Water flow through the soil-plant-atmosphere continuum (SPAC) is driven by a gradient of water potential and regulated by a series of variable hydraulic conductances (or resistances, their inverse). It is widely acknowledged that plants continually adjust to variable atmospheric and soil conditions by modifying the hydraulic conductances of key elements both below- and aboveground of the SPAC (Abdalla et al., 2021). However, our mechanistic understanding of these hydraulic adjustments remains elusive. On a short timescale, stomatal opening and closing regulate the transpiration rate of plants that in turn affects the difference between leaf and soil water potential. This safety mechanism allows the plant to operate at less negative water potentials, thereby delaying the formation of embolisms to avoid mortality, for example when the plant is in water deficit (Anderegg et al., 2017; Draye et al., 2010). It has been shown that stomatal regulation is linked to hydraulic and/or chemical (e.g. abscisic acid) signals. However, the extent to which these underlying mechanisms interact and vary among species and environmental conditions is still a subject of debate (Hochberg et al., 2018; Tardieu, 2016). How edaphic stress impacts transpiration and stomatal regulation is still not fully understood (Abdalla et al., 2022).
Stomatal control has been broadly studied in relation to xylem cavitation, especially to xylem vulnerability on the aboveground part (canopy) of the SPAC (Anderegg et al., 2017; Bartlett et al., 2016; Henry et al., 2019; Martin-StPaul et al., 2017; Sperry and Love, 2015; Wolf et al., 2016). However, other hydraulic constraints arise along the SPAC prior to xylem cavitation (Albuquerque et al., 2020; Corso et al., 2020; Scoffoni et al., 2017), especially belowground (Abdalla et al., 2022; Koehler et al., 2022; Rodriguez-Dominguez and Brodribb, 2020). The quantification of these above- and belowground hydraulic conductances and their evolution with time allows identifying the main hydraulic limitation in SPAC, which affect the water potential and stomatal closure of the plant (Novick et al., 2022; Whalley et al., 2013). In wet soils, the soil hydraulic conductivity is typically much higher than that of roots, and water flow is primarily governed by root hydraulic conductivity (Draye et al., 2010; Passioura, 1980; Zarebanadkouki et al., 2013). As the soil dries out, the soil water potential decreases, resulting in a significant reduction in soil hydraulic conductivity, particularly in the vicinity of the roots. This soil limitation restricts root water extraction and may limit the supply of water for transpiration (Carminati and Javaux, 2020; de Jong van Lier et al., 2006; Gardner, 1960; Passioura, 1980). The loss of soil hydraulic conductance results in large gradients in soil water potential close to the roots, leading to a significant decrease in leaf water potential to support a slight increase in transpiration. Consequently, the relationship between stomatal control and leaf water potential should be specific to the soil and root characteristics (Carminati and Javaux, 2020). The soil texture determines soil hydraulic properties, thereby influences plant hydraulics and response to drought conditions (Cai et al., 2022; Javaux and Carminati, 2021). In theory, stomatal closure is sharper in coarse-textured soils than in fine-textured soils, and is also more abrupt for a plant with a short root system compared to a long root system (Wankmüller and Carminati, 2024). Recent studies investigated the hypothesis that the soil rather than the xylem vulnerability has a dominant role on stomatal closure on tomato (Abdalla et al., 2021, 2022), maize (Cai et al., 2022; Koehler et al., 2022; Nguyen et al., 2024) and olive trees (Rodriguez-Dominguez and Brodribb, 2020). However, these studies are based on well-controlled laboratory experiments. It is still unclear if these results obtained on these species under laboratory conditions can be generalized to field conditions and other species (Wankmüller and Carminati, 2024).
Grapevines (Vitis vinifera L.) stand as one of the world’s most widely cultivated and economically significant fruit crops (Yang et al., 2023). Water use and grapevine water status are very important in viticulture, since it has a huge impact on fruit composition and wine quality (Gambetta et al., 2020; Matthews and Anderson, 1988; Van Leeuwen et al., 2009). It is well known that soil plays a major role in grapevine water status, through its capacity to retain and conduct water (Van Leeuwen et al., 2018). Previously, grapevine water use and stomatal control were regarded as a plant-specific strategy, categorizing grapevine cultivars as either (near-)isohydric or (near-)anisohydric (Schultz, 2003). However, depending on the study and the environmental conditions, a same vine variety may be considered iso- or anisohydric (Hochberg et al., 2013; Tamayo et al., 2023; Tramontini et al., 2014). This is also in line with soil hydraulic model predictions (Javaux and Carminati, 2021). Rootstock-scion combinations can contribute to the variability of the hydraulic behaviour of same cultivar, due to the intrinsic rooting patterns and hydraulic properties of a rootstock (Coupel-Ledru et al., 2014; Vandeleur et al., 2009). Recent studies emphasize that environmental parameters play a significant role in the transpiration limitation of grapevines, and that the whole soil-rootstock-variety system contribute to the complex hydraulic dynamics across grapevine cultivars (Hochberg et al., 2018; Lavoie-Lamoureux et al., 2017). However, the influence of soil type on grapevine hydraulic dynamics is scarcely documented in the scientific literature (Lovisolo et al., 2016). Xylem embolisms has been extensively studies on grapevine and thought to trigger stomatal closure (Alsina et al., 2007; Choat et al., 2010; McElrone et al., 2012). Yet, recent studies that simultaneously measured stomatal conductance and grapevine water potential showed that grapevine stomata closed at less negative water potentials (< -1 MPa - Albuquerque et al., 2020; Gowdy et al., 2022; Herrera et al., 2022; Morabito et al., 2021) than those at which xylem cavitation was observed in the leaf (< -1.2 MPa - Albuquerque et al., 2020; Hochberg et al., 2017), in the stem (< -1.3 MPa - Alsina et al., 2007; Charrier et al., 2016; Lovisolo et al., 2010; McElrone et al., 2012), and the roots (< -1.8 MPa - Cuneo et al., 2016), suggesting that xylem embolism is not the driving mechanism triggering stomatal closure in grapevines. Influence of soil type on the transpiration limitation of grapevine is still unclear, as belowground of the soil-grapevine system has been less studied than the aboveground part (Ferlito et al., 2020). However, several studies showed the influence of soil type on soil-root interactions and grapevine water status. In a recent metanalysis on different cultivars, Lavoie-Lamoureux et al. (2017) highlighted that for a same variety and for a same leaf water potential, the stomatal conductance and transpiration rate are lower in coarse-textured soils than in fine-textured soils. Tramontini et al. (2013) conducted statistical analysis on grapevine water potentials and gas exchanges and showed the predominance of the soil effect, while cultivar effect was subordinate. Finally, it has been shown that soil texture influences the growth of root system, with deeper but less dense root systems in sandy soils compared to loamy soils for a same rootstock (Nagarajah, 1987; Ollat et al., 2015). This also directly impacts the belowground hydraulic conductance of the soil-grapevine system. Nevertheless, none of these studies quantified the evolution of the aboveground and belowground hydraulics conductances to identify what triggers stomatal closure and limits grapevine transpiration during drought. There is no conclusive experimental evidence indicating that stomatal closure of grapevine is driven by the decline in belowground hydraulic conductances.
The aim of this work is to understand the roles of the belowground (soil and roots) and aboveground (stem) parts of the soil-grapevine system on the transpiration control of in situ grapevine during drought. We hypothesize that transpiration limitation during drought is significantly impacted by the belowground hydraulic properties and is therefore soil-texture specific. For the first time, this hypothesis is tested on grapevine and on in situ plants. We devised an integrative approach to exhaustively characterize the hydraulic response of in situ grapevines, in different soil types, during drought.