Abstract
Background and goals Berry shrivel (BS), a grape ripening disorder which is linked to arrested sugar accumulation and metabolic alterations, is thought to be of physiological origin. Its underlying causes remain unknown, but abrupt environmental changes might be involved. We tested whether BS may be triggered by plant water stress leading up to veraison followed by irrigation with water at different temperatures.
Methods and key findings In a two-year field trial with deficit-irrigated Cabernet Sauvignon winegrapes in arid southeastern Washington, irrigation was suspended during the lag phase of berry development, then resumed at veraison, using either water at ambient temperature (20 to 24°C) or ice-cooled water (0°C). Measurements of soil moisture, leaf water potential, and leaf gas exchange showed that interrupting irrigation induced moderate-to-severe plant water stress before rewatering. Compared with ambient-temperature water, cooling the irrigation water used for rewatering reduced the soil temperature by 4 to 8°C for 1 to 3 days, but had a minor effect on the vines’ response to water stress. Rewatering at 50% veraison, but not at 5% veraison, significantly increased BS incidence. Cooling the irrigation water also tended to increase BS incidence, but not consistently so.
Conclusions and significance This study showed that sudden alterations in plant water availability and water temperature may be involved in triggering BS. Though the cause-effect relationship remains unclear, this knowledge may be useful in devising vineyard irrigation or soil management strategies that avoid abrupt changes in soil moisture and soil temperature around veraison.
Introduction
Following seed and fruit set, grape (Vitis sp.) berries grow in a double-sigmoid fashion, with two growth phases separated by a short phase of little growth, called the lag phase (Keller 2020). Fruit ripening starts at the end of the lag phase with berry softening, followed by sugar accumulation, malate depletion, and renewed berry growth (Shahood et al. 2020, Hernández-Montes et al. 2021). Additionally, anthocyanins begin to accumulate in cultivars with dark-skinned berries once the berry sugar concentration, estimated as total soluble solids (TSS), exceeds 9 to 10 Brix (Keller 2020). Thus, grape berries grow and ripen at the same time. Each berry may initiate its own ripening program independently of the other berries on the same cluster or vine (Keller et al. 2015b, Zhang and Keller 2017, Shahood et al. 2020, Hernández-Montes et al. 2021). In doing so, it pulls phloem sap into the berry and unloads the dissolved sugar for storage. Under favorable conditions (i.e., adequate light, temperature, water, nutrients, and plant health), the photosynthesizing leaves also push the phloem sap toward all berries (Keller et al. 2015b). Thus, phloem flow follows a pressure gradient that is established within the phloem’s sieve tubes by the production and loading of sugar in sources and its unloading and use or storage in sinks (Knoblauch et al. 2016).
Despite the asynchronous ripening onset and progression, grape clusters can suffer from ripening disorders that are seemingly initiated independent of the maturity status of the individual berries (Griesser et al. 2024). Among different disorders, berry shrivel (BS; also referred to as sour shrivel or sugar accumulation disorder) and bunch-stem necrosis (BSN) are especially intractable. Both are thought to be of physiological origin, but their internal or external triggers remain unknown (Griesser et al. 2024). While the rachis of clusters affected by BSN develops necrotic lesions that interrupt phloem flow, it typically remains green in BS-affected clusters, although cell death has sometimes been observed in their rachis phloem (Hall et al. 2011, Bondada and Keller 2012, Zufferey et al. 2015, Griesser et al. 2024). However, premature loss of mesocarp cell membrane integrity during early ripening is a prominent internal symptom of berries from BS clusters (Krasnow et al. 2008, 2009, Hoff et al. 2021). Membrane failure, more specifically rupture of the vacuolar membrane, leads to cell death and might be associated with oxidative stress as a result of hypoxia in the mesocarp cells surrounding the seeds (van Doorn and Woltering 2004, Xiao et al. 2018). Affected berries lose the ability to accumulate sugar, though they still metabolize malate (Keller et al. 2016, Griesser et al. 2024). As phloem inflow stops while evaporative water loss continues, the berries begin to shrink, and their low sugar-to-acid ratio and low potassium content results in their sour taste (Keller et al. 2016). In contrast, the cellular membranes of healthy berries remain intact until late in ripening (Krasnow et al. 2008, Fuentes et al. 2010, Keller and Shrestha 2014).
While BSN will affect all berries downstream of necrotic lesions on the rachis regardless of the ripening status of each berry, membrane failure leading to BS starts in individual berries after their seeds are mature and sugar accumulation has started (Hall et al. 2011, Keller et al. 2016, Hoff et al. 2021). Therefore, rather than appearing simultaneously across entire clusters, BS may develop in individual berries but spread quickly over the cluster as each berry initiates its ripening process. Compared with normal ripening whose onset can span 20 to 30 days across the berries of a cluster (Hernández-Montes et al. 2021), this change might be accelerated in BS clusters because sugar accumulation stops as each berry in turn fails to properly execute its ripening program. Nevertheless, it remains unknown why entire clusters rather than individual berries or groups of berries typically develop BS symptoms (Griesser et al. 2024).
As grape berries begin to ripen, they undergo a change in vascular flow to and from the berries. Green hard berries receive most of their water via the xylem, but as they enter the ripening period, the berries’ rapid rise in sugar demand leads them to rely on phloem-derived water (Keller et al. 2015b, Zhang and Keller 2017). While the berries retain a small portion of that water for renewed growth, the surplus is discharged via berry transpiration (especially under conditions of high evaporative demand) and xylem backflow to the leaves (Zhang and Keller 2015, 2017). At the same time, the berries’ phloem-associated cells close their plasmodesmata to switch from symplastic to apoplastic phloem unloading and facilitate sugar import and storage (Zhang et al. 2006). It is possible that the direction and magnitude of these changes, coupled with the shifts in gene expression required for ripening initiation, make the berries vulnerable to abrupt changes in their environment (Zufferey et al. 2015, Fasoli et al. 2018, Hewitt et al. 2023, Griesser et al. 2024). Such changes may include temperature fluctuations, as well as fluctuations in water supply.
Observations in Italy’s South Tyrol region suggested BS may have been especially prominent in vineyards that experienced soil water deficit leading up to veraison followed by rainfall at veraison (Raifer et al. 2023). In addition, BS was prevalent in a mountain valley in southwestern Switzerland in years with fluctuating temperatures and rainfall around veraison, and was exacerbated by irrigation (Zufferey et al. 2015). Though neither the water temperature nor the soil temperature were measured in those studies, one might assume both rainwater and irrigation water in those Alpine regions to be rather cold. Applying cold water to dry soil can lead to a rapid, transient decline in soil temperature, which has been found to inhibit growth of some plant species (Brockwell and Gault 1976). By decreasing the roots’ hydraulic conductance, low soil temperature may exacerbate water stress responses such as stomatal closure and reduced photosynthesis (Ameglio et al. 1990, Rogiers and Clarke 2013). When severe enough, the ensuing imbalance between root water uptake and leaf water demand may trigger xylem cavitation and leaf wilting (Scheenen et al. 2007).
To our knowledge, the effect of fluctuations in rootzone temperature on fruit ripening has not been investigated. In addition to the effects of water stress (and its alleviation) and root chilling on plant responses at the leaf and canopy level, it is possible that responses also occur at the fruit level, especially during a potentially vulnerable phenological stage such as veraison. Consequently, we speculated that alleviating water stress at the beginning of grape ripening might trigger processes that culminate in the BS syndrome in susceptible cultivars. We further hypothesized that applying cold irrigation water during periods of high evaporative demand might temporarily exacerbate the stress perceived by the vines. Taking advantage of eastern Washington's arid climate and the relatively frequent appearance of BS in this region (Keller et al. 2016, Hoff et al. 2021), we tested the influence of a period of soil drydown during the lag phase of berry development followed by rewatering at veraison with irrigation water that was either left at ambient temperature or cooled with ice on physiological responses and BS and BSN incidence in Cabernet Sauvignon. The field trial was repeated in two growing seasons to test whether any potential effects were consistent across years.
Materials and Methods
Site and plant material
A field experiment was conducted in 2017 and 2018 in a vineyard at Washington State University’s Irrigated Agriculture Research and Extension Center near Prosser, WA (46°17′N; 119°44′W; 365 m asl). The region receives less than 200 mm annual precipitation and has warm and very dry summers and moderately cold winters. The vineyard soil is a Warden silt loam with a pH ~8 and organic matter content of 0.25% (https://websoilsurvey.sc.egov.usda.gov). A caliche layer at 50 to 100 cm depth limits root growth. The soil volumetric water content (θv) is 26% (v/v) at field capacity (FC) and 8% at permanent wilting point (PWP) (Groenveld et al. 2023). Own-rooted Vitis vinifera L. cv. Cabernet Sauvignon (clone FPS 07) vines propagated from certified material were planted in 2010 at 2.7 m between rows and 1.8 m within rows. Rows were oriented north-south on a 2% slope with a southwestern aspect. Vines were trained to two trunks with bilateral cordons 95 cm above the ground, spur-pruned in winter to 24 buds per vine, and vertically shoot-positioned between two pairs of foliage wires 30 cm apart and 30 and 75 cm above the cordon. A 1.2-m herbicide strip was maintained in the rows, and permanent but summer-dormant volunteer vegetation grew between rows. The vineyard was drip-irrigated using two 2-L/hr emitters per vine. Fertilizer and pest management practices were applied uniformly across the vineyard according to regional standards. Annual disease testing and rogueing (if necessary) kept the vineyard as free from viral and bacterial diseases as possible. Budbreak occurred on day of year (DOY) 122 and 123, bloom (50% capfall) on DOY 163 and 156, fruit set on DOY 179 and 165, and veraison (50% berry color change) on DOY 230 and 225 in 2017 and 2018, respectively.
Experimental design
The 2017 experiment tested vines that experienced a temporary suspension of water supply during the lag phase of berry growth, followed by rewatering at veraison with either ambient irrigation water or ice-cooled water against deficit-irrigated control vines. The 2018 experiments included the same treatments but additionally tested the supply of ice-cooled water to control vines. Treatments (three in 2017 and four in 2018) were applied in a randomized complete block design with three replicates and 25 consecutive vines per replicate. Following an initial drydown period after fruit set to control shoot growth, control vines were irrigated weekly at 70% of crop evapotranspiration (ETc) calculated from reference evapotranspiration (ETo) and a crop coefficient that increased from zero at budbreak to 0.8 at veraison. To generate transient vine water stress during the lag phase, irrigation was interrupted on DOY 213 (2017) or DOY 205 (2018) and resumed at 50% veraison on DOY 230 (2017) or DOY 225 (2018). In 2018, we additionally tested rewatering at 5% veraison (DOY 213) in an adjacent block with an otherwise identical experimental design. In 2017, the temperature of the incoming ambient irrigation water, measured with iButton temperature loggers (DS1922L, Maxim Integrated Products), varied diurnally from 20.1 to 23.6°C, and cooled water was supplied to the drip tubes from a 1000-L container with an ice-water mixture (i.e., water at 0°C), using a diaphragm pump. In addition, a preliminary experiment conducted with five vines in one row of the water stress treatment tested water cooling by passing it through perforated plastic boxes containing 14 kg of ice placed under the drip emitters. This latter approach was used for water cooling in 2018, when the ambient water temperature ranged from 21.6 to 24.4°C.
Weather and soil data collection
Daily weather data were obtained from the Roza AgWeatherNet station located ~400 m from the vineyard (https://weather.wsu.edu). Growing degree days (GDD) for the April-October growing season were estimated from daily minimum (Tmin) and maximum (Tmax) temperatures, applying a base temperature of 10°C. Soil moisture (θv) was measured weekly starting at budbreak to support irrigation management. Measurements were taken at three depths (30, 60, and 90 cm) using a neutron probe (503 DR Hydroprobe, CPN International) in four access tubes installed equidistant between pairs of drip emitters. To permit comparisons across different soil types, soil moisture was normalized relative to that at FC and PWP by converting θv to extractable soil water: ESW = [θv ‒ θPWP]/[θFC ‒ θPWP] (Groenveld et al. 2023). Because the irrigation water temperature changes gradually as water runs through drip tubes and percolates into the soil, we measured the resulting soil temperature (Tsoil) at 30-min intervals during the experiment, using iButton temperature loggers buried at a depth of 25 cm beneath five (2017) or three (2018) drip emitters per treatment replicate.
Physiological measurements
Physiological measurements were taken on three leaves, each on a different vine, per treatment replicate (i.e., nine leaves per treatment) at maximum water stress (day before irrigation) and the day after rewatering. A Scholander pressure chamber (model 600, PMS Instrument Company) was used to measure leaf water potential at predawn (Ψpd) and midday near solar noon (Ψmd), as described previously (Keller et al. 2015a). Leaf net assimilation rate (A), stomatal conductance (gs), transpiration rate (E), and leaf temperature (Tleaf) were measured at midmorning (0900 to 1000 hr) on recently mature sun-exposed leaves, using a portable infrared gas analyzer (LCi, ADC BioScientific). Earlier diurnal measurements in Merlot and Syrah winegrapes under similar environmental and viticultural conditions as the vines in the present study had indicated that gs reached its daily minimum before 0900 hr and did not begin to recover until late afternoon at this time of year (Keller et al. 2015a, Romero et al. 2017). Gas exchange measurements were taken under ambient light (photosynthetic photon flux >1000 μmol/m2sec) and CO2 (~400 μmol/mol) conditions using a broad-leaf chamber (6.25 cm2) and flow rate of 200 mL/min. The evaporative flux method was used to estimate the leaf area-specific whole-plant hydraulic conductance (Kl = E/[Ψsoil – Ψmd]), assuming steady-state conditions (Keller et al. 2015a). We further assumed the soil water potential (Ψsoil) to be equal to Ψpd at ESW ≤ 0.4, but 0.11 MPa higher than Ψpd at ESW > 0.4, based on data presented by Groenveld et al. (2023) for this vineyard site.
Ripening disorder assessment
At harvest time, the incidence of BS and BSN was quantified by visually assessing and counting all clusters on five vines per treatment replicate (i.e., 15 vines per treatment). Following the definition by Seem (1984), incidence was expressed as the percentage of symptomatic clusters per vine. Clusters were evaluated on DOY 299 in 2017, and DOY 299 and 303 in 2018. Symptomatic clusters were distinguished from healthy clusters by the typical symptoms of flaccid, shriveled berries for BS, and necrotic rachis portions for BSN (Bondada and Keller 2012, Griesser et al. 2024). To further confirm the presence of these ripening disorders, the TSS concentration of symptomatic and healthy clusters from each vine was measured with a handheld refractometer (PAL-1, Atago). Individual clusters were manually crushed in plastic bags, and the juice was analyzed immediately.
Data analysis
Data were analyzed in R (Rx64 3.5.0 Core Team) and Statistica 14.2 (Cloud Software Group). We used one-way analysis of variance (ANOVA) to test treatment effects in 2017 and two-way ANOVA to test main and interactive effects of water stress and water temperature in 2018. Means were separated by F-test at 5% significance. Data are presented as means ± standard error (SE) where appropriate. Pearson correlation analysis was used to test associations between response variables.
Results
Weather
The two growing seasons were slightly warmer than the long-term (24 yrs) average. The cumulative seasonal GDD was 1485°C in 2017 and 1471°C in 2018 (long-term average 1442°C). There were 7 days with Tmax > 35°C (peak 36.6°C) during the 17-day preveraison water stress period in early to mid-August of 2017, and 5 days with Tmax > 35°C (peak 37.3°C) during the 20-day stress period in 2018 (Figure 1). At the same time, there were 5 days with Tmin < 15°C (minimum 9.1°C) in 2017, and 8 days with Tmin < 15°C (minimum 10.0°C) in 2018. Total annual precipitation was 240 mm in 2017 and 158 mm in 2018 (long-term average 175 mm). Only 3.1 mm rain fell during the 2017 water stress period, and 9.9 mm fell early during the 2018 stress period. The daily ETo during the water withholding period varied from 4.1 to 6.6 mm (cumulative 93 mm) in 2017, and from 4.1 to 7.4 mm (cumulative 125 mm) in 2018.
Daily changes in maximum (red line) and minimum (blue line) temperatures during the lag phase and early ripening period in a Cabernet Sauvignon vineyard in southeastern Washington in 2017 and 2018. Blue bars indicate water withholding periods lasting 17 and 20 days in 2017 and 2018, respectively, and ending at 50% veraison.
Soil moisture and soil temperature
Following budbreak, irrigation maintained the ESW across the soil profile above 0.3 through fruit set, after which it declined through mid-July to ~0.2 in the top 30 cm and to 0.1 at lower depths as a result of deficit irrigation (Figure 2). A further decrease occurred at the 90-cm depth; from veraison onwards, θv at 90-cm depth remained near the PWP through harvest in both 2017 and 2018, while irrigation increased θv at the 30- and 60-cm depths. In both years, withholding irrigation water during the lag phase of berry growth led to rapid soil drying. The average ESW in the top 60 cm of the drying soil declined below 0.15, while in the control it remained above 0.25 in both 2017 (Table 1) and 2018 (Tables 2 and 3). Rewatering at veraison rapidly increased ESW but did not fully restore soil moisture as it was not possible to apply differential amounts of water to the different treatments.
Changes in extractable soil water (ESW; varying from 0 at permanent wilting point to 1 at field capacity) at three depths, from fruit set through harvest, in a Cabernet Sauvignon vineyard in southeastern Washington in 2017 and 2018. Days of year were 163 and 156 for bloom, 179 and 165 for fruit set, and 230 and 225 for veraison in 2017 and 2018, respectively. Blue bars indicate water withholding periods lasting 17 and 20 days in 2017 and 2018, respectively, and ending at 50% veraison.
Effect of transient water stress (Stress) during the lag phase of berry growth followed by irrigation (Recovery) with ambient or ice-cooled (Cold) water at 50% veraison on soil moisture and physiological traits, measured the day before and the day after recovery irrigation in Cabernet Sauvignon vines in a vineyard in southeastern Washington in 2017.
Effect of transient water stress (Stress) during the lag phase of berry growth followed by irrigation (Recovery) with ambient or ice-cooled (Cold) water at 5% veraison on soil moisture and physiological traits, measured the day before and the day after recovery irrigation in Cabernet Sauvignon vines in a vineyard in southeastern Washington in 2018.
Effect of transient water stress (Stress) during the lag phase of berry growth followed by irrigation (Recovery) with ambient or ice-cooled (Cold) water at 50% veraison on soil moisture and physiological traits, measured the day before and the day after recovery irrigation in Cabernet Sauvignon vines in a vineyard in southeastern Washington in 2018.
The soil temperature at 25-cm depth was primarily driven by, and lagged, diurnal changes in air temperature, but was modulated by irrigation water cooling. The Tsoil peaked between dusk and midnight, and the daily minimum occurred between sunrise and midday (Figure 3). Compared with irrigation water at ambient temperature, irrigating with ice-cooled water in 2017 reduced Tsoil by a maximum of 3.8°C over the course of the subsequent day, after which the temperature recovered to the level of the soil irrigated with ambient-temperature water (Figure 3). The Tsoil in the ice-box test dropped by 7.8°C during the afternoon (from 25.4 to 17.6°C within 7 hr) and recovered after sunrise the following morning. In 2018, interrupting the irrigation water supply raised Tsoil by a maximum of 2.9°C, and an average of 1.9°C during the week before rewatering, compared with the control. Applying ice-cooled water to the previously unirrigated, and hence warmer, soil decreased Tsoil by 8.2°C, whereas in the irrigated, and hence cooler, soil the decrease was only 4.3°C (Figure 3). The cooling effect gradually lessened until it disappeared after 3 days.
Diurnal changes in soil temperature (25-cm depth) during and after irrigation following water withholding in a Cabernet Sauvignon vineyard in southeastern Washington. Water-stressed and control vines were irrigated at 50% veraison on 18 Aug 2017 (n = 5) or 13 Aug 2018 (n = 3) with ambient (amb) or ice-cooled (cold) water. Temperature was not monitored in control vines in 2017. Blue bars indicate irrigation periods (i.e., rewatering events).
Physiological traits
Withholding irrigation decreased Ψpd and Ψmd and led to almost complete stomatal closure (gs < 0.05 mol/m2sec), along with large reductions in A and E and an increase in Tleaf, in both 2017 (Table 1) and 2018 (Tables 2 and 3). The vines did not fully recover a day after rewatering at veraison. Water withholding also strongly decreased Kl, but the day after water was resupplied, Kl recovered to the level of control vines. While ice-cooling the irrigation water consistently reduced Ψpd the next morning, the effect on Ψmd, Kl, and leaf gas exchange was minor and mostly nonsignificant (Tables 1 to 3). Across measurements before and after each irrigation event over the two years, gs correlated with Ψpd (Figure 4), Ψmd (r > 0.53), E (r > 0.90), and A (r > 0.95) (all p < 0.001). Stomatal conductance varied widely at high Ψpd as a result of variable vapor pressure deficit, but gs declined at Ψpd < −0.3 MPa and the stomata were essentially closed (gs < 0.05 mol/m2sec) at Ψpd < −0.8 MPa (Figure 4). Consequently, both E (r > 0.76) and A (r > 0.68) also decreased with decreasing Ψpd (p < 0.001). However, unlike gs, Kl was driven much more strongly by Ψmd (Figure 5) than by Ψpd (r > 0.29, p < 0.025). Manipulating the irrigation water temperature did not alter any of these relationships between physiological variables.
Relationship between predawn leaf water potential (Ψpd) and stomatal conductance (gs) at veraison in a Cabernet Sauvignon vineyard in southeastern Washington over two years.
Relationship between midday leaf water potential (Ψmd) and leaf area-specific whole-vine hydraulic conductance (Kl) at veraison in a Cabernet Sauvignon vineyard in southeastern Washington over two years.
Ripening disorders and TSS
Across the two years, both transient preveraison water stress (p = 0.001) and cold irrigation water (p = 0.021) increased BS incidence, with no significant interaction (p = 0.41). However, the variation due to water stress was more than twice that due to water temperature. In 2017, interrupting irrigation during the lag phase followed by rewatering at veraison increased BS incidence 21-fold relative to the control (p = 0.023). While only 0.5% of the clusters on control vines developed BS, on previously water-stressed vines, 10% of the clusters developed BS (Figure 6). The cold-water treatment was applied only to the water-stressed vines and had no significant effect on BS incidence (p = 0.26). In the ice-box test, however, 50% of the clusters on cold-water-treated vines developed BS (p < 0.001), and those clusters had a TSS of 14.3 ± 0.5 Brix at harvest compared with 23.5 ± 0.5 Brix for the unaffected clusters on the same vines (p < 0.001). The cluster number across the water stress experiment varied from 34 to 91 per vine and correlated positively with BS incidence (Figure 7). At harvest time, the berries from healthy clusters had 24.8 ± 0.4 Brix, whereas those from BS clusters had only 15.0 ± 0.7 Brix (p < 0.001). The preveraison water stress did not affect TSS in either the healthy clusters (p = 0.67) or the BS clusters (p = 0.55). The BSN incidence was minimal in 2017; only two vines, both in the cold-water treatment, had a cluster with BSN symptoms.
Effect of transient water stress during the lag phase of berry growth followed by irrigation with ambient or ice-cooled (Cold) water at 50% veraison on berry shrivel incidence in a Cabernet Sauvignon vineyard in southeastern Washington over two years. Bars show means ± SE (n ≥ 9), and letters denote significant differences according to Tukey’s honest significant difference test (p < 0.05); water cooling was not tested in the control in 2017.
Relationship between cluster number per vine and berry shrivel incidence in a Cabernet Sauvignon vineyard in southeastern Washington over two years.
In 2018, there was very little BS (0.2%) and no BSN in the block where rewatering occurred at 5% veraison, and neither water stress (p = 0.60) nor water cooling (p = 0.33) increased BS incidence relative to the control. In the adjacent block that was used to test rewatering at 50% veraison (the same block as in 2017), BS was much more prevalent (12%). There also was some BSN, but its incidence was again very low (Table 4). Here, irrigation of previously water-stressed vines more than doubled the BS incidence (17.3%) compared to the control (6.9%; p < 0.001). The main effect of water cooling was not significant (p = 0.25), but a Tukey test across all treatment combinations showed that continuously irrigating with ambient-temperature water was once again associated with the lowest BS incidence (Figure 6). Neither water stress nor water cooling significantly altered the BSN incidence, though there was a trend (p = 0.07) of more BSN in the cold-water treatment (Table 4). The incidence of both BS (Figure 7) and BSN (r = 0.34, p = 0.008) correlated with the number of clusters per vine, which ranged from 52 to 123. Moreover, there was a weak correlation (r = 0.33, p = 0.01) between BS incidence and BSN incidence. While there was again no treatment effect on berry TSS at harvest, both BS and BSN reduced TSS to similar degrees relative to healthy clusters (Table 4).
Effect of transient water stress during the lag phase of berry growth followed by irrigation with ambient or ice-cooled (Cold) water at 50% veraison on bunch-stem necrosis (BSN) incidence and berry total soluble solids (TSS) at harvest in a Cabernet Sauvignon vineyard in southeastern Washington in 2018.
Discussion
In this two-year field trial in arid southeastern Washington, suspending irrigation water supply during the lag phase of Cabernet Sauvignon berry development followed by rewatering at 50% veraison markedly increased the incidence of BS compared with vines that did not experience an interruption in water supply. Rewatering at 5% veraison in one year did not affect BS incidence. Compared with water at ambient temperature, using ice-cooled water to release the water stress had a comparatively minor effect on BS incidence, but the least BS occurred consistently on vines that were regularly irrigated with ambient-temperature water. Conversely, the incidence of BSN remained low and unaltered by manipulation of irrigation water supply or temperature. Though there was a trend of increasing BS and BSN incidence in more heavily cropped vines, the variation in cluster number explained only 18% of the variation in BS and 12% of the variation in BSN. Nevertheless, the (albeit weak) correlation between BS and BSN incidence, and the similarly low TSS of BS and BSN clusters, suggests the two disorders were initiated at the same time shortly after the onset of ripening and lends some support to the idea that they, or their causal factors, might be related (Hall et al. 2011).
Our results concur with the observation that preveraison water stress followed by rainfall at veraison was associated with the appearance of BS (Raifer et al. 2023), but they seemingly contrast with the results obtained by Zufferey et al. (2015) in a 13-yr field trial with Humagne rouge winegrapes. Those authors found that irrigation before or after veraison increased BS incidence relative to unirrigated vines, with a steep rise in BS incidence when the average Ψpd > −0.3 MPa during veraison ±2 wk. While the deficit-irrigated control vines in our experiment experienced mild-to-moderate water stress according to the Ψpd, Ψmd, and gs thresholds defined by Rienth and Scholasch (2019), the temporary suspension of irrigation water supply led to moderate water stress in 2017 and moderate-to-severe stress in 2018. Since the vineyard was deficit irrigated, the soil was already quite dry at the beginning of the water withholding period. Thus, the development of vine water stress during water withholding likely resulted from a combination of relatively dry soil meeting high evaporative demand, as this period included several days with Tmax > 35°C and had a cumulative ETo of 93 mm in 2017 and 125 mm in 2018.
The incomplete recovery of physiological traits the day after irrigation that was observed here is common in field-grown vines (Romero et al. 2017). Contrary to our expectation, however, the decrease in soil temperature following application of ice-cooled irrigation water to the dry (and warm) soil had only a minor influence on the vines’ recovery from water stress. In both years, Ψpd was slightly lower the day after irrigation with cold water compared with water at ambient temperature. Though this effect was more pronounced in 2018 than in 2017, gs and E were affected only in 2017, and only mildly so. A study with pot-grown Syrah winegrapes had found positive correlations between rootzone temperature and gs or E, though the measurement variability was substantial (Rogiers and Clarke 2013). Unlike earlier work with cucumber (Scheenen et al. 2007), we observed no leaf wilting when the water-stressed vines were irrigated with cold water.
Despite the consistent appearance over two years of BS symptoms in vines that experienced transient water stress leading up to veraison, identifying an underlying physiological cause remains challenging. It seems likely that BS was triggered at or shortly after the onset of ripening, as TSS values of 15 to 18 Brix are indicative of red-purple berries, which have not completed their color change (Hernández-Montes et al. 2021). It is not clear, however, if BS was triggered by the water stress going into veraison, the rewatering event at a time when the berries were initiating their ripening program, or a combination of the two. The role of cold irrigation water in BS induction also remains uncertain, especially considering that water cooling had only a minor influence on the vines’ recovery from water stress. While the present results support our first hypothesis that alleviating water stress at veraison promotes BS, they provide no conclusive support for our second hypothesis of cold water exacerbating BS. Though we tested an earlier time of stress release only in 2018, it may be significant that rewatering at 50% veraison, but not at 5% veraison, seemed to trigger BS. Previously we had found that alleviating severe water stress at ripening onset did not result in BS in potted Merlot and Concord grapevines, but instead accelerated both renewed berry growth and sugar accumulation (Keller et al. 2015b). Withholding irrigation water from field-grown Cabernet Sauvignon vines during the period leading up to veraison followed by irrigation at 100% of ETc in a hot Australian region reduced berry size and malate content, but neither BS nor any physiological indicators of water stress were evaluated in that study (Cooley et al. 2017). In pot-grown Sangiovese vines, transient water stress during the lag phase through the “beginning of veraison” reduced anthocyanin accumulation during berry ripening but had no effect on sugar accumulation (Palai et al. 2022). However, sugar accumulation was reduced in potted Sangiovese and Montepulciano vines that were water-stressed from fruit set to veraison (no definition provided) and not thereafter, though BS was not evaluated (Palliotti et al. 2014). It is possible that cultivars differ in their response to rewatering at the beginning of ripening after a period of water stress, but if the impact of minor shifts in the timing of environmental fluctuations, such as water availability or temperature, can be confirmed, this might help to explain the seemingly erratic spatial and temporal nature of BS appearance in vineyards (cf. Keller et al. 2016).
Oxidative stress and membrane failure in the mesocarp cells have been observed in association with both early-ripening BS of different cultivars and late-ripening shriveling of Syrah (Xiao et al. 2018, Griesser et al. 2024). Moreover, pressurizing the root system of fully irrigated grapevines at veraison was found to inhibit xylem backflow and berry sugar accumulation (Zhang and Keller 2017). We speculate that releasing moderate-to-severe water stress, leading to recovery of leaf photosynthesis and hence phloem export, at a time when most berries are transitioning to ripening, or perhaps just after the berries have initiated the processes involved in the mesocarp cell wall modifications that result in berry softening, might lead to flooding of the berry apoplast from incoming phloem water. In some cases, or in susceptible cultivars, the resulting hypoxia in the interior mesocarp might induce oxidative stress through accumulation of reactive oxygen species, which may culminate in loss of membrane integrity and thus trigger BS. In other cases, or in other cultivars, the buildup of internal pressure might result in failure of the cuticle and culminate in berry cracking or splitting (Keller et al. 2015b, Chang et al. 2019, Chang and Keller 2021).
Conclusion
The present study showed that suspending water supply during the lag phase of berry development followed by rewatering at 50% veraison led to BS in field-grown, own-rooted Cabernet Sauvignon vines in arid southeastern Washington. Ice-cooling the irrigation water led to a comparatively minor increase in BS incidence. Though the underlying causes remain unclear, fluctuations in vine water status during the transition to berry ripening may be involved in triggering BS. This knowledge may be useful for developing vineyard management strategies that avoid sudden changes in soil moisture, and perhaps soil temperature, around veraison. In irrigated vineyards, large fluctuations might be avoided by increasing the irrigation frequency where possible, especially during the period leading up to veraison and through early ripening. While unirrigated vineyards do not have that option available, growers might be able to manage cover crops with the same goal in mind.
Footnotes
This project was funded by a scholarship from Free University of Bozen-Bolzano, the Italian Ministry of University and Research Foundation (TN 2043), the National Institute of Food and Agriculture of the U.S. Department of Agriculture (Hatch project 7003737), and the Chateau Ste. Michelle Distinguished Professorship in Viticulture. We thank Alan Kawakami and Lynn Mills for skilled technical assistance.
Wenter A, Andreotti C, Zanotelli D and Keller M. 2025. Alleviating water stress at veraison may trigger berry shrivel disorder in susceptible grapevines. Am J Enol Vitic 76:0760010. DOI: 10.5344/ajev.2025.25009
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The data underlying this study are available on request from the corresponding author.
- Received February 2025.
- Accepted February 2025.
- Published online April 2025
This is an open access article distributed under the CC BY 4.0 license.
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