Introduction

Most of the world's non-irrigated vineyards may experience seasonal drought with a negative impact on vine vigour and yield potential depending on intensity, duration and rate of water deficit progression (Medrano et al., 2002; Costa et al., 2007; Chaves et al., 2010). It is well known that stomatal closure and consequent decline in photosynthesis due to restriction on CO₂ diffusion are among the earliest physiological processes driven by water deficit. Field-grown grapevine is considered drought resistant due to a large and deep root system associated with physiological drought avoidance mechanisms, such as efficient stomatal control of transpiration, xylem embolism and osmoregulation capacity (Chaves et al., 2010; Simonneau et al., 2017). Moreover, alterations in leaf area, root/shoot ratio, xylem vessel size and hydraulic conductivity have also been revealed as adaptive strategies by grapevine cultivars under low soil water availability (Gómez-del-Campo et al., 2003; Lovisolo et al., 2010; Gerzon et al., 2015; Dayer et al., 2017; Zufferey et al., 2017).

Considering that most vineyards worldwide are grafted mainly to cope with Phylloxera and also the possibility of water scarcity in the near future in some regions due to global warming (IPCC, 2008), the interest in drought tolerance induced by rootstocks has increased in viticulture (Serra et al., 2014; Ollat et al., 2016). This interest is supported by the fact that phenology, shoot growth, biomass accumulation and repartition, yield and grape quality of scion can be modified by rootstock genotype (Keller 2010; Kidman et al., 2013; Souza et al., 2015; Dias et al., 2017). Under low soil moisture, grapevine rootstock may affect scion growth and drought responses by controlling and adjusting the water supply to shoot transpiration demand through stomatal control, hydraulic conductivity and capacity of water extraction from the soil (Soar et al., 2006a; Soar et al., 2006b; Alsina et al., 2011; Tramontini et al., 2013). Therefore, rootstock selection could become an important tool for mitigating water deficit.

Although rootstock classifications based on drought tolerance exist and evidence for the contribution of rootstock to the genetic variability of water use efficiency has been reported (Carbonneau, 1985; Marguerit et al., 2012; Lovisolo et al., 2016, Ollat et al., 2016), field observations do not always confirm published classification, when based on potted experiments (Bauerle et al., 2008; Stevens et al., 2010; Chaves et al., 2016). This fact could be attributed to scion effects and the influence of soil type on root distribution (Smart et al., 2006; Tandonnet et al., 2010). The depth and distribution of the grapevine root system may vary according to the soil texture, water and nitrogen availability, soil salinity, vine spacing and climatic conditions (Smart et al., 2006; Koundouras et al., 2008). During periods of water deficit, high vigour and drought-resistant rootstocks may induce deep root production during the hot and dry summer (Alsina et al., 2011) or enhance root growth in more humid soil zone favouring water supply to the scion (Bauerle et al., 2008). On the other hand, Tramontini et al. (2013) showed that grapevine water deficit responses are not only dependent on the rootstock but also influenced by stomatal control of the scion cultivar.

The stem xylem tissue development can also be affected by the rootstock. Santarosa et al. (2016) showed that during the first growth cycle, the vegetative growth of Merlot and Cabernet Sauvignon grafted onto three different rootstocks was associated with a larger proportion of stem xylem vessels with greater mean diameters. Several authors have also shown that an increased vegetative vigour was linked to high hydraulic conductance induced by vigorous rootstocks in apple (Atkinson et al., 2003) and cherry (Gonçalves et al., 2005; Zoric´ et al., 2012) because of larger xylem vessels. If confirmed, the anatomical differences induced by rootstock in the stem xylem of the scion might improve water uptake and transport capacity.

The effects of rootstock on hydraulic conductivity and xylem vessel size of grapevine under water deficit remain unclear. This study reports how rootstocks differing in their effect on scion vigour, as previously reported by Spring et al. (2016) on the same experimental vineyard, affect gas exchanges, water relations, petiole hydraulic conductivity, xylem anatomy, yield and grape composition of field-grown Pinot noir under water deficit conditions. It provides a preliminary dissection of the main grapevine responses to water deficit in interaction with rootstock genotypes and feeds our understanding of the major mechanisms involved. Furthermore, it provides preliminary data about scion-rootstock interactions under cool climate viticulture, as most published experiments were carried out under warmer or potted conditions.

Materials and methods

Results

This study was conducted in 2017, a year considered warmer than the long-term records of temperature. The average monthly mean temperatures (Tmean) and amount of rainfall during the 2017 growing season were, respectively, 2.6 ºC and 21 mm higher than long-term averages (Table 1). The highest Tmean (around 22 ºC) were recorded from the fruit set (June) to the ripening stage (July–August), the period under higher rainfall (189 mm) as compared with values recorded from March to May (127 mm).

The water status of field-grown Pinot noir was significantly influenced by rootstocks, as shown by predawn (Ψ_pd) and stem (Ψ_stem) water potential measured throughout the season (Figure 1). Over the season, Ψ_pd of vines grafted onto Kober 5BB and 3309C was statistically higher mainly compared to values of Ψ_pd induced by 41B MGt and 101-14MGt rootstocks (Figure 1A) (Supplementary Table 1). The Ψ_pd decreased from –0.2 to –0.7 MPa for vines grafted on 41B MGt and 101-14MGt, whereas the highest values (around –0.4 MPa) were recorded for Kober 5BB and 3309C at the end of the season (247 DOY, Figure 1A). For the last three dates of measurement, Ψ_pd of vines grafted onto Riparia Gloire did not show significant differences when compared to 3309C and it was significantly higher than 101-14MGt and 41B MGt and lower than Kober 5BB (Supplementary Table 1). Similarly to Ψ_pd, Ψ_stem was also significantly higher in vines grafted onto Kober 5BB and 3309C compared to 41B MGt and 101-14MGt (Figure 1B) (Supplementary Table 2). At the end of the season (last two weeks), the rootstocks were discriminated into three different significant groups: 41B MGt induced the lowest Ψ_stem (around –1.4 MPa), whereas the highest Ψ_stem values were recorded for Kober 5BB and 3309C (around –1.0 MPa) and the intermediate values for 101-14MGt and Riparia Gloire (around –1.20 MPa) (Supplementary Table 2).

Figure 1. Seasonal pre-dawn water potential (A, Ψpd) and stem water potential (B, Ψstem) of field-grown Pinot noir grafted onto different rootstocks.

Save View full size Expand inline Collapse inline

Values are means ± standard error (n = 6). The asterisks show significant differences among treatments at p < 0.05 by Fisher’s LSD test.

Based on the values of the cumulative integral of predawn leaf water potential (S_Ψ, MPa d^-1), rootstocks could be significantly separated into three water deficit levels (table 2). The lowest water deficit intensity was recorded for 3309C and Kober 5BB (6.8 MPa d^-1), the intermediate level for Riparia Gloire (13.4 MPa d^-1), whereas the highest water deficit intensity (16.5 MPa d^-1) was observed for vines grafted onto 101-14 MGt and 41B MGt.

During most days, photosynthesis (A), stomatal conductance (gs), transpiration (E) and intrinsic water use efficiency (A/gs) did not differ among rootstocks measured in both times (Figure 2) (Supplementary Tables 3, 4, 5 and 6). During the morning, A was significantly lower in vines grafted onto 41B MGt, 101-14 MGt and Riparia Gloire at 240 DOY only, whereas vines grafted onto 3309C and Kober 5BB showed higher A than other rootstocks at 233 and 240 DOY, during the afternoon (Figure 2A, E) (Supplementary Table 3). Vines grafted onto 41B MGt exhibited, during the afternoon, the largest A reduction at 225, 233 and 240 DOY mainly when compared to 3309C and Kober 5BB, but there were no significant differences among 41B MGt, 101-14 MGt and Riparia Gloire at 240 DOY. During the morning, gs was also significantly reduced for 41B MGt at 213, 225 and 240 DOY when compared to 3309C and Kober 5BB, but there were no significant differences when compared to 101-14 MGt and Riparia Gloire at 213 and 240 DOY (Figure 2B) (Supplementary Table 4). During the afternoon, at 225, 233 and 240 DOY, the largest differences in gs were observed between vines grafted onto 41B MGt and 3309C, whereas at 240 DOY, Kober 5BB and 3309C induced higher gs than other rootstocks (Figure 2F). Vines grafted onto 41B MGt, 101-14 MGt induced lower E than Kober 5BB and 3309C only at 240 DOY during the morning, whereas Riparia Gloire was statistically different only when compared to Kober 5BB (Figure 2C). During the afternoon, Kober 5BB and 3309C induced the highest E mainly when compared to 41B MGt at 233 and 240 DOY, but E was significantly higher in vines grafted onto Kober 5BB and 3309C at 240 DOY (Figure 2G) (Supplementary Table 5). In general, the largest differences in A/gs were recorded between 41B MGt and 3309C (at 213, 225, 233 and 240DOY) during the morning (Figure 2D) (Supplementary Table 6). During the afternoon, 41B MGt induced the highest A/gs mainly when compared to 3309C and 101-14 MGt (Figure 2H). At harvest (on 247 DOY), there were no statistical differences among rootstocks for gas exchange variables.

Figure 2. Seasonal trends of photosynthesis (A), stomatal conductance (gs), transpiration (E) and intrinsic water use efficiency (A/gs) of field-grown Pinot noir grafted onto different rootstocks during the morning (A,B,C,D) and afternoon (E,F,G,H).

Save View full size Expand inline Collapse inline

Values are means ± standard error (n = 6). The asterisks show significant differences among treatments at p < 0.05 by Fisher’s LSD test.

Gs was significantly correlated with leaf water pressure deficit (VPDL) and Ψ_pd for every individual rootstock (except for Kober 5BB) (Figure 3A, B). However, there are no significant differences among rootstocks slopes (t_exp < t_tab) (Supplementary Table 7), indicating that stomatal sensitivity to VPDL and Ψ_pd were not influenced by rootstock genotype.

Figure 3. Rootstock effects on stomatal conductance response (gs) of Pinot noir to leaf to air vapour pressure deficit (VPDL) (A) and to predawn leaf water potential (Ψpd) (B).

Save View full size Expand inline Collapse inline

Equations of liner regression of rootstocks are shown in each panel (n = 6).

Seasonal water deficit progression did not influence the petiole specific hydraulic conductivity (K_petiole) for any grafting combinations and no interaction with the rootstocks could be observed (Table 2). The lowest K_petiole was observed for vines grafted onto 41B MGt (5.3 mmol m^-2 s^-1 MPa^-1), the intermediate values for 101-14 MGt and Riparia Gloire (7.9 mmol m^-2 s^-1 MPa^-1) and the highest for 3309C and Kober 5BB (12.6 mmol m^-2 s^-1 MPa^-1) (Table 2).

The chlorophyll index was significantly lower in vines grafted on 41B MGt during most of the season, whereas there were no significant differences among other rootstocks (Figure 4). Although the vines grafted onto 3309C and Kober 5BB displays the highest shoot weight, the differences were only significant between vines grafted on Riparia Gloire and Kober 5BB and between 41BMGt on one side and 3309C and 5BB on the other side (Table 3). The highest yield (0.9 kg m^-2) was recorded for vines grafted onto Kober 5BB compared to the other rootstock combinations (0.7 kg m^-2). The lowest malic acid content and yeast available nitrogen (YAN) were observed in grapes from vines grafted onto 41B MGt (Table 3). There were no significant differences in sugars, total acidity and tartaric acid among rootstock combinations (Table 3).

Figure 4. Chlorophyll index (N tester) in leaves of field-grown Pinot noir grafted onto different rootstocks.

Save View full size Expand inline Collapse inline

Values are means ± standard error (n = 90).

Carbon isotope composition (δ¹³C) measured on sugars in must at ripeness ranged from –24.81‰ for vines grafted onto 3309C to –23.28‰ for vines grafted onto 41B MGt (Table 2). The differences were not statistically significant (P = 0.19).

The anatomical analyses revealed that most xylem vessels had a cross-sectional area lower than 1000 µm², both stems and petioles (Tables 4 and 5). Petioles of Pinot noir grafted onto 41B MGt had the highest proportion of vessels with a cross-sectional area smaller than 500 µm² and the lowest proportion with a cross-sectional area higher than 1001 µm² (Table 4).

For most category sizes, there was no difference among 101-14 MGt, Riparia Gloire, Kober 5BB and 3309C. In the category size above 2500 µm², most differences were observed between vines grafted onto 41B MGt and Kober 5BB, but for a very low frequency.

Stems of vines grafted onto Riparia Gloire and 3309C were characterised by the highest and lowest frequency of small vessels (200–500 µm²), respectively, whereas there was no significant difference for the other rootstocks (Table 5). The highest frequency of vessels number with a cross-section area higher than 10,000 µm² was observed for vines grafted onto 3309C and Kober 5BB compared to 41B MGt and Riparia Gloire. There was no similar pattern among rootstocks between smaller (200–500 µm²) and larger stem vessels (>10,000 µm²) (Table 5).

An inverse correlation was found between S_Ψ and K_petiole while shoot weight, petiole vessel size higher than 2000 µm² and stem vessel sizes higher than 10,000 µm² seemed not to be affected by S_Ψ (Table 6). On the other hand, increased shoot weight and petiole vessel size higher than 2000 µm² were associated with increased K_petiole. A/gs measured at harvest was also significantly correlated with δ¹³C (Table 6).

Discussion

The use of drought-tolerant rootstocks has been considered a low-cost adaptive strategy to cope with the decrease in soil water availability in viticultural areas predicted under the context of global change (Fraga et al., 2013; van Leeuwen and Darriet, 2016). This study reports data recorded during one season regarding rootstock genotype effects on ecophysiological and agronomical responses to water deficit of field-grown Pinot noir under cool climatic conditions and how these effects could be related to vigour. In comparison to references, rainfalls were slightly higher during the spring and summer of 2017, but both seasons were considered the third warmest ones since records began in 1864 (MétéoSuisse database). This higher mean temperature recorded during the 2017 growing season associated with the water shortage imposed by soil coverage of the experimental plot with waterproof plastic, equivalent to the year 2009 situation (Spring et al., 2016), contributed to simulating stressful climatic projections for a non-irrigated and well-established vineyard.

Studies regarding scion-rootstocks interactions under water deficit in cool-climate countries have not been well explored as most published data have been carried out under very hot and dry summer conditions such as usually recorded in the Mediterranean (Koundouras et al., 2008; Romero et al., 2018) and Australian (Soar et al., 2006a; Stevens et al., 2010) vineyards. Moreover, most of these studies were carried out in deficit-irrigated vineyards. Our findings showed that, in a non-irrigated vineyard of a cool country such as Switzerland, invigorating rootstocks favoured the water supply to the scion and it was associated with some features such as increased xylem hydraulic conductivity, high nitrogen uptake and probably also due to larger root system.

The soil coverage used in this experiment promoted a progressive water deficit throughout the growing season, as revealed by the reduction in Ψ_pd and Ψ_stem. According to the literature, the water deficit intensity observed during the ripening period was classified from weak to moderate (Ψ_pd = –0.3 to –0.5 MPa; Ψ_stem= –0.9 to –1.1) and severe (Ψ_pd < –0.6 MPa; Ψ_stem=< –1.4 MPa) depending on rootstocks and physiological indicators of vine water status (Deloire et al., 2004; van Leeuwen et al., 2009). Based on Ψ_stem values, water deficit could be classified as severe for vines grafted onto 41B MGt, moderate for vines grafted onto 101-14 MGt and Riparia Gloire and weak for vines grafted onto 3309C and Kober 5BB. Based on Ψ_pd values, only two levels of water deficit could be defined with severe water deficit for 101-14 MGt and 41B MGt (Ψ_pd < –0.6 MPa) and mild (–0.3 to –0.5 MPa) for Riparia Gloire, Kober 5BB and 3309C, confirming that Ψ_stem is a more sensitive indicator of water status than Ψ_pd (Choné et al., 2001; Patakas et al., 2005; Souza et al., 2009). S_Ψ was shown to be a useful parameter for estimating and integrating water stress in different crops (Meyers, 1988), including grapevine (Souza et al., 2005a). Indeed in this study, S_Ψ followed similar patterns as Ψ_stem values for the different rootstock combinations. The S_Ψ values of Pinot noir grafted onto 3309C and Kober 5BB were similar to values found for Moscatel and Castelão cultivars under full irrigated conditions (100%ETc) in a Mediterranean vineyard during the driest year, while 41B MGt and 101-14MGt induced values near to deficit irrigated Castelão (50%ETc) as shown by Souza et al. (2005a). These results indicate that Pinot noir, even under a non-irrigated vineyard in a cool climate region, expressed a lower intensity of water stress than other field-grown cultivars under warmer and drier conditions.

Rootstocks had a more pronounced impact on vine water status than on the gas exchange of Pinot noir. The differences among rootstocks for gas exchange traits were hardly significant, except during the last weeks of the ripening period depending on variables and time of measurements. In general, at later stages of ripening, Kober 5BB and 3309C exhibited higher A, gs and E, mainly as compared to 41B MGt during the afternoon. A, gs and E decreased for all rootstocks from the onset (166DOY) to the last date of measurements (247DOY), with a more pronounced decrease before the 210DOY when Ψ_pd values were still above –0.4 MPa and Ψ_stem above –1.0 MPa. Nevertheless, differences among rootstocks appeared to be more pronounced afterwards when Ψ_pd and Ψ_stem further decreased. Grapevines have been considered resistant to drought mainly due to the early and efficient stomatal control to regulate water losses during mild to moderate water stress (Chaves et al., 2010). Even under water deficit characterised as severe (Ψ_pd = –0.7 MPa) (240 and 247 DOY), the values of mid-morning gs were lower than 0.10 mol m^-2 s^-1 in vines grafted onto 41B MGt and 101-14 MGt only at 240DOY due to the higher VPDL (2.3 kPa). However, at 247 DOY, all rootstocks induced values of mid-morning gs higher than 0.10 mol m^-2 s^-1 when VPDL was lower (1.8 kPa), indicating still active gas exchanges and the absence of metabolic limitations of photosynthesis as previously suggested (Medrano et al., 2002).

Gs was significantly correlated with Ψ_pd (excepted for Kober 5BB) and with VPDL, suggesting control by both the soil water status (dependent on the rootstocks) and the evaporative demand of the atmosphere (independent of the rootstock) (Davies et al., 2002; Chaves et al., 2016). However, the relationships of gs versus VPDL and Ψ_pd suggested a similar stomatal response among rootstocks, even though it was previously shown that the sensitivity of gs to VPDL and Ψ_pd could be affected by the scion cultivar and rootstock (Soar et al., 2006a,b; Tramontini et al., 2013). In our study, in some few days, A, gs and E were higher for the more vigorous vines (higher stem weight) grafted on 3309C and Kober5BB, in agreement with the observations of Soar et al. (2006a), who reported, in an irrigated vineyard, that the most vigorous rootstocks such as Teleki 5C and Ramsey induced the highest gs in Syrah. According to these authors, rootstock effects on canopy gas exchange would be initially driven by differences in root capacity to extract soil water, mediated via dynamic variation in physiological-active leaf abscisic acid (ABA).

Along the water deficit progression, an increase in intrinsic water use efficiency (A/gs) was reported for all rootstocks, agreeing with previous authors (Souza et al., 2005a; Chaves et al., 2016; Zufferey et al., 2017). Leaf ageing along the growing season could also affect A/gs. The highest A/gs has been observed in vines grafted onto 41B MGt, mainly due to the lowest stomatal conductance induced by this rootstock during the days where significant differences among rootstocks were found. In contrast to gas exchange techniques that provide measurements of photosynthesis rates at a single point in time, δ¹³C measured on must integrate the ratio of net photosynthesis to water transpired over the growing season. It has been shown to be a useful tool for evaluating vine water use efficiency over the ripening period (Gaudillère et al., 2002; Souza et al., 2005a; Zufferey et al., 2017). Although δ¹³C was correlated with mid-morning A/gs measured at harvest, the rootstocks could not be discriminated by δ¹³C, probably due to the small range of δ¹³C values among rootstocks (van Leeuwen et al., 2009). It could also be related to a short period of water deficit and small differences in the level of water stress intensity among rootstocks, while in other studies, the authors found larger differences in vine water status among water treatments (Souza et al., 2005a; Zufferey et al., 2017).

A pronounced effect of rootstock on K_petiole of Pinot noir leaves was observed. The seasonal average of K_petiole was closely correlated with S_Ψ, petiole xylem vessel frequency higher than 2000 µm² and shoot weight, suggesting a link between petiole hydraulic conductivity, petiole xylem anatomy, stem vigour and water status. K_petiole was high for Kober 5BB and 3309C as compared to other rootstocks. 101-14 MGt was characterised by a higher K_petiole and a greater frequency of xylem vessels with a larger cross sectional area in the petiole than 41B MGt. It was previously shown that petiole specific hydraulic conductivity (K_petiole) of grapevine cultivars could be affected by vine water status (Zufferey et al., 2017; Dayer et al., 2017) and our data show that it can also be affected by rootstock genotype, probably in a relationship with conferred vigour.

Shoot vigour was significantly correlated with the frequency of the largest vessels in the stem. It supports the findings reported by Santarosa et al. (2016) for grapevine and by Gonçalves et al. (2005) for sweet cherries, which show that vigorous rootstocks affect the size of scion xylem vessels. Atkinson et al. (2003) also reported that the stem hydraulic conductivity of grafted apple trees was increased by invigorating rootstock in relation to xylem anatomical changes. In peach, xylem vessel characteristics of the dwarfing rootstock genotypes appear to influence tree growth directly rather than through an effect on the xylem vessel size of the scion (Tombesi et al., 2010).

Although the negative relationship between shoot weight and S_Ψ was not significant, drought responses of field-grown Pinot noir appeared to vary according to differences in shoot vigour induced by rootstock over the growing season. Vines grafted onto high vigorous rootstocks (3309C and Kober 5BB) were characterised by higher Ψ_pd and Ψ_stem compared to 41B MGt, Riparia Gloire and 101-14 MGt, which induced a lower shoot weight and more negative Ψ_pd and Ψ_stem. These observations agree with those of Souza et al. (2009), who showed that vigorous rootstocks promoted water status and vegetative vigour of Syrah vines. They also agree with the results reported by Spring et al. (2016) under rainfed conditions, suggesting that rootstocks conferring a high vegetative vigour appear to limit the appearance of water deficit in vineyards.

The lowest shoot vigour measured in vines grafted onto 41B MGt was probably not explained by water deficit as the largest water status differences on Ψ_pd appeared only after the 2 August once shoot growth was largely completed and because of the absence of correlation between S_Ψ and shoot vigour. The absence of a relationship between S_Ψ and frequency of vessel sizes larger than 2000 µm² in petiole and larger than 10,000 µm² in stem also suggests that vascular anatomy was not affected by water deficit but most probably related to differences of vigour promoted by rootstocks. The reduced stem xylem vessel size observed for the less vigorous vines can decrease the shoot hydraulic conductivity and the efficiency of the water flux in vine shoots under a soil water restriction, as demonstrated by Pagay et al. (2016).

The lowest chlorophyll index values measured in vines grafted onto 41B MGt at the beginning of the season, under not-yet limiting water conditions, indicate that shoot vigour was also reduced due to low nitrogen uptake rather than water limitation. This is also in agreement with the lower yeast assimilable nitrogen of grape must observed for this rootstock. It is well known that nitrogen is one of the most important nutrients for vegetative development because it is a component of proteins, enzymes, chlorophyll and nucleic acids (Taiz and Zeiger, 2004) and, therefore, under low N supply, vine shoot growth can be compromised (Keller, 2010; van Leeuwen et al., 2018). As root system development is correlated with vegetative vigour (Southey and Archer, 1988), it may be hypothesised that a reduced root system development for the vines grafted onto 41MGt may have impaired both nitrogen and water uptake. In addition, the negative effect of water deficit on nitrogen uptake and content in leaves and berries could have further limited YAN content in grape must of vines grafted onto 41B MGt (Spring et al., 2012; Zufferey et al., 2017). Low vigour may also explain the lowest malic acid content for this combination, probably due to an increased berry exposure to sunlight, favouring malic acid degradation by rising in temperature as shown by other authors (Souza et al., 2005b; Santos et al., 2007; Zufferey et al., 2017). A direct effect of drought level on malic acid content has also been reported occasionally (Kizildeniz et al., 2018).

There is no accordance in the literature regarding the degree of drought tolerance among these five rootstocks ranging from low to highly drought-sensitive depending on scions and experimental conditions (Serra et al., 2014; Ollat et al., 2016; Spring et al., 2016). Under semi-arid conditions, Romero et al. (2018) reported that Monastrell vines grafted onto 41B MGt exhibited a lower vigour and yield than vines grafted onto 1103P, without any differences in vine water status. It was also shown that Sultana vines grafted onto 41B MGt grown in pots showed a reduced root system development and shoot biomass in comparison to vines grafted onto Kober 5BB (Yıldırım et al., 2018). Our field study brings additional data to show that of the responses to water restriction of Pinot noir vines were affected by the vigour conferred by rootstocks. Although 41B MGt was supposed to be the most lime tolerant rootstock among the five studied, it did not perform well in these alkaline conditions. Kober 5BB and 3309 provided the slowest water deficit progression throughout the growing season, probably due to a better water supply supported by a larger and deeper root system. From a practical point of view, our one-year data contribute to support that the use of vigorous rootstocks could avoid the need for supplemental irrigation in vineyards during the periods of water scarcity. Nevertheless, experiments should be replicated to identify the most relevant traits to characterise drought responses induced by different rootstocks under field conditions to be used in breeding programs for a cool climate region.

Acknowledgements

This study was supported by the Agroscope Research Institute to develop technical practices for sustainable resources and balanced grapevine nutrition (project number 18.02.15.6.02) Souza, C.R. thanks to Minas Gerais State Foundation for Research Support (FAPEMIG) for granting the postdoctoral fellowship. The authors are grateful to Cyril Toche and Nicolas Leclerq for ecophysiological analysis support in the vineyard, to Francine Laprand for anatomical analyses in the laboratory and to Dr Carlos Gava for assistance with statistical analyses.

References

• Alsina, M. M., Smart, D. R., Bauerle, T., de Herralde, F., Biel, C., Stockert, C., Negron, C., & Save, R. (2011). Seasonal changes of whole root system conductance by a drought-tolerant grape root system. Journal of Experimental Botany, 62(1), 99-109. https://doi.org/10.1093/jxb/erq247
• Andrade, J. M., & Estévez-Pérez, M. G. (2014). Statistical comparison of the slopes of two regression lines: A tutorial. Analytica Chimica. Acta, 838, 1-12. https://doi.org/10.1016/j.aca.2014.04.057
• Atkinson, C. J., Else, M. A., Taylor, L., & Dover, C. J. (2003). Root and stem hydraulic conductivity as determinants of growth potential in grafted trees of apple (Malus pumila Mill.). Journal of Experimental Botany, 54(385), 1221-1229. https://doi.org/10.1111/j.1469-8137.2008.02489.x
• Bauerle, T. L., Smart, D. R., Bauerle, W. L., Stockert, C., & Eissenstat, D. M. (2008). Root foraging in response to heterogeneous soil moisture in two grapevines that differ in potential growth rate. The New Phytologist, 179(3), 857-866. https://doi.org/10.1111/j.1469-8137.2008.02489.x
• Carbonneau, A. (1985). The early selection of grapevine rootstocks for resistance to drought conditions. American Journal of Enology and Viticulture, 36(3), 195–198.
• Chaves, M. M., Zarrouk, O., Francisco, R., Costa, J. M., Santos, T., Regalado, A. P., Rodrigues, M. L., & Lopes, C. M. (2010). Grapevine under deficit irrigation: hints from physiological and molecular data. Annals of Botany, 105(5), 661-676. https://doi.org/10.1093/aob/mcq030
• Chaves, M. M., Costa, J. M., Zarrouk, O., Pinheiro, C., Lopes, C. M., & Pereira, J. S. (2016). Controlling stomatal aperture in semiarid regions - The dilemma of saving water or being cool? Plant Science, 251(special issue), 54-64. https://doi.org/10.1016/j.plantsci.2016.06.015
• Choné, X., van Leeuwen, C., Dubourdieu, D., & Gaudillère, J. P. (2001). Stem water potential is a sensitive indicator of grapevine water status. Annals of Botany, 87(4), 477-483. https://doi.org/10.1006/anbo.2000.1361
• Costa, J. M., Ortuño, M. F., & Chaves, M. M. (2007). Deficit irrigation as strategy to save water: physiology and potential application to horticulture. Journal of Integrative Plant Biology, 49(10), 1421–1434. https://doi.org/10.1111/j.1672-9072.2007.00556.x
• Dayer, S., Peña, J. P., Gindro, K., Torregrosa, L., Voinesco, F., Martínez, L., Pietro, J. A., & Zufferey, V. (2017). Changes in leaf stomatal conductance, petiole hydraulics and vessel morphologyy in grapevine (Vitis vinífera cv. Chasselas) under different light and irrigation regimes. Functional Plant Biology, 44(7), 679-693. https://doi.org/10.1071/FP16041
• Davies, W. J., Wilkinson, S., & Loveys, B. (2002). Stomatal control by chemical signaling and the exploitation of this mechanism to increase water use efficiency in agriculture. New Phytologist, 153(3), 449-460. https://doi.org/10.1046/j.0028-646X.2001.00345.x
• Deloire, A. A., Carbonneau, A., Wang, Z. P., & Ojeda, H. (2004). Vine and water: a short review. Journal International des Sciences de la Vigne et du Vin, 38(1), 1-13. https://doi.org/10.20870/oeno-one.2004.38.1.932
• Dias, F. A. N., Mota, R. V., Souza, C. R., Pimentel, R. M. A., Souza, L. C., Souza, A. L., & Regina. M. A. (2017). Rootstock on vine performance and wine quality of ‘Syrah’ under double pruning. Scientia Agricola, 74(2), 134-141. https://doi.org/10.1590/1678-992x-2015-0384
• Fraga, H., Malheiro, A. C., Moutinho-Pereira, J., & Santos, J. A. (2013). Future scenarios for viticultural zoning in Europe: Ensemble projections and uncertainties. International Journal. Biometeorology, 57(6), 909-925. https://doi.org/10.1007/s00484-012-0617-8
• Gaudillère, J. P., van Leeuwen, C., & Ollat, N. (2002). Carbon isotope composition of sugars in grapevines, an integrated indicator of vineyard water status. Journal of Experimental Botany, 53(369), 757-763. https://doi.org/10.1093/jexbot/53.369.757
• Gómez-del-Campo, M., Ruiz, C., Baeza, P., & Lissarragu, J. R. (2003). Drought adaptation strategies of four grapevine cultivars (Vitis vinifera L.): modification of the properties of the leaf area. Journal International des Sciences de la Vigne et du Vin, 37, 131-143. https://doi.org/10.20870/oeno-one.2003.37.3.950
• Gerzon, E., Biton, I., Yaniv, Y., Zemach, H., Netzer, Y., Schwartz, A., Fait, A., & Ben-Ari, G. (2015). Grapevine anatomy as a possible determinant of isohydric or anisohydric behavior. American Journal of Enology and Viticulture, 66(3), 340-347. https://doi.org/10.5344/ajev.2015.14090
• Gonçalves, B., Pereira, J. M., Santos, A., Silva, A. P., Bacelar, E., Correia, C., & Rosa, E. (2005). Scion–rootstock interaction affects the physiology and fruit quality of sweet cherry. Tree Physiology, 26(1), 93-104. https://doi.org/10.1093/treephys/26.1.93
• IPCC (2008). Climate change and water. In: IPCC Tech. Paper VI (Eds. B.C. Bates, Z.W. Kundzewicz, S. Wu, J.P. Palutikof) (IPCC Secretariat, Geneva).
• Kidman, C. M., Dry, P. R., McCarthy, M. G., & Collins, C. (2013). Reproductive performance of Cabernet Sauvignon and Merlot (Vitis vinifera L.) is affected when grafted to rootstocks. Australian Journal of Grape and Wine Research, 19(3), 409-421. https://doi.org/10.1111/ajgw.12032
• Keller, M. (2010). The Science of Grapevine. Anatomy and Physiology. California:vAcademic Press.
• Koundouras, S., Tsialtas, I.T., Zioziou, E., & Nikolaou, N. (2008). Rootstock effects on the adaptive strategies of grapevine (Vitis vinifera L. cv. Cabernet Sauvignon) under contrasting water status: leaf physiological and structural responses. Agricultural Ecosystem and Environment, 128(1-2), 86-96. https://doi.org/10.1016/j.agee.2008.05.006
• Kizildeniz, T., Pascual, I., Irigoyen, J. J., & Morales, F. (2018). Using fruit-bearing cuttings of grapevine and temperature gradient greenhouses to evaluate effects of climate change (elevated CO2 and temperature, and water deficit) on the cv. red and white Tempranillo. Yield and must quality in three consecutive growing seasons (2013–2015). Agricultural Water Management, 202(4), 299-310. https://doi.org/10.1016/j.agwat.2017.12.001
• Lovisolo, C., Perrone, I., Carra, A., Ferrandino, A., Flexas, J., Medrano, H., & Schubert, A. (2010). Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and nonhydraulic interactions at the whole-plant level: a physiological and molecular update. Functional Plant Biology, 37(2), 98-116. https://doi.org/10.1071/FP09191
• Lovisolo, C., Lamoureux, A. L., Tramontini, S., & Ferrandino, A. (2016). Grapevine adaptations to water stress: new perspectives about soil/plant interactions Grapevine adaptations to water stress: new perspectives about soil/plant interactions. Theoretical and Experimental Plant Physiology, 28(1), 53-66. https://doi.org/10.1007/s40626-016-0057-7
• Marguerit, E., Brendel, O., Lebon, E., Van Leeuwen, C., & Ollat, N. (2012). Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes. New Phytologist, 194(2), 416–429. https://doi.org/10.1111/j.1469-8137.2012.04059.x
• Medrano, H., Escalona, J. M., Bota, J., Gulías, J., & Flexas, J. (2002). Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Annals of Botany, 89(7), 895–905. https://doi.org/10.1093/aob/mcf079
• Meyers, B. J. (1988). Water stress integral: a link between short-term stress and long-term growth. Tree Physiology. 4(4), 315–323. https://doi.org/10.1093/treephys/4.4.315
• Ollat, N., Peccoux, A., Papura, D., Esmenjaud, D., Marguerit, E., Tandonnet, J. P., Bordenave, L., Cookson, S. J., Barrieu, F., Rossdeutsch, L., Lecourt, J., Lauvergeat, V., Vivin, P., Bert, P. F., & Delrot, S. (2016). ‘Rootstocks as component of adaptation to environment’, In: Grapevine in a Changing Environment: A Molecular and Ecophysiological Perspective. Ed. H. Gerós, M. M. Chaves, H. Medrano, S. Delrot (John Wiley & Sons, Ltd Press), 68-108. https://doi.org/10.1002/9781118735985.ch4
• Pagay, V., Zufferey, V., & Lakson, A. N. (2016). The influence of water stress on grapevine (Vitis vinifera L.) shoots in a cool, humid climate: growth, gas exchange and hydraulics. Functional Plant Biology 43(9), 827–837. https://dx.doi.org/10.1071/FP16017
• Patakas, A., Noitasakis, B., & Chouzouric, A. (2005). Optimization of irrigation water use in grapevines using the relationship between transpiration and plant water status. Agriculture, Ecosystems and Environment, 106 (2-3), 253–259. https://doi.org/10.1016/j.agee.2004.10.013
• Roland, J. C., & Vian, B. (1991). General preparation and staining of thin sections. In ‘Electron microscopy of plant cells. (Eds JL Hall, C Hawes). (Academic Press: London), 1–66. https://doi.org/10.1016/B978-0-12-318880-9.50006-5
• Romero, P., Botía, P., & Navarro, J. M. (2018). Selecting rootstocks to improve vine performance and vineyard sustainability in deficit irrigated Monastrell grapevines under semiarid conditions. Agricultural Water Management, 209(15), 73-93. https://doi.org/10.1016/j.agwat.2018.07.012
• Santarosa, E., Souza, P. V. D., Mariath, J. E. A., & Lourosa, G. V. (2016). Physiological interaction between rootstock-scion: effects on xylem vessels in Cabernet Sauvignon and Merlot grapevines. American Journal of Enolgy and Viticulture, 67(1), 65-76. https://doi.org/10.5344/ajev.2015.15003
• Santos, T. P., Lopes, C. M., Rodrigues, M. L., de Souza, C. R., Ricardo-da-Silva, J. M., Maroco, J. P., Pereira, J. S., & Chaves, M. M. (2007). Effects of deficit irrigation strategies on cluster microclimate for improving fruit composition of Moscatel field-grown grapevines. Scientia Horticulturae. 112(3), 321-330. https://doi.org/10.1016/j.scienta.2007.01.006
• Serra, I., Strever, A., Myburgh, P. A., & Deloire, A. (2014). Review: the interaction between rootstocks and cultivars (Vitis vinifera L.) to enhance drought tolerance in grapevine. Australian Journal of Grape and Wine Research, 20(1), 1-14. https://doi.org/10.1111/ajgw.12054
• Simonneau, T., Lebon, E., Coupel-Ledru, A., Marguerit, E., Rossedeutsch, L., & Ollat, N. (2017). Adapting plant material to face water stress in vineyards: which physiological targets for an optimal control of plant water status? OENO one, 51(2), 167-179. https://doi.org/10.20870/oeno-one.2016.0.0.1870
• Smart, D. R., Schwass, E., Lakso, A., & Morano, L. (2006). Grapevine rooting patterns: a comprehensive analysis and a review. American Journal of Enology and Viticulture, 57(1), 89–104.
• Soar, C. J., Dry, P. R., & Loveys, B. (2006a). Scion photosynthesis and leaf gas exchange in Vitis vinifera L. cv. Shiraz: Mediation of rootstock effects via xylem sap ABA. Australian Journal of Plant Physiology, 12(2), 82-96. https://doi.org/10.1111/j.1755-0238.2006.tb00047.x
• Soar, C. J., Speirs, J., Maffei, S. M., Penrose, A. B., McCarthy, M. G., & Loveys, B. R. (2006b). Grape vine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue. Australian Journal of Grape and Wine Research, 12(1), 2-12. https://doi.org/10.1111/j.1755-0238.2006.tb00038.x
• Southey, J. M., Archer, E. (1988). The effect of rootstock cultivar on grapevine root distribution and density. In: The Grapevine Root and its Environment. Ed. J.L. van Zyl (Republic of South Africa Department of agriculture and water supply: Pretoria) 57–73.
• Souza, C. R, Maroco, J. P., Santos, T. P., Rodrigues, M. L., Lopes, C. M, Pereira J. S., & Chaves, M. M. (2005a). Impact of deficit irrigation on water use efficiency and carbon isotope composition (δ13C) of field-grown grapevines under Mediterranean climate. Journal of Experimental Botany, 56(418), 2163–2172. https://doi.org/10.1093/jxb/eri216
• Souza, C. R., Maroco, J. P., Santos, T. P., Rodrigues ,M. L., Lopes, C. M., Pereira, J. S., & Chaves, M. M. (2005b). Grape berry metabolism in field-grown grapevines exposed to different irrigation strategies. Vitis, 44(3), 103-109. doi:10.5073/vitis.2005.44.103-109
• Souza, C. R., Bassoi, L. H., Lima Filho, J. M. P., Silva, F. S., Viana, L. H., Dantas, B. F., Pereira, M. S., & Ribeiro, P. R. A. (2009). Water relations of field-grown grapevines in the São Francisco Valley, Brazil, under different rootstocks and irrigation strategies. Scientia Agricola, 66(4), 436-446. https://doi.org/10.1590/S0103-90162009000400002
• Souza, C. R., Mota, R. V., França, D. V. C., Pimentel, R. M. A., & Regina, M. A. (2015). Performance of Cabernet Sauvignon grafted onto different rootstocks during the autumn-winter season in Brazilian Southeast. Scientia Agricola, 72(2), 168-146. https://doi.org/10.1590/0103-9016-2014-0031
• Spring, J. .L., Zufferey V., Verdenal T., & Viret O. (2012). Nitrogen dilution in excessive canopy of cvs. Chasselas and Pinot noir. Journal International des Science de la Vigne et du Vin, 46(3), 233-240. https://doi.org/10.20870/oeno-one.2012.46.3.1520
• Spring, J. L., Zufferey, V., Verdenal, T., & Viret, O. (2016). Influence du porte-greffe sur le comportement du Pinot noir dans les conditions du Valais Central. Revue Suisse Viticulture, Arboriculture, Horticulture, 48(2), 112-122.
• Stevens, R .M., Pech, J. M., Gibberd, M. R., Walker, R. R., & Nicholas, P. R. (2010). Reduced irrigation and rootstock effects on vegetative growth, yield and its components, and leaf physiological responses of Shiraz. Australian Journal of Grape and Wine Research, 16(3), 413-425. https://doi.org/10.1111/j.1755-0238.2010.00102.x
• Taiz, L., & Zeiger, E. (2004). Plant Physiology. 3th ed. Porto Alegre: Artmed.
• Tandonnet, J. P., Cookson, S. J., Vivin, P., & Ollat, N. (2010). Scion genotype controls biomass allocation and root development in grafted grapevine. Australian Journal of Grape and Wine Research, 16(2), 290–300. https://doi.org/10.1111/j.1755-0238.2009.00090.x
• Tombesi, S., Johnson, R. S., Day, K. R., & DeJong, T. M. (2010). Interactions between rootstock, inter-stem and scion xylem vessel characteristics of peach trees growing on rootstocks with contrasting size-controlling characteristics. AoB Plants, 2010 ( plq013). https://doi.org/10.1093/aobpla/plq013
• Tramontini, S., Vitali, M., Centioni, L., Schubert, A., & Lovisolo, C. (2013). Rootstock control of scion response to water stress in grapevine. Environmental and Experimental Botany, 93(9), 20-26. https://doi.org/10.1016/j.envexpbot.2013.04.001
• van Leeuwen, C., Friant, P., Soyer, J. P., Molot, C., Chone, X., & Dubourdieu, D. (2000). L’intérêt du dosage de l’azote total et de l’azote assimilable dans le môut comme indicateur de la nutrition azotée de la vigne. Journal International des Sciences de la Vigne et du Vin, 34(2), 75–82.
• van Leeuwen, A., Tregoat, O., Choné, X., Bois, B., Pernet, D., & Gaudièllere, J. P. (2009). Vine water status is a key factor in grape ripening and vintage quality for red Bordeaux wine. How can it be assessed for vineyard management purposes. Journal International des Sciences de la Vigne et du Vin, 43(3), 121-134. https://doi.org/10.20870/oeno-one.2009.43.3.798
• van Leeuwen, C., & Darriet, P. (2016). The Impact of climate change on viticulture and wine quality. Journal of Wine Economics, 11(1), 150–167. https://doi.org/10.1017/jwe.2015.21
• van Leeuwen, C., Roby, J. P., & de Rességuier, L. (2018). Soil-related terroir factors: a review. OENO one, 52(2), 173-188. https://doi.org/10.20870/oeno-one.2018.52.2.2208
• Verdenal, T., Nagy, A. D, Zufferey, V., Spring, J. L., Viret, O., Carbonne, J. M., & van Leeuwen, C. (2021). Understanding and managing nitrogen nutrition in grapevine: a review. OENO one, 55(1), 1-44. https://doi.org/10.20870/oeno-one.2021.55.1.3866
• Yıldırım, K., Yağcı, A., Sucu, S., & Tunç, S. (2018). Responses of grapevine rootstocks to drought through altered root system architecture and root transcriptomic regulations. Plant Physiology and Biochemistry, 127(6), 256-268. https://doi.org/10.1016/j.plaphy.2018.03.034
• Zoric´, L., Ljubojevic´, M., Merkulov, L. J., Lukovic´, J., & Ognjanov, V. (2012). Anatomical characteristics of cherry rootstocks as possible preselecting tools for prediction of tree vigor. Journal of Plant Growth Regulation, 31(4), 320-331. https://doi.org/10.1007/s00344-011-9243-7
• Zufferey, V., Spring, J. L., Verdenal, T., Dienes, A., Belcher, S., Lorenzini, F., Koestel, C., Rösti, J., Gindro, K., Spangenberg, J., & Viret, O. (2017). Influence of water stress on plant hydraulics, gas exchange, berry composition and quality of Pinot Noir wines in Switzerland. OENO one, 51(1), 37-57. https://doi.org/10.20870/oeno-one.2017.51.1.1314