Introduction

Fungus-resistant grapevine cultivars, also named “PIWIs” (short form for German “pilzwiderstandsfähige Rebsorten” = fungus-resistant grapevine cultivars), were developed by multiple backcrossing of interspecific hybrids (the cross-breeding of Vitis vinifera L. and North American and Asian Vitis species) with Vitis vinifera (Montaigne et al., 2016; Pedneault and Provost, 2016; Töpfer and Trapp, 2022). The advantage of these new genotypes is to interlink the resistance of most American species to fungal diseases (mainly Erysiphe necator, Plasmopara viticola) while retaining the high fruit quality characteristics for the vinification of Vitis vinifera cultivars (Hofmann et al., 2014; Fischer-Colbrie et al., 2015). In addition to the expediency of fungus resistance, there are economic advantages since the seasonal treatments of plant protection can be decreased and subsequently lead to lower annual doses of pesticides and fuel (Pedneault and Provost, 2016; Pertot et al., 2017). As winegrower's decisions towards sustainable management strongly depend on national and regional regulations (Chen et al., 2022), and the European Commission aims to halve the use of pesticides by 2030 according to the "Farm to Fork" strategy (European Commission, 2020), the demand for robust new cultivars with low susceptibility to pathogens is raising. However, while the screening of resistance against pathogens and pests is part of the breeding and selection program (Reynolds, 2015; Merdinoglu et al., 2018), there is limited information on the agronomic performance of PIWIs in different climates (Casanova-Gascón et al., 2019) and on their response to abiotic stresses (e.g., drought).

Extensive world viticultural regions are located in areas characterised by warm and dry summers, often managed in rainfed conditions, with periods of drought and heatwaves (Moriondo et al., 2013). Moreover, droughts are further forecasted to increase due to climate change (Schultz and Stoll, 2009; Cook et al., 2018), and irrigation may not be sustainable in several regions (Costa et al., 2016; Gambetta et al., 2020). Stomatal regulation is considered a proxy to describe how grapevines respond to drought stress (Medrano et al., 2002; Chaves et al., 2010). Since stomata are responsible for CO₂ intake, their regulation is of great importance in terms of photosynthesis and water use efficiency (Schultz and Stoll, 2009; Medrano et al., 2018). There are biochemical (mainly driven by the plant hormone abscisic acid) and hydraulic mechanisms involved in the stomatal reaction to drought stress which are hard to disentangle (Buckley, 2019; Gambetta et al., 2020). Although V. vinifera cultivars may respond differently to drought, some exhibiting a tighter or a looser stomatal control in response to water deficit (Tombesi et al., 2014; Hochberg et al., 2016; Dayer et al., 2020; Levin et al., 2019), it is not yet clear to what extent such differences result from genetical or environmental factors or the combination of both (Van Leeuwen et al., 2019; Gambetta et al., 2020). Furthermore, to the best of our knowledge, no study has assessed the stomatal regulation of grapevine PIWIs nor compared it against V. vinifera cultivars. In this study, we set out to investigate the response to the drought of three PIWI grape cultivars of commercial importance in Europe, focusing on their stomatal regulation dynamics during soil dehydration.

Materials and methods

3. Irrigation treatments

In season 2020, on July 7th (day of the year DOY 189; after the 80 days of establishment period), two treatments were randomly established in half of the plants (i.e., eight vines per cultivar): (i) water-stressed “ws”, where irrigation drippers were removed from the pots for 13 days; (ii) well-watered controls “ww”, where daily irrigation was maintained to field capacity as before. After 13 days without irrigation (DOY 202), all vines of the ws treatment were manually re-watered to saturation, and thereafter daily irrigation was resumed to the same levels of control. Gas exchange after re-watering was monitored for the successive 10 days (until DOY 212) (Figure 1A).

In season 2021, half of the plants were always maintained under well-watered conditions by daily irrigating the plants just as during the establishment period. The second half of the plants (i.e., 20 vines per cultivar) were exposed to three cycles of drought (water-stressed “ws”; water-stressed plants remained the same throughout all three cycles) by removing the irrigation drippers from the pots for 8 days; after each drought cycle, all vines were re-watered and maintained under “ww” conditions until the next drought cycle. The first ws cycle was imposed on DOY 214 (August 2nd; after 86 days of establishment period) and lasted until DOY 221. The second ws cycle started at DOY 242 until DOY 249, and the third ws cycle occurred from DOY 253 to DOY 260 (Figure 1B).

Figure 1. Experimental set-up of the two trials in 2020 (A) and 2021 (B).

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2020: laterals were removed; 2021: no growth restrictions were imposed. Treatments were applied on half of the plants in both seasons: D, Donauriesling; M, Muscaris; S, Souvignier gris; R, Riesling/G, Grüner Veltliner; ww, well-watered; ws, water-stressed.

Results

1. Vegetative growth

Despite different conditions (experimental set-ups, environmental conditions, rootstocks) within the two experiments, results show connective significances in some vegetative growth parameters (Figure 2, Table 1).

As observed in Figure 2, Muscaris (M) was the cultivar with the largest leaves (average area of single leaves on the main shoot of ca. 150 cm² across seasons), followed by Souvignier gris (S) (ca. 130 cm²) and Donauriesling (D) (ca. 95 cm²). Such differences translated into M recording a higher total leaf area per plant than the other cultivars only in 2020, while in 2021, all cultivars showed similar values of total leaf area per plant (Table 1). In detail, in 2020, before the imposition of drought treatments (DOY 189), the plant leaf area recorded was 3680.3, 2536.9, and 2898.6 cm² vine^-1 in M, S, and D, respectively; after 23 days of experiments (at DOY 212), M, S, and D recorded (average across treatments) 4996.7, 3394.5, and 3896.2 cm² vine^-1, respectively. As expected, drought treatments limited growth in all cultivars that resulted in leaf areas of ws vines being, on average, 15 % smaller than ww ones. Similar growth restriction was observed in 2021 after the three cycles of ws treatments (DOY 261). Statistical interactions of treatment × cultivar were not significant (p > 0.05) in both seasons (Table 1).

Figure 2. Single leaf area (average area of a single leaf on the main shoot) per cultivar in seasons 2020 (A) and 2021 (B).

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Values are averages per cultivar + standard error of the mean (n > 15 and n = 10 in 2020 and 2021, respectively) sampled during the experiments (DOY 189 and DOY 214 in 2020 and 2021, respectively). Different letters identify significant differences between cultivars after a Tukey-HSD post-hoc test (p < 0.05).

Table 1. Leaf area (cm2 vine-1) at the beginning and end of experiments in 2020 and 2021.

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	2020		2021
	DOY 189	DOY 212	DOY 214	DOY 261
Cultivar	***	***	ns	ns
Muscaris	3680.3 a	4996.7 a	3581.2	6486.2
Donauriesling	2536.9 b	3394.5 b	3568.6	5691.8
Souvignier gris	2898.6 b	3896.2 b	3237.4	7120.9
Riesling / G. Veltliner	2658.6 b	4067.0 b	3456.4	6904.7
Treatment		***		*
ww		4359.7		6969.1
ws		3737.0		6132.6
Cultivar × Treatment		ns		ns

Values are the average of four (at the beginning; DOY 189 and 214) and three (at the end; DOY 212 and 261) vines per cultivar and treatment combination. Statistics are reported after one-way ANOVA (DOY 189 and 214) and two-way ANOVA (DOY 212 and 261) with cultivar and irrigation treatment as main factors and its interaction: ***, *, ns, state p < 0.001, p < 0.05, and p > 0.05, respectively. Different letters denote significant differences (p < 0.05) among cultivars after a Tukey-HSD post-hoc test.

2. Water potential and gas exchange

According to our expectations, drought imposition determined a decrease in stem water potential (Ψ_stem), and values recorded for the V. vinifera cultivars were not significantly different from those from the tested PIWI cultivars in both seasons (Figure 3, Supplementary Figure 2). In 2020, it is notable that the average Ψ_stem of Souvignier gris (S) vines recorded significantly higher values as compared to all other cultivars on DOY 189, 196, and 202 after irrigation withholding (Figure 3A). The Ψ_stem of well-watered control vines ranged between –0.32 and –0.57 MPa without significant differences between cultivars (Figure 3C). Starting from equal Ψ_stem values of –0.35 MPa at DOY 189, water-stressed vines of all cultivars showed a decrease in Ψ_stem that reached the lowest values at the peak of drought stress on DOY 202, ranging from –1.10 MPa (in S) to –1.35 MPa (in M) (Supplementary Figure 2). During all three cycles in 2021, drought treatment decreased the average Ψ_stem of all cultivars (Figure 3B). Speaking of statistical significances, in the first cycle, the minimum of Ψ_stem was at –0.62 and –1.07 MPa for averaged ww and ws vines, respectively (Figure 3D); during the second cycle, significant change in the Ψ_stem was only shown in Grüner Veltliner (G) vines (DOY 248) (Supplementary Figure 2 right column), while in the third cycle the Ψ_stem of the ws averages decreased to –0.81 MPa as compared to the –0.58 MPa of the ww vines (Figure 3D).

Figure 3. Midday stem water potential (Ψstem in MPa) in season 2020 (A,C) and 2021 (B,D).

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Vertical lines indicate the imposition of drought (red) and re-watering (blue) treatment. The figures represent a two-way ANOVA analysis with cultivars and treatments as main factors; therefore, values are presented as averages ± standard error per cultivar (A, 2020: n = 6; B, 2021: n = 8) or per treatment (C, 2020: n = 12; D, 2021: n = 16) on each date (DOY, day of the year). Different letters denote significant differences (p < 0.05) between the main factor cultivar (in A and B) or treatment (in C and D). No significant interactions were recorded between main factors at any date of measurement (p > 0.05). D, Donauriesling; M, Muscaris; S, Souvignier gris; R, Riesling/G, Grüner Veltliner; ww, well-watered; ws, water-stressed.

The tested cultivars in our study exhibited differences in stomatal conductance (g_s) both under well-watered conditions and under drought (Figure 4 and Supplementary Figure 3). When under drought, S exhibited higher rates of g_s as compared to the other PIWIs. Particularly in season 2020, S showed a slower stomatal closure than M and D (Figure 4A and Supplementary Figure 3 left column); indeed, while M and D reached values of g_s < 0.05 mol m^-2 s^-1 (considered a severe stress for grapevines according to Medrano et al., 2002) already after three days of irrigation withholding, S reached similar g_s values only after six days without irrigation. In season 2021, during each cycle of drought, S never reached g_s values below 0.05 mol m^-2 s^-1 and had statistically higher g_s values (p < 0.05) than the other cultivars during most of the experimental time (Figure 4B and Supplementary Figure 3 right column). Under well-watered conditions, S recorded the highest maximum stomatal conductance among PIWIs in both seasons (g_{s max} of 0.343 and 0.248 mol m^-2 s^-1 in 2020 and 2021, respectively), surpassed only by R in 2020 (g_{s max} = 0.360 mol m^-2 s^-1) (Supplementary Figure 3). On the other hand, M was consistently the cultivar with the lowest maximum stomatal conductance (g_{s max} of 0.238 and 0.168 mol m^-2 s^-1 in 2020 and 2021, respectively), closely followed by D (g_s of 0.317 and 0.163 mol m^-2 s^-1 in 2020 and 2021, respectively).

Re-watering in 2020 at DOY 203 resulted in stomata reopening of ws plants that did not reach the values of ww controls until DOY 208 (Figure 4C). In 2021, re-watering after the first drought cycle lasted for 20 days, and, even if not monitored, it is assumed that ws vines reached similar g_s values as the ww ones. Indeed, there are no significative differences between ww and ws at the beginning of the second cycle at DOY 242 (Figure 4D); between the second and third cycles of drought, re-watering of two days did not produce a significant effect in g_s (Figure 4D).

Transpiration (E) and net assimilation (A_N) values are presented in Supplementary Figures 4 and 5. Both parameters resembled the stomatal conductance (g_s) behaviour previously described. After a two-way ANOVA analysis with cultivars and treatments as main factors, the results showed that the averaged transpiration rates (E) of M and D decreased faster and reached lower values than S shortly after the drought imposition in both seasons. For example in season 2020, values of E in M and D were significantly lower than in S already at DOY 190 (one day after irrigation withholding) (M = 3.15, D = 3.39 and S = 4.59 mol m-2 s-1; Supplementary Figure 4A). Similarly, in 2021 at DOY 217 (three days after irrigation withholding) E values of M and D were as well statistically lower than S (M = 1.33, D = 1.72 and S = 2.03 mmol m^-2 s^-1; Supplementary Figure 4B).

Drought stress resulted in lower assimilation rates (A_N), especially in season 2020, where averaged A_N values in ws plants were below 7 μmol m^-2s^-1 at all dates after drought imposition (Supplementary Figure 5C). The statistical analysis of different PIWI cultivars during drought showed higher A_N values in S as compared to D and M (e.g., averaged A_N in season 2020 at DOY 194: S = 7.71, D = 5.64 and M = 5.05 μmol m^-2s^-1; Supplementary Figure 5A), despite in season 2021 fewer differences in cultivars were apparent (Supplementary Figure 5B).

Figure 4. Stomatal conductance (gs in mol m-2 s-1) measured in 2020 (A,C) and 2021 (B,D).

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Vertical lines indicate the imposition of drought (red) and re-watering (blue) treatment. The figures represent a two-way ANOVA analysis with cultivars and treatments as main factors; therefore, values are presented as averages ± standard error per cultivar (A, 2020: n = 6; B, 2021: n = 8) or per treatment (C, 2020: n = 12; D, 2021: n = 16) on each date (DOY, day of the year). No interaction between main factors was observed for almost any date of observation. In the figure, different letters denote significant differences (p < 0.05) between the main factor cultivar (A, B) or treatment (C, D); eventual significant interactions are represented with an asterisk (*) between the main factors cultivar and treatment (p < 0.05): No differences among cultivars were recorded within the ws treatment, but within the ww treatment Souvignier gris and Riesling were significantly higher than Donauriesling and Muscaris. D, Donauriesling; M, Muscaris; S, Souvignier gris; R, Riesling/G, Grüner Veltliner; ww, well-watered; ws, water-stressed.

Discussion

The results obtained in this study allowed the comparison of the water use and response to drought of three commercial PIWI cultivars. We found that Souvignier gris (S) recorded the highest maximum stomatal conductance (g_{s max}) values among the PIWI cultivars tested (Figure 4), and it was also the one with the lowest (most negative) turgor loss point (Ψ_tlp) and osmotic potential at full turgor (π₁₀₀) as compared to Muscaris (M) and Donauriesling (D) (Table 2). Dayer et al. (2020) showed that these leaf traits (g_{s max},Ψ_tlp, π₁₀₀) are coordinated within grapevine cultivars in a way that when maximum water use (represented in our case with g_{s max}) increases, leaf hydraulic traits allow the leaf to operate across a wider range of water potentials (i.e., by exhibiting a more negative Ψ_tlp and π₁₀₀). In our case, this may signify that S would provide increased resilience against drought events. However, under the experimental conditions in our study, S did not reach lower water potentials than M and D despite maintaining higher stomatal conductance (and thus a consequent faster soil water depletion), highlighting the difficulty of inferring plant behaviour from single leaf measurements as other factors also play an important role such as the canopy size and the variability among leaves. For instance, in 2020, M was the cultivar with the lowest g_{s max} but also the one with the largest canopy (and therefore a bigger evaporative surface as compared to S), a combination of factors that could explain a faster depletion of soil water, in turn resulting in a lower midday water potential than S. Furthermore, despite the differences observed among cultivars when plotting g_s or Ψ_stem against time, our data showed that the water potential ranges for stomatal closure did not differ among cultivar as all of them reached g_s < 0.05 mol m^-2 s^-1 between Ψ_stem of –0.8 and –0.9 MPa (Figure 5); such results are comparable to what is reported in similar studies on potted grapevine cultivars such as Merlot (Hochberg et al., 2016), Grenache and Syrah (Dayer et al., 2020), or Montepulciano (Tombesi et al., 2014). Therefore, the different drought stress degrees experienced by the PIWI cultivars in our study were more related to the different dynamics of water use by transpiration (and thus the time needed to deplete the soil water reservoir and reach the critical Ψ_stem for stomatal closure) than to an intrinsic difference in their stomatal sensitivity to drought.

Figure 5. Relationship between stem water potential (Ψstem in MPa) and stomatal conductance (gs in mol m-2 s-1) during the entire experiment in seasons 2020 (A) and 2021 (B).

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D, Donauriesling; M, Muscaris; S, Souvignier gris; R, Riesling/G, Grüner Veltliner.

A closer look at the cultivar's gas exchange under well-watered conditions provides a useful picture of their water use behaviour. As shown in Supplementary Figure 6, differences in g_s between cultivars existed only at Ψ_stem > –0.75 MPa, with S, exhibiting higher stomatal conductance than M and D. In particular, M was the most conservative cultivar among the PIWIs studied in terms of stomatal conductance (i.e., M recorded g_{s max} values that were lower by 30 % than the values measured for S) and transpiration. Our results suggest that M and D might be more suitable for non-irrigated conditions than S as they would deplete the soil water reservoir slower, while S, by maintaining higher transpiration rates longer, could face more intense drought stress situations and, therefore, some irrigation strategy would be needed, consistent with the idea of a “stress distance” introduced by Gambetta et al. (2020).

Interestingly, from the A_N ~ g_s relationship (Figure 6), it is worth noting that M consistently showed lower A_N values than the other PIWIs at g_s > 0.15 mol m^-2 s^-1, while D and S recorded largely similar A_N rates across a wide range of g_s values. The A_N ~ g_s curve (Figure 6) showed a plateau at maximum assimilation rates of 14 μmol m^-2 s^-1 for S and D (consistent with values frequently reported in grapevines; Medrano et al., 2002; Bota et al., 2005; Bota et al., 2016), while M reached an assimilation rate plateau between 10 to 12 μmol m^-2 s^-1, suggesting a lower intrinsic water use efficiency (WUEi) at the leaf level and under well-watered conditions for M as compared to S and D leaves. However, as discussed before, M presented larger leaves and a bigger canopy than the other cultivars, a fact that could compensate for a lower WUEi. It remains difficult to upscale single-leaf WUEi to whole-plant WUE (Medrano et al., 2015; Tomás et al., 2014), and more studies are needed to further explore this trait, including yield components and total biomass production.

Figure 6. Relationship between stomatal conductance (gs in mol m-2 s-1) and net assimilation rate (AN in μmol m-2 s-1) during the entire experiment in seasons 2020 (A) and 2021 (B).

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Data were fit using a LOESS function. Shadows represent the confidence interval. D, Donauriesling; M, Muscaris; S, Souvignier gris; R, Riesling / G, Grüner Veltliner.

The results of this study provide important hints on the water relations of three PIWI cultivars, but we cannot exclude that under natural settings, the plant response to drought would differ from what was observed in young potted vines. Firstly, the stomatal closure thresholds would be different since, as suggested by Sorek et al. (2021) and Herrera et al. (2022), a seasonal osmotic adjustment in the leaves of grapevines can shift their sensitivity to drought towards lower (more negative) water potentials. In this regard, an open question remains whether different grapevine genotypes can osmotically adjust at different rates, perhaps contributing at least in part to the differences in stomata sensitivity to drought among grapevine cultivars often reported in the literature (Lavoie-Lamoureux et al., 2017). Secondly, under field conditions, a large soil root explored volume (as normally observed in vineyards) would result in a longer time needed to dehydrate the soil (Gambetta et al., 2020). Both factors combined would mean more time for the plants to react and acclimate to water deficit conditions (Hochberg et al., 2017), an aspect still poorly explored in general for grapevines and even more in PIWIs. Finally, we shall not forget that important research questions concerning the impact of drought on the yield and fruit composition of PIWIs are to be approached to have a complete picture and be able to provide viticulturists and oenologists with the necessary information to manage PIWIs under dryer climatic conditions.

Conclusion

Taken together, the results of this study showed more conservative water use (i.e., lower maximum stomatal conductance values) of Donauriesling (D) and Muscaris (M) as compared to Souvignier gris (S) under no water limitations. Under mild-drought conditions, S maintained higher rates of gas exchange compared to D and M, but such differences vanished with the intensification of drought. While several important points are still to be studied (grape berry composition), we stress that our experiment produced similar results under greenhouse and semi-controlled field conditions and, therefore, under highly heterogeneous environments. Therefore, the study outputs might be generalised towards a hypothesis-driven validation at the field level to fully address best water management practices for PIWI vineyards.

Acknowledgments

This work was performed with the financial support of the Österreichische Hagelversicherung (Josef Pleil Forschungspreis Preis 2020). The authors thank Rudi Rizzoli, Francesco Flagellato and Johanna Moser for their support in plant management and data acquisition, Rebschule Backknecht for providing the plant material in season 2021.

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