH), and VPD were 25.5 • C, 48.8%, and 1.7 kPa, respectively. Initially, the vines were irrigated to field capacity based on the pot weight: the pots were weighed every morning to bring them back to their original weight by irrigation.…”

“…They showed that Shiraz promoted a sustained g s and an unaltered berry growth under field conditions with manipulated high temperatures. Recently, Faralli et al [16] reported that the lower stomatal sensitivity of Shiraz might support leaf heat dissipation under fluctuating environmental conditions. However, Lehr et al observed that WS under high temperatures dramatically reduced g s regardless of isohydric or anisohydric behaviour [17].…”