Journal of Experimental Botany, Vol. 53, No. 369, pp. 757–763, April 2002
Carbon isotope composition of sugars in grapevine,
an integrated indicator of vineyard water status
Jean-Pierre Gaudillère1,4, Cornelius Van Leeuwen2 and Nathalie Ollat3
1
INRA Agronomie, BP 81, 33883 Villenave d’Ornon, France
ENITA de Bordeaux, 1 Cours du Général de Gaulle, 33175 Gradignan cedex, France
3
INRA UREFV, BP 81, 33883 Villenave d’Ornon, France
2
Received 30 July 2001; Accepted 23 November 2001
Abstract
Photosynthetic carbon isotope composition (d13C)
was measured on sugars in mature fruits from fieldgrown grapevines. Sugar d13C and summer predawn
leaf water potential were significantly correlated.
The survey of different vineyards during four growing
seasons showed that sugar d13C in must at harvest
varied from 20ø to 26ø when conditions during
berry maturation varied from dry to wet. This range
allows a very sensitive detection of grapevine water
status under natural conditions. However, local differences due to soil capacity to supply water to
grapevines are maintained, whatever the annual
water balance. Leaf nitrogen content variations of
field-grown grapevines did not change d13C values.
Genetic variability of d13C between 31 grapevine
varieties for d13C was observed. Must sugar d13C
can be used to characterize vineyards for their soil
structural capacity to provide water to grapevines.
It was concluded that isotope carbon composition
in grapevine measured on sugars at harvest can be
applied to compare the capacities of vineyard soils
and canopy management to induce mild water stress
in order to produce premium wines.
Key words: d13C, genetic variability, Vitis vinifera L., water
stress.
Introduction
Unlike other agricultural species, grapevines (Vitis
vinifera L.) are generally cultivated under sub-optimum
conditions, particularly mild water stress, in order to
4
enhance quality. The water stress can be the result of
particular pedoclimatic conditions (rainfall timing or
available soil water in the root zone) in locations selected
for high quality potential, or can be induced by vineyard
management techniques (modification of canopy architecture or irrigation). Water stress reduces shoot growth
which improves berry composition, either by limiting the
number of sinks for carbohydrates or by improving
the microclimate inside the canopy (Smart et al., 1990).
Berry size is smaller when grapevines are submitted to
mild water deficits, especially those occurring between
flowering and veraison (beginning of maturation; Becker
and Zimmermann, 1984; Hardie and Considine, 1976;
Van Leeuwen and Seguin, 1994), but water deficits
occurring from veraison through to harvest cause little
reduction in berry size (Becker and Zimmermann, 1984).
Early and late mild water deficits increase berry sugar and
anthocyanin concentration (Matthews et al., 1990), partly
because of reduced berry size. These impacts on vine
development and berry composition enhance enological
quality potential, especially for red wine production. The
extent and timing of mild water deficits have been shown
to be a major factor in the ‘terroir’ effect (Seguin, 1983;
Koundouras et al., 1999).
Many studies exist on water relations in grapes. Several
techniques, using soil moisture status (soil water potential
or soil water content), and physiological indicators
can assess environmental water supply and actual grapevine water status. However, no existing single method
is convenient for assessing vine water uptake conditions
over the growing season in a large number of plots at a
reasonable cost. Because of the modifications induced by
water stress on vine physiology and the positive effects
of mild water stress on a balanced vine canopy and berry
constitution, an integrative tool for the diagnosis of vine
water status is required.
To whom correspondence should be addressed. Fax: q33 5 56 84 30 54. E-mail: [email protected]
ß Society for Experimental Biology 2002
758
Gaudillère et al.
Stable carbon isotope uptake is discriminated by diffusion and photosynthesis at the carboxylation step
(Farquhar et al., 1980). A robust model computes whole
plant water use efficiency from the 13Cu12C (denoted d13C)
in primary photosynthetic products (Brugnoli and
Farquhar, 2000). Basically d13C is determined by
the gradient of CO2 between the atmospheric and the
intercellular CO2 concentrations (CiuCa) and the main
factor which affects this ratio is water stress (Farquhar
et al., 1989). In oak and pine trees, nitrogen starvation
has also been shown to decrease CiuCa and d13C value in
leaf sugars (Guehl et al., 1995). However,the water use
efficiency of other species was not affected by leaf N
content (e.g. Douglas fir: Mitchell and Hinkley, 1993).
There is no information on the effect of nitrogen nutrition
and water use efficiency in grapevine.
During berry ripening, sucrose is translocated from
leaves to fruit and rapidly converted to glucose and fructose (Davies and Robinson, 1996). Therefore, the carbon
isotope ratio in the sugars of mature berries should
integrate leaf photosynthetic isotopic discrimination
of carbon during berry ripening. Previously published
results on grapes (Di Marco et al., 1977) showed that d13C
in berry juice and water-soluble leaf extracts collected on
field-grown vines were very similar during maturation.
In this work, a full set of d13C measured in purified sugars
from ripe berries is reported. The purpose of this paper is
to establish, for field-grown grapevines, the relationship
between d13C and summer water stress. The sensitivity of
the response to nitrogen nutrition, water availability and
genotype was studied in order to assess the use of carbon
isotope composition as an integrative tool for vine water
status diagnosis.
Materials and methods
Plant material and growing conditions
All the samples were collected in rain-fed vineyards in the
Bordeaux Region, on grapevines older than 5 years.
Vines were managed according to the traditional local
training systems (vertical shoot positioning, Guyot pruned,
5000–7000 plants ha1). All vineyards were trained to produce
7000–10 000 kg of fruits ha1.
In the Bordeaux region (448519 N) grapes were collected
in INRA experimental fields (Château Couhins, Cadaujac and
Ferrade, Villenave d’Ornon) and in the vineyard Cheval Blanc,
Saint Emilion from 1997 to 2000. Berries were harvested at
commercial maturity, when the Brix value of the must was
higher than 20 (Smart et al., 1990).
The relationships between soil water availability, leaf water
potential and d13C in berry sugars at maturity were studied in
a trial comparing three soils (sandy, clay and stony soils) in the
same location (Saint Emilion), bearing three varieties (Merlot,
Cabernet Sauvignon, Cabernet franc), during four growing
seasons (1997, 1998, 1999, 2000). The description of soil water
availability in this trial has been previously reported
(Van Leeuwen and Seguin, 1994). Briefly, soil water availability
at the beginning of the growing season changed with soil depth,
clay content and depth of the water table. The sandy soil
had a low water content, but a shallow water table provided
water to the roots all through the growing season. The clay and
stony soils could provide approximately 235 mm and 190 mm of
water, respectively, at bud burst.
Grapevine genetic variability for the d13C content was tested
in the INRA genetic conservatory set in the Ferrade domain.
The 31 varieties were grafted on the same rootstock (Fercal) in
1994. Each variety was represented by 5–10 individuals and
trained collectively in the same plot. The trellis size and green
pruning maintained a constant canopy area (1.3 m2 m2 soil) for
all the varieties, from 15 June to harvest. Berries were sampled
on five individuals in 1999 at the same date for all the varieties
when the must Brix value of the latest variety reached 20. The
canopy light interception and seasonal water balance (Table 2)
was calculated from mean canopy light interception (estimated
at 50%), daily rainfall and potential evapotranspiration
(Penman calculation) (Riou et al., 1994). The year of sampling,
1999, was representative of a rainy season with 170 mm in July
and August compared to the mean rainfall (100 mm) observed
in the Bordeaux area.
The effects of different soil nitrogen was studied in an experimental vineyard (Chateau Couhins, three blocks) with three
soil management systems: tillage, 25% or 50% of the soil
covered by Festuca elatior L. grass (Rodriguez-Lovelle and
Gaudillère, 1999). Soil mineral nitrogen is made less available
for grapevine by the competing grass.
Water and nitrogen status assessment
Predawn leaf water potential was measured every 10 d from
June to September in the Saint Emilion vineyard with a pressure
chamber (Scholander et al., 1965; Precis 2000 Gradignan,
France) on freshly cut, healthy, primary leaves from six plants
for each of the three soils and the three varieties.
Primary leaves were sampled at veraison for the measurement
of nitrogen content. Each leaf was sampled by punching three
leaf discs (85 mm2). N content (g m2) of freeze-dried samples
was measured using a CN analyser (NA2100 Protein, CE
Instruments, San Jose, California, USA). Pruning and weighing
of growth of annual wood removed, in winter, was used to
estimate vine vegetative vigour.
Berry juice and sugar preparation
Samples were made of 200 berries harvested randomly in the
vineyards just before commercial harvest, defined by the sugar
content and titrable acidity of the must. Berry juice was obtained
by hand pressing. Ten ml of juice were sampled, rapidly sterilized
by autoclaving (120 8C, 20 min), and stored at room temperature to prevent mono potassium tartaric salt precipitation until
the preparation of the samples for 13C measurements. Each
sample contained approximately 200 g l1 hexose. The hexose
fraction was purified by anion and cation exchange. One ml of
juice was gently pushed onto a 1 ml column filled with ion
exchange resin (Bio-Rad; Mixed bed resin AG501-X8).
Isotopic analysis
Ten ml of purified must containing approximately 1 mg sugars
or 5 ml of berry juice were put in a tin capsule, dried and oxidized
under oxygen. Carbon isotope content was measured using a
continuous flow isotope ratio mass spectrometer (Europa
Scientific Ltd., Crewe, UK) as described earlier (Avice et al.,
1996). The conventional expression was used with reference
Carbon isotope composition of grapevine
to the Pee Dee Belemnite standard (Farquhar et al., 1989):
Rs Rb
1000
d13 C ¼
Rb
where Rs is the 13Cu12C ratio of the sample and Rb is the 13Cu12C
of the PBD Standard. The isotopic composition of atmospheric
CO2 gives a d13C equal to 8ø (Farquhar et al., 1989).
Statistical comparisons were done with Excel (Microsoft)
and Systat 10 (SPSS Inc.) software.
Analytical precision was estimated with replicates of a single
sample. One single measure on a sample can estimate the
mean d13C value better than 0.15 unit of isotope composition
(-0.65% of the measure) with a confidence interval of 95%. The
field sampling error was measured in 1998 and 1999 on
12 samples collected in the same plot. One single measure on
juice made with 200 berries can estimate the mean of the d13C
value of the plot "0.7 unit with a probability of 95% or "3%
of the measure.
The d13C measured in the must and the purified sugars were
significantly linearly correlated (R2 ¼ 0.995, 66 samples). Sugar
d13C content could therefore be assessed on must at maturity
without any preliminary treatments. However, in this study all
the d13C values were obtained on purified sugar from mature
berry must.
Results
Relationship between predawn leaf water potential
during fruit maturation and d13C measured at harvest
759
four growing seasons. The linear relationship between
Ymin and d13C is highly significant (P-0.001). A general
relationship can be drawn (Fig. 3) with data collected
from the three red vine varieties (Cabernet Sauvignon,
Merlot and Cabernet franc, in 1997, 1998, 1999, and 2000)
and a highly significant linear correlation (P-0.001) was
obtained.
ANOVA analysis of the four seasons, three soils and
three varieties data showed a significant year, soil and
variety effect with significant soil 3 year and variety 3 year
interactions (Table 1). The 1998 year and the stony soil
combined to cause the driest conditions.
Table 2 shows the mean d13C measured on all the
samples from the three plots in the Saint Emilion vineyard
from 1997 to 2000. Mean water balance from May to
August was calculated as the difference between rainfall and half the potential evapotranspiration (Penman
calculation). The ranking of the d13C values matches well
with that of the summer mean water balance (July and
August), but not the May to August values.
Genetic variability of grapevine carbon isotope content
Leaf water status was measured on three soils types and
three varieties (Cabernet Sauvignon, Merlot, Cabernet
franc) from the vineyard Cheval Blanc, Saint Emilion,
in 1997, 1998, 1999, and 2000. Figure 1 shows an example
of the seasonal predawn leaf water potential measured
in summer 1998 for the Merlot variety. Minimum predawn leaf water potential measured in August (Ymin) was
used as a water stress indicator for each crop. Figure 2
shows the relationship between Ymin and d13C for the
Merlot variety sampled on the three soils and over the
The ANOVA analysis of d13C recorded on the Saint
Emilion vineyard reveals a significant variety effect and
a significant variety 3 year interaction (Table 1). A pairwise comparison with the Bonferroni test showed that
the Merlot variety response was significantly different (P-0.01) from the two other varieties (mean
d13C ¼ 23.63). Cabernet Sauvignon and Cabernet Franc
were not different (mean d13C ¼ 23.25 and 23.29,
respectively). Variability for d13C was examined on a
large set of 31 varieties. Samples were collected in 1999.
All berries were harvested at the same date. Sugar d13C
varied significantly according to the varieties (Table 3).
Fig. 1. Vine leaf predawn water potential during the growing season in
1998. Saint Emilion vineyard, Merlot variety, grown on three soils with
different water reserves (mean of six replicates "SE).
Fig. 2. The relationship between minimum predawn leaf water potential
recorded in August and d13C. Grapevine, Merlot variety, grown on
sandy, clay and gravely soils in 1997, 1998, 1999, and 2000. Each point
represents one soil type and one growing season (R2, significant at 99%
confidence level).
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Gaudillère et al.
Table 2. Mean plot water balance during the growing season
(May–August) and the fast berry growth phase (July–August), and
mean d13C measured on sugars from berries harvested at maturity
in the Saint Emilion vineyard (three varieties, and two soils)
Water balance was calculated according to the equation:
wRainfall0.5 3 (Potential evapotranspiration)x in mm of water). R2 is
correlation between d13C and the calculated water balance from
meteorological data; figure in brackets is probability of no correlation.
Year
1997
1998
1999
2000
R2
d13Cø
Water balance (mm)
May–August
July–August
206
115
42
16
0.74 (42%)
28.5
102
28
28
0.99 (0.3%)
24.1"0.2
22.2"0.5
24.1"0.3
23.2"0.5
Table 3. d13C measured on grape sugar at maturity from
31 grapevine varieties grafted on the same rootstock (Fercal)
and cultivated at Ferrade domain in 1999
The four groups were defined by the K-means clustering method, for
four groups.
Fig. 3. Minimum predawn leaf water potential and d13C relationship.
(A) Year effect, all varieties mixed. (B) Variety effect (Merlot, Cabernet
Sauvignon and Cabernet Franc), all years mixed (R2, significant at 99%
confidence level).
Group
Variety
d13C
(ø)
Mean d13C
(ø)
Standard
deviation
1
Riesling
Petit Verdot
Malbec
Viognier
21.6
21.7
22.2
22.3
21.9
0.33
2
Cabernet franc
Pinot meunier
Grenache noir
Chardonnay
Aramon
Mourverdre
Tannat
Muscadelle
Pinot gris
Merlot
Gamay
22.5
22.6
22.6
22.8
22.9
23.0
23.0
23.0
23.1
23.2
23.2
22.9
0.22
3
Sémillon
Ugni Blanc
Cabernet Sauvignon
Chasselas
Sauvignon blanc
Muscat Ottonel
Sylvaner
Pinot noir
Sirah
Aligoté
Colombard
Guewurtztraminer
Folle blanche
23.3
23.4
23.4
23.4
23.5
23.5
23.6
23.6
23.7
23.7
23.7
23.7
23.8
23.5
0.16
4
Carignan
Chenin
Muscat de Hambourg
24.1
24.5
24.9
24.5
0.4
Table 1. ANOVA analysis of the year, soil and genotype effect on
the d13C of sugars in mature berries from three grapevine varieties
grown on three different soils at Saint Emilion in 1997, 1998,
1999, and 2000
Source
Sum of
squares
Degrees of
freedom
F-ratio
Probability
Year
Soil
Variety
Soil 3 Year
Variety 3 Soil
Year 3 Variety
Error
22.24
37.99
1.04
4.08
0.17
0.95
0.35
3
2
2
6
4
6
12
251.5
644.4
17.7
23.0
1.5
5.3
-0.1%
-0.1%
-0.1%
-0.1%
25.8%
0.6%
A k-means clustering test for four classes which minimized the sums of square within each group was applied to
partition the data set (Systat 10). It showed a significant
varietal effect on d13C in sugars. For the same growing
conditions, Riesling, Petit Verdot, Malbec, and Viognier
had a high similar d13C value. Conversely Carignan,
Chenin and Muscat de Hambourg showed the lowest
d13C value of the variety set. The other varieties were
ranked in two clusters.
Soil nitrogen supply and d13C
Low leaf nitrogen content showed nitrogen starvation in
grassed plots (Table 4) and this was correlated with reduced
pruned wood and yield. However, there was no effect of
grapevine nitrogen nutrition on d13C in berry sugars.
Carbon isotope composition of grapevine
Table 4. Leaf nitrogen content at veraison, dry weight of winter
pruned wood, yield and d13C in berry sugars at harvest (cv. Merlot
grafted on Fercal)
Grapevines were grown in the INRA experimental domain of Chateau
Couhins in 1999 in a long-term soil tillage trial testing soil nitrogen
availability effects and grapevine N nutrition. Soil treatments were,
respectively, tillage, and 25% and 50% of the soil covered by Festuca
grass. Treatment effects on nitrogen in leaves, growth and d13C were
tested by analysis of variance and Bonferroni test. Different letters
indicate means differ with 99% confidence, nine repetitions for each soil
treatment.
Soil management
d13C
Leaf N Pruned wood Grape
(g m2) (g dw plant1) (kg plant1)
Tillage, bare soil
1.81 a
Grass cover, 25% area 1.67 b
Grass cover, 50% area 1.42 c
259 a
181 b
128 c
3.38 a
3.21 a
2.83 c
25.7 a
25.8 a
25.8 a
Discussion
Precision, and ecological use of d13C
This work has shown that carbon isotope composition
can be measured with good precision and allows a comparison of the effect of water stress response on grapevines. Basically d13C is related to the ratio of intercellular
and atmospheric CO2 concentration (CiuCa) and water use
efficiency and it is well documented that water stress
changes water use efficiency and carbon isotopic composition. While low nitrogen nutrition has been shown to
reduce CiuCa in pine and oak leaves and increase the d13C
value (Guehl et al., 1995), in grape no significant nitrogen
effect was observed on d13C, at least in the range of
variation of leaf nitrogen content observed in the trial
(Table 4). Therefore it can be suggested that most of
the d13C change observed in field-grown grapevines was
related to water stress. Grape sugar is mainly composed
of glucose and fructose, produced after sucrose hydrolysis
by invertase during grapevine maturation (Davies and
Robinson, 1996). Sugars are stored from the beginning of
maturation (veraison) to full maturity, reaching at that
time a concentration higher than 1 M l1. This period of
development lasts approximately 45 d from the beginning
of August to the end of September depending on variety
and location. Sugar carbon at harvest is a large carbon
pool without turnover. It can be easily sampled to
measure d13C of primary photosynthetic products during
maturation. Carbon remobilization would interfere by
providing carbon previously stored. Under normal growing conditions, however, remobilization is unlikely as
it has been shown that a significant amount of carbon
is only remobilized to supply berries after major leaf
removal (Candolfi-Vasconcelos and Koblet, 1990).
A significant correlation between d13C measured in
sugars of ripe berries, and plant water status measured by
minimum predawn leaf water potential was demonstrated
for field-grown grapevines. However, occasional predawn
761
leaf water potential is not a reliable measure of the longterm water status of field-grown plants submitted to
uneven rainfall. The integration of the water stress cannot
simply be assessed by computing the mean of several
changing predawn leaf water potentials during a period of
interest because plant stress response is not additive or
linearly related to the environmental stress intensity.
Moreover, it has been shown that predawn leaf water
potential did not reveal moderate water stress as did stem
water potential (Choné et al., 2001). The scatter of data
around the relationship between Ymin and d13C reported
in Figs 2 and 3 can be ascribed to some extent to the
inaccuracy of predawn leaf water potential as a measure
of mean plant water status. Therefore, d13C composition
in berry sugars is proposed as a potent indicator of
grapevine water status during maturation, not only for
ecophysiological research but also for practical application in commercial vineyards to improve training systems.
All the data collected over four seasons in various locations showed a range in sugar d13C from 20ø to 26ø.
This range is large considering the precision of the
measure (error -3% of the measure), and allows very
discriminating comparisons to be made between season
or soil condition effects on grapevine water status.
Differences in water availability for grapevine between
years and soils was clearly and consistently reflected
in sugar d13C measured at harvest. Variation of d13C in
relation to site characteristics has been demonstrated for
annual species (Robinson et al., 2000) and for perennials
(Saurer et al., 1997; Brooks et al., 1997). This measure
can be used to quantify the general ability of vineyards
to supply water and the degree of stress in different
vineyards. Water stress cannot be controlled precisely
in rain-fed vineyards but, according to the level of stress
expected, in order to get well-matured berries grapevine
management can be adapted to fit grapevine water
demand to the local water supply. Canopy leaf area can
be adjusted by the planting density, the height of trellising
and pruning to fit the canopy structure to the soil and the
local mean rainfall.
Genetic variability of carbon isotope composition
Grapevine is an isohydric species (Tardieu and
Simonneau, 1998). In the field, grapevine stomata close
early to control water loss and midday leaf water
potential (Smart and Coombe, 1983). At the leaf level,
the Farquhar theory predicts a high water use efficiency
related to lower net photosynthetic activity (Jones, 1983)
and water stress-tolerant genotypes. According to Schultz,
grapevine varieties with a low water use efficiency have
a lower capacity to control midday leaf potential (Schultz,
1997). Genetic variability of d13C has been reported for
different perennials and annual species (Sun et al., 1996;
Handley et al., 1997). Genetic variability was observed
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Gaudillère et al.
among different grapevine varieties d13C. The range of
variation, from 22 to 24.5, is large and could be used
to study the genetic determinism of d13C in response to
environmental stress.
Muscat de Hambourg, Chenin, Carignan, Riesling,
and a few other varieties showed very different d13C
values, indicating significant variability of the stomatal
control in Vitis vinifera species (Table 3). Drought tolerance of grapevine varieties have been reported previously
(Düring and Scienza, 1980; Schultz, 1997). Riesling and
Grenache are classified as water stress-resistant, while
Syrah is poorly resistant to water stress. This hierarchy is
in accordance with the hypothesis that high d13C values
would be related to water stress tolerance reported
for these varieties (Table 2). The extensive comparison
of three varieties, grown on three soils over four years
showed significant genetic differences and year interaction
in the d13C value (Table 1). Merlot was shown to have
lower d13C value than Cabernet Sauvignon and Cabernet
franc. Surprisingly the genetic effect was significant when
the season was rainy, in 1997 and 1999 (data not shown).
It is concluded that grapevine varieties have different
genetic capacities for response to water limitation, and
this study is the first large survey of stress response
variability. A detailed ranking of grapevine varieties for
stress response will require a multi-year survey to take
account of the interactions. It was tempting to presume
that this behaviour would be related to the geographic
origin of the varieties. However, there was no simple
relationship between the d13C ranking of varieties
studied and the climate of their geographical origin
(Ambrosi et al., 1997).
Conclusion
Berry sugar d13C composition correlated well with
summer grapevine water status. It was less sensitive to
the genotype and not affected by nitrogen nutrition.
This marker integrates conditions during the ripening
phase and allows a precise comparison of mild water
stress conditions. d13C is well suited to characterize the
mean water regime during berry maturation in relation
to the training, the soil and the water supply rate
(rain or irrigation). This indicator will be very useful
to adjust grapevine water demand anduor irrigation to
obtain the sought-after mild water stress for grape
quality. Grapevine genotype appears as a secondary but
significant factor contributing to variations in d13C.
Acknowledgements
Grants from INRA (Agraf ) and the ‘Conseil Régional
d’Aquitaine’ supported this work. We thank A Ourry,
R Dewar, C Molot and workers of the INRA experimental
domains for their excellent assistance.
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