Annals of Botany 105: 661 –676, 2010

doi:10.1093/aob/mcq030, available online at [Link]

INVITED REVIEW

Grapevine under deficit irrigation: hints from physiological and molecular data
M. M. Chaves 1,2,*, O. Zarrouk 2, R. Francisco 2, J. M. Costa 1,2, T. Santos 1,2, A. P. Regalado 2, M. L. Rodrigues 1
and C. M. Lopes 1
1
Instituto Superior de Agronomia, Technical University of Lisbon, Tapada da Ajuda 1349-017 Lisbon, Portugal and 2Instituto de
Tecnologia Quı́mica e Biológica, Oeiras, Universidade Nova de Lisboa, Portugal
* For correspondence. E-mail mchaves@[Link]

Received: 14 September 2009 Returned for revision: 16 October 2009 Accepted: 7 January 2010 Published electronically: 18 March 2010

† Background A large proportion of vineyards are located in regions with seasonal drought (e.g. Mediterranean-
type climates) where soil and atmospheric water deficits, together with high temperatures, exert large constraints
on yield and quality. The increasing demand for vineyard irrigation requires an improvement in the efficiency of
water use. Deficit irrigation has emerged as a potential strategy to allow crops to withstand mild water stress with
little or no decreases of yield, and potentially a positive impact on fruit quality. Understanding the physiological
and molecular bases of grapevine responses to mild to moderate water deficits is fundamental to optimize deficit
irrigation management and identify the most suitable varieties to those conditions.
† Scope How the whole plant acclimatizes to water scarcity and how short- and long-distance chemical and
hydraulic signals intervene are reviewed. Chemical compounds synthesized in drying roots are shown to act
as long-distance signals inducing leaf stomatal closure and/or restricting leaf growth. This explains why some
plants endure soil drying without significant changes in shoot water status. The control of plant water potential
by stomatal aperture via feed-forward mechanisms is associated with ‘isohydric’ behaviour in contrast to ‘any-
sohydric’ behaviour in which lower plant water potentials are attained. This review discusses differences in this
respect between grapevines varieties and experimental conditions. Mild water deficits also exert direct and/or
indirect (via the light environment around grape clusters) effects on berry development and composition; a
higher content of skin-based constituents (e.g. tannins and anthocyanins) has generally being reported.
Regulation under water deficit of genes and proteins of the various metabolic pathways responsible for berry
composition and therefore wine quality are reviewed.

Key words: Vitis vinifera, varieties, stomatal conductance (gs), intrinsic water-use efficiency (WUEi An/gs),
isohydric, anisohydric, abscisic acid, berry composition.

I N T RO D U C T I O N : VI N E YA R D S A N D WAT E R
improving wine quality (Dry and Loveys, 1998; Medrano
S CA R C I T Y
et al., 2003; Chaves et al., 2007) and other associated manage-
Most of the world’s wine-producing regions experience seaso- ment techniques (e.g. soil cover) to minimize the effects of
nal drought. With an increase in aridity predicted in the near concentrated rainfall (Monteiro and Lopes, 2007; Schultz,
future according to global climate models (IPCC, 2007), 2007). The search for varieties adapted to growing seasons
water deficits may become a limiting factor in wine production with altered length and displaying higher resilience to environ-
and quality. Global warming is also affecting grapevine devel- mental stress is also critical to optimum berry ripening.
opment, as indicated by changes in phenology and earlier har- By contrast, the enhanced pressure on water resources
vests observed throughout the world (Jones and Davies, 2000; increased the global perception of the need to reduce the
Webb et al., 2007), with some European regions coming closer ‘water footprint’ for irrigated crops ([Link]/nr/water/
to the thresholds of temperature and rainfall for optimum aquastat/data/query/[Link]; Cominelli et al., 2009). An
grapevine growth (Jones et al., 2005). In recent years, water improvement in the productivity of water use is therefore
deficit is also occurring in cool climate wine regions that required in vineyard management, with finely tuned deficit irri-
exhibit special topography (van Leeuwen and Seguin, 2006; gation being able to fulfil that role.
Zsófi et al., 2009a). The frequency of extreme events such To understand the physiological and molecular bases of
as heat waves or heavy rains is also predicted to increase, plant responses to mild to moderate water deficits is therefore
with negative effects on yield and quality of grapes. Sudden of utmost importance to modulate the appropriate balance
supra-optimal temperatures under conditions of water scarcity between vegetative and reproductive development, to
may lead to massive leaf shedding, with a consequent source – improve crop water use (Blum, 2009) and to control fruit
sink imbalance and incomplete berry maturation due to insuf- quality under deficit irrigation (Chaves et al., 2007).
ficient available carbohydrates. These effects are unlikely to be Chemical signals are important players in plant adaptation to
uniform across varieties (Schultz, 2000; Jones et al., 2005). environmental stresses. Since the mid-1980s evidence has
The constraints posed by climate change require adaptive man- been provided on the signalling role of compounds synthesized
agement, namely irrigation to stabilize yield, maintaining or in drying roots of different species (including grapevines);
# The Author 2010. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: [Link]@[Link]
662 Chaves et al. — Grapevine under deficit irrigation

they have been associated with leaf stomatal closure and/or supply of water most effectively (Passioura, 2007). The use
inhibition of meristematic development (Loveys, 1984; of deficit irrigation strategies, implying that water is supplied
Davies and Zhang, 1991). Although root-sourced chemical sig- at levels below full crop evapotranspiration (ETc) throughout
nalling is widely accepted, the identity and regulation of these the growing season or in specific phenological stages, relies
signals is still under debate (Holbrook et al., 2002; on observations in several crops subjected to moderate water
Schachtmann and Goodger, 2008). Nevertheless, such knowl- deficits that yield is not significantly reduced and quality of
edge has enabled us to manipulate responses to soil water production may even increase under such conditions. This
availability in some crops, so that changes in shoot water has been the case for several fruit tree crops (see review by
status are minimized and performance under moderate stress Fereres and Soriano, 2007) and grapevines (Dry et al., 2001;
is improved (Davies et al., 2002; Chaves and Oliveira, 2004). Chaves et al., 2007). In addition to the classic deficit irrigation
The timing and intensity of water deficits influence the extent (DI), which does not require specific technical control, two
of alterations occurring in berry metabolism and therefore in other deficit irrigation strategies – regulated deficit irrigation
wine colour and flavour (namely aroma). Whether these effects (RDI) and partial rootzone drying (PRD) – have been
are acting predominantly through berry size or the synthesis of applied in recent years by finely tuning deficit irrigation in
berry compounds is also discussed here. The accumulated know- the scales of time (specific timing of the application) and
ledge made possible by studies of transcriptomics and proteomics space (alternating dry – wet zones), respectively. Although
during different stages of berry development in different varieties deficit irrigation is already applied to vast regions worldwide
and environmental conditions will also be highlighted. in a more or less uncontrolled/unsophisticated way, the scien-
tific knowledge underlying its optimal functioning is still
needed.
T HE R AT I ON AL E FOR D E F I C I T I R R IG AT I ON –
Under RDI plant water status is maintained within prede-
W HY M I L D TO M O DE R AT E WAT E R DE FI CI T
fined limits of deficit (with respect to maximum water poten-
M AY B E FAVO U R A B L E TO G R A P E B E R RY
tial) during certain phases of the seasonal development,
Q UA L IT Y
normally when fruit growth is least sensitive to water
Grapevines are well adapted to semi-arid climate such as that reductions (Kang and Zhang, 2004). The rationale underlying
of the Mediterranean, due to the large and deep root system this practice is that optimization of numbers of fruits, fruit size
and physiological drought avoidance mechanisms, such as an and quality will be achieved by keeping grapevine vigour in
efficient stomatal control of transpiration and of xylem embo- balance with potential production. If water deficit is applied
lism (Lovisolo et al., 2002), and/or the ability to adjust osmo- early in the season, the effects will be achieved mostly
tically (Rodrigues et al., 1993; Patakas and Noitsakis, 1999). through a reduction of berry cell division (McCarthy et al.,
However, the combined effect of drought, high air temperature 2002); if water deficits are imposed at later stages, the major
and high evaporative demand during summer in these areas is effect will be an inhibition of berry growth (Williams and
known to limit grapevine yield and berry and wine quality Matthews, 1990).
(Escalona et al., 1999; Chaves et al., 2007; Costa et al., In PRD, roots are exposed to alternate drying and wetting
2007). Dramatic reductions in plant carbon assimilation may cycles. Theoretically, roots of the watered side of soil will
occur due to severe decline in photosynthesis under maintain favourable plant water relations, whereas dehydration
supra-optimal leaf temperatures combined with water deficits, in the other side will induce chemical signalling that will reach
as well as to a partial loss of canopy leaf area (Flexas et al., the leaves via the transpiration stream, reducing stomatal con-
1998, 2002; Maroco et al., 2002; Chaves et al., 2003, 2007; ductance and/or growth (Davies et al., 1994; Santos et al.,
Souza et al., 2003, 2005b; Santos et al., 2007). The use of irri- 2003; Kang and Zhang, 2004; Costa et al., 2007). This will
gation in these environments arises as a solution to prevent bring about an increase in water-use efficiency (WUE). PRD
excessive canopy temperature, maintain quality in wine pro- irrigation may also have an impact on root growth, leading
duction and, in more extreme cases, guarantee plant survival. to increased root development in the deeper soil layers (Dry
Nevertheless, irrigation remains of considerable debate. On et al., 2000; Santos et al., 2007). Moreover, an increase in
the one hand, small water supplements may increase yield root hydraulic conductance, putatively resulting from aqua-
and maintain or even improve berry quality (Matthews and porin stimulation by abscisic acid (ABA), and the induction
Anderson, 1989; Santos et al., 2003, 2005). On the other of new secondary roots was reported in fruit trees subjected
hand, irrigation may promote excessive vegetative growth to PRD (Kang and Zhang, 2004).
with a negative impact on berry pigments (colour) and sugar There are, however, contrasting results in the literature,
content, and therefore decrease wine quality (Bravdo et al., several studies in grapevine reporting no significant differ-
1985; Dokoozlian and Kliewer, 1996). Larger canopy leaf ences between PRD and DI (Pudney and McCarthy, 2004;
area will also tend to increase the incidence of fungal diseases Bravdo et al., 2004; Gu et al., 2004; Baeza and Lissarrague,
(Dry and Loveys, 1998). 2005). These apparent contradictions may be related to differ-
Modern irrigation management is shifting from an emphasis ences in the intensity of the chemical signalling under PRD
on production per unit soil area towards maximizing water pro- irrigation that seems to be dictated by the type of soil, the
ductivity ( production per unit of consumed water) (Fereres and prevalent rainfall and evaporative demand in the region, as
Soriano, 2007). Consideration must be given not only to the well as the frequency of switching irrigation from one side
total seasonal water available in a region but also the timing of the rootzone to the other (Dry et al., 2001; Chaves et al.,
when water deficits are likely to occur, in order to adjust 2007). Genotypic differences in stomatal sensing of water def-
water needs to the available resources, using a limited icits or the delivery of ABA by the root-stock may also explain
 Chaves et al. — Grapevine under deficit irrigation 663

different results (Antolı́n et al., 2006; De la Hera et al., 2007). to high vapour pressure deficit (VPD) and high irradiance
Drought-sensitive varieties may respond better to PRD (Souza (Correia et al., 1995) and/or to decreased stem hydraulic con-
et al., 2005a). The type of soil will impact on the extent of soil ductance (Salleo and Lo Gullo, 1989; Vandeleur et al., 2009).
water redistribution, which in turn will buffer dehydration in Although several lines of evidence suggest that grapevines are
the dry rootzone. Bravdo (2005) suggests that hydraulic redis- resistant to photoinhibition (Correia et al., 1990; Chaumont
tribution from deeper to shallower roots may prevent under et al., 1997; Flexas et al., 2001; Medrano et al., 2002; Souza
field conditions the clear results obtained in potted plants sub- et al., 2003), maximum efficiency of photosystem II (measured
jected to PRD under split root systems (Davies et al., 2002). by the dark-adapted Fv/Fm fluorescence ratio) was shown to
Dry (2005) also suggested that PRD may not be successful decline under intense drought (Quick et al., 1992).
when soil porosity favours lateral spread of irrigation water, Photosynthetic rates generally decline at lower pre-dawn
or when an insufficient volume of irrigation is applied for res- water potentials than stomatal conductance, when grapevines
toration of the wet side to field capacity at the time of the are subjected to moderate water deficits. As a consequence,
switch. In fact, when soil water status of the wet part of the intrinsic water use efficiency (A/gs or WUEi) is usually
root system is low, there is insufficient soil water in the dry higher in vines under deficit irrigation (mild to moderate
part of the root system to maximize ABA export from the water deficits) than under well-watered conditions. This is
entire root system (Dodd et al., 2008a, b). There is also evi- reflected in a lower water use and higher WUE by the crop,
dence that in low-vigour vineyards PRD is unable to induce an important aim of deficit irrigation strategies in vineyards
better agronomical output than the conventional DI strategy, (Gaudillère et al., 2002; Chaves et al., 2004; Souza et al.,
as the growth inhibition that is more pronounced in PRD 2005b).
than in DI will decrease source (leaves) to sink ratio below When water supply declines, stomatal guard cells respond to
the optimum, resulting in yield losses without any improve- leaf water potential and both respond to and control the supply
ment in berry quality (C. M. Lopes et al., unpubl. res.). and loss of water by the leaves (Leuning et al., 2003). Under
Moreover, Sadras (2009) in a meta-analysis of a broad range these circumstances, intercellular CO2 partial pressure ( pi)
of horticultural crops showed that in general there was no can control stomatal opening via the supply of CO2 to the
improvement in irrigation water productivity (yield per unit chloroplast or via the demand for CO2 by photosynthesis.
irrigation water applied) under PRD, as compared with DI. The decrease in gs in response to mild water stress usually
leads to a linear decline in transpiration (under constant
VPD) and of pi, because CO2 demand by the chloroplasts
P HY S I OLO GI CA L RE S PON S E TO M OD E R AT E
( photosynthetic capacity) remains the same (Chaves and
WAT E R DEF ICI T S IN GR APE VI NE
Oliveira, 2004). Under low light intensity but high air humid-
Under mild to moderate water deficits stomata closure is ity, as occurs in the morning or evening, grapevine stomata
among the early plant responses, restricting water loss and may be widely open at low photosynthetic rates, leading to
carbon assimilation (Chaves et al., 2003). Direct effects on low WUEi. By contrast, stomatal closure at midday, an impor-
photosynthetic metabolism (Lawlor and Tezara, 2009) and tant adaptation to high VPD in some species of xeric habitats
on the expression of a multitude of genes (Chaves et al., (Maroco et al., 1997), may lead to an increase in WUEi when
2009) may also be present at early stages. Under long-standing photosynthesis is maintained. This has been observed in grape-
water deficits acclimatization responses do occur, including vine (Souza et al., 2003). When analysing WUEi it is therefore
those related to growth inhibition and to osmoregulation; important to study it throughout the day. Field studies using
these are key elements for the maintenance of plant water ‘Moscatel’, ‘Castelão’ and ‘Aragonez’ (syn. ‘Tempranillo’)
status and therefore plant carbon assimilation under water showed that deficit irrigation strategies (e.g. PRD and conven-
scarcity. tional DI, both at 50 % ETc) promoted an increase in WUE,
In grapevine, it has been reported for several varieties and when compared with fully irrigated grapevines (100 % ETc),
different experimental conditions (greenhouse and field; both in the short term (as expressed by the A/gs ratio) and
short- and long-term) that photosynthesis is quite resistant to the long term (estimated via d13C) (Souza et al., 2005b). An
water stress (Flexas et al., 2002; Souza et al., 2003, 2005a; increase in WUE and related water savings under deficit irriga-
Chaves et al., 2007). Under low to moderate water availabil- tion was also reported in studies carried out in different grape-
ities occurring under deficit irrigation, maintenance of the vine varieties and in different locations (Dry et al., 2000; Stoll
activity of Calvin Cycle enzymes and of the maximum rates et al., 2000; Loveys et al., 2004; Poni et al., 2007; Marsal
of carboxylation (Vcmax) and electron transport (Jmax) has gen- et al., 2008).
erally been observed (Souza et al., 2005a). However, when
stress is intensified a decline in those parameters occurs,
G E N OT Y P E - D E P E N D E N T R E S PO N S E S TO
more markedly in Jmax (Maroco et al., 2002; Souza et al.,
WAT E R D E F I C I T S I N V I T I S V I N I F E R A
2005a), possibly a result of decreased ATP production.
Lawlor and Tezara (2009) raised the hypothesis that reactive It is acknowledged that the timing and intensity of the response
oxygen species produced under conditions of low CO2 and to soil and atmospheric water deficits, namely in what con-
excess light might induce oxidative damage to chloroplastic cerns stomatal control, depends greatly on genotype. This
ATPase. has profound implications in irrigation management, in par-
Grapevine is prone to down-regulation of photosynthesis in ticular the timing and amount of irrigation to optimize
the afternoon, a phenomenon that might also occur in well- source – sink relationships, in order to achieve optimal fruit
watered vines mainly as a result of stomatal closure in response quality in each variety (Medrano et al., 2003; Chaves et al.,
664 Chaves et al. — Grapevine under deficit irrigation

2007; Poni et al., 2007). Vitis vinifera L. is characterized by moisture stress was found by Soar et al. (2006), who attributed
large genetic variability with several thousand varieties/var- the higher sensitivity of stomata in ‘Grenache’ to the higher
ieties being cultivated worldwide (Alleweldt et al., 1990; concentration of ABA in the xylem sap as compared with
Galet, 2000; Schultz, 2003). European countries like France, ‘Syrah’. They provided evidence of a midday increment of
Spain or Portugal host a large number of native V. vinifera var- the expression of key genes involved in the ABA biosynthetic
ieties. However, most of those genotypes remain uncharacter- pathway, significantly higher in the leaves of ‘Grenache’ than
ized, which limits their use for breeding, for example to in ‘Syrah’. This was not observed in the roots.
increase WUE or improve berry quality traits. However, contradictory reports appeared in the literature
Genotype-related differences in WUE and water stress showing that the same variety could behave differently depend-
resistance may arise from constitutive differences in leaf ing on experimental conditions (see Table 1 and the review by
gas-exchange, the plant’s capacity to osmoregulate and plant Lovisolo et al., 2010). For example, ‘Syrah’ and ‘Grenache’
hydraulics. Photosynthesis, stomatal conductance and WUEi that exhibited an anisohydric and near-isohydric behaviour,
were shown to vary with grapevine variety (Chaves et al., respectively, in field experiments (Schultz, 2003; Soar et al.,
1987; Schultz, 1996, 2003; Bota et al., 2001; Soar et al., 2006) did not display the same stomatal behaviour when
2006; Palliotti et al., 2009). Yet variation in photosynthetic experiments were performed with potted plants (Chouzouri
efficiency seems to be small (Bota et al., 2001), suggesting and Schultz, 2005).
that genotypic variation in WUE is largely linked to diversity Recent studies performed in our group have also revealed
in stomatal conductance, under both well-watered and water- differences between varieties [‘Touriga Nacional’,
deficit conditions (Escalona et al., 1999; Gaudillère et al., ‘Trincadeira’, ‘Aragonez’ (syn. ‘Tempranillo’), ‘Cabernet
2002; Chaves and Oliveira, 2004). Under drought conditions, Sauvignon’ and ‘Syrah’, see Table 2] in the response of leaf sto-
a close relationship was found between stomatal function matal conductance to deficit irrigation under field conditions.
and plant hydraulics (Sperry, 1986; Cochard et al., 2002; Stomatal conductance of ‘Touriga Nacional’ remained highest
Sperry et al., 2002). Stomata keep water flow within safe during the day (morning and afternoon) for similar leaf water
limits preventing the plants from exceeding those limits at potential, suggesting an anisohydric type of response (Fig. 1).
any particular water potential, therefore avoiding xylem embo- In contrast, ‘Syrah’ showed the lowest conductance of the five
lism (Sperry et al., 2002). Higher stomata sensitivity to water varieties, particularly at noon, therefore exhibiting a near-
deficits may compensate for higher vulnerability to cavitation isohydric response, contrary to earlier reports (Schultz, 2003;
under drought (Schultz, 2003). Vitis vinifera shows high Soar et al., 2006).
hydraulic conductivity in the main stem axis (Lovisolo For ‘Sangoviese’, Poni et al. (2007) pose questions regard-
et al., 2007). However, leaf hydraulic conductance can sub- ing its classification with respect to response to water stress.
stantially constrain water transport, being a more important The authors discuss in their paper that because the first cri-
hydraulic bottleneck than the stem (Sack et al., 1993). It is terion to classify genotypes as being isohydric or anysohydric
also known that hydraulic conductance of roots and shoots is how their leaf-water status (namely midday leaf-water
influences stomatal regulation and plant transpiration potential) responds to a soil-water deficit treatment, they
(Lovisolo and Schubert, 1998; Aasamaa et al., 2001; Rogiers would classify ‘Sangoviese’ as anisohydric. However,
et al., 2009). The distribution of vessel sizes varies with several effects posed by partial rootzone drying on these
variety and the larger sizes often result in higher sensitiveness vines, such as a fast cessation of shoot growth, leaves
to embolism under drought conditions (Chouzouri and tending to assume a vertical orientation during midday to
Schultz, 2005). reduce light interception, and a pronounced and steady
Leaf morpho-anatomy and related biochemistry (epicuticu- increase of WUEi, have been reported as being more typical
lar wax composition, lipid composition, mesophyll thickness, of an isohydric strategy.
etc.) may also play a role in explaining plant adaptation to Bearing in mind the available data, a classification of
water stress (Syvertsen et al., 1995; Boyer et al., 1997; grapevine varieties as strictly iso- or anisohydric may prove
Cameron et al., 2006). Differences among V. vinifera have inappropriate. It seems plausible that stomatal responses to
been reported in these characteristics (Schultz, 1996; water deficits in a specific variety will vary according to
Moutinho-Pereira et al., 2007). the particular combination of the rootstock, the climate
Grapevine is generally considered a ‘drought-avoiding’ (VPD and temperature), and the intensity and duration of
species, with an efficient stomatal control over transpiration water deficits. In fact, under prolonged water deficits more
(Chaves et al., 1987; Schultz, 2003). However, some geno- rigid cell walls may develop, leading to a larger decline in
types have shown a better control of stomata than others in plant water potential at midday, characteristic of the anyso-
response to water deficits and accordingly have been classified hydric response. Moreover, osmotic adjustment may contrib-
as isohydric (drought avoiders or ‘pessimistic’); the others, ute to the maintenance of open stomata at lower water
showing lower control over stomatal aperture under water potentials, by enabling an improved turgor in response to a
stress, were considered anisohydric, with an ‘optimistic’ slowly imposed water deficits. This combination of responses
response (Schultz, 2003; Soar et al., 2006). Schultz (2003) will interact with scion structural factors such as water-
considered ‘Grenache’ to be a nearly isohydric genotype conducting capacity of stems and petioles to dictate response
showing a marked regulation of stomatal conductance to to water deficits.
decreasing soil water, whereas ‘Syrah’ exhibited a response This is an area of research deserving further investigation in
closer to an anisohydric type. The same contrasting behaviour order to clarify the relative importance of the factors involved
between ‘Grenache’ and ‘Syrah’ in response to atmospheric in the dynamic response of stomata to water deficits.
 Chaves et al. — Grapevine under deficit irrigation 665

TA B L E 1. List of grapevine varieties categorized as a function of the response of the water potential to water deficit (iso- or
anisohydric), cultivated in soil (F) or in pots (P), with the corresponding range of values of water potential measured in each
experiment

Variety Category Set-up Range of c (MPa) References

‘Chardonnay’ Anisohydric F and P 20.4 to 21.0 Tyerman (2007), Vandeleur et al. (2009), Rogiers et al. (2009)
‘Cabernet Sauvignon’ Anisohydric F 20.7 to 21.5 Williams and Baeza (2007)
Isohydric F 20.25 to 21.5 Chalmers (2007)
‘Falanghina’ Near-isohydric F 20.7 to 21.8 Giorio et al. (2007)
‘Kékfrancos’ Near-isohydric F 20.1 to 21.2 Zsófi et al. (2008, 2009a, b)
‘Grenache’ Near-isohydric F and P 20.2 to 21.4 Schultz (2003), Santesteban et al. (2009)
(Not clear) P 20.2 to 20.4 Chouzouri and Schultz (2005)
‘Lambrusco’ Isohydric P 20.6 to 21.2 Poni et al. (2009)
‘Montepulciano’ Anisohydric F – Silvestroni et al. (2005)
‘Manto Negro’ Isohydric F 20.05 to 20.7 Medrano et al. (2003)
Anisohydric – – Lovisolo et al. (2010)
‘Merlot’ Anisohydric F 20.8 to 21.3 Williams and Baeza (2007), Shellie and Glenn (2008)
‘Portugiesier’ Near-isohydric – 20.1 to 20.9 Zsófi et al. (2008)
‘Riesling’ Anysohydric – – Lovisolo et al. (2010)
‘Sangiovese’ Isohydric F and P 20.2 to 21.3 Poni et al. (2007), Silvestroni et al. (2005)
Anysohidric P 20.55 to 21.3 Poni et al. (2007)
‘Seedless Thomson’ Anysohidric F 20.7 to 21.3 Williams and Baeza (2007)
‘Semillon’ Anisohydric F and P 20.4 to 21.8 Rogiers et al. (2009)
‘Soultanina’ Isohydric P 20.15 to 20.8 Paranychianakis et al. (2004)
‘Syrah Anisohydric F and P 20.2 to 20.8 Schultz (2003), Chalmers (2007), Rogiers et al. (2009),
Santesteban et al. (2009)
20.2 to 21.4
(Not clear) P 20.2 to 20.4 Chouzouri and Schultz (2005)
‘Tempranillo’ (syn. ‘Aragonez’) Isohydric F and P 20.05 to 21.3 Medrano et al. (2003), Antolı́n et al. (2006), Sousa et al. (2006)
Near-isohydric F 20.2 to 21.5 Intrigliolo et al. (2005)
Anisohydric F and P – Lovisolo et al. (2010), Santesteban et al. (2009)
‘Touriga Nacional’ Anisohydric F 20.2 to 21.5 Moutinho-Pereira et al. (2004)
‘Viognier’ Near-isohydric F – Shellie and Glenn (2008)

TA B L E 2. Pre-dawn leaf water potential (cpd), leaf temperature (Tleaf ), leaf stomatal conductance to water vapour (gsw), net
assimilation (An), intrinsic water use efficiency (WUEi) and d13C measured for five Vitis vinifera varieties

Variety cpd (MPa) Tleaf (8C) gsw (mol H2O m22 s21) An (mmol CO2 m22 s21) WUEi (mmol CO2 mol H2O21) d13C (‰)

ARA 20.25 + 0.01 30.5 + 0.2 0.076 + 0.006 15.2 + 0.8 59 + 5 227.60 + 0.47
TRI 20.10 + 0.06 30.7 + 1.6 0.074 + 0.005 14.1 + 0.5 54 + 4 227.96 + 0.75
SYR 20.19 + 0.02 34.4 + 1.5 0.049 + 0.008 12.1 + 0.7 93 + 12 227.39 + 0.66
CAB 20.21 + 0.07 31.4 + 1.6 0.085 + 0.008 12.4 + 0.5 45 + 4 227.66 + 1.07
TOU 20.10 + 0.02 29.5 + 1.5 0.115 + 0.007 15.6 + 0.7 69 + 14 228.54 + 0.69

ARA, ‘Aragonez’ (¼ ‘Tempranilho’); TRI, ‘Trincadeira’; SYR, ‘Syrah’; CAB, ‘Cabernet Sauvignon’; TOU, ‘Touriga Nacional’. Vines were grown in field
conditions in southern Portugal (38 8480 N, 7 8290 W) and were 6 –8 years old. Plants were grafted on the 1103-P rootstock, planted at a density of 4000 plants
21
ha and trained on a bilateral Royal Cordon system. Leaf water potential was measured with a pressure chamber (Model 1000; PMS instrument Co.). Leaf
temperature was assessed by thermal imaging (IR Snapshot 525, 8– 12 mm detector) at midday, and was immediately followed by measurements of leaf
stomatal conductance using a portable photosynthesis system (Licor-6400, Li-COR Inc.) equipped with a transparent leaf chamber. Values of An and WUEi
were determined at saturating light (1200 mmol m22s21), 360 p.p.m. CO2 and block temperature of 25 8C, using a Licor-6400 equipped with a 6400-02B LED
light source. Measurements were carried at the beginning of August 2007. Values are means + s.d. (n ¼ 3–8 replicates) (J. M. Costa and M. F. Ortuño,
unpubl. res.).

LON G- DI S TAN C E S I GN AL L IN G O F WAT E R

limitation may dominate over root chemical signalling
DEFI CI TS
(Comstock, 2002; Voisin et al., 2006; Neumann, 2008;
Under soil drying plants reduce water use by stomatal closure Ahmadi et al., 2009). This seems to be the case in some
and decreased growth. Hydraulic and chemical signals sent woody species, where chemical root-to-shoot signalling
from drying roots to the shoot are involved in the regulation appears to be inefficient in controlling stomatal behaviour
of these responses (Davies et al., 1994; Dodd et al., 1996; (Augé and Moore, 2002) or when other abiotic stresses
Liu et al., 2003). However, the relative importance of the co-occur with drought, as usually happens when plants are
two types of signalling in the control of stomatal aperture growing in their natural environment. Nevertheless, the
and leaf growth is still the subject of discussion. Depending primary role of a root-to-shoot hydraulic signal is generally
on the species and/or experimental conditions hydraulic followed by an increased ABA biosynthesis in the shoot that
666 Chaves et al. — Grapevine under deficit irrigation

Touriga Nacional
0·35 Syrah
TOU Aragonez
0·30 TOU Cabernet Sauvignon
Trincadeira
TOU

0·25
gsw (mol H2O m–2 s–1)
y = 0·159x 2 + 0·334x + 0·329
TOU TOU
0·20 TOU

SYR
SYR
0·15 TOU
TOU
SYR SYR
0·10 SYR SYR
y = 0·097x 2 + 0·220x + 0·196
SYR
SYR
0·05

0·00
0·0 –0·2 –0·4 –0·6 –0·8 –1·0 –1·2 –1·4 –1·6 –1·8
Leaf water potential (MPa)

F I G . 1. Relationship between leaf stomatal conductance to water vapour (gsw) and leaf water potential (c) measured throughout the day ( pre-dawn and midday)
for five different Vitis vinifera varieties, ‘Touriga Nacional’, ‘Syrah’, ‘Aragonez’ (‘Tempranilho’), ‘Cabernet Sauvignon’ and ‘Trincadeira’, as [Link]
were grown in field conditions in southern Portugal (38 8480 N, 7 8290 W) and were 6– 8 years old. Vines were grafted on the 1103-P rootstock, planted at a density
of 4000 plants ha21 and trained on a bilateral Royal Cordon system. Measurements took place during the summer season (beginning of August) of three con-
secutive years: 2006, 2007 and 2008. c was measured with a pressure chamber (Model 1000; PMS instrument Co., Corvallis, OR, USA) and gsw was measured
with a portable photosynthesis system (Licor-6400, LI-COR Inc., Lincoln, NE, USA) equipped with a transparent leaf chamber. Horizontal and vertical bars
indicate the standard deviation (n ¼ 8). Lines represent regression lines estimated for the varieties ‘Touriga’ and ‘Syrah’, as indicated.

regulates stomata (Christmann et al., 2007) and leaf growth at berry maturity, whereas earlier in the season (véraison) a
(Chazen et al., 1995; Neumann et al., 1997). Moreover, a low xylem pH was measured and no correlation between
great deal of evidence highlights the importance of ABA as ABA and gs was found (Fig. 2). Sharp and Davies (2009)
a root-sourced signal transported via the xylem and involved found that drought-induced change in pH is more common
in stomatal regulation of droughted plants (reviewed by in herbaceous than in woody perennial species. In fact,
Dodd et al., 1996, 2006; Wilkinson and Davies, 2002; among 22 woody species they observed an increase in pH in
Davies et al., 2005). Even so, other compounds such as the only four of them, the majority maintaining a pH similar to
precursors of ABA (Sauter et al., 2002; Lee et al., 2006; the well-watered plants (Sharp and Davies, 2009).
Jiang and Hartung, 2008), low concentration of cytokinins Grapevine stomata also strongly respond to plant water
(Shashidhar et al., 1996; Stoll et al., 2000; Hansen and status, through hydraulic tensions developed in the xylem
Dorffling, 2003) and changes in mineral composition or pH affecting leaf turgor. Positive correlations between pre-dawn
of the xylem (Wilkinson and Davies, 1997; Hartung et al., water potential and maximum gs have generally been found
1998; Prokic et al., 2006; Jia and Davies, 2007) might also in grapevines subjected to water deficits (Correia et al.,
be implicated in the regulation of water use at the leaf level 1995; Flexas et al., 1998; Rodrigues et al., 2008). As in
(reviewed by Schachtmann and Goodger, 2008). Much evi- other species a decrease in shoot hydraulic conductivity has
dence suggests that xylem sap pH can indeed modulate stoma- been shown to occur in water-stressed grapevines (Schultz
tal and growth responses to root chemical signals produced in and Matthews, 1988; Lovisolo and Schubert, 1998; Lovisolo
drying soils (Wilkinson and Davies, 1997, 2002; Wilkinson, et al., 2002) and is linearly correlated with gs under mild
2004). For acidic xylem sap pH, ABAH is taken by the leaf stress levels (Lovisolo and Schubert, 1998). Moreover, it was
and metabolized or partitioned into alkaline compartments in shown that a decline in leaf water potential might enhance sto-
the symplast of leaf cells, away from the sites of action of matal sensitivity to ABA. This interactive effect can explain
the hormone on stomata. Conversely, as pH increases, the pro- the decrease in gs observed at midday in grapevines growing
portion of ionized ABA transported in the xylem sap rises (not under field conditions, including well-watered ones, in spite
taken up by mesophyll cells) and so is maintained longer in the of constant diurnal [ABA] in the xylem stream (Correia
leaf apoplast adjacent to the guard cells, having greater control et al., 1995; Rodrigues et al., 2008)
on stomatal behaviour (Hartung et al., 1998; Wilkinson, 2004). When considering deficit irrigation, there is no clear picture
This effect is particularly important in grapevines as usually of the relative importance of hydraulic and chemical signalling
they have pH values close to the pKa of ABA ( pH 4.8), as on plant response to water deficit. There are studies indicating
shown by Stoll et al. (2000) and Rodrigues et al. (2008). a marked decrease of gs in PRD grapevines relative to conven-
Indeed, work done with the grapevine variety ‘Castelão’ tionally irrigated vines, in spite of comparable shoot water
(Rodrigues et al., 2008) provided evidence for a synergistic status (Dry and Loveys, 1999; Du et al., 2006), therefore
effect of increased pH and ABA, explaining stomatal closure suggesting the involvement of a non-hydraulic signal in
 Chaves et al. — Grapevine under deficit irrigation 667

A B
2·0
NI
PRD
DI
1·5 FI a
ABA (mmol m–3)

n.s.
a
a
1·0 a
a
b
ab b b
b
0·5 b b bc
b
b c
b
0·0

6·0

5·5
n.s.
n.s.

5·0 n.s.
pH

4·5 n.s. n.s. n.s.

4·0

3·5
10:00 14:00 18:00 10:00 14:00 18:00
Time of the day (hours) Time of the day (hours)

F I G . 2. Diurnal changes in concentration of abscisic acid (ABA) in the xylem sap and pH of the xylem sap of field-grown Castelão grapevines in Pegões,
Portugal, under four water treatments (NI, non-irrigated; PRD, partial rootzone drying; DI, deficit irrigated; FI, fully irrigated), measured on two days of the
2002 growing season: (A) veraison (25 July) and (B) mid-ripening (22 August). For each measurement time values are the mean of four measurements.
Error bars indicate the standard error. Different letters show statistically significant differences among treatments at P , 0.05. (Rodrigues et al., 2008).

stomatal regulation. Several other studies, however, did not to irrigation by exhibiting higher sap flow rates than usually
find evidence for a more marked stomatal closure in PRD occurs when the entire root zone is watered. This increase in
than in DI grapevines (Souza et al., 2003; Dorji et al., 2005; root hydraulic conductivity seems to be mediated by aquaporin
De la Hera et al., 2007; Marsal et al., 2008; Rodrigues activity (Martre et al., 2002; Lovisolo and Schubert, 2006) as a
et al., 2008). The higher water status of PRD plants may be significant part of the radial water transport takes place through
derived from the observed restriction in vegetative growth of the cell-to-cell pathway (Martre et al., 2002; Siefritz et al.,
PRD plants (Santos et al., 2003, 2005; Chaves et al., 2007), 2002).
leading to lower plant water use and thus more water available Considering the causes for the observed restriction of vege-
in the soil near the root system. Differences in root architec- tative growth under similar or better water status in PRD
ture, with an increased ability to exploit deeper soil layers grapevines as compared with DI, chemical signals are the
(Dry et al., 2000; Mingo et al., 2004; Santos et al., 2007), likely candidates to explain these results (Chaves et al.,
have also been reported as well as an increase of root hydraulic 2007). Such chemical root-to-shoot signalling probably
conductivity after root rewatering. In fact, recent work in an involves a reduction of cytokinins (CKs) (Kudoyarova et al.,
irrigated pear orchard showed that root sap flow on the wet 2007) or an increase of ethylene (Sobeih et al., 2004). CKs
side of PRD plants was enhanced compared with control are synthesized mainly in the roots (Aloni et al., 2005) and
plants equally watered on both sides of the root system were shown to play an important role as long-distance signal-
(Kang et al., 2003). Also, Green et al. (1997) observed in ling molecules (Schmulling, 2002; Werner et al., 2003; Hirose
mature apple trees that previously dehydrated roots responded et al., 2008). Dry et al. (2001) observed shoot growth
668 Chaves et al. — Grapevine under deficit irrigation

inhibition in PRD grapevines in parallel with a marked such as at the green berry stage, may have a profound effect on
decrease in the concentration of CK in shoots and roots. the final berry maturity (R. Francisco et al., unpubl. res.).
This effect was reversed by exogenous application of a syn- Vine water status is known to influence fruit composition
thetic CK. Similarly, a marked reduction in zeatin and zeatin through an indirect effect on berry size, and therefore the ratio of
riboside concentrations in roots, shoot tips and buds was skin to pulp, which increases in the smaller berries of vines sub-
found in PRD grapevines (Stoll et al., 2000). Although most jected to water deficits (Bravdo et al., 1985; Kennedy et al.,
results in other species also point to a decrease in the delivery 2002). There is, however, a direct, possibly greater effect on skin
of CKs to the xylem sap in water-stressed plants (Bano et al., tannin and anthocyanin contents (Roby et al., 2004). The reported
1993; Shashidhar et al., 1996; Hansen and Dorffling, 2003), increase in skin tannin and anthocyanin that accompanies water
there are exceptions with the opposite effect (CK increase) deficits seems to result from different sensitivity of berry
(Pospı́silová et al., 2005). tissues to water deficits, with the exocarp being less affected
than the inner mesocarp (Roby et al., 2004). Proteomic studies
in berries from grapevines subjected to different irrigation treat-
ments that suggest that metabolic differences in response to
C H A N G E S I N B E R RY G ROW T H , M E TA B O L I S M
water status occur at early stages of berry development (R.
A ND CO M PO SITI ON UN DER WATER D E FIC IT
Francisco et al., unpubl. res.) confirm that they are partly indepen-
Water deficit influences berry development, metabolism and dent of the effect on berry size.
final composition, and its timing and intensity dictate the
extent of alterations occurring in wine colour and flavour.
Berry growth
Interestingly, water deficit was also shown to enhance photo-
protection mechanisms in berries (Deluc et al., 2009). In Grape berry is a non-climacteric fruit with a double sigmoid
general, mild water deficits were shown to have a positive growth curve (Coombe, 1976). Stages I and III of growth are sep-
impact on wine quality in red varieties (Bravdo et al., 1985). arated by a lag phase (stage II). During stage I, imported carbo-
In this context, deficit irrigation can provide the means to hydrates are used for seed development, cell proliferation and
manipulate wine sensory characteristics. However, the effects expansion, and synthesis of organic acids (Coombe, 1992). At
of deficit irrigation on berry and wine quality will depend on this stage the berry is exclusively connected to the vine through
the climatic characteristics during the growing season, soil the xylem, and the impact of water deficit on berry growth is
type, grapevine variety and timing of application (Dry and thought to occur directly by changes in water import by the
Loveys, 1998; Santos et al., 2003, 2005). xylem, which possibly induces a decrease in mesocarp cell
Transcriptional analysis of grape berries from vines sub- turgor (Thomas et al., 2006). There is consequently a reduction
jected to moderate water deficits at the end-ripening stage in the expansion of grape berries. However, it is also possible
showed alterations in mRNA expression patterns particularly that the ABA synthesized under water stress limits cell division
associated with cell-wall, sugar and hormone metabolism and consequently small berries are produced. The second hypoth-
(Deluc et al., 2007). The most profound alterations were esis correlates well with the observed inhibition of grape develop-
related to ethylene, auxin and ABA, but an enhancement of ment following water deficit at pre-véraison. This leads to a
the expression of several genes of the phenylpropanoid cascade of events culminating in earlier grape ripening (e.g. accel-
pathway was also observed. erating sugar and anthocyanin accumulation and malic acid break-
The impact of water deficit on grape berry proteomes was down) (Castellarin et al., 2007a, b). The beginning of the second
reported by Grimplet et al. (2009). These authors studied the phase of berry growth (stage III), known as véraison, is character-
alterations observed in the skin, pulp and seed proteomes of ized by softening and colouring of the berry and a size increase.
fully ripe berries when comparing water-deficit vines (no irriga- After véraison a reduction in berry size due to water deficit is prob-
tion) with well-watered plants (irrigation from pre-véraison to ably the result of more than one mechanism (Thomas et al., 2006).
the end of berry maturity) and showed that 7 % of pericarp pro- At this stage, the berry’s connectivity to the vine is via the phloem
teins were water-stress responsive. Using such an approach, we (Thomas et al., 2006). Moreover, a reduction of berry size might be
are currently studying the proteome dynamics of grapevines of only indirectly caused by water stress, through a decrease in photo-
the variety ‘Aragonez’ (syn. ‘Tempranillo’) along berry devel- synthesis (Wang et al., 2003). Post-véraison water deficit increases
opment using three irrigation strategies. When comparing the proportion of whole-berry fresh mass represented by seeds and
berries of fully irrigated (FI) vines with ones from deficit irri- skin (Roby and Matthews, 2004) and berries present ‘thicker
gated (RDI) and rain-fed (NI) vines, several proteins were ident- skins’ at harvest probably due to a decrease in the activity of
ified as stress responsive. One such protein was vacuolar pectin methylesterase enzyme (Deytieux-Belleau et al., 2008),
invertase (GIN1), which was significantly down-regulated as was shown in water-stressed tomato cherry fruit (Barbagallo
under NI and RDI when compared with FI conditions (Fig. 3). et al., 2008). This results in higher content of skin-based constitu-
These alterations were observed at green stage ( pre-véraison) ents (e.g. tannins and anthocyanins) on a berry mass basis and as a
and véraison. Moreover, the peak of expression of this protein, consequence the must from those berries is much richer in skin-
which was reported to occur at véraison by others (Deluc derived extractives (Chatelet et al., 2008).
et al., 2007; Giribaldi et al., 2007; Negri et al., 2008), was
observed later in RDI than in FI berries. These results suggest
Accumulation of sugars and organic acids
that water availability modulates not only the amount but also
the timing of protein expression. It suggests as well that Grape quality largely depends on sugar/acid balance at
changes taking place very early during berry development, harvest. Prior to véraison, most sucrose imported into the
 Chaves et al. — Grapevine under deficit irrigation 669

400 A Sucrose 6
Fructose

Invertase (% normalized volume)

350

Sugar content (mmol g–1 f· wt)

Glucose 5
300 GIN
4
250

200 3

150
2
100
1
50

0 0

400 B 6

Invertase (% normalized volume)

350
Sugar content (mmol g–1 f· wt)

5
300
4
250

200 3

150
2
100
1
50

0 0

400 C 6

Invertase (% normalized volume)

350
Sugar content (mmol g–1 f· wt)

5
300
4
250

200 3

150
2
100
1
50

0 0
G stage Véraison Maturation Full maturation

F I G . 3. The influence of water deficit on sugar metabolism and vacuolar invertase (GIN1) expression profile along fruit ripening. (A) Plants under full irrigation
conditions; (B) plants under regulated deficit irrigation conditions and (C) plants under no irrigation but rain-fed. 2-DE spot volume is represented as the per-
centage of normalized volume. Symbols represent means + s.e. (n ¼ 3).

berries is metabolized with little if any storage. However, fol- up by monosaccharide transporters. In grape berry, it is
lowing véraison hexoses accumulate in the berries at high con- known that invertase expression considerably precedes the
centration (1 M or even more). Grapevine is thought to be a onset of sugar accumulation (Davies and Robinson, 1996).
symplastic phloem ‘loader’ due to the presence of plasmodes- This suggests that the triggering of ripening depends on the
mata connecting mesophyll cells with phloem-associated cells activation of sugar transporters (for a review, see Conde
(Gamalei, 1989). It has been suggested that the symplastic et al., 2007).
connections via plasmodesmata between the sieve tubes and Moderate water deficit promotes sugar accumulation either
the mesocarp cells remain for quite a long period during as a result of inhibiting lateral shoot growth, which induces
berry development. Phloem unloading seems to occur via a reallocation of carbohydrates to fruits, or as a direct effect
efflux into the apoplast and subsequent uptake by sink cells. of ABA signalling on fruit ripening (Coombe, 1989). Indeed,
Sucrose from the phloem can be imported from the apoplast experimental evidence suggested activation of ABA-mediated
via direct sucrose transporters or it can be hydrolysed to uptake of hexose (Deluc et al., 2009). However, the
glucose and fructose by cell-wall-bound invertases and taken
670 Chaves et al. — Grapevine under deficit irrigation

mechanisms underlying accumulation of hexoses under water timing of imposition of water deficit (Castellarin et al.,
deficit have not been elucidated completely. 2007a).
The effects of water deficit on sugar content of grapevine Flavonols play a fundamental role in grape quality, as they
berries are variety-dependent (Gaudillère et al., 2002). For act as co-pigments with anthocyanins and stabilize colour in
example, no significant changes were observed in ‘Merlot’ young red wines (Boulton, 2001). Flavonol biosynthesis is
sugar content under water deficits, while a significant increase closely related to that of anthocyanins (Jeong et al., 2006).
in sugar content was observed in ‘Cabernet Sauvignon’ berries However, in contrast to anthocyanins, a small number of flavo-
(Castellarin et al., 2007a, b). Similarly, Deluc et al. (2009) nols were identified and available data were limited to a few
observed an increase in berry sugar content under water defi- grape varieties (Mattivi et al., 2006). The main flavonols
cits in ‘Cabernet Sauvignon’ but not in ‘Chardonnay’. This reported in grape berries are quercetin-3-glucoside and
may be explained either by differences in vigour, and therefore quercetin-3-O-glucuronide (Downey et al., 2003). Deficit irri-
source/sink equilibrium, between varieties, or by different gation was reported to have a moderate effect on flavonol syn-
mechanisms underlying the response of grape berry develop- thesis in red grapevines (Grimplet et al., 2007). In turn, the
ment to water limitation according to the timing and intensity timing of water deficit does not change flavonol content
of water stress imposition. Indeed, it was shown that water (Kennedy et al., 2002). Mattivi et al. (2006) have suggested
deficit has more effect on berry sugar accumulation when that anthocyanins and flavonols share the same biosynthetic
imposed before véraison (Keller, 2005; Keller et al., 2006). enzymes. This may indicate that, like anthocyanins, changes
In most cases, no titratable acidity changes have been to flavonol under water deficits may occur rather in compo-
observed in the must from moderately water-stressed vines sition than in accumulation. More recently, in a white grape-
(Matthews and Anderson, 1989; Esteban et al., 1999). vine (‘Chardonnay’), flavonol concentrations were reported
However, some studies report a reduction of titratable acidity to increase under water deficits, which was not the case in a
due to deficit irrigation as compared with full irrigation red grapevine (‘Cabernet Sauvignon’) in the same study
(Sheltie, 2006; Santos et al., 2007). Malate/tartarate ratio is (Deluc et al., 2009). This suggests a greater need for berry
in general lower due to malate breakdown in vines with low photoprotection in these varieties, as previously shown in
water status (Matthews and Anderson, 1989). apples with low levels of anthocyanins (Merzlyak et al., 2008).
Proanthocyanidins or condensed tannins are flavan-3-ol oli-
gomers. They are important sensory components, providing
Polyphenols
wine with bitterness and astringency. However, little is
Among the different classes of polyphenols present in grape known about proanthocyanidins (for reviews, see Dixon
berries the most important are flavonoids [anthocyanins, flavo- et al., 2005; Xie and Dixon, 2005) and a standardized
nols and proanthocyanidins (also called condensed tannins)] measure of tannins has not yet been adopted (Downey et al.,
and stilbenes. They are mainly localized in exocarp and seed 2006). Besides, changes occurring in proanthocyanidins
endocarp tissues and it is well known that vine water status during grape development are complex, involving increases
affects accumulation of polyphenols in these tissues. in the degree of polymerization, in the proportion of
Regulating grapevine water deficit is a powerful tool to (– )-epigallocatechin extension units, and in polymer-
manage the amount of these compounds and improve wine associated anthocyanins (Kennedy et al., 2002).
quality (Kennedy et al., 2002). Proanthocyanidins appear to be only slightly affected by
Anthocyanins are synthesized via the flavonoid pathway in water deficit (Downey et al., 2006) and the increases in skin
the berry skin of red grapevines from the onset of ripening tannin that accompany water deficits appear to result more
(véraison) but they are non-existent in white grapevine var- from differential growth sensitivity of the inner mesocarp
ieties due to a multi-allelic mutation (Walker et al., 2007). and the exocarp than from direct effects on phenolic biosyn-
Water deficit has been considered to enhance accumulation thesis (Roby et al., 2004). The effect of concentration of
of anthocyanins, through the stimulation of anthocyanin seed tannins on wine characteristics is not known (Matthews
hydroxylation, probably by upregulating the gene encoding and Nuzzo, 2007). Moreover, few works have reported
the enzyme F30 50 H (Mattivi et al., 2006; Castellarin et al., whether water status influences seed proanthocyanidin
2007b). This enzyme converts hydroxylated anthocyanins content. Two studies performed with the same variety
(cyanidin and delphinidin) into their methoxylated derivates (although in different environments) did not show any signifi-
( peonidin, petunidin and malvidin) (Kennedy et al., 2002; cant effects of water deficit on seed proanthocyanidins
Castellarin et al., 2007b). Indeed, the major anthocyanins syn- (Kennedy et al., 2000; Geny et al., 2003). A gene expression
thesized in the berries under water deficits are peonidin study undertaken by our team (O. Zarrouk et al., unpubl.
3-O-b-glucoside and malvidin 3-O-b-glucoside, because res.) demonstrated differential expression during grape berry
methoxylation of delphinidin to produce its derivate petunidin development of the ANR gene in grape seeds and a slight
rarely occurs (Castellarin et al., 2007b; Deluc et al., 2009). downregulation under water stress.
Water stress seems to have a greater impact on anthocyanin Stilbenes belong to the non-flavonoid class of phenolic com-
composition than on its total concentration. Early imposition pounds. Generally, stilbenes are considered as phytoalexins,
of water stress led to increased sugar accumulation, which and their formation in grape leaves was correlated with
accelerates anthocyanin synthesis (Castellarin et al., 2007b), disease resistance. Resveratrol is considered the most bioactive
probably due to ‘sucrose boxes’ in the promoters of LDOX stilbene in grapevines (Bavaresco et al., 2008). In grape
and DFR genes (Gollop et al., 2001, 2002). Gene regulation berries, resveratrol synthesis is catalysed by stilbene synthase
of the anthocyanin pathway was known to be affected by the (STS), which shares the same substrates used by chalcone
 Chaves et al. — Grapevine under deficit irrigation 671

synthase for flavonoid production (Versari et al., 2001). It studies of varieties in response to environmental stresses are
accumulates mainly in the grape skin and seeds, and it has instrumental to the understanding of grapevine adaptation to
been found both in red and white grapes at a large range of more arid climates. Further knowledge on berry development,
concentrations, depending on biotic and abiotic conditions including the timing of accumulation of various berry com-
(Jimenez et al., 2007). Conflicting results have been found ponents, and their dependence on water availability, is critical
on the effects of water deficit on resveratrol synthesis. for an optimal choice of irrigation strategy. Proteomic and
Research conducted by Vezzuli et al. (2007) observed little transcriptomic studies are providing new avenues for that
effect of drought on resveratrol concentrations in grape berry understanding. Available data suggest that water deficits inter-
skin. An increase in mRNA abundance of STS was reported act with development to alter the expression of genes respon-
by Grimplet et al. (2007), which suggests an increase in sible for some grape berry compounds and metabolite
resveratrol accumulation (Versari et al., 2001). Under moder- transporters. Although some of those changes seem to be tran-
ate water deficit, gene expression of STS1 and STS2 in grape sient, it is plausible that they will have an impact on berry
seeds showed an upregulation at berry maturity (O. Zarrouk maturity and final wine quality.
et al., unpubl. res.).

Aromas ACK NOW LED GE MENTS

The aroma that builds up in grapes results from several com- R.F., O.Z., A.R., T.S. and J.M.C. are supported by fellowships
pounds (terpenoids and their derivatives, esters, aldehydes and granted by Fundação para a Ciência e Tecnologia (FCT).
thiols) stored as non-volatile precursors mainly in exocarp WATERWEB, POCI/AGR/59079/2004 and PPCDT/AGR/
vacuoles. 61980/2004 projects provided funds to support part of the
The influence of the irrigation strategy on grape berry research presented. We are very grateful to Olga Grant for
aromas has not received much research. However, two major help with the English text and for judicious comments.
studies suggest that deficit irrigation alters several sensory
attributes of the wine as well as the concentration of caroten-
oids and their derivatives in berries, as compared with standard L I T E R AT U R E CI T E D
irrigation grapevines (Chapman et al., 2005; Bindon et al., Aasamaa K, Sõber A, Rahi M. 2001. Leaf anatomical characteristics associ-
2007). Chapman et al. (2005) reported that water deficits led ated with shoot hydraulic conductance, stomatal conductance and stoma-
to wine with more fruity and less vegetal aromas than those tal sensitivity to changes of leaf water status in temperate deciduous trees,
from vines with high water status, in the variety ‘Cabernet Australian Journal of Plant Physiology 28: 765–774.
Ahmadi SH, Andersen MN, Poulsen RT, Plauborg F, Hansen S. 2009. A
Sauvignon’. According to these authors water deficits may quantitative approach to developing more mechanistic gas exchange
have led to a greater flux of carbon through alternative biosyn- models for field grown potato: a new insight into chemical and hydraulic
thetic pathways leading to an increase in amino acids ( precur- signalling. Agricultural and Forest Meteorology 149: 1541–1551.
sors of esters in wines) and in carotenoids, resulting in a Alleweldt G, Spiegel-Roy P, Reisch B. 1990. Grapes (Vitis). Acta
more fruity aroma. Bindon et al. (2007) observed that Horticulturae 290: 291–327.
Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI. 2005.
deficit irrigation led to an increase in the concentration of Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by
hydrolytically released C13-norisoprenoids (b-damascenone, the transpiration stream. Journal of Experimental Botany 56: 1535–1544.
b-ionone and 1,1,6- trimethyl-1,2-dihydronaphthalene) in Antolı́n MC, Ayari M, Sánchez-Dı́az M. 2006. Effects of partial rootzone
‘Cabernet Sauvignon’ grape berries at harvest. Furthermore, drying on yield, ripening and berry ABA in potted Tempranillo grape-
vines with split roots. Australian Journal of Grape and Wine Research
transcriptomic analysis of genes encoding enzymes involved 12: 13–20.
in the biosynthesis of volatile compounds revealed an increase Augé RM, Moore JL. 2002. Stomatal response to nonhydraulic root-to-shoot
in the transcript abundance of one terpenoid synthase, one communication of partial soil drying in relation to foliar dehydration tol-
carotenoid cleavage dioxygenase and several lipoxygenases erance. Environmental and Experimental Botany 47: 217 –229.
under conditions of water deficits (Deluc et al., 2009). Baeza P, Lissarrague JR. 2005. Agronomic and ecophysiological responses
of field-grown Cabernet Sauvignon grapevines to three irrigation treat-
However, we should emphasize that the correlation of ments. Acta Horticulturae 689: 373– 379.
enzyme transcript abundance with the reaction products they Bano A, Dorffling K, Bettin D, Hahn H. 1993. Abscisic acid and cytokinins
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