American Journal of Plant Sciences, 2012, 3, 1232-1240 Published Online September 2012 (
Understanding Differential Responses of Grapevine (Vitis
vinifera L.) Leaf and Fruit to Water Stress and Recovery
Following Re-Watering
Bhaskar Bondada*, Janani Shutthanandan
Washington State University Tri-Cities, Richland, USA.
Received July 4th, 2012; revised July 31st, 2012; accepted August 10th, 2012
Among all fruit crops of horticultural importance, grapevines (Vitis vinifera L.) stand out as the most drought tolerant
crop species whose tolerance is credited to their proficiency to recover from water stress in both the natural and vine-
yard growing conditions. However, information on the recovery responses is relatively scant. Studies were conducted to
address this issue using potted vines of the grapevine cultivar, Cabernet Sauvignon, which was subjected to water stress
and along with anatomical and ultrastructural characterizations, physiological status was assessed in healthy and water
stressed vines, and following recovery via rewatering from the water stressed vines. Water stress induced wilting of
leaves, drooping of tendrils, and desiccation followed by abscission of shoot tip leaving behind a brown scar at the
shoot apex. The wilted leaves accumulated ABA, which correspondingly reduced stomatal conductance and leaf water
potential. Upon re-watering, both these parameters made a recovery with values similar to healthy leaves. Likewise, leaf
anatomical features following rewatering resembled to that of healthy leaves. In clusters, water stress caused shriveling
of preveraison (unripened) berries, which regained full turgor following water resupply, whereas the postveraison (rip-
ening) berries in the same cluster remained unaffected as evidenced by the presence of viable mesocarp cells and epicu-
ticular wax in the form of platelets. The study revealed that shoot tip with leaf primordia was most sensitive to water
stress followed by fully expanded leaves and preveraison berries, whereas the postveraison berries remained unaffected.
This information could be valuable to implementing irrigation strategies towards sustaining grape production in existing
vineyards experiencing episodic droughts and targeted areas prone to drought.
Keywords: ABA; Berry; Leaf Water Potential; Water Stress; Vitis vinifera
1. Introduction
Horticultural crops of commercial importance grown as
non-irrigated crop in temperate and as an irrigated crop
in semi-arid climates recurrently encounter drought pe-
riods due to either inadequate rainfall or a lack of irriga-
tion frequency. Because among all abiotic factors, drought
elicits substantial changes in plant metabolism, it has
become a custom to specify the destructive effects of
drought by examining the physiological and anatomical
responses of plants to varied levels of water stress and
desiccation [1-4]. However, equally important is gaining
an insight into the efficacy and the underlying mecha-
nisms involved in recovery from water stress following
water resumption. This premise has ignited an increasing
interest in exploring the recovery responses of water
stressed plants following watering events. For instance,
in recent years, several studies have examined the reco-
very responses after a water stress event for a wide range
of plants including annuals [5,6] and perennials [7,8].
While there exists plethora of information on drought in-
duced changes in grapevine (Vitis vinifera) development
and function [4,9-10], not much is known about recovery
responses from water stress, especially in own-rooted
vines, which serve as the propagatory material for estab-
lishing vineyards in many parts of the world. This is cru-
cial information as the capacity to overcome and recover
from water stress after rainfall or irrigation would aid in
ascertaining adaptive features for planting grapevines in
areas facing severe drought conditions. Having made that
remark, it must be emphasized that there exist a few
studies pertaining to recovery responses of water-stressed
grapevines; however, these studies primarily dealt with
rootstocks showing increases in its water use efficiency
(WUE) after a period of water deficit [11], but upon
grafting, the grafted vines failed to show similar response
*Corresponding author.
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
As opposed to other fruit crops, grapevine is unique in
that it is among the most ancient and widely cultivated
fruit crops grown both as a non-irrigated crop in temper-
ate and an irrigated crop in semi-arid climates worldwide
wherein it encounters continuous cycles of water stress
and re-watering either via rainfall or irrigation. Hence,
the need for studies focusing on the recovery responses
of water stressed grapevines is well justified especially in
view of the recent trends and most climate models that
project summer drought conditions to be aggravated in
the foreseeable future by increasing the severity as well
as the frequency of severe droughts [13]. In such situa-
tions, an understanding of recovery responses of water-
stressed grapevines can play a major role in maximizing
growth and production eventually leading to sustainabil-
ity of grape production. Furthermore, given the availabil-
ity of the grapevine genome sequence [14] and the fact
that grapevine is used as a model plant to study ecophy-
siological responses to water stress, the information gar-
nered from this study will be crucial not only to grape
production but also to better managing and sustaining
other perennial fruit crops under droughted conditions.
Therefore, the objective of this study was to gain an un-
derstanding of grapevine’s recovery by characterizing
morpho-anatomical and physiological responses of leaves
and clusters to water stress.
2. Materials and Methods
2.1. Plant Material
We used two-year old own rooted potted vines of Ca-
bernet Sauvignon propagated using cuttings acquired
from Inland Desert Nursery Inc. (Benton City, WA, USA)
for our experiment (2006 and 2007). The vines were
grown in 20 L PVC pots containing a mixture of 50%
sandy loam, 25% peat moss, 25% pumice and 30 g/L
dolomite. The bulk density of these mixtures was ~1
g·cm3. Volumetric water content at field capacity was
~34%. The vines were grown outside at Richland, WA
(46˚28N; 119˚28W; elevation 120 m).
A Hydrosense soil water sensor (Campbell Scientific
Inc., North Logan, Utah, USA) was used to control soil
moisture. During early season (before water stress treat-
ment), vines were irrigated completely i.e. until water
exuded from the pores on the pot’s bottom in which case
the soil moister was around 30% corresponding to field
capacity (~34%). This amount of water was used to
compose 100% irrigation treatment (control), which equ-
ated to 3 liters of water per pot per day and the water
stress treatment received 33% of the control (1 liter per
pot per day with a soil moisture of around 7% - 10%).
Pots were irrigated by manually watering mid-morning to
achieve the target water content. The stress treatment was
initiated prior to veraison when ripening commences in
grape berries.
2.2. Stomatal Conductance
Single leaf measurements were taken using a leaf poro-
meter (SC-1, Decagon Devices, Pullman, WA). Fully
expanded sun exposed leaves were selected to make
measurements between 10 am and noon.
2.3. Leaf Water Potential (Ψ)
A portable pressure chamber (PMS Instruments, Albany,
OR) was used to estimate mid-day Ψ according to Wil-
liams and Araujo (2002) [15].
2.4. ABA Analysis
ABA concentrations in the leaves were measured with
the Phytodetek ABA enzyme immunoassay test kit
(Agdia Inc., Elkhart, IN) following manufacturer’s in-
2.5. Light Microscopy
To examine the internal morphological features of leaves
and berries, small tissue samples were cut using a razor
blade; subsequently, the tissues were fixed and preserved
in formalin-acetic acid-alcohol. The fixed tissues were
dehydrated using the tertiary butyl alcohol series, infil-
trated and embedded in paraffin, sectioned at 10 µm
with a microtome (MT 990; Boeckeler Instruments,
Tucson, AZ), affixed to glass slides (8 × 3 cm), and
stained with the Toluidine blue (1%) and Johansen’s sa-
franin [1% (w/v) dissolved in 50% ethanol] and fast
green [0.2% (w/v) dissolved in 95% ethanol] protocol
[16]. The staining procedure involved rehydration in de-
scending strengths of alcohol, staining with safranin, de-
hydration in ascending strengths of alcohol, and counter-
staining with fast green. When staining was complete, a
drop of Permount mounting medium (Fisher Scientific,
Fair Lawn, NJ) was used to affix coverslips to the slides.
Slides were placed under a compound microscope (Ax-
ioskop 2 plus; Carl Zeiss, Thornwood, NY) attached with
a digital camera (DXM 1200C; Nikon Instruments, Mel-
ville, NY), which was used for capturing digital images.
2.6. Cell Viability (Membrane Integrity)
Cell viability was assessed first by staining cut surfaces
of berries with 5,(6)-Carboxyfluorescein Diacetate (5,6-
CFDA SE) and then observing stained berries with con-
focal laser scanning microscopy (CLSM). Stock CFDA
was made up as follows: 1 ml of dimethyl sulphoxide
(DMSO) was added to 100 mg of 5,6-CFDA (Invitrogen,
Carlsbad, CA, USA). Thereafter, 1 - 2 μl of the stock was
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
added to polypropylene vials containing 1ml distilled
water. Stock and working strength 5,6-CFDA were kept
foil-wrapped and stored at –4˚C until needed. Healthy
and berry shrivel berries were cut longitudinally through
the median into two equal halves, and each half was
stained with CFDA solution for 15 min.
A Zeiss Confocal microscope (LSM 510 Meta Laser
Scanning Microsope, Carl Zeiss Inc., Thornwood, NY,
USA) was used to image fluorescence as quickly as pos-
sible to minimize the dye loss. The fluorescence of
CFDA was analyzed by excitation at 488 nm, and emi-
ssion was detected at bandpath of 505 - 570 nm. The
fluorescence of cells was captured using a digital camera.
All quantitative data were analyzed by one-way
ANOVA using SPSS (SPSS Statistical Package 11; SPSS,
Chicago, IL, USA).
3. Results and Discussion
3.1. Water Stress Effects on Vegetative
Shoot Morphology, ABA, and Leaf Physiology
It is well known that plants experiencing water stress
undergo morphological and physiological changes. For
instance, Schultz and Matthews (1988) [17] showed that
the hydraulic conductivity of grapevine shoot diminished
when the soil water was depleted. Our study provided a
morpho-physiological manifestation of such hydraulic
challenge in the form of dehydrated shoot apex followed
by its abscission leaving behind a brown scar at the distal
end of the stem (Figure 1(a)). The leaves of the same
shoot exhibited a wilted appearance while the tendrils
first drooped, then desiccated and finally turned brown
(Figure 1). In contrast, the well irrigated shoot system
had turgid leaves and upward growing tendrils that out-
grew the shoot tip (Figure 1(b)) organized with several
leaf primordia and a young bifuricated tendril with hy-
dathodes at their tips (Figure 1(c)). The particular se-
quence in which these organs exhibited wilting in water
stressed shoot was not recorded but it generally first
starts with tendrils, then summer laterals followed by
main leaves [18]; however, the sensitivity to growth does
not differ among these organs during their ontogeny [19].
These adverse indices are typical expression of grape-
vines exposed to water stress conditions. In plants dis-
playing such symptoms, it is common to interpret them
in terms of a fall in leaf turgor and water potential, which
arises from the roots failing to extract water quickly
enough from the drying soil [20]. Accordingly, water
stress activates removal of water from the cytoplasm to
the extracellular space causing a reduction in the cytoso-
lic and vacuolar volumes, hence the wilted appearance of
the grapevine shoot system. Concomitant with these mo-
Figure 1. Photographs of (a) a water-stressed Cabernet
Sauvignon shoot with desiccated and drooping apex, desic-
cated and brown tendrils (upper inset) and the shoot apex
with a brown scar following the abscission of the apex (lower
inset); (b) a well irrigated Cabernet Sauvignon shoot system
showing turgid leaves and upward growing tendrils that
outgrew the shoot tip; and (c) a close up of shoot tip from B
showing several leaf primordia and a young bifuricated
tendril with hydathodes at their tips.
difications, biochemical changes ensued in the form of
ABA (abscisic acid) accumulation (Figure 2) occurring
most probably in the petiole xylem and leaf [21,22]. Such
response is a highly accepted testament to plants experi-
encing water stress as this phytohormone serves as the
predominant chemical message in plants experiencing
water stress [23]. It is well known that whenever ABA
accumulates, stomatal conductance de- clines as evi-
denced by correlations between stomatal conductance
and the ABA from both xylem and leaf tissues [24]. This
explains the low stomatal conductance of water-stressed
leaves (Figure 3), which most plausibly also endured a
reduction in the hydraulic conductivity of its vascular
system as a decline in stomatal conductance due to con-
strained stomatal aperture [4] parallels with reduced hy-
draulic conductivity [25]. The limited stoma- tal conduc-
tance has been considered to be an immediate response
of grapevines to water stress originating either from par-
tial root drying [26] or to soil water deficits on both a
diurnal and seasonal basis [27]. Thus, it is quite evident
that a reduction in stomatal conductance is the first
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
Xylem sap ABA (picomoles ml
Figure 2. Changes in ABA accumulation in leaves of well
watered and water-stressed Cabernet Sauvignon (WW: well
water; WS: water stress). Bars (Mean ± SE) sharing a
common letter are not significantly different (P < 0.05).
Stomatal conductance
b (A)
b (B)
Stomatal conductance
Figure 3. Changes in stomatal conductance as influenced by
water stress and recovery following rewatering in Cabernet
Sauvignon in (A) 2006 and (B) 2007. (WW: well water; WS:
water stress; RW: rewatering).
physiological consequence of roots deprived of water.
As is well known that both leaves and roots synthesize
ABA under water stress conditions [11,22] and the fact
we did not perform separate ABA analysis for roots and
leaves, implicit in our study was the uncertainty about
the source of ABA. However, based on the observations
made so far in grapevines dealing with water stress,
(Lovisolo et al., 2010) [4] posited that root ABA syn-
thesis most likely in the vascular parenchyma cells [28]
transported through the xylem into leaves as conjugate
forms [29] facilitates most of the stomatal response. This
is in contrast to the model plant, Arabidopsis whose
stomatal conductance response to soil water stress is due
to increased ABA synthesis in the shoots, not in the roots
Since stomata are the major control point for plant
water relations controlling water loss and gas exchange
[31], the decline in stomatal conductance unequivocally
implied that the steepest gradient in the soil-vine-atmo-
sphere continuum occurred at the leaf surface. In such a
situation, the leaf water potential is expected to be un-
changed. However, this did not occur in the water
stressed leaves (Figure 4), so it was possible that the
reduced leaf water status influenced stomatal conduc-
tance either directly or by inducing ABA accumulation.
Support for this contention can be derived from grafting
experiments entailing wild type and ABA-deficient to-
mato mutants [32]. They found that stomatal closure in
response to root drying was rather associated with trans-
mission of some signal, for example, a precursor other
than ABA from the roots. While examining the stomatal
response of different grapevine cultivars to VPD, Soar et
al. (2006) [33] speculated that such a precursor could
trigger aquaporin operation leading to a change in hy-
draulic properties, which is likely to reduce leaf water
potential and stomatal conductance concurrently. Hence
it appears that in addition to ABA metabolism, hydraulic
signals (cavitation), and expression and activity of aqu-
aporins [4], drought-induced stomatal closure is linked to
changes in leaf water status measured as leaf water po-
3.2. Recovery of Vegetative Structures
Leaf Morphological and Physiological Features
Upon re-watering, the leaves recovered fully as indicated
by their anatomical (Figure 5(A)) and physiological re-
sponses (Figures 3 and 4). For instance, physiologically,
the stomatal conductance and leaf water potential (Fig-
ures 3 and 4) were almost similar to and the anatomical
details resembled to that of fully watered leaves (Figure
5(A)) whose detailed structures have been well described
in recent studies [34,35]. This will restore photosynthetic
function, which generally declines during water stress
[36], due to its strong correlation with stomatal conduc-
tance [37]. While at a molecular level, recovery from
water stress elicits complex transcriptomic responses in
grapevine [38]. Similar to our study, Chaves and Rodri-
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
Leaf water potential (MPa
Le a f w a te r p o te nti a l (MPa
Figure 4. Changes in midday leaf water potential as influ-
enced by water stress and recovery following rewatering in
Cabernet Sauvignon in (A) 2006 and (B) 2007 (WW: well
water; WS: water stress; RW: rewatering).
Figure 5. Transverse light micrograph of a (A) well-irri-
gated leaf showing adaxial epidermis, abaxial epidermis,
palisade parenchyma cells, and spongy mesophyll cells, se-
veral vascular bundles and rib tissues; (B) scanning electron
micrograph of berry surface showing fine, loose, shiny, and
off-white aggregates of epicuticular wax platelets and (C) a
confocal laser scanning micrograph of mesocarp showing
green fluorescence as thin oblong illumination from the
parenchyma cells. Scale bars: 20 µm (A); 1.25 µm (B); 50 µm
(C). ade: adaxial epidermis; abe: abaxial epidermis; pm:
palisade mesophyll; sm: spongy mesophyll; vb: vascular
bundle; rt: rib tissues.
gues (1987) [39] reported full recovery after re-watering
the stressed vines that exhibited minimum leaf water
potential of –2.2 to –3 MPa. These observations indi-
cated that re-watering reversed the effects of water stress
on leaf physiology enabling the vines to survive much
stronger water stress conditions. On the contrary, the
decreased leaf water potential of apical shoot xylem in
maize did not recover even during extended periods of no
transpiration [40]. In a similar context, although water
stressed lemon plant (Citrus lemon) recovered leaf water
potential fully, the stomatal conductance did not make a
recovery [41]. Bases on these observations, it is reason-
able to suggest that compared to other crops, grapevines
are lot more elastic in their capacity to cope up with wa-
ter stress.
The mechanistic basis of recovery from water stress is
not clear from our study, yet we propose that the water
stress induced ABA accumulation in addition to causing
reductions in stomatal conductance facilitated growth
resumption following re-watering in both leaves as well
as berries. This conjecture is based on its role in recovery
process observed in other crops. For instance, ABA trig-
gered leaf growth in water-stressed maize by impeding
overload of the growth-inhibitory hormone ethylene [42].
With respect to grapevine, Perrone et al. (2011) [38]
contended that ABA also aids in the recovery of water
stressed grapevines. Although this could be possible by
increasing solute transport [43] and photosynthetic im-
port [44] towards growing cells or by stimulating hy-
draulic conductivity [45], their argument was based on
the different patterns of ABA accumulation in recovering
vines under different levels of transpiration [36,46].
3.3. Effect of Water Stress on Berries
3.3.1. Pre-Veraison Berries
In the cluster, the pre-veraison (un-ripened) berries re-
sponded to water stress by wrinkling their exocarp (Fig-
ure 6). As has been previously reported [47-49] and the
fact that girdled clusters develop shriveled berries [50],
such behavior was indicative of un-ripened (preveraison)
berries receiving saps from both xylemic (predominantly)
and phloemic pathways from the vine not only under
well watered conditions but also during water stress con-
ditions. Furthermore, it can be said that as grapevines
experience water stress, first the leaf water potential de-
clines (Figure 4), which in turn triggers water efflux
mechanism primarily for backflow into the vine in an
attempt to maintain stomatal conductance and leaf water
potential. However, despite stomatal closure, the leaf
water potential was not maintained (Figure 4). This was
not surprising since pre-veraison berries are known to
transpire water [48,51], which would downsize the pool
of water intended for backflow into the vine. From these
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
Figure 6. Photographs of (A) water-stressed cluster showing
shriveling of primarily preveraison (unripened) berries
(encircled) and (B) same cluster showing full expansion of
previously shriveled berries (encircled) following irrigation.
responses, it is evident that leaves are more sensitive to
water stress than berries. Nevertheless, insufficient water
supply during berry cell division and cell expansion will
inhibit berry size causing large and significant changes in
the metabolism and composition [52]. Although water
stress significantly reduced the volume and modified the
global structure of the berry affecting the macroscopic
characteristics, the wax morphology was unaltered (Fig-
ure 5(B)). Whether or not the berries underwent quanti-
tative and qualitative changes in wax composition is not
clear from this study; however, plant fruiting organs are
known to dramatically change their wax composition to
withstand water stress [53].
3.3.2. Post-Veraison Berries
On the contrary, the post-veraison berries i.e. berries that
started to accumulate anthocyanins, in the same cluster
(Figure 6) did not deform and maintained integrity of
their pericarp as revealed by their viable cells and epicu-
ticular wax in the form of platelets (Figure 5(B)). Based
on the findings by Keller et al. (2006), it is logical to
infer that even under water stress conditions, phloem in-
flux alone was suffice to cause the second phase of berry
expansion and that the xylem influx was unnecessary
even though a structurally intact xylemic pathway is al-
ways available for use [49,57]. Consequently, the berries
were spherical (Figure 6(B)) caused by turgid mesocarp
cells with semipermeable plasmalemma and a very low
osmotic potential as evidenced by a thin fluorescence
emitting from their cytoplasm (Figure 5(C)). A low os-
motic potential of the mesocarp cells is expected to bal-
ance the negative pressure in the apoplast and the tension
generated in vine xylem by leaf transpiration allowing
high hydraulic conductance to the vine [58]. This crafts
an ideal setting for backflow to occur especially in the
event of water stress [49] causing shriveling of berries as
observed with un-ripened (no or less color) berries, not
with ripened berries of the present study. This indicated
that despite the reversal of xylem flow during veraison
[49], the ripening berries are relatively less sensitive to
water stress. A similar conclusion was made by Creasy
and Lombard (1993) [59] who reported that berry growth
rate and deformability were much more sensitive to vine
water stress before veraison than after. This type of be-
havior can be interpreted as stimulating phloem unload-
ing while preventing fruits from undergoing diurnal flu-
ctuations of water potential [60]. On the other hand, if
the water deficit prolonged, then the ripening berries will
certainly shrivel via dehydration as in that case the xylem
efflux plus berry transpiration will exceed phloem influx
[49]. Another scenario for grape berries to shrivel include
when berries develop various physiological disorders
associated with ripening [61-63]. Many of these disor-
ders are characterized by cell death rendering the cell
membranes non selective [62,64].
3.4. Recovery Following Re-Watering
Pre-Veraison Berries
Upon re-watering, the preveraison berries fully recovered
(Figure 6) analogous to leaves. Thus, it appeared that
re-watering reversed the gradients of water potential and
reestablished the hydraulic conductivities of the water
pathway from vine to berry cells. Such conditions will
restore expansive growth as shown by these un-ripened
berries by generating turgor pressure via water entry into
cells. Hence, the recovery following watering was a clear
evidence of water loss occurring from the vacuolar com-
partment of the parenchymatous mesocarp cells during
water stress with minor changes in the water content of
both the cytoplasm and the cell wall compartments. On
the other hand, the color development following recovery
had less to do with both water stress effect and the re-
covery process even though water deficits accelerate ri-
pening and induce changes in gene expression regulating
flavonoid biosynthesis in grape berries [54]. Instead,
since the vines were stressed before veraison, the post
recovery period happened to coincide with ripening
phase and thereafter the recovered berries appeared to be
unaffected by water stress (Figure 6). The water stress
induced shriveling and recovery of un-ripened berries is
comparable to diurnal and seasonal transpiration and
shriveling of fruits including grapes that use this rhythm-
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
mic cycle to lower fruit water potential for enhancing
vascular import into the fruit [55,56].
To conclude, this study demonstrated that the shoot tip
with leaf primordia was most sensitive to water stress
followed by fully expanded leaves and pre-veraison ber-
ries, whereas the post-veraison berries remained unaf-
fected. Following watering, the stressed organs and fruits
regained full growth. Thus it appears that by taking the
sensitivity of vine organs into consideration, increased
irrigation efficiency is possible in areas with water
[1] N. D. Hallam and S. E. Luff, “Fine Ultrastructural
Changes in the Mesophyll Tissues in the Leaves of the
Xerophyta Villosa during Desiccation,” Botanical Gazette,
Vol. 141, No. 2, 1980, pp. 173-179.
[2] K. Chartzoulakisa, A. Patakasb, G. Kofidisc, A. Bosa-
balidisc and A. Nastou, “Water Stress Affects Leaf Ana-
tomy, Gas Exchange, Water Relations and Growth of
Two Avocado Cultivars,” Scientia Horticulturae, Vol. 95,
No. 1-2, 2002, pp. 39-50.
[3] H. R. Schultz and M. Stoll, “Some Critical Issues in En-
vironmental Physiology of Grapevines: Future Challenges
and Current Limitations,” Australian Journal of Grape
and Wine Research, Vol. 16, No. s1, 2010, pp. 4-24.
[4] C. Lovisolo, I. Perrone, A. Carra, A. Ferrandino, J. Flexas,
H. Medrano and A. Schubert, “Drought-Induced Changes
in Development and Function of Grapevine (Vitis spp.)
Organs and in Their Hydraulic and Non-Hydraulic Inter-
actions at the Whole-Plant Level: A Physiological and
Molecular Update,” Functional Plant Biology, Vol. 37,
No. 2, 2010, pp. 98-116. doi:10.1071/FP09191
[5] G. H. Salekdeh, J. Siopongco, L. J. Wade and B. Ghare-
yazie, “John Bennett1proteomic Analysis of Rice Leaves
during Drought Stress and Recovery,” Proteomics, Vol. 2,
No. 9, 2002, pp. 1131-1145.
[6] M. G. D. Dos Santos, R. V. Ribeiro, R. F. D. Oliveira, E.
C. Machado and C. Pimentel, “The Role of Inorganic
Phosphate on Photosynthesis Recovery of Common Bean
after a Mild Water Deficit,” Plant Sciences, Vol. 170, No.
3, 2006, pp. 659-674. doi:10.1016/j.plantsci.2005.10.020
[7] B. Dichio, C. Xiloyannis, A. Sofo and G. Montanaro,
Osmotic Regulation in Leaves and Roots of Olive Trees
during a Water Deficit and Rewatering,” Tree Physiology,
Vol. 26, No. 2, 2006, pp. 179-185.
[8] A. Galle, P. Haldimann and U. Feller, “Photosynthetic
Performance and Water Relations in Young Pubescent
Oak (Quercus pubescens) Trees during Drought Stress
and Recovery,” New Phytologist, Vol. 174, No. 4, 2007,
pp. 799-810. doi:10.1111/j.1469-8137.2007.02047.x
[9] L. E. Williams and M. A. Matthews, “Grapevine,” In: B.
A. Stewart and D. R. Nielsen, Eds., Irrigation of Agricul-
tural Crops, Agronomy Monograph No. 30, ASA-CSSA-
SSSA, Madison, 1990, pp. 1019-1055.
[10] M. Keller, “Managing Grapevines to Optimise Fruit De-
velopment in a Challenging Environment: A Climate
Change Primer for Viticulturists,” Australian Journal of
Grape and Wine Research, Vol. 16, No. s1, 2010, pp. 56-
69. doi:10.1111/j.1755-0238.2009.00077.x
[11] A. Pou, J. Flexas, M. D. Alsina, J. Bota, C. Carambula, F.
de Herralde, J. Galmes, C. Lovisolo, M. Jimenez, M.
Ribas-Carbo, D. Rusjan, F. Secchi, M. Tomas, Z. Zsofi
and H. Medrano, “Adjustments of Water Use Efficiency
by Stomatal Regulation during Drought and Recovery in
the Drought-Adapted Vitis hybrid Richter-110 (V. ber-
landieri × V. rupestris),” Physiologia Plantarum, Vol.
134, No. 2, 2008, pp. 313-323.
[12] M. Gomez-del-Campo, P. Baeza, C. Ruiz, V. Sotes and J.
R. Lissarrague, “Effect of Previous Water Conditions on
Vine Response to Rewatering,” Vitis, Vol. 46, No. 2,
2007, pp. 51-55.
[13] F. Giorgi and P. Lionello, “Climate Change Projections
for the Mediterranean Region,” Global and Planetary
Change, Vol. 63, No. 1-2, 2008, pp. 90-104.
[14] O. Jaillon, J. M. Aury, B. Noel, et al., “The Grapevine
Genome Sequence Suggests Ancestral Hexaploidization
in Major Angiosperm Phyla,” Nature, Vol. 449, No. 7162,
2007, pp. 463-468. doi:10.1038/nature06148
[15] L. E. Williams and F. J. Araujo, “Correlations among
Predawn Leaf, Midday Leaf, and Midday Stem Water
Potential and Their Correlations with Other Measures of
Soil and Plant Water Status in Vitis vinifera,” Journal of
the America Society for Horticultural Science, Vol. 127,
No. 3, 2002, pp. 448-454.
[16] S. E. Ruzin, “Plant Microtechnique and Microscopy,”
Oxford University Press, New York, 1999.
[17] H. R. Schultz and M. A. Matthews, “Resistance to Water
Transport in Shoots of Vitis vinifera L.: Relation to
Growth at Low Water Potential,” Plant Physiology, Vol.
88, No. 3, 1988, pp. 718-724.
[18] E. T. Thorne, J. F. Stevenson, T. L. Rost, J. M. Labavitch
and M. A. Matthews, “Pierce’s Disease Symptoms: Com-
parison with Symptoms of Water Deficit and the Impact
of Water Deficits,” American Journal of Enology and
Viticulture, Vol. 57, No. 1, 2006, pp. 1-11.
[19] H. R. Schultz and M. A. Matthews, “Vegetative Growth
Distribution during Water Deficits in Vitis vinifera L,”
Australian Journal of Plant Physiology, Vol. 15, No. 5,
1988, pp. 641-656. doi:10.1071/PP9880641
[20] T. Gollan, J. B. Passioura and R. Munns, “Soil Water
Status Affects the Stomatal Conductance of Fully Turgid
Wheat and Sunflower Leaves,” Australian Journal of
Plant Physiology, Vol. 13, No. 4, 1986, pp. 459-464.
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
[21] B. R. Loveys, “Abscisic Acid Transport and Metabolism
in Grapevine (Vitis vinifera L.),” New Phytologist, Vol.
98, No. 4, 1984, pp. 575-582.
[22] M. L. Rodrigues, T. P. Santos, A. P. Rodrigues, C. R. de
Souza, C. M. Lopes, J. P. Maroco, J. S. Pereira and M. M.
Chaves, “Hydraulic and Chemical Signalling in the
Regulation of Stomatal Conductance and Plant Water Use
in Field Grapevines Growing under Deficit Irrigation,”
Functional Plant Biology, Vol. 35, No. 7, 2008, pp. 565-
579. doi:10.1071/FP08004
[23] I. C. Dodd, “Root-to-Shoot Signalling: Assessing the
Roles of ‘Up’ in the Up and Down World of Long-Dis-
tance Signalling in Planta,” Plant and Soil, Vol. 274, No.
1-2, 2005, pp. 251-270.
[24] C. Lovisolo, W. Hartung and A. Schubert, “Whole-Plant
Hydraulic Conductance and Root-to-Shoot Flow of Ab-
scisic Acid Are Independently Affected by Water Stress
in Grapevines,” Functional Plant Biology, Vol. 29, No.
11, 2002, pp. 1349-1356. doi:10.1071/FP02079
[25] A. S. Cohen, Z. Attia and M. Moshelion, “Bundle-Sheath
Cell Regulation of Xylem-Mesophyll Water Transport via
Aquaporins under Drought Stress: A Target of Xylem-
Borne ABA?” The Plant Journal, Vol. 67, No. 1, 2011,
pp. 72-80. doi:10.1111/j.1365-313X.2011.04576.x
[26] P. R. Dry and B. R. Loveys, “Grapevine shoot Growth
and Stomatal Conductance Are Reduced When Part of the
Roots are Dried,” Vitis, Vol. 38, No. 4, 1999, pp. 151-
[27] L. E. Williams, N. K. Dokoozlian and R. Wample,
“Grape,” In: B. Schaffer and P. C. Anderson, Eds., Hand-
book of Environmental Physiology of Fruit Crops, CRC
Press, Boca Raton, 1994, pp. 85-133.
[28] A. Endo, Y. Sawada, H. Takahashi, M. Okamoto, K. Ike-
gami, H. Koiwai, M. Seo, T. Toyomasu, W. Mitsuhashi,
K. Shinozaki, M. Nakazono, Y. Kamiya, et al., “Drought
Induction of Arabidopsis 9-Cis-Epoxycarotenoid Dioxy-
genase Occurs in Vascular Parenchyma Cells,” Plant
Physiology, Vol. 147, No. 4, 2008, pp. 1984-1993.
[29] R. Munns and R. E. Sharp, “Involvement of Abscisic
Acid in Controlling Plant Growth in Soils of Low Water
Potential,” Australian Journal of Plant Physiology, Vol.
20, No. 5, 1993, pp. 425-437. doi:10.1071/PP9930425
[30] A. Christmann, E. W. Weiler, E. Steudle and E Grill, “A
Hydraulic Signal in Root-to-Shoot Signalling of Water
Shortage,” The Plant Journal, Vol. 52, No. 1, 2007, pp.
167-174. doi:10.1111/j.1365-313X.2007.03234.x
[31] H. Lambers, F. S. Chapin and T. L. Pons, “Plant Physio-
logical Ecology,” Springer-Verlag, New York, 2008.
[32] N. M. Holbrook, V. R. Shashidar, R. A. James and R.
Munns, “Stomatal Control in Tomato with ABA-Defi-
cient Roots: Response of Grafted Plants to Soil Drying,”
Journal of Experimental Botany, Vol. 53, No. 373, 2002,
pp. 1503-1514. doi:10.1093/jexbot/53.373.1503
[33] C. J. Soar, J. Speirs, S. M. Maffei, A. B. Penrose, M. G.
McCarthy and B. R. Loveys, “Grape Vine Varieties Shi-
raz 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, Vol. 12, No. 1, 2006, pp. 2-12.
[34] B. Bondada, “Anomalies in Structure, Growth Character-
istics, and Nutritional Composition as Induced by 2, 4-D
Drift Phytotoxicity in Grapevine (Vitis vinifera L.) Leaves
and Clusters,” Journal of the American Society for Hor-
ticultural Science, Vol. 136, No. 3, 2011, pp. 165-176.
[35] B. Bondada, “Micromorpho-Anatomical Examination of
2, 4-D Phytotoxicity in Grapevine (Vitis vinifera L.)
Leaves,” Journal of Plant Growth Regulation, Vol. 30,
No. 2, 2011, pp. 185-198.
[36] J. Flexas, M. Baron, J. Bota, J. M. Ducruet, A. Galle, J.
Galmes, M. Jimenez, A. Pou, M. Ribas-Carbo, C. Sajnani,
M. Tomas and H. Medrano, “Photosynthesis Limitations
during Water Stress Acclimation and Recovery in the
Drought-Adapted Vitis Hybrid Richter-110 (V. ber-
landieri × V. rupestris),” Journal of Experimental Botany,
Vol. 60, No. 8, 2009, pp. 2361-2377.
[37] S. C. Wong, I. R. Cowan and G. D. Farquhar, “Stomatal
Conductance Correlates with Photosynthetic Capacity,”
Nature, Vol. 282, 1979, pp. 424-426.
[38] I. Perrone, C. Pagliarani, C., Lovisolo, W. Chitarra, F.
Roman and A. Schubert, “Recovery from Water Stress
Affects Grape Leaf Petiole Transcriptome,” Planta, Vol.
235, 2012, pp. 1383-1396.
[39] M. M. Chaves and M. L. Rodrigues, “Photosynthesis and
Water Relations of Grapevines Growing in Portugal. Re-
sponse to Environmental Factors,” In: J. D. Tenhunen, et
al., Eds., Plant Response to Stress. Functional Analysis in
Mediterranean Ecosystems, NATO AS1 Series G, Springer
Verlag, Berlin, Vol. 15, 1987, pp. 379-90.
[40] M. E. Westgate and J. S. Boyer, “Osmotic Adjustment
and Inhibition of Leaf, Root, Stem, and Silk Growth at
low Water Potentials in Maize,” Planta, Vol. 164, No. 4,
1985, pp. 540-549. doi:10.1007/BF00395973
[41] M. C. Ruiz-Sanchez, R. Domingo, R. Save, C. Biel and A.
Torrecillas, “Effect of Water Stress and Rewatering on
Leaf Water Relations of Lemon Plants,” Biologia Planta-
rum, Vol. 39, No. 4, 1997, pp. 623-631.
[42] R. E. Sharp and M. E. Lenoble, “ABA, Ethylene and the
Control of Shoot and Root Growth under Water Stress,”
Journal of Experimental Botany, Vol. 53, No. 366, 2002,
pp. 33-37. doi:10.1093/jexbot/53.366.33
[43] S. K. Roberts and B. N. Snowman, “The Effects of ABA
on Channel Mediated K+ Transport across Higher Plant
Roots,” Journal of Experimental Botany, Vol. 51, No.
350, 2000, pp. 1585-1594.
[44] H. Jones, R. A. Leigh, A. D. Tomos and R. G. Wyn Jones,
Copyright © 2012 SciRes. AJPS
Understanding Differential Responses of Grapevine (Vitis vinifera L.) Leaf and Fruit to Water Stress and
Recovery Following Re-Watering
Copyright © 2012 SciRes. AJPS
“The Effect of Abscisic Acid on Cell Turgor Pressures,
Solute Content and Growth of Wheat Roots,” Planta, Vol.
170, No. 2, 1987, pp. 257-262.
[45] B. Parent, C. Hachez, E. Redondo, T. Simonneau, F.
Chaumont and F. Tardieu, “Drought and Abscisic Acid
Effects on Aquaporin Content Translate into Changes in
Hydraulic Conductivity and Leaf Growth Rate: A
Trans-Scale Approach,” Plant Physiology, Vol. 149, No.
4, 2009, pp. 2000-2012. doi:10.1104/pp.108.130682
[46] C. Lovisolo, I. Perrone, W. Hartung and A. Schubert, “An
Abscisic Acid-Related Reduced Transpiration Promotes
Gradual Embolism Repair When Grapevines Are Rehy-
drated after Drought,” New Phytologist, Vol. 180, No. 3,
2008, pp. 642-651.
[47] M. A. Matthews and M. M. Anderson, “Fruit Ripening in
Vitis vinifera L.: Responses to Seasonal Water Deficits,”
American Journal of Enology and Viticulture, Vol. 39,
No. 4, 1988, pp. 313-320.
[48] M. D. Greenspan, H. R. Schultz and M. A. Matthews,
“Field Evaluation of Water Transport in Grape Berries
during Water Deficits,” Physiologia Plantarum, Vol. 97,
No. 1, 1996, pp. 55-62.
[49] M. Keller, J. P. Smith and B. R. Bondada, “Ripening
Grape Berries Remain Hydraulically Connected to the
Shoot,” Journal of Experimental Botany, Vol. 57, No. 11,
2006, pp. 2577-2587. doi:10.1093/jxb/erl020
[50] S. Rogiers, D. H. Greer, J. M. Hatfield, B. A. Orchards
and M. Keller, “Solute Transport into Shiraz Berries dur-
ing Development and Late-Ripening Shrinkage,” Ameri-
can Journal of Enology and Viticulture, Vol. 57, No. 1,
2006, pp. 73-80.
[51] M. D. Greenspan, K. A. Shackel and M. A. Matthews,
“Developmental Changes in the Diurnal Water Budget of
the Grape Berry Exposed to Water Deficits,” Plant, Cell
and Environment, Vol. 17, No. 7, 1994, pp. 811-820.
[52] G. Roby and M. A. Matthews, “Relative Proportions of
Seed, Skin and Flesh, in Ripe Berries from Cabernet Sau-
vignon Grapevines Grown in a Vineyard Either Well Ir-
rigated or under Water Deficit,” Australian Journal of
Grape and Wine Research, Vol. 10, No. 1, 2004, pp. 74-
82. doi:10.1111/j.1755-0238.2004.tb00009.x
[53] B. R. Bondada, D. M. Oosterhuis, J. B. Murphy and K. S.
Kim, “Effect of Water Stress on the Epicuticular Wax
Composition and Ultrastructure of Cotton (Gossypium
hirsutum L.) Leaf, Bract, and Boil,” Environmental and
Experimental Botany, Vol. 36, No. 1, 1996, pp. 61-69.
[54] S. D. Castellarin, M. A. Matthews, G. Di Gaspero and G.
A. Gambetta, “Water Deficits Accelerate Ripening and
Induce Changes in Gene Expression Regulating Flavon-
oid Biosynthesis in Grape Berries,” Planta, Vol. 227, No.
1, 2007, pp. 101-112.
[55] H. G. Jones and K. H. Higgs, “Surface Conductance and
Water Balance of Developing Apple (Malus pumila Mill.)
Fruits,” Journal of Experimental Botany, Vol. 33, No.
132, 1982, pp. 67-77. doi:10.1093/jxb/33.1.67
[56] L. M. McFadyen, R. J. Hutton and E. W. R. Barlow, “Ef-
fects of Crop Load in Fruit Water Relations and Fruit
Growth in Peach,” Journal of Horticultural Science, Vol.
71, 1996, pp. 469-480.
[57] B. R. Bondada, M. A. Matthews and K. A. Shackel,
“Functional Xylem Exists in Post Veraison Grape Berry,”
Journal of Experimental Botany, Vol. 56, No. 421, 2005,
pp. 2949-2957. doi:10.1093/jxb/eri291
[58] J. Tilbrook and S. D. Tyerman, “Cell Death in Grape
Berries: Varietal Differences Linked to Xylem Pressure
and Berry Weight Loss,” Functional Plant Biology, Vol.
35, No. 3, 2008, pp. 173-184. doi:10.1071/FP07278
[59] G. L. Creasy and P. B. Lombard, “Vine Water Stress and
Peduncle Girdling Effects on Pre- and Post-Veraison
Grape Berry Growth and Deformability,” American
Journal of Enology and Viticulture, Vol. 44, No. 2, 1993,
pp. 193-197.
[60] W. Van Ieperen, V. S. Volkov and U. Van Meeteren,
“Distribution of Xylem Hydraulic Resistance in Fruiting
Truss of Tomato Influenced by Water Stress,” Journal of
Experimental Botany, Vol. 54, No. 381, 2003, pp. 317-
324. doi:10.1093/jxb/erg010
[61] G. Hall, B. R. Bondada and M. Keller, “Loss of Rachis
Cell Viability Is Associated with Ripening Disorders in
Grapes,” Journal of Experimental Botany, Vol. 62, No. 3,
2011, pp. 1145-1153. doi:10.1093/jxb/erq355
[62] B. R. Bondada and M. Keller, “Morpho-Anatomical
Symptomatology and Osmotic Behavior of Grape Berry
Shrivel,” Journal of the American Society for Horticul-
tural Science, Vol. 137, No. 1, 2012, pp. 20-30.
[63] B. R. Bondada and M. Keller, “Not All Shrivels Are Cre-
ated Equal—Morpho-Anatomical and Compositional
Characteristics Differ among Different Shrivel Types
That Develop during Ripening of Grape (Vitis vinifera L.)
Berries,” American Journal of Plant Sciences, Vol. 3,
2012 (In Press). doi:10.4236/ajps.2012.37105
[64] M. Krasnow, M. A. Matthews and K. A. Shackel, “Evi-
dence for Substantial Maintenance of Membrane Integrity
and Cell Viability in Normally Developing Grape (Vitis
vinifera L.) Berries throughout Development,” Journal of
Experimental Botany, Vol. 59, No. 4, 2008, pp. 849-859.