Foliar Application of Abscisic Acid Induces Dormancy Responses in Greenhouse-grown Grapevines

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  • 1 Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691
  • 2 Department of Horticulture and Crop Science, The Ohio State University, 2021 Coffey Road, Columbus, OH 43210
  • 3 Department of Horticulture and Crop Science, Ohio Agricultural Research and Development Center, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691

The purpose of this study was to investigate the influence of foliar application of abscisic acid (ABA) on grapevine dormancy, specifically to: 1) determine the optimum foliar application concentration of ABA and 2) evaluate the morphological and physiological changes of greenhouse-grown grapevines in response to exogenous ABA application. Vitis vinifera ‘Cabernet Franc’ and Vitis spp. ‘Chambourcin’ with different leaf ages (40, 50, 80, 100, 110, and 120 days) were subjected to foliar ABA application at different concentrations (0, 100, 200, 400, 600, 800, 1600, and 3200 mg·L−1) and to a cold-acclimated regime. Concentrations of 800 mg·L−1 or higher were phytotoxic and the optimum concentrations were between 400 and 600 mg·L−1. Optimum concentrations of ABA inhibited shoot growth and advanced growth cessation, periderm formation, and leaf senescence, which led to advanced dormancy in both cultivars. In this study, it was concluded that exogenous ABA induced endodormancy because single cuttings (not paradormant) under favorable growing conditions (not ecodormant) were used. Furthermore, grapevine response to ABA was influenced by leaf age and cold treatment. ABA was effective in inhibiting shoot growth and increasing periderm formation in the young vines with 40- to 50-day old leaves and the old grapevines with 80- to 120-day old leaves. However, ABA was effective in inducing early shoot cessation, leaf senescence and abscission, and dormancy in old vines with 100- to 120-day old leaves only. The advanced morphological and physiological changes induced by exogenous ABA mimicked those triggered by environmental cues during the cold acclimation process. It was suggested that advancing the cold acclimation process using foliar ABA application may be beneficial for long-season grape cultivars grown in regions with short growing seasons and early fall frost events.

Abstract

The purpose of this study was to investigate the influence of foliar application of abscisic acid (ABA) on grapevine dormancy, specifically to: 1) determine the optimum foliar application concentration of ABA and 2) evaluate the morphological and physiological changes of greenhouse-grown grapevines in response to exogenous ABA application. Vitis vinifera ‘Cabernet Franc’ and Vitis spp. ‘Chambourcin’ with different leaf ages (40, 50, 80, 100, 110, and 120 days) were subjected to foliar ABA application at different concentrations (0, 100, 200, 400, 600, 800, 1600, and 3200 mg·L−1) and to a cold-acclimated regime. Concentrations of 800 mg·L−1 or higher were phytotoxic and the optimum concentrations were between 400 and 600 mg·L−1. Optimum concentrations of ABA inhibited shoot growth and advanced growth cessation, periderm formation, and leaf senescence, which led to advanced dormancy in both cultivars. In this study, it was concluded that exogenous ABA induced endodormancy because single cuttings (not paradormant) under favorable growing conditions (not ecodormant) were used. Furthermore, grapevine response to ABA was influenced by leaf age and cold treatment. ABA was effective in inhibiting shoot growth and increasing periderm formation in the young vines with 40- to 50-day old leaves and the old grapevines with 80- to 120-day old leaves. However, ABA was effective in inducing early shoot cessation, leaf senescence and abscission, and dormancy in old vines with 100- to 120-day old leaves only. The advanced morphological and physiological changes induced by exogenous ABA mimicked those triggered by environmental cues during the cold acclimation process. It was suggested that advancing the cold acclimation process using foliar ABA application may be beneficial for long-season grape cultivars grown in regions with short growing seasons and early fall frost events.

The grape and wine industries in Midwestern and Eastern states have been expanding rapidly and demand for premium wine grapes has also increased. Unfortunately, several premium cultivars do not ripen properly in those regions as a result of the short growing season. This impacts not only the quality of the fruit and wine, but also the cold acclimation process and ultimately the winter hardiness of grapevines (Zabadal et al., 2007). Freeze protection methods have been developed for grapevines, including active and passive methods. Active protection methods include wind machines, heaters, and over-vine sprinkling (Poling, 2007). Passive methods include site and variety selection (Striegler, 2007; Zabadal et al., 2007) and application of chemical protectants (Dami and Beam, 2004; Dami et al., 2000). Among chemicals, growth regulators such as ABA have been applied to crops including Secale cereale L. (Churchill et al., 1998) and Malus domestica (L.) Borkh. (Guak and Fuchigami, 2001) to improve their cold hardiness.

ABA is a plant hormone that plays several physiological roles, including regulation of shoot and root growth (Saab et al., 1990), stomatal closure (Liang and Zhang, 1999), and leaf senescence (Thomas and Stoddart, 1980). Additionally, ABA has been suggested as a dormancy-inducing hormone because it accumulates in dormant nodes and increases after the tissue is exposed to low temperatures (Dogramaci et al., 2010). The variation of ABA concentration in plant tissues, mostly in nodes and xylem tissues, correlates with the cold acclimation process of plants (Mader et al., 2003; Rinne et al., 1994). Therefore, ABA has been proven to play an important role in the development of cold acclimation and ultimately the increase of freezing tolerance in plant species such as Arabidopsis thaliana (L.) Heynh. (Mantyla et al., 1995), Betula pendula Roth. (Li et al., 2003), Hordeum vulgare L. (Bravo et al., 1998), Secale cereale L. (Churchill et al., 1998), Triticum aestivum L. (Dallaire et al., 1994), Solanum tuberosum L. (Mora-Herrera and Lopez-Delgado, 2007), and Acer saccharum Marsh. (Bertrand et al., 1997).

Exogenous application of ABA has also been investigated with grapes. ABA was used to delay budburst for spring frost protection but was not effective on field-grown grapevines (Hellman et al., 2006). ABA has also been used on table grapes to enhance color development and advance fruit maturity (Amiri et al., 2009; Peppi et al., 2007). To our knowledge, there are no published reports on the effect of exogenous ABA on inducing dormancy of grapevines. The purpose of this study was to investigate the influence of foliar application of ABA on grapevine dormancy. Our hypothesis stated that ABA would induce morphological and physiological changes in grapevines that mimic environmental cues including low temperature and/or a short photoperiod that lead to dormancy. The specific objectives were to: 1) determine the optimum foliar application concentration of ABA; and 2) evaluate the morphological and physiological changes of greenhouse-grown grapevines in response to exogenous ABA application.

Materials and Methods

Plant materials, growing conditions, and abscisic acid treatment

In the first year, 1-year-old dormant Vitis vinifera ‘Cabernet Franc’ (CF) grafted on V. riparia × V. rupestris ‘Couderc 3309’ were planted in 7.6-L pots and placed on benches in the greenhouse in Dec. 2008. In the second year, the same potted vines were used after being pruned back to two nodes and stored in a 4 °C cooler to satisfy their chilling requirement. In Year 2, 1-year-old Vitis spp. ‘Chambourcin’ (CHB) grapevines were also used. Before applying ABA, the average leaf number and shoot length per vine were 16 and 120 cm, respectively.

In the first year, the plants were grown in a climate-controlled greenhouse for the non-acclimated condition and a growth chamber (Conviron, Pembina, ND) for the cold-acclimated regime. The greenhouse conditions were as follows: 22/19 °C and 50/50% relative humidity (day/night). The light intensity in the greenhouse was maintained at 300 μmol·m−2·s−1 using 1000-W metal halide and 1000-W high-pressure sodium lights (Sunlight Supply, Woodland, WA) with a 12-h photoperiod. The growth chamber conditions for the cold acclimation experiment were 23.0/15.0 °C and 50/50% relative humidity (day/night) in the first week and then 15.0/7.0 °C (day/night) for 3 weeks (Grant et al., 2009). The light intensity in the growth chamber was maintained at 300 μmol·m−2·s−1 with an 8-h photoperiod. All grapevines were watered daily and fertilized every other day with 100 mg·L−1 20–20–20 fertilizer (Peters Professional, Marysville, OH). In the second year, the conditions in the greenhouse were the same as in Year 1 with the exception that the growth chamber for the cold acclimation experiment was maintained at 12-h photoperiod. The ABA (VBS 350001) sample was provided by Valent Bioscience (Libertyville, IL). The a.i. was 20.0% (w/w) S-ABA. The ABA sample was dissolved in deionized water with 0.05% Tween-20 (Acros Organic, Hampton, NH). Whole vines were sprayed with ABA solutions to runoff with a 7.6-L handheld sprayer (Gilmour Gardening Innovation, Peoria, IL) averaging a spray volume of 0.2 L/vine.

Leaf age was determined based on Eichorn-Lorenz (EL) stages of shoot development (Eichhorn and Lorenz, 1977) with 1-d leaf age corresponding to the first unfolded leaf (EL stage 7) originating from the third basal node.

In Year 1, two experiments were conducted. The first experiment consisted of applying ABA to CF in the greenhouse at a concentration of 0, 100, 200, 400, 800, 1600, and 3200 mg·L−1 when leaf age averaged 40 d. The second experiment consisted of applying ABA to CF in the greenhouse at concentrations of 0, 200, 400, and 600 mg·L−1 in the greenhouse and growth chamber when leaf age averaged 110 d. In Year 2, experiments were repeated to confirm ABA concentrations and plant response relative to leaf age and growing conditions. The first experiment was conducted at 50- and 100-d leaf age stages in the greenhouse (non-acclimated) and growth chamber (cold-acclimated) with ABA concentrations of 0, 200, 400, and 600 mg·L−1. The second experiment was conducted in the greenhouse by applying ABA (0 and 600 mg·L−1) at 40, 80, and 120-d leaf age stages. In the Year 1 experiment, a randomized block design was used with five replications per treatment of two vines per replication; in the Year 2 experiment, four replications per treatment were used with one vine per replication. Four vines of uniform growth per cultivar were selected for ABA treatments. In all experiments in both years, the shoot tips of the grapevines were cut back to 14 to 16 nodes a week before ABA application.

Abscisic acid phytotoxicity

The phytotoxicity of ABA was evaluated in leaves and nodes. Visual observation of leaf distortion was made 24 h after ABA application and leaf injury was assessed and recorded a week after ABA treatments and based on leaf damage incidence (LDI) and leaf damage severity (LDS). LDI is the ratio of number of damaged leaves to the total number of leaves. Leaves with scorching-like dots and flecks were recorded as damaged leaves. Damaged leaf area larger than 0.1 cm2 was counted in severity assessment. Abscised leaves were counted as damaged leaves as well. LDS assessed the percentage of damaged leaf area using a score rating as follows: 0: 0% (no symptom); 1: 1% to 25%; 2: 26% to 50%; 3: 51% to 75%; and 4: 76% to 100% damaged leaf area. An LSD = 4 was also assigned to abscised leaves. Bud injury assessment was measured by assessing shoot growth resumption ≈2 months after ABA application. Nodes that did not break were excised and visually evaluated whether they were alive (green) or injured (brown).

Vegetative growth

Shoot growth.

Each shoot was marked at 15 cm from the tip before ABA application. Then the distance between the tip and marker was measured three times a week and the shoot growth rates (cm·d−1) were calculated as the total new growth divided by the number of days.

Growth cessation.

In the first year, all lateral shoots were removed during the course of the experiment. Shoot tip abscission was used to determine growth cessation but it did not occur for CF. Therefore, in the second year, growth cessation was estimated by proxy using the methods by Garris et al. (2009) on both CF and CHB. This method consisted of monitoring the summer lateral shoot emergence. The number of nodes with a lateral shoot having at least one fully expanded leaf was recorded. Growth cessation was determined when no summer laterals were produced (Garris et al., 2009).

Periderm development and leaf senescence

Periderm development.

Periderm formation was determined by counting shoot internodes that changed color from green to tan or brown 4 weeks after ABA application. Periderm formation was expressed as the ratio of number of brown to total number of internodes per shoot.

Leaf senescence and abscission.

This physiological stage was assessed by monitoring chlorophyll concentration and eventually counting leaf abscission. The measurement of chlorophyll concentration was conducted twice a week using a SPAD-520 chlorophyll meter (Spectrum Technologies, Inc., East Plainfield, IL) for 4 weeks. Five random measurements were taken on the upper surface of the fifth basal leaf. These measurements were conducted on CF and CHB grapevines in the second year. Leaf abscission was determined as the percent of abscised leaves to the total number of leaves 30 d after ABA application (DAA).

Dormancy

Lignified shoots with periderm formation from the base were excised into one-node cuttings ≈5 cm long, then inserted into 2.5 cm × 2.5-cm foam medium (Smithers-Oasis, Kent, OH) and placed in 55 cm × 25 cm × 7 cm plastic trays (T.O. Plastics, Clearwater, MN) filled with water. For each replication, 10 to 12 brown cuttings were used with the exception of young grapevines (leaf age = 40 or 50 d), from which green cuttings were used. Trays were then placed under forcing conditions on benches in a growth chamber (Conviron, Pembina, ND) with the following settings: 24-h photoperiod with 300 μmol·m−2·s−1, 22 °C, and 80% relative humidity. Budburst was recorded as EL stage 5 and monitored three times a week for 30 d. Dormancy was estimated as the number of days to 50% budburst (D50BB). The higher D50BB, the more nodes are dormant. An increased D50BB indicated that nodes went into endodormancy.

Statistical analysis

All data were subjected to analysis of variance using Minitab statistical software (Minitab Inc., State College, PA). The model tested for main effects of application timing and concentration and for potential interaction between timing and concentration. When appropriate, means were separated using least significant difference (α = 0.05).

Results

Abscisic acid phytotoxicity.

Leaf damage symptoms in CF grapevines were observed 24 h after ABA spray application at the concentrations of 800 mg·L−1 and above. CF grapevines treated with ABA concentrations of 100, 200, 400, and 600 mg·L−1 showed the same symptoms 6, 5, 3, and 2 d after ABA spray application, respectively (Fig. 1). A week after ABA application, leaf damage was detected on all ABA-treated grapevines in both cultivars. On mature leaves treated with ABA at all concentrations, the damage started with black spots on the lower surface of the blade, then the spots expanded and appeared on the upper surface as yellow (CF) or red (CHB) spots and flecks ≈0.25 cm2 in size (Fig. 1). At the shoot apical zone, ABA concentrations of 1600 and 3200 mg·L−1 burned shoot tips and young leaves. ABA concentrations of 800 mg·L−1 and lower caused shoot stunting but growth resumed later. Two to 4 DAA, leaf deformation was apparent on the first unfolded leaf treated with ABA at or above 400 mg·L−1. Deformed leaves had abnormal margins and failed to develop the typical five-lobe leaf shape in CF. ABA concentrations of 400, 800, 1600, and 3200 mg·L−1 caused a proportional increase of deformed leaves of one, three, five, and five, respectively. The growth of normally shaped leaves resumed after the emergence of the apical five leaves. This demonstrated that ABA concentrations equal to 400 mg·L−1 or higher caused a transient disturbance of the normal development of shoot tips, which led to leaf deformation. A week after ABA application, LDI increased proportionally with ABA concentrations. ABA concentrations of 0, 100, 200, 400, 800, 1600, and 3200 mg·L−1 led to LDI values of 0%, 8%, 24%, 26%, 52%, 64%, and 72%, respectively. LDS followed a similar pattern as LDI and was concentration-dependent as well (Fig. 2A). ABA concentrations at 1600 mg·L−1 or above had LDS values above 1, indicating damage above 25% leaf area (Fig. 2A). Bud injury occurred at ABA concentrations of 800 (28%), 1600 (47%), and 3200 mg·L−1 (57%). In Year 2, the highest concentration of ABA application was 600 mg·L−1 and resulted in no bud injury (data not shown). Therefore, it was concluded that the treatments with concentrations of 800 mg·L−1 or higher caused not only extensive leaf damage, but also bud injury.

Fig. 1.
Fig. 1.

Leaf damage shown on ‘Cabernet Franc’ leaves 1 week after abscisic acid (ABA) application. (A–G) ABA concentration of 0, 100, 200, 400, 800, 1600, 3200 mg·L−1.

Citation: HortScience horts 46, 9; 10.21273/HORTSCI.46.9.1271

Fig. 2.
Fig. 2.

(A) Effect of abscisic acid (ABA) and concentration on leaf damage severity (LDS) of potted ‘Cabernet Franc’ grapevines (leaf age = 40 d) a week after ABA foliar application. (B) Effect of ABA and concentration on LDS of potted ‘Cabernet Franc’ grapevines under non-acclimated and cold-acclimated conditions (leaf age = 110 d) 1 week after ABA application. (C) Effect of ABA (0 mg·L−1 or control, and 600 mg·L−1) and leaf age on LDS of potted ‘Cabernet Franc’ grapevines a week after ABA application.

Citation: HortScience horts 46, 9; 10.21273/HORTSCI.46.9.1271

In the cold acclimation experiment, CF grapevines with 110-d-old leaves were used. LDI and LDS also increased with increasing ABA concentrations, which indicated foliar application of ABA was phytotoxic under both cold- and non-acclimated conditions (Fig. 2B). Therefore, the combination of ABA application and cold treatment increased leaf damage, and the severity of the damage was concentration-dependent (Fig. 2B).

LDS values in the grapevines with older leaves (leaf age = 110 d; Fig. 2B) were generally higher than those with younger leaves (leaf age = 40 d; Fig. 2A). This prompted a leaf age experiment to verify whether ABA phytotoxicity increased with leaf age. This experiment demonstrated an increase of LDI (data not shown) and LDS, which were proportional to leaf age (Fig. 2C). Therefore, phytotoxicity of ABA was also leaf age-dependent.

To verify whether these responses were cultivar-dependent, CHB was also used. Generally, results from CHB were similar to those from CF with the exception that the color of CHB leaf damage was red, which was different from the yellow color damage on CF leaves. Additionally, the values of LDI and LDS of CHB were less than those of CF grapevines, which indicates that different cultivars have different concentrations of tolerance to ABA (data not shown).

Vegetative growth.

Shoot inhibition was observed at the first measurement, 48 h after ABA application. The shoot length was reduced by ABA and was concentration-dependent with 200 mg·L−1 having the least inhibition and 600 mg·L−1 having the most inhibition (Fig. 3). At 28 DAA, shoot length and growth rate were reduced by 50% and 39%, respectively, with 600 mg·L−1 as compared with control (Fig. 3; Table 1). The numbers of nodes was not different between ABA-treated vines and control (data not shown), indicating that ABA inhibited shoot growth by shortening the internode length. Furthermore, the growth rate decreased with increased leaf age (Table 1).

Table 1.

Effect of abscisic acid (ABA) and leaf age on shoot growth, leaf senescence, periderm formation, and dormancy of potted ‘Cabernet Franc’ grapevines.

Table 1.
Fig. 3.
Fig. 3.

Effect of abscisic acid (ABA) and concentration on shoot length progression of potted ‘Cabernet Franc’ grapevines (leaf age = 50 d).

Citation: HortScience horts 46, 9; 10.21273/HORTSCI.46.9.1271

Under cold-acclimated conditions, shoot length and growth rate were further reduced by ABA as compared with non-acclimated conditions (Table 2). The ABA-treated and cold-acclimated vines had shoot lengths 59% and 66% less than that of acclimated and non-acclimated control, respectively (Fig. 4). Furthermore, control grapevines under cold-acclimated condition had similar growth rates as those from 400 to 600 mg·L−1 ABA-treated grapevines under non-acclimated conditions (Table 2). In other words, the shoot inhibition in control vines under cold-acclimated conditions was similar to that by ABA-treated vines (400 and 600 mg·L−1) under non-acclimated conditions.

Table 2.

Effects of abscisic acid (ABA) and concentrations on shoot growth, leaf senescence, periderm formation, and dormancy of potted ‘Cabernet Franc’ grapevines.

Table 2.
Fig. 4.
Fig. 4.

Effect of abscisic acid (ABA) on shoot length progression of potted ‘Cabernet Franc’ grapevines under cold-acclimated and non-acclimated conditions (leaf age = 50 d).

Citation: HortScience horts 46, 9; 10.21273/HORTSCI.46.9.1271

Shoot tip abscission of CF was monitored to determine the occurrence of growth cessation, but no abscission was observed from either control or ABA-treated grapevines when leaf age averaged 40 to 80 d (Tables 1 and 2). However, growth cessation occurred at leaf age of 100 to 120 d when treated with 600 mg·L−1 ABA (Tables 1 and 2).

Periderm development and leaf senescence.

The increase of periderm formation was observed on ABA-treated grapevines with 50- and 100-d-old leaves (Table 2). The ABA-induced periderm formation was concentration-dependent, with 200 mg·L−1 having the least increase and 400 mg·L−1 and above having the most increase (Table 2). Periderm formation increased by 86% in treated vines with 600 mg·L−1 ABA as compared with control (Table 1). Furthermore, periderm formation was affected by ABA and leaf age and the interaction between ABA and older leaves led to maximum periderm formation (Table 1).

There was no difference of leaf chlorophyll concentration between control and ABA-treated vines with 50-d leaf age (Table 2). However, ABA at 600 mg·L−1 induced leaf senescence in vines with 100-d-old leaves (Table 2). This was confirmed with the leaf age experiment at which 600 mg·L−1 ABA induced leaf senescence in the grapevines with 120-d-old leaves. The decrease of chlorophyll concentration in treated vines started 14 DAA and continued until the end of the experiment (Fig. 5). This indicates that ABA accelerated the leaf senescence process and under these conditions was advanced by a minimum of 14 d as compared with the control. In addition, there was an interaction between concentration and leaf age, indicating that leaf senescence was induced by both ABA and leaf age and was enhanced by higher ABA concentration and older leaves (Table 1).

Fig. 5.
Fig. 5.

Effect of abscisic acid (ABA) (0 mg·L−1 or control, and 600 mg·L−1) on leaf chlorophyll concentration progression of potted ‘Cabernet Franc’ grapevines (leaf age = 120 d).

Citation: HortScience horts 46, 9; 10.21273/HORTSCI.46.9.1271

No leaf abscission occurred when leaf age averaged 40 to 50 d (Tables 1 and 2). However, leaf abscission increased with ABA concentration when leaf age averaged 100 d (Table 2). At equal concentration, leaf abscission in vines with leaf age 120 d increased 4.5-fold as compared with that in vines with leaf age 80 d (Table 1).

Dormancy.

All grape cuttings had budburst at the end of the 30-d long dormancy assay (≈58 DAA). The ABA treatments did not promote bud dormancy on grapevines with leaf age averaging 40 to 50 d (Tables 1 and 2). The shoots and nodes from the young vines were still green when placed under forcing condition and100% budburst occurred within 2 weeks. However, ABA concentrations of 400 and 600 mg·L−1 delayed budburst in older grapevines with leaf age averaging 80 to 100 d (Tables 1 and 2). The delay of budburst between ABA-treated and control vines indicated that the former entered dormancy earlier than the latter. Under forcing conditions, ABA concentrations of 400 and 600 mg·L−1 advanced dormancy by 6 to 7 d as compared with control (Table 2). Furthermore, the leaf age experiment not only confirmed that ABA advanced dormancy, but also demonstrated that ABA effect was enhanced by leaf age (Table 1).

Discussion

ABA concentrations of 800 mg·L−1 or higher caused severe leaf and bud injuries. Therefore, it was concluded that ABA concentrations of 800 mg·L−1 and higher were phytotoxic. Phytotoxicity at these concentrations has been linked to oxidative damage. In fact, Jiang and Zhang (2001) reported that ABA is a promoter of the antioxidant defense system when plants are under oxidative stress, but high ABA concentration (1000 mg·L−1) induced an excessive production of active oxygen species, which led to an oxidative damage to leaves of maize seedlings. Waterland et al. (2010) demonstrated that application of S-ABA in bedding plants induced phytotoxicity. It was also suspected that phytotoxicity was associated with the low pH of ABA solutions, which varied from pH = 2.8 for 3200 mg·L−1 to pH = 3.8 for 200 mg·L−1. However, buffered ABA solutions to neutral pH led to more injury at equal concentration (data not shown). Therefore, the extreme low pH was not the cause of injury. In addition, leaves of CHB showed less damage than those of CF at the same ABA concentration, which indicates a differential response among grape genotypes to ABA. The published non-phytotoxic concentrations of ABA applied to clusters in vineyards varied between 100 mg·L−1 and 1000 mg·L−1 (Amiri et al., 2009; Peppi et al., 2007). It is possible that ABA phytotoxic concentrations are different between greenhouse- and field-grown grapevines as well as between leaves and clusters.

Furthermore, deformation of newly grown leaves in treated grapevines is termed heterophylly and has been reported on Marsilea quadrifolia L. after ABA application. This response was confirmed to be ABA-inducible by the upregulation of ABA-responsive heterophylly genes (Lin et al., 2005).

The shoot growth of grapevines was consistently inhibited by ABA for both cultivars regardless of leaf age. This resulted in short internode length in ABA-treated grapevines. This observation is consistent with previous reports on ABA reducing the internode length of rice (Hoffmann-Benning and Kende, 1992), tobacco (Steadman and Sequeira, 1970), and apple (Guak and Fuchigami, 2001). Furthermore, the shoot length inhibition by ABA in young and old leaves indicates that this is an early response that is independent of leaf age. Shoot growth inhibition has been linked to ABA in several reports, which proposed mechanisms that ABA interacts with other plant hormones such as cytokinin (Vysotskaya et al., 2009), gibberellin (Hoffmann-Benning and Kende, 1992), and ethylene (Hansen and Grossmann, 2000), which led to promotion or inhibition of growth. The growth cessation is an early step in the senescence process and has been considered an early response of cold acclimation (Williams et al., 1972). During the process of cold acclimation in grapevine, a key change is the progression of periderm formation from shoot base to tip (Fennel and Hoover, 1991; Zabadal et al., 2007). The increased rate of periderm formation in ABA-treated vines may indicate an acceleration of the cold acclimation process.

Leaf senescence is another step in the cold acclimation and dormancy processes (Kozlowski and Pallardy, 2002). In this study, advanced leaf senescence was observed in ABA-treated grapevines of both cultivars. Previous research on cotton rootstocks indicated that leaf senescence was closely associated with the ABA accumulation in the roots (Dong et al., 2008). The linkage between ABA and leaf senescence has been demonstrated in Arabidopsis thaliana with upregulation of two senescence-associated mRNA, pSEN4 and pSEN5, after exogenous ABA application (Park et al., 1998).

In this study, the exogenous application of ABA may have led to an increase in the concentration of endogenous ABA, which was closely related to the extent of dormancy. In fact, concentrations of endogenous ABA were found to increase as the grape nodes entered dormancy and were the highest at maximum dormancy (Mochioka et al., 1996; Or et al., 2000). ABA was considered a positive regulator of dormancy induction and maintenance (Kucera et al., 2005). Bud dormancy in woody species including grapes is categorized into three different types based on the inhibition sources: 1) paradormancy, the inhibition is from distal organs; 2) endodormancy, the inhibition is from internal bud signals; and 3) ecodormancy, the inhibition is from unfavorable environmental conditions (Lang et al., 1987). In this study, it was concluded that exogenous ABA induced endodormancy because we used single cuttings (not paradormant) under favorable growing conditions (not ecodormant).

This study also demonstrated that ABA was effective in inducing early responses, including shoot growth inhibition and periderm formation, in the grapevines with young leaves (leaf age 40 to 50 d). However, ABA was ineffective in inducing growth cessation, leaf senescence and abscission, and dormancy in young vines. The latter responses were affected by ABA only with the grapevines with old leaves (leaf age 80 to 120 d), thus deemed age-related. The age-related effect of ABA has been explained by the function of an ABA-induced, age-induced gene RPK1 in Arabidopsis, which encodes a receptor kinase (Lee et al., 2011). The conditional overexpression of RPK1 at the mature stage accelerated the senescence and cell death and upregulated various ABA inducible genes, which indicated the effect of ABA was age-dependent (Lee et al., 2011).

Based on this greenhouse study, the optimum concentration of ABA was between 400 and 600 mg·L−1 and its exogenous application led to morphological and physiological changes similar to those induced by environmental cues including low temperature and/or a short photoperiod during the cold acclimation process. Furthermore, this study demonstrated the chronological sequences of morphological and physiological changes in CF and CHB starting with early responses, including shoot inhibition and periderm formation, followed by later responses, including growth cessation and leaf senescence and abscission, which ultimately led to bud dormancy. Therefore, the exogenous application of ABA initiated a cascade of steps that advanced the cold acclimation process in the absence of environmental cues. It was suggested that advancing the cold acclimation process using foliar ABA application may be beneficial for long-season grape cultivars grown in regions with short growing seasons and early fall frost events.

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  • Eichhorn, K.W. & Lorenz, D.H. 1977 Phenological development stages of the grapevine Nachrichtenbl. Dt. Pflanzenschutzd 29 119 120

  • Fennel, A. & Hoover, E. 1991 Photoperiod influences growth, bud dormancy, and cold acclimation in Vitis labruscana and V. riparia J. Amer. Soc. Hort. Sci. 116 270 273

    • Search Google Scholar
    • Export Citation
  • Garris, A., Clark, L., Owens, C., McKay, S., Luby, J., Mathiason, K. & Fennell, A. 2009 Mapping of photoperiod-induced growth cessation in the wild grape Vitis riparia J. Amer. Soc. Hort. Sci. 134 261 272

    • Search Google Scholar
    • Export Citation
  • Grant, T.N., Dami, I.E., Ji, T., Scurlock, D. & Streeter, J. 2009 Variation in leaf and bud soluble sugar concentration among Vitis genotypes grown under two temperature regimes Can. J. Plant Sci. 89 961 968

    • Search Google Scholar
    • Export Citation
  • Guak, S. & Fuchigami, L.H. 2001 Effects of applied ABA on growth cessation, bud dormancy, cold acclimation, leaf senescence and N mobilization in apple nursery plants J. Hort. Sci. Biotechnol. 76 459 464

    • Search Google Scholar
    • Export Citation
  • Hansen, H. & Grossmann, K. 2000 Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition Plant Physiol. 124 1437 1448

  • Hellman, E., Shelby, S. & Lowery, C. 2006 Exogenously applied abscisic acid did not consistently delay budburst of deacclimating grapevine J. Amer. Pom. Soc. 60 178 186

    • Search Google Scholar
    • Export Citation
  • Hoffmann-Benning, S. & Kende, H. 1992 On the role of abscisic-acid and gibberellin in the regulation of growth in rice Plant Physiol. 99 1156 1161

  • Jiang, M.Y. & Zhang, J.H. 2001 Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings Plant Cell Physiol. 42 1265 1273

    • Search Google Scholar
    • Export Citation
  • Kozlowski, T.T. & Pallardy, S.G. 2002 Acclimation and adaptive responses of woody plants to environmental stresses Bot. Rev. 68 270 334

  • Kucera, B., Cohn, M.A. & Leubner-Metzger, G. 2005 Plant hormone interactions during seed dormancy release and germination Seed Sci. Res. 15 281 307

  • Lang, G.A., Early, J.D., Martin, G.C. & Darnell, R.L. 1987 Endodormancy, paradormancy, and ecodormancy—Physiological terminology and classification for dormancy research HortScience 22 371 377

    • Search Google Scholar
    • Export Citation
  • Lee, I.C., Hong, S.W., Whang, S.S., Lim, P.O., Nam, H.G. & Koo, J.C. 2011 Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves Plant Cell Physiol. 52 651 662

    • Search Google Scholar
    • Export Citation
  • Li, C.Y., Junttila, O., Heino, P. & Palva, E.T. 2003 Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application Tree Physiol. 23 481 487

    • Search Google Scholar
    • Export Citation
  • Liang, J.S. & Zhang, J.H. 1999 The relations of stomatal closure and reopening to xylem ABA concentration and leaf water potential during soil drying and rewatering Plant Growth Regulat. 29 77 86

    • Search Google Scholar
    • Export Citation
  • Lin, B.L., Wang, H.J., Wang, J.S., Zaharia, L.I. & Abrams, S.R. 2005 Abscisic acid regulation of heterophylly in Marsilea quadrifolia L.: Effects of R-(-) and S-(+) isomers J. Expt. Bot. 56 2935 2948

    • Search Google Scholar
    • Export Citation
  • Mader, J.C., Emery, R.J.N. & Turnbull, C.G.N. 2003 Spatial and temporal changes in multiple hormone groups during lateral bud release shortly following apex decapitation of chickpea (Cicer arietinum) seedlings Physiol. Plant. 119 295 308

    • Search Google Scholar
    • Export Citation
  • Mantyla, E., Lang, V. & Palva, E.T. 1995 Role of abscisic-acid in drought-induced freezing tolerance, cold-acclimation, and accumulation of Lt178 and Rab18 proteins in Arabidopsis-Thaliana Plant Physiol. 107 141 148

    • Search Google Scholar
    • Export Citation
  • Mochioka, R., Tohbe, M., Horiuchi, S., Ogata, T., Shiozaki, S., Kawase, K.J., Kurooka, H. & Matsui, H. 1996 The relationship between bud dormancy and the endogenous ABA and water contents of several wild grape species native to Japan J. Jpn. Soc. Hort. Sci. 65 49 54

    • Search Google Scholar
    • Export Citation
  • Mora-Herrera, M.E. & Lopez-Delgado, H.A. 2007 Freezing tolerance and antioxidant activity in potato microplants induced by abscisic acid treatment Amer. J. Potato Res. 84 467 475

    • Search Google Scholar
    • Export Citation
  • Or, E., Belausov, E., Popilevsky, I. & Ben Tal, Y. 2000 Changes in endogenous ABA level in relation to the dormancy cycle in grapevines grown in a hot climate J. Hort. Sci. Biotechnol. 75 190 194

    • Search Google Scholar
    • Export Citation
  • Park, J.H., Oh, S.A., Kim, Y.H., Woo, H.R. & Nam, H.G. 1998 Differential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis Plant Mol. Biol. 37 445 454

    • Search Google Scholar
    • Export Citation
  • Peppi, M.C., Fidelibus, M.W. & Dokoozlian, N.K. 2007 Application timing and concentration of abscisic acid affect the quality of 'Redglobe' grapes J. Hort. Sci. Biotechnol. 82 304 310

    • Search Google Scholar
    • Export Citation
  • Poling, E.B. 2007 Overview of active frost, frost/freeze and freeze protection methods Understanding and Preventing Freeze Damage in the Vineyards Workshop Proc 47 64

    • Search Google Scholar
    • Export Citation
  • Rinne, P., Tuominen, H. & Junttila, O. 1994 Seasonal changes in bud dormancy in relation to bud morphology, water and starch content, and abscisic acid concentration in adult trees of Betula pubescens Tree Physiol. 14 549 561

    • Search Google Scholar
    • Export Citation
  • Saab, I.N., Sharp, R.E., Pritchard, J. & Voetberg, G.S. 1990 Increased endogenous abscisic-acid maintains primary root-growth and inhibits shoot growth of maize seedlings at low water potentials Plant Physiol. 93 1329 1336

    • Search Google Scholar
    • Export Citation
  • Steadman, J.R. & Sequeira, L. 1970 Abscisic acid in tobacco plants—Tentative identification and its relation to stunting induced by Pseudomonas Solanacearum Plant Physiol. 45 691 697

    • Search Google Scholar
    • Export Citation
  • Striegler, R.K. 2007 Passive freeze prevention methods Understanding and Preventing Freeze Damage in the Vineyards Workshop Proc 39 46

  • Thomas, H. & Stoddart, J.L. 1980 Leaf senescence Annu. Rev. Plant Physiol. Plant Mol. Biol. 31 83 111

  • Vysotskaya, L.B., Korobova, A.V., Veselov, S.Y., Dodd, I.C. & Kudoyarova, G.R. 2009 ABA mediation of shoot cytokinin oxidase activity: Assessing its impacts on cytokinin status and biomass allocation of nutrient-deprived durum wheat Funct. Plant Biol. 36 66 72

    • Search Google Scholar
    • Export Citation
  • Waterland, N.L., Finer, J.J. & Jones, M.L. 2010 Benzyladenine and gibberellic acid application prevents abscisic acid-induced leaf chlorosis in Pansy and Viola HortScience 45 925 933

    • Search Google Scholar
    • Export Citation
  • Williams, B.J., Pellett, N.E. & Klein, R.M. 1972 Phytochrome control of growth cessation and initiation of cold-acclimation in selected woody plants Plant Physiol. 50 262 265

    • Search Google Scholar
    • Export Citation
  • Zabadal, T.J., Dami, I.E., Goffinet, M.C., Martinson, T.E. & Chien, M.L. 2007 Winter injury to grapevines and methods of protection Mich. State Univ Ext. Bul. 2930.

    • Export Citation

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Contributor Notes

We are thankful for the financial support provided by the Department of Horticulture and Crop Science, OARDC/OSU, and the Lonz Foundation. The ABA sample was provided by Valent Bioscience Co. (Libertyville, IL). We also thank Trudi Grant and Dave Scurlock for their technical assistance to grow potted grapevines and Lee Duncan and Kesia Hartzler with environmental control of the greenhouses and growth chambers.

To whom reprint requests should be addressed; e-mail dami.1@osu.edu.

  • View in gallery

    Leaf damage shown on ‘Cabernet Franc’ leaves 1 week after abscisic acid (ABA) application. (A–G) ABA concentration of 0, 100, 200, 400, 800, 1600, 3200 mg·L−1.

  • View in gallery

    (A) Effect of abscisic acid (ABA) and concentration on leaf damage severity (LDS) of potted ‘Cabernet Franc’ grapevines (leaf age = 40 d) a week after ABA foliar application. (B) Effect of ABA and concentration on LDS of potted ‘Cabernet Franc’ grapevines under non-acclimated and cold-acclimated conditions (leaf age = 110 d) 1 week after ABA application. (C) Effect of ABA (0 mg·L−1 or control, and 600 mg·L−1) and leaf age on LDS of potted ‘Cabernet Franc’ grapevines a week after ABA application.

  • View in gallery

    Effect of abscisic acid (ABA) and concentration on shoot length progression of potted ‘Cabernet Franc’ grapevines (leaf age = 50 d).

  • View in gallery

    Effect of abscisic acid (ABA) on shoot length progression of potted ‘Cabernet Franc’ grapevines under cold-acclimated and non-acclimated conditions (leaf age = 50 d).

  • View in gallery

    Effect of abscisic acid (ABA) (0 mg·L−1 or control, and 600 mg·L−1) on leaf chlorophyll concentration progression of potted ‘Cabernet Franc’ grapevines (leaf age = 120 d).

  • Amiri, M.E., Fallahi, E. & Mirjalili, M. 2009 Effects of abscisic acid or ethephon at veraison on the maturity and quality of ‘Beidaneh Ghermez’ grapes J. Hort. Sci. Biotechnol. 84 660 664

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  • Bertrand, A., Robitaille, G., Castonguay, Y., Nadeau, P. & Boutin, R. 1997 Changes in ABA and gene expression in cold-acclimated sugar maple Tree Physiol. 17 31 37

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  • Bravo, L.A., Zuniga, G.E., Alberdi, M. & Corcuera, L.J. 1998 The role of ABA in freezing tolerance and cold acclimation in barley Physiol. Plant. 103 17 23

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  • Churchill, G.C., Reaney, M.J.T., Abrams, S.R. & Gusta, L.V. 1998 Effects of abscisic acid and abscisic acid analogs on the induction of freezing tolerance of winter rye (Secale cereale L.) seedlings Plant Growth Regulat. 25 35 45

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  • Dallaire, S., Houde, M., Gagne, Y., Saini, H.S., Boileau, S., Chevrier, N. & Sarhan, F. 1994 Aba and low-temperature induce freezing tolerance via distinct regulatory pathways in wheat Plant Cell Physiol. 35 1 9

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  • Dami, I.E. & Beam, B.A. 2004 Response of grapevines to soybean oil application Amer. J. Enol. Viticult. 55 269 275

  • Dami, I.E., Hamman, R.A., Stushnoff, C. & Wolf, T.K. 2000 Use of oils and alginate to delay budbreak of grapevines Proc. Amer. Soc. Enol. Viticult. 50th Anniv. Abb. Mtg 51 73 76

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  • Dogramaci, M., Horvath, D.P., Chao, W.S., Foley, M.E., Christoffers, M.J. & Anderson, J.V. 2010 Low temperatures impact dormancy status, flowering competence, and transcript profiles in crown buds of leafy spurge Plant Mol. Biol. 73 207 226

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  • Dong, H., Niu, Y., Li, W. & Zhang, D. 2008 Effects of cotton rootstock on endogenous cytokinins and abscisic acid in xylem sap and leaves in relation to leaf senescence J. Expt. Bot. 59 1295 1304

    • Search Google Scholar
    • Export Citation
  • Eichhorn, K.W. & Lorenz, D.H. 1977 Phenological development stages of the grapevine Nachrichtenbl. Dt. Pflanzenschutzd 29 119 120

  • Fennel, A. & Hoover, E. 1991 Photoperiod influences growth, bud dormancy, and cold acclimation in Vitis labruscana and V. riparia J. Amer. Soc. Hort. Sci. 116 270 273

    • Search Google Scholar
    • Export Citation
  • Garris, A., Clark, L., Owens, C., McKay, S., Luby, J., Mathiason, K. & Fennell, A. 2009 Mapping of photoperiod-induced growth cessation in the wild grape Vitis riparia J. Amer. Soc. Hort. Sci. 134 261 272

    • Search Google Scholar
    • Export Citation
  • Grant, T.N., Dami, I.E., Ji, T., Scurlock, D. & Streeter, J. 2009 Variation in leaf and bud soluble sugar concentration among Vitis genotypes grown under two temperature regimes Can. J. Plant Sci. 89 961 968

    • Search Google Scholar
    • Export Citation
  • Guak, S. & Fuchigami, L.H. 2001 Effects of applied ABA on growth cessation, bud dormancy, cold acclimation, leaf senescence and N mobilization in apple nursery plants J. Hort. Sci. Biotechnol. 76 459 464

    • Search Google Scholar
    • Export Citation
  • Hansen, H. & Grossmann, K. 2000 Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition Plant Physiol. 124 1437 1448

  • Hellman, E., Shelby, S. & Lowery, C. 2006 Exogenously applied abscisic acid did not consistently delay budburst of deacclimating grapevine J. Amer. Pom. Soc. 60 178 186

    • Search Google Scholar
    • Export Citation
  • Hoffmann-Benning, S. & Kende, H. 1992 On the role of abscisic-acid and gibberellin in the regulation of growth in rice Plant Physiol. 99 1156 1161

  • Jiang, M.Y. & Zhang, J.H. 2001 Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings Plant Cell Physiol. 42 1265 1273

    • Search Google Scholar
    • Export Citation
  • Kozlowski, T.T. & Pallardy, S.G. 2002 Acclimation and adaptive responses of woody plants to environmental stresses Bot. Rev. 68 270 334

  • Kucera, B., Cohn, M.A. & Leubner-Metzger, G. 2005 Plant hormone interactions during seed dormancy release and germination Seed Sci. Res. 15 281 307

  • Lang, G.A., Early, J.D., Martin, G.C. & Darnell, R.L. 1987 Endodormancy, paradormancy, and ecodormancy—Physiological terminology and classification for dormancy research HortScience 22 371 377

    • Search Google Scholar
    • Export Citation
  • Lee, I.C., Hong, S.W., Whang, S.S., Lim, P.O., Nam, H.G. & Koo, J.C. 2011 Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves Plant Cell Physiol. 52 651 662

    • Search Google Scholar
    • Export Citation
  • Li, C.Y., Junttila, O., Heino, P. & Palva, E.T. 2003 Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application Tree Physiol. 23 481 487

    • Search Google Scholar
    • Export Citation
  • Liang, J.S. & Zhang, J.H. 1999 The relations of stomatal closure and reopening to xylem ABA concentration and leaf water potential during soil drying and rewatering Plant Growth Regulat. 29 77 86

    • Search Google Scholar
    • Export Citation
  • Lin, B.L., Wang, H.J., Wang, J.S., Zaharia, L.I. & Abrams, S.R. 2005 Abscisic acid regulation of heterophylly in Marsilea quadrifolia L.: Effects of R-(-) and S-(+) isomers J. Expt. Bot. 56 2935 2948

    • Search Google Scholar
    • Export Citation
  • Mader, J.C., Emery, R.J.N. & Turnbull, C.G.N. 2003 Spatial and temporal changes in multiple hormone groups during lateral bud release shortly following apex decapitation of chickpea (Cicer arietinum) seedlings Physiol. Plant. 119 295 308

    • Search Google Scholar
    • Export Citation
  • Mantyla, E., Lang, V. & Palva, E.T. 1995 Role of abscisic-acid in drought-induced freezing tolerance, cold-acclimation, and accumulation of Lt178 and Rab18 proteins in Arabidopsis-Thaliana Plant Physiol. 107 141 148

    • Search Google Scholar
    • Export Citation
  • Mochioka, R., Tohbe, M., Horiuchi, S., Ogata, T., Shiozaki, S., Kawase, K.J., Kurooka, H. & Matsui, H. 1996 The relationship between bud dormancy and the endogenous ABA and water contents of several wild grape species native to Japan J. Jpn. Soc. Hort. Sci. 65 49 54

    • Search Google Scholar
    • Export Citation
  • Mora-Herrera, M.E. & Lopez-Delgado, H.A. 2007 Freezing tolerance and antioxidant activity in potato microplants induced by abscisic acid treatment Amer. J. Potato Res. 84 467 475

    • Search Google Scholar
    • Export Citation
  • Or, E., Belausov, E., Popilevsky, I. & Ben Tal, Y. 2000 Changes in endogenous ABA level in relation to the dormancy cycle in grapevines grown in a hot climate J. Hort. Sci. Biotechnol. 75 190 194

    • Search Google Scholar
    • Export Citation
  • Park, J.H., Oh, S.A., Kim, Y.H., Woo, H.R. & Nam, H.G. 1998 Differential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis Plant Mol. Biol. 37 445 454

    • Search Google Scholar
    • Export Citation
  • Peppi, M.C., Fidelibus, M.W. & Dokoozlian, N.K. 2007 Application timing and concentration of abscisic acid affect the quality of 'Redglobe' grapes J. Hort. Sci. Biotechnol. 82 304 310

    • Search Google Scholar
    • Export Citation
  • Poling, E.B. 2007 Overview of active frost, frost/freeze and freeze protection methods Understanding and Preventing Freeze Damage in the Vineyards Workshop Proc 47 64

    • Search Google Scholar
    • Export Citation
  • Rinne, P., Tuominen, H. & Junttila, O. 1994 Seasonal changes in bud dormancy in relation to bud morphology, water and starch content, and abscisic acid concentration in adult trees of Betula pubescens Tree Physiol. 14 549 561

    • Search Google Scholar
    • Export Citation
  • Saab, I.N., Sharp, R.E., Pritchard, J. & Voetberg, G.S. 1990 Increased endogenous abscisic-acid maintains primary root-growth and inhibits shoot growth of maize seedlings at low water potentials Plant Physiol. 93 1329 1336

    • Search Google Scholar
    • Export Citation
  • Steadman, J.R. & Sequeira, L. 1970 Abscisic acid in tobacco plants—Tentative identification and its relation to stunting induced by Pseudomonas Solanacearum Plant Physiol. 45 691 697

    • Search Google Scholar
    • Export Citation
  • Striegler, R.K. 2007 Passive freeze prevention methods Understanding and Preventing Freeze Damage in the Vineyards Workshop Proc 39 46

  • Thomas, H. & Stoddart, J.L. 1980 Leaf senescence Annu. Rev. Plant Physiol. Plant Mol. Biol. 31 83 111

  • Vysotskaya, L.B., Korobova, A.V., Veselov, S.Y., Dodd, I.C. & Kudoyarova, G.R. 2009 ABA mediation of shoot cytokinin oxidase activity: Assessing its impacts on cytokinin status and biomass allocation of nutrient-deprived durum wheat Funct. Plant Biol. 36 66 72

    • Search Google Scholar
    • Export Citation
  • Waterland, N.L., Finer, J.J. & Jones, M.L. 2010 Benzyladenine and gibberellic acid application prevents abscisic acid-induced leaf chlorosis in Pansy and Viola HortScience 45 925 933

    • Search Google Scholar
    • Export Citation
  • Williams, B.J., Pellett, N.E. & Klein, R.M. 1972 Phytochrome control of growth cessation and initiation of cold-acclimation in selected woody plants Plant Physiol. 50 262 265

    • Search Google Scholar
    • Export Citation
  • Zabadal, T.J., Dami, I.E., Goffinet, M.C., Martinson, T.E. & Chien, M.L. 2007 Winter injury to grapevines and methods of protection Mich. State Univ Ext. Bul. 2930.

    • Export Citation
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