17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023].

See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
306 Vegetative indicators of water stress Australian Journal of Grape and Wine Research 11, 306–315, 2005

Towards a simple indicator of water stress in grapevine

(Vitis vinifera L.) based on the differential sensitivities
of vegetative growth components
ANNE PELLEGRINO1,3,4, ERIC LEBON2,THIERRY SIMONNEAU2 and JACQUES WERY1
1
Centre de Coopération Internationale en Recherche Agronomique, Avenue Agropolis,
34 398 Montpellier Cedex 5, France.
2
Institut National de Recherche Agronomique, 2 place Viala, 34060 Montpellier Cedex 01, France.
3
Current address: CSIRO Division of Plant Industry, Horticulture Unit, Private Mail Bag, Merbein,Vic 3505,Australia).
4
Corresponding author: Dr Anne Pellegrino, facsimile + 61 3 5051 3111, email anne.pellegrino@csiro.au
Abstract
Responses of grapevine vegetative growth components to mild, medium and severe soil water deficits were
used to identify simple and sensitive indicators for early diagnosis of water stress. Soil water deficit was
characterised as the fraction of transpirable soil water (FTSW) remaining in a water-depleted rootzone.
Growth components included the number of emerged leaves on first (Ist) and second (IInd) order lateral
branches, the leaf area and internode length of each phytomer of Ist order lateral branches, and the
frequency of IInd order lateral branching. These components were measured in a greenhouse on Shiraz
(syn. Syrah) grapevines, over a 38-day period of stabilised soil water regimes. Leaf emergence rate, final
leaf area and final internode length of lateral branches I were relatively insensitive to mild and medium
water deficits. They only decreased in response to severe water deficits. The frequency of IInd order lateral
branching showed a similar trend, but was inhibited at severe water deficits. The leaf emergence rate of
lateral branches II was highly sensitive to FTSW, and decreased even in response to mild water deficits.
Because measurement of leaf emergence rate is a time consuming process, further analysis of the data was
undertaken to identify a simpler but similarly effective indicator of cumulative water deficit. Accordingly,
we established that the final length of lateral branches I was sensitive to medium water deficits, while the
final ratio of the number of leaves on lateral branches II to the number of leaves on lateral branches I, was
sensitive to even mild water deficits. Both of these composite indicators (derived variables) were relatively
easy to measure and showed potential as early indicators of water deficits. They were more sensitive to
FTSW than was predawn leaf water potential. Moreover, the final ratio of the number of leaves on lateral
branches II to the number of leaves on lateral branches I was even more sensitive to FTSW than was
stomatal conductance.

Keywords: plant water stress, vegetative indicators, shoot emergence, shoot morphology, stomatal conductance,
predawn leaf water potential, Vitis vinifera L.

Introduction quality (Hardie and Considine 1976, Smart et al. 1990,

Taken to extremes, either excessive water or severe
drought have detrimental influences on vineyard yield
and grape quality. At one extreme, unrestricted water
supply leads to luxuriant vegetative growth at the expense
of reproductive sinks (berries). Indeed, under luxury irri-
gation, canopies can even close, having a negative effect
on flower bud initiation and fruit ripening, as well as
encouraging development of diseases due to increased air
humidity (Gubler et al. 1987, Jackson and Lombard 1993,
Dry and Loveys 1998, Zahavi et al. 2001). At the other
extreme, severe water deficit reduces leaf area, thereby
decreasing intercepted light which in turn combines with
stomatal closure to limit photosynthesis and the produc-
tion of assimilates (Delgado et al. 1995, Pellegrino et al.
2002). Reduced leaf area also results in an excessive fruit
exposure to sunlight with undesirable impacts on wine
Jackson and Lombard 1993).
On balance, moderate water deficits are beneficial for
vineyard productivity because fruit growth is less affected
than vegetative growth (Matthews et al. 1987) and mat-
uration is improved (Smart et al. 1990, Van Leeuwen and
Seguin 1994, Koundouras et al. 1999). There is therefore
a need for sensitive indicators of water deficits during a
cropping season.
Indicators of vine water status based on soil water
measures (soil water potential or soil water content) are
time consuming and have questionable value in those
vineyards with considerable spatial variation in depth and
lateral spread of roots. Furthermore, grapevine roots may
explore localised water confined in cracks or soil pockets
that develop in heterogeneous soils. Under such condi-
tions, it is not possible to infer the quantity of water that

Pellegrino, Lebon, Simonneau & Wery
is, in effect, available for grapevine growth and cropping.
Provided that they respond sensitively to soil water status,
indicators based on plant attributes may represent a use-
ful alternative to direct physical measurements of soil
water availability (Jones 2004). Predawn leaf water poten-
tial (Ψp) is the reference indicator of soil water potential in
many species including grapevine (Lebon et al. 2003).
However, discrepancies between soil water content and Ψp
have been reported, most likely due to soil heterogeneity
(Améglio et al. 1999). Moreover, while plant growth
responds to high soil water availability (Jones 2004), Ψp
may not respond similarly.
Indicators of grapevine water status based on daily
measures of plant-based criteria can also prove inappro-
priate, and especially with near-isohydric grapevine cul-
tivars that are subject to homeostatic regulation of water
status (Schultz 2003, Jones 2004). Stomatal conductance
(gs), which decreases as soil water deficit develops, is piv-
otal in this regulation and is therefore a potential indica-
tor of water stress. In the short term, gs is among the first
physiological processes in expanded leaves to respond to
drought. However, gs is a spot measurement, presents a
huge sampling problem when trying to gauge whole
canopy behaviour, and generally requires specialised
instrumentation. Such issues augur against practical
implementation for irrigation scheduling. Other measure-
ments, such as those inferred from either gs or plant
transpiration – water potential, sap flow, trunk diameter
variations, canopy temperature, or those measurements
based on optical properties such leaf reflectance index or
photochemical indexes such as steady-state chlorophyll
fluorescence, all hold promise as possible indicators of
critical changes in grapevine water status (Choné et al.
2001, Cifre et al. 2005) but have yet to find general prac-
tical application in viticulture.
Compared to such physical and/or physiological
indicators of water deficit (as discussed above), vegetative
growth offers several advantages. During long-term
drought, as stress develops progressively, tissue expan-
sion underlying vegetative growth is the most sensitive
indicator of diminished water status (Hsiao 1973, Moriana
and Fereres 2002) and integrates water deficit effects over
extended periods. Vegetative growth is easy to measure
and is interrelated with crop yield and grape quality.
Regrettably however, vegetative growth and morpholog-
ical development of shoots have only rarely been investi-
gated as a putative indicator of soil water status.
In grapevines, internode extension, leaf expansion
and elongation of tendrils all respond to changes in soil
water potential (Schultz and Matthews 1988, Hardie and
Martin 2000). Close relationships have been obtained
with potted vines of the cultivars Grenache Noir and
Sangiovese between the Fraction of Transpirable Soil
Water (FTSW) remaining within a root zone, and the
growth rate of the main stem and its lateral branches
(Lebon et al. 2001, Bindi et al. 2005). In other species,
relationships between FTSW and vegetative growth were
shown to be stable between growth conditions (both pot
and field), between varieties, and between years (Lecoeur
and Sinclair 1996, Lecoeur and Guilioni 1998 on pea,
17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vegetative indicators of water stress 307
Soltani et al. 2000 on chickpea). Such relationships pro-
vide an analytical framework to identify sensitive vegeta-
tive growth indicators that could be used to achieve a
good balance between grapevine vigour, grape yield and
grape quality.
One major difficulty in characterising vine growth
response to soil water deficit is in accurately quantifying
the soil water status over the period of time in which the
growth response occurs. Characteristics of plant growth
that take several days to settle cannot be related to a
unique soil water availability in natural conditions because
soil water status will have fluctuated (spatially and tem-
porally) over the period in question. Experiments in pots
may overcome these problems, enabling water regimes to
be strictly controlled over long periods of time and accu-
rately quantified – an approach that was applied here
with Shiraz grapevines.
Accordingly, the aims of this study were (i) to establish
quantitative relationships between FTSW and the basic
components of vegetative growth on first and second
order lateral branches, (ii) assess the sensitivities of the dif-
ferent components of vegetative growth, (iii) identify sim-
ple and sensitive vegetative growth-based indicators for
early diagnosis of water stress, and (iv) compare their
sensitivity to that of predawn leaf water potential and
stomatal conductance. A watering device was developed
to produce a range of soil water deficits which were spa-
tially uniform within the pots and which stabilised during
the long period (38 days) necessary for experimentation.
In addition, the main stem of each pot-grown Shiraz
grapevine was topped immediately above node 15 to
mimic field conditions.
Materials and methods
Plant material and growing conditions
The experiment was conducted in a greenhouse at the
INRA-ENSA M. campus in Montpellier (southern France;
43°38’N, 3°53’E) in 2001. Two-year-old plants (Vitis
vinifera L., cultivar Shiraz (syn. Syrah) grafted onto Fercal
rootstock) were grown in soil columns (0.3 m in diame-
ter, 0.7 m high) filled with a mixture of clay, loam and
sand (in volume proportions of 0.17, 0.36 and 0.47 respec-
tively) and covered with a 0.01 m layer of perlite to limit
evaporation. Irrigation treatments (see below) were ran-
domised among the row of pots. Buffer pots were used at
each row extremity. Plants (one per column) were pruned
to two latent buds, and subsequently thinned to one
branch. To mimic field conditions, the main stems were
vertically trained and topped at the fifteenth node when
the ‘19 separated leaves’ stage was reached. Inflorescences
were removed as soon as they appeared to avoid complex
interactions between soil water deficit, reproductive devel-
opment and vegetative growth.
Micrometeorological conditions and calculation of thermal time
Measurements of air temperature, relative humidity and
photosynthetic photon flux density (PPFD) were record-
ed by a weather station located in the middle of the col-
lection of pots. Data were collected every 30 s, and means
were calculated and stored every 1800 s. Daily mean VPD

308 Vegetative indicators of water stress
ranged from 0.5 to 1.3 kPa and daily cumulative PPFD
from 6.5 to 25.7 mol/m2.d. Daily mean temperature from
the beginning (March 01) to the end of the experiment
(July 02) varied between 16.3 and 24.6ºC. Thermal time
was calculated by cumulating the daily differences
between mean temperature and a base temperature of
10°C (Winkler and Williams 1939).
Watering regimes
Pots were initially irrigated with water only, and then
with water plus nutrients to avoid differences of plant
nutritional status between soil water treatments. Four
water regimes with 7 replicates per regime were applied:
well-watered control – C – and three levels of soil water
deficit with increasing intensities – S1 (mild), S2 (medi-
um) and S3 (severe). Irrigation was scheduled to achieve
the target soil water content for each regime and to main-
tain soil water status at those levels during the growing
cycle, while still maintaining uniformity of soil moisture
throughout the soil columns. This was controlled by mea-
surements of soil water potential at 0.15 and 0.55 m depth
and volumetric soil moisture content over 0.6 m depth
(see below). To prevent the development of soil water
gradients, irrigation was supplied by two tricklers (2
L/hour) per column, positioned in two 0.6 m long woven
sleeves filled with sand and inserted into the soil. Irrigation
was activated only during the period of higher water con-
sumption by the plant, which limited the accumulation of
unused free water. Soil water deficit was imposed after the
main stem was topped. In order to achieve a rapid onset
of the soil water deficit, pea (Pisum sativum L.) was sown
in the pots at grapevine budburst. Pea plants were topped
at the soil surface a few days before the soil water deficit
stabilised.
Soil water status
Soil water content was measured each day, using a time
domain reflectometry device (TDR – Trase System I, Soil
moisture Equipment Corp, Santa Barbara, CA, USA). A
0.6 m long stainless steel guide was vertically inserted
into each soil column. In order to obtain the lower limit of
the grapevine’s Total Transpirable Soil Water (TTSW, see
definition below), supplementary measurements were
made after the experiment, when soil water extraction by
the plant was maximal. TDR values were calibrated
against a range of soil water contents, measured on soil
cores sampled at 0.15 and 0.55 m depths. Daily measure-
ments of soil water potential (Ψs) were also performed
with tensiometers installed at 0.15 and 0.55 m depth in
each column.
Calculations of the total transpirable soil water and the fraction
of transpirable soil water
Total Transpirable Soil Water (TTSW) is defined as the
difference, over the soil depth explored by the roots,
between the soil water content at field capacity (SWCfc),
and the minimum soil water content (SWCmin) observed
after complete extraction of water by the grapevine
(Pellegrino et al. 2004). SWCfc and SWCmin were deter-
mined over the whole depth of the soil column since it
17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Australian Journal of Grape and Wine Research 11, 306–315, 2005
was totally explored by the roots. SWCmin was determined,
after a drying period (following the experiment), when
the daily variation of the pot weight was negligible, indi-
cating that transpiration had ceased. The Fraction of
Transpirable Soil Water (FTSW) was calculated through-
out the experiment as the ratio of the Available Soil Water
at any given date (ASW) to TTSW, with ASW defined
as the difference between actual soil water content
and SWCmin over the soil depth explored by the roots
(Pellegrino et al. 2004).
Predawn leaf water potential and stomatal conductance
Leaf water potential was measured with a pressure cham-
ber (Soil Moisture Equipment Corp., Santa Barbara, USA)
before dawn using one leaf per plant, and on four occa-
sions over the cropping season. Stomatal conductance for
water vapour (gs) was measured for each pot on one
mature leaf exposed to saturating sunlight (PAR > 800
µmol quanta/m2.s) with an ADC-LCA 3-type open-
system gas analyser (ADC, Hoddeston, UK). The analyser
was enclosed in a shade chamber to avoid overheating,
and was equipped with a Parkinson leaf cuvette.
Measurements of gs were undertaken weekly or fort-
nightly.
Vegetative growth
Vegetative growth was measured on one first order later-
al branch (branch I) on the main stem of each plant, and
on all the second order lateral branches (branches II) on
this branch I (Figure 1a, b). The selected branch I emerged
from the 15th phytomer of the main stem (i.e. the branch
immediately under the topping zone). This branch exhib-
ited the highest rate of leaf emergence for all the water
deficit treatments (Pellegrino 2003). Grapevine branches
have been described as repeated sequences of three types
of phytomers with specific morphologies and growth
dynamics: P0 with no tendril or inflorescence/ bunch, P1
and P2 carrying a tendril or an inflorescence/ bunch in
alternate position (Jacquinet and Simon 1971, Schultz
and Matthews 1988, Lebon et al. 2004). The influence of
the phytomer type on the vegetative growth components
was tested when appropriate, and significant differences
for specific growth components between phytomer types
were taken into account in the analysis of the data.
The number of unfolded leaves on branches I and II
(LN I, LN II), the lengths of individual leaf lamina (L I) and
internodes (INL I) were measured on branch I two to
three times a week. Individual leaf area on branches I
(LA I) was estimated from the length of the leaf lamina
using the parameter of a regression fitted from an inde-
pendent set of 420 leaves (Eqn 1). LI and LA I were deter-
mined for each leaf by image analysis (Optimas V6.5;
Media Cybernetics, Silver Spring, MD, USA).
LA I = 5.87 × LI2 + 1.18 (r2 = 0.91; CVe = 12%) 1
The final LA I and INL I were determined at the end of
the period with stabilised soil water deficit for fully elon-
gated leaves and internodes respectively.
The rates of leaf emergence were calculated for
branches I (LER I) and II (LER II) as the slope of the lin-

Pellegrino, Lebon, Simonneau & Wery
a b
Main stem
Main stem
Topping 15th node
First order
P2
lateral branch
P0 P1
P2
P1
P0
P0, P1 and P2 : phytomers, P0, P1 or P2
ear regressions between the number of unfolded leaves
and thermal time. Final periods of slowed or stopped
growth were excluded from the analysis. To determine
this period, an average phyllochron was calculated from
observations on actively growing branches (at least one
new leaf emerged between two successive observations).
When the period of time with no newly emerged leaf
exceeded this average phyllochron, growth was consid-
ered to have stopped. Then, the frequency of second order
lateral branching (FB II) was determined.
Since our primary objective was to identify simple
parameters indicative of early water deficits, two com-
posite growth parameters based on ‘easy to measure’ com-
ponents (composite indicators) were defined. The final
length of branches I (BL I) which gives information on
overall vigour of branches I was measured. It combines
the previous components as follows:
BL I = LER I × INL I × GD I
where GD I is the growth duration of branch I.
An indicator of vigour for branches II was also calcu-
lated. To dissociate it from the vigour of branch I, the
final number of leaves on all branches II was divided by
the number of leaves on the bearing branch I. The result
is related to the basic growth processes as follows:
N the reduced heterogeneity over the soil columns and the
LN II ∑ [LER II ×GD II × FB II]
i =1
= throughout that 38-day period. The gradient of soil water
LN I LER I × GD I
Where i indicates the number of the phytomer on branch
I, N is the total number of branching positions on branch
I, and GDIIi is the growth duration of the branch II insert-
ed onto phytomer i.
Statistical analysis
Comparison of means (Student-Newman-Keuls tests,
SNK) was performed with SAS (V8.0, SAS Institute 1999).
Relationships between FTSW and individual or composite
vegetative growth parameters, were fitted with linear or
non linear functions using the conventional least squares
method (GRG2 algorithm, Excel, Microsoft).
17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vegetative indicators of water stress 309
First order
Figure 1. Diagram of the vegetative
lateral branch structure in grapevine: main stem,
nº15 first order lateral branches
(branches I, a) and second order
lateral branches (branches II, b).
The ternary modular structures
(phytomers P0, P1 and P2) of the
main stem and branches I are
represented. The main stem was
Second order topped at the 15th node and
lateral branch individual parameters and
composite indicators of vegetative
growth were determined on branch I
: leaf emerged from the 15th phytomer of
the main stem, and on branches II
: tendril or infloresence / bunch
on this branch I.
Results
Characterisation of the fraction of transpirable soil water
during the period of stabilised soil water deficit
Once the targeted soil water deficits (S1 to S3) were
reached, they were maintained at these stabilised levels for
the period beginning on 15 May, when the available soil
water (ASW), and stomatal conductance (gs) relative to
the control had stabilised, and ending on 22 June, when
gs relative to the control, had increased (Figure 2c). This
latter increase of gs was probably due to the higher
amounts of water supplied each day that were necessary
to match the increase in plant water uptake as leaf area
developed. At this time, transient accumulation of free
water in the soil columns after irrigation was inevitable,
probably causing short oscillations in soil water availabil-
ity that could not be detected. The period after 22 June
was therefore disregarded. ASW calculated over the whole
2 depth of soil columns (0.7 m) averaged, for this period
from 15 May to 22 June, 94.3 mm, 66.7 mm, 44.1 mm
and 21.3 mm respectively for the treatments C, S1, S2 and
S3. Over the same period, average values of FTSW,
defined as the ratio of ASW to the total transpirable soil
water (TTSW), were 0.87, 0.61, 0.40 and 0.19 respective-
ly for C, S1, S2 and S3 (Figure 2a). Daily measurements of
soil water potential at 0.15 and 0.55 m depths confirmed
3 stability of the soil water deficits for each treatment
potential between 0.15 and 0.55 m ranged from 13 to
329 mbars for C and S2 respectively. The gradient of soil
water potential over the 38-day period ranged from 61 (C)
to 551 mbars (S2) at 0.15 m, and from 28 (C) to 473
mbars (S2) at 0.55 m. The individual parameters and
composite indicators of vegetative growth were analysed
during this period.
Predawn leaf water potential is only sensitive to severe soil
water deficit while stomatal conductance is sensitive to mild soil
water deficit
During the period of stabilised soil water deficits, predawn
leaf water potential (Ψp) was slightly decreased for mild
 17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
310 Vegetative indicators of water stress Australian Journal of Grape and Wine Research 11, 306–315, 2005

1.2 es S1 and S2 (Figure 3b, c). Over the whole range of soil
C a
S1 water deficits, a curvilinear relationship could be drawn
Fraction of transpirable

1.0 S2 between LER I and FTSW determined for each individual

S3
0.8 plant (Figure 4a). The fitted curve demonstrated the low
soil water

sensitivity of LER I in the upper range of FTSW (higher

0.6
than 0.4).
0.4 The leaf emergence rate on branches II (LER II) was
much lower than LER I, and varied with the type of the
0.2
bearing phytomer (P0, P1 or P2) on branch I (P < 5%).
Branches II emerged from phytomer 5 and 8 (numbered
Predawn leaf water potential (MPa)

0.0
b
-0.05 from the base of the bearing branch I) were retained
because they were of the same type P0 and they exhibit-
-0.10 ed the highest rates of development. No difference was
-0.15
detected between these two positions that were both
included in the calculations (Figure 3e, f, g). This mini-
-0.20 mised the errors associated with the low values of LER II.
-0.25
Despite this, LER II values remained scattered and only a
*
* loose relationship between leaf emergence rate and FTSW
-0.30 was obtained for branches II compared to branches I
1.2 c
(Figure 4d). LER II averaged 0.016 leaves/°C.d for the
Stomatal conductance
relative to the control

1.0 well watered regime C (one-third of the rate observed

0.8
0.6
0.4
0.2
0.0
01/03 01/04
Figure 2. Characterisation of the watering regimes (well watered
control C, and the water deficit treatments S1, S2 and S3) by the
changes in the fraction of transpirable soil water (a), and the
responses of predawn leaf water potential (Ψp, b) and stomatal
conductance (gs) relative to the control (c). The period of stabilised
soil water deficit is delimited by the dashed lines (see text). Significant
differences of Ψp or gs during this period between the water deficit
treatments (S1 to S3) and the control plants (C) (P < 5%) are
indicated by asterisks. Symbols with bars in the left-hand panel
indicate average 95% confidence intervals over the period of
stabilised soil water deficit.
(S1) and medium (S2) water deficits compared to the
control plants C (to 87% and 85% of C for S1 and S2
respectively) (Figure 2b). However, the differences
between C, S1 and S2 at each date during this period
were not significant (P > 5%). In contrast, Ψp significant-
ly decreased to 56% of C plants at severe water deficit
(S3). For the same period, gs showed a small decrease for
S1 (to 83% of C), while significant (P < 5%) for most of
the dates (Figure 2c). It decreased to 75% and 19% of C
for S2 and S3 respectively. The differences of gs between
C and S2 or S3 were significant at each date, except the
first date for S2.
Leaf emergence rate is more sensitive to soil water deficit for
laterals branches II than for lateral branches I
Leaf emergence rate on branches I (LER I) averaged 0.05
leaves/°C d (base 10°C) for control plants C (Figure 3a). In
comparison to C, the most severe stress S3 significantly
reduced LER I down to 0.018 leaves/°C.d (P < 5%, Figure
3d). LER I was only slightly altered by intermediate stress-
on branches I for the same water regime). All the water
* * **
*
*
* *
deficits reduced LER II in comparison with C, although the
* reduction was similar for S1 and S2 (0.012 and 0.010
leaves/°C.d, respectively). The most severe water deficit S3
completely stopped the growth of branches II (Figures
*
* ** * 3h, 4d). The leaf emergence rate was more sensitive to
water stress for branches II than for branches I even for
01/05 01/06 01/07
mild water deficit. Relative to the control, LER II for each
Date
water deficit treatment decreased to 71% (S1), 60% (S2)
and 0% (S3) while the corresponding values for LER I
decreased to 96%, 93% and 34% of control plants
(Figures 4a, d).
Final leaf area and internode length of lateral branches I have
similar responses to soil water deficit
The final individual leaf area on branches I (LA I) was
determined, excluding the first leaves with lower areas.
This comprised leaves 5 to 10 for C, S1 and S2, and only
leaf 5 for S3 because of the slower development for this
regime (Figure 5 a). LA I of C, S1 and S2 plants did not
depend on the type of phytomer (P0, P1 or P2) (P > 5%),
and was uniform from phytomer 5 to 10 on branches I
(two phytomer sequences). Mean leaf area was not
significantly reduced for plants submitted to water deficits
S1 and S2 (Figure 4b). In an unexpected way, LA I was
slightly but significantly higher for S1 than control plants
(110% of the control, P < 5%, Figure 4b). LA I was
significantly reduced for S3 plants (P < 5%).
The first internodes were excluded for the determina-
tion of the final internode length on branches I (INL I)
because of their limited elongation. This comprised intern-
odes 8 to 16 for treatments C, S1 and S2, and internodes
8 to 10 for S3 (Figure 5b). INL I depended on the type of
phytomer, internodes on phytomers P2 being longer than
on P0 and P1 (P < 5%). This effect could not be detected
at the more severe water deficit S3 where internode
length was smaller. Only S3 significantly reduced intern-
ode lengths whatever the phytomer type (P < 5%) (Figure
4c).
 17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Pellegrino, Lebon, Simonneau & Wery Vegetative indicators of water stress 311

25 25
C a C n°1 e
C n°2 C
20 20 C n°3
C n°4
C n°5
15 15 C n°6
C n°7
10 10 ajust. C

Number of unfolded leaves on branches II

5 5
Number of unfolded leaves on branches I

0 0
S1 b S1 n°1 S1 f
20 20 S1 n°2
S1 n°3
S1 n°4
15 15 S1 n°5
S1 n°6
10 10 ajust. C
ajust. S1
5 5

0 0
S2 c S2 n°1 S2 g
20 20 S2 n°2
S2 n°3
S2 n°4
15 15 S2 n°5
S2 n°6
10 10 ajust. C
ajust. S2
5 5

0 0
S3 d S3 n°1 S3 h
20 20 S3 n°2
S3 n°3
15 15 S3 n°4
S3 n°5
S3 n°6
10 10 ajust. C
ajust. S3
5 5

0 0
500 600 700 800 900 1000 1100 0 100 200 300 400
Thermal time from budburst (°C d) Thermal time from IInd branch emission (°C d)

Figure 3. Number of unfolded leaves on lateral branches I (15th phytomer) (a to d) or II (5th and 8th phytomer) (e to h) as a function of thermal
time for the control plants (C) or the water deficit treatments (S1 to S3). The 5th and 8th phytomers for the branches II are not distinguished.
Each value corresponds to one plant. The fitted lines for the water deficit treatment (thin line) are represented with the adjustment obtained
for control plants (thick line).

Frequency of IInd lateral branching is relatively insensitive to of lateral branches I (BL I), was reduced by water deficit
soil water deficit except for severe deficit for all the water regimes, although the differences were
For all the water regimes, 4 to 5 apical phytomers on the only significant for medium and severe water deficits (S2
apical zone of branches I were not branched. The fre- and S3 respectively, P < 5%) (Figure 6 a). It decreased to
quency of IInd lateral branching (FB II) was therefore 89% (S1), 74% (S2) and 7% (S3), of C plants, while Ψp
calculated excluding the top 5 phytomers for all the treat- only decreased to 87% (S1), 85% (S2) and 56% (S3) of C
ments (Figure 4e). The remaining phytomers on branch I plants (Figure 2b).
all developed branches II for control plants (FB II close to The intensity of secondary branching on lateral
100%). Intermediate soil water deficits S1 and S2 did not branches I, indicated by the final ratio of the number of
significantly alter this branching frequency (P > 5%). leaves on lateral branches II to the number of leaves on
Only the most severe deficit S3 eventually inhibited the lateral branches I (LN II/LN I) was significantly reduced for
development of branches II (FB II down to zero) (P < 5%). the range of water deficits (S1 to S3, P < 5%). It decreased
to 75% and 62% of C plants for S1 and S2 respectively
Composite indicators of Ist lateral branches growth and of and was reduced to zero for S3. LN II/LN I was therefore
branching intensity on branches I are sensitive to medium and more sensitive to water deficit than BL I, and even more
mild soil water deficits, respectively than gs which decreased to 83%, 75% and 19% of C for
The Ist lateral branch growth, indicated by the final length S1, S2 and S3, respectively (Figures 6b, 2c)
 17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
312 Vegetative indicators of water stress Australian Journal of Grape and Wine Research 11, 306–315, 2005

120 120
a d

branches I (% of control)

branches II (% of control)
Leaf emergence rate on

Leaf emergence rate on

100 100

C C
80 S1 80
S2
60 60 S1*
40 40 S2*

20 S3* 20
S3*
0 0

Frequency of lateral branching

120 b 120 e
branches I (% of control)

100 100
Final leaf area on

S1*

(% of control)
C C S1
80 S2 80 S2

60 60

40 40
S3*
20 20
S3*
0 0
120 c
branches I (% of control)
Final internode length on

1.0 0.8 0.6 0.4 0.2 0.0

100 Fraction of transpirable soil water
C
80 S1
S2
60

40

20 S3*

0
1.0 0.8 0.6 0.4 0.2 0.0
Fraction of transpirable soil water

Figure 4. Vegetative growth individual parameters, as a percentage of control plants, of branches I (15th phytomer: leaf emergence rate, LER I;
final leaf area, LA I and final internode length, INL I) (a to c), or branches II (5th and 8th P0 type phytomer for leaf emergence rate, LER II; all
the phytomers for frequency of lateral branching, FB II) (d and e) plotted as a function of the average value of the fraction of transpirable soil
water during the period of stabilised soil water deficit (Figure 2a, c).
LER I (% of control) = 101.2 – 246.2 × exp(–7.1 × FTSW) (r 2 = 0.81; CVe = 15%)
LA I (% of control) = –22.7 + 394.0 × FTSW – 289.4 × FTSW2 (r 2 = 0.85; CVe = 11%)
INL I (% of control) = 98.1 – 221.6 × exp(–7.3×FTSW) (r 2 = 0.83; CVe = 9%)
LER II (% of control = 108.7 + 63.8 × ln(FTSW) (r 2 = 0.83; CVe = 27%)
FB II (% of control) = 103.2 – 480.1 × exp(–8.1 × FTSW) (r 2 = 0.92; CVe = 16%)
Final leaf area on branches I (cm2)

350
a 160 b
300
Final internode length
on branches I (mm)

250
120
200
150 80
C
100
40 S1
50 S2
0 1 2 0 1 2 S3
0 0
5 6 7 8 9 10 5 6 7 8 9 10 11 12 13 14 15 16
Leaf position on branches I Leaf position on branches I

Figure 5. Final leaf area (LA I, a) and internode length (INL I, b) of each phytomer of branches I (15th phytomer) for the control plants (C) or
the water deficit treatments (S1 to S3). LA I and INL I are represented for the phytomers 5 to 10 and 5 to 16 respectively. Leaves and internodes
are fully expanded for these phytomers. The type of phytomer (P0, P1 and P2) is represented for the first sequence in each figure. The phytomers
with constant values of INL I per type of phytomer are delimited by the dashed-line. Bars indicate 95% confidence intervals.

Comparison of the sensitivities to soil water deficit of the trend to soil water deficit (Figure 7). They were all rela-
individual parameters and composite indicators of vegetative tively insensitive to mild and medium soil water deficits
growth (S1 and S2 respectively, FTSW > 0.4), but were reduced
The leaf emergence rate on lateral branches I (LER I), for severe water deficits (S3, FTSW = 0.19). In contrast
their final individual leaf area (LA I) and internode length with LA I, LER I and INL I did not increase for mild water
(INL I) all plotted as a function of FTSW showed a similar deficits (FTSW = 0.61). The frequency of IInd lateral
 17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Pellegrino, Lebon, Simonneau & Wery Vegetative indicators of water stress 313

120 a 120

on branches II to the number of leaves

b

Final ratio of the number of leaves

Final length of branches I
100 100

on branches I (% of control)
C
(% of control)

80 80 C
S1
60 60 S1*
S2*
40 40 S2*

20 20
S3* S3*
0 0
1.0 0.8 0.6 0.4 0.2 0.0 1.0 0.8 0.6 0.4 0.2 0.0
Fraction of transpirable soil water Fraction of transpirable soil water

Figure 6. Vegetative growth composite indicators, in percentage of control plants, of branches I (15th phytomer: final length of branches, BL
I) (a), or branches II (all the phytomers: final ratio of the number of leaves on branches II to the number of leaves on branches I, LN II/LN I)
(b) plotted as a function of the average value of the fraction of transpirable soil water during the period of stabilised soil water deficit (Figure
2 a, c). Significant differences of the vegetative growth composite indicators between the water deficit treatments (S1 to S3) and the control
plants (C) (P < 5%) are indicated by asterisks. Bars indicate 95% confidence intervals.
BL I(% of control) = 135.4 – 30.0/FTSW + 1.15/FTSW2 (r 2 = 0.88; CVe = 19%)
LN II/LN I(% of control) = 110.7 + 64.2 × ln(FTSW) (r 2 = 0.87; CVe = 24%)

branching (FB II) was also only sensitive to severe deficits, Discussion
at which it was inhibited (Figure 7). Overall, the leaf Consistent with the results of Belaygue et al. (1996) on
emergence rate on lateral branch II (LER II) was the most white clover, Lecoeur and Guilioni (1998) on pea and Lebon
sensitive individual parameter to water stress (Figure 7). et al. (2001) and Bindi et al. (2005) on grapevine, present
It was reduced for mild and medium water stress. data for individual parameters of vegetative growth were
The composite indicators of Ist lateral branch growth closely linked to soil water deficit, as characterised by
(BL I) and of branching intensity on branches I (LN II/LN FTSW (r 2 > 0.81). Existing knowledge on the production
I) showed a severe sensitivity to water stress compared of root signals (including abscisic acid and cytokinins) in
with all the individual parameters of vegetative growth response to soil drying and their effect on leaf emergence,
(Figure 7). The sensitivity to water deficit of BL I was leaf expansion and lateral branching (Dry and Loveys
higher than the sensitivities of all the individual parame- 1998, Stoll et al. 2000) provides a sound physiological
ters measured on lateral branches I and of FB II, but lower basis for this type of empirical relationship between soil
than the sensitivity of LER II, providing an intermediate water deficit in the root zone and shoot behaviour.
shape of vegetative growth response to water deficit. Individual parameters for shoot growth and morphol-
LN II/LN I was more sensitive to soil water deficit than the ogy showed contrasted sensitivities to water stress,
growth of the lower order branch (indicated by BL I). Its increasing with the branch order (I, II). These sensitivities
sensitivity was similar to that of LER II. were used to identify two composite indicators (BL I,
LN II/LN I) based on simple measurements (branch length
and leaf number). They showed a higher sensitivity to
water deficits than Ψp or even than gs for LN II/LN I.
Individual parameters or composite

120
Strong correlations were observed between these com-
indicators (% of control

100
80
60
40
20
0
1.0
Figure 7. Differential sensitivities of the individual parameters and
composite indicators of vegetative growth to the fraction of
transpirable soil water (FTSW). Parameters of the regression are
detailed in Figure 4 (branches I: leaf emergence rate, LER I; final leaf
area, LA I and final internode length, INL I – branches II: leaf
emergence rate, LER II and frequency of lateral branching, FB II), and
in Figure 6 (branches I: final length of branches, BL I – branches II:
final ratio of the number of leaves on branches II to the number of
leaves on branches I, LN II/LN I).
posites indicators and FTSW (r2 > 0.88). They can there-
fore be used to diagnose mild to medium water deficits
which may impact on canopy development and optimi-
sation of the balance between yield and grape quality.
LER I
LER II
LA I The sensitivities of the individual vegetative growth parameters
INL I
FB II to water deficit mainly depend on the branches order (I, II)
BL I The parameters LER I, LA I, INL I and FB II showed a low
LN II/LN I
0.8 0.6 0.4 0.2 0.0 sensitivity for a large range of water deficits (FTSW >
Fraction of transpirable soil water 0.4), and were only reduced for severe water deficits
(FTSW = 0.19) (Figure 7). The low sensitivity of the leaf
emergence process to water stress was also observed by
Lebon et al. (2001) on the non-topped main stem of
Grenache Noir, by Belaygue et al. (1996) on white clover
and by Lecoeur and Guilioni (1998) on pea. LER I, LA I
and INL I all exhibited similar decrease to water deficit in
grapevine. Other species showed in contrast higher sen-
sitivity of phytomer expansion compared to phytomer
production (Randall and Sinclair 1988, Belaygue et al.

314 Vegetative indicators of water stress
1996, Lecoeur and Guilioni 1998). Leaf expansion (the
underlying process of LA I) surprisingly improved for mild
water deficit (FTSW of 0.61, Figure 7). This increase was
consistent with the results of Jun (1994) on rice. This
was potentially linked to the higher level of assimilates
available for leaves under mild stress, which was in term
linked with the reduction of the vegetative sinks repre-
sented by lateral branches (decrease of LER II, see below)
while photosynthesis (and thereby the carbon source)
was maintained to its maximum value for this range of
water deficit (Pellegrino 2003). The inhibition of FB II by
water deficit was consistent with the observations on
other species (Steinberg et al. 1990 on peach tree,
Belaygue et al. 1996).
The development of branches II (LER II) was more
affected by soil water deficit than the development of the
stems bearing these branches (LER I) (Figure 7). The
almost linear reduction of LER II with FTSW is quite
unique among all the relationships of this type published
to date, suggesting that the production of phytomers on
branches II is the most sensitive process in plant response
to drought. Lebon et al. (2001), similarly, observed that
the leaf emergence rate of branches I was the most sensi-
tive parameter for non-topped main stems of grapevine.
The composite indicators of vegetative growth can be used to
diagnose mild to medium water deficits
As expected (Eqn 2), the final length of branches I (com-
posite indicator BL I), showed a higher sensitivity to soil
water deficit in comparison with its underlying processes
of node production (LER I) and internode elongation (INL
I) (Figure 7). The final ratio of the number of leaves on
branches II to the number of leaves on branches I (com-
posite indicator LN II/LN I), showed a higher sensitivity to
soil water deficit than BL I. Its sensitivity was similar to
that of LER II for a large range of soil water deficit as LER
I and FB II were only slightly reduced (Eqn 3).
LN II/LN I and BL I are therefore sufficiently sensitive
to soil water deficits to be used as indicators of respectively
mild (FTSW = 0.61) and medium water deficits
(FTSW = 0.40). They are more sensitive to water stress
than Ψp (Figure 2 b), which is widely used as an indicator
of plant water stress in grapevine. The sensitivity of
LN II/LN I to water stress is even higher than that of gs
(Figure 2c). The low sensitivity of Ψp or gs observed
respectively for medium and mild water deficits is consis-
tent with the results of Lebon et al. (2003) and Pellegrino
et al. (2004) in vineyard conditions. Compared to Ψp or gs,
LN II/LN I and BL I offer the advantage of being integra-
tive indicators of water stress and require therefore a
lower number of measurements to characterise the water
deficit experienced by a grapevine over the cropping season.
Extrapolation to field conditions
Present relationships between FTSW and either individual
parameters or composite indicators of vegetative growth
should remain stable in vineyards, because such relation-
ships did not change between different pedoclimatic con-
ditions, nor between varieties of other species (Lecoeur
and Sinclair 1996, Lecoeur and Guilioni 1998, Soltani et
17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Australian Journal of Grape and Wine Research 11, 306–315, 2005
al. 2000). However, the parameters of some relationships
could be affected by different factors including cultivar and
rootstock, crop load and mineral status. Competition for
assimilates between the vegetative and reproductive sinks
decreased vegetative growth to similar levels as experi-
enced for water stress (Hardie and Martin 2000). Nitrogen
deficiency also reduced grapevine vigour (Gaudillère et al.
2002). However, Tréogat et al. (2002) showed that vege-
tative growth was generally more reduced by water stress
than by nitrogen deficiency for grapevines growing under
standard rain-fed conditions, which serves to emphasise
the over-riding importance of water as a driving variable.
In this same connection, the diagnosis of water deficit
in the field could be completed by simple observations or
measurements (using a N-tester) of leaf colour to assess
vine nitrogen status. Non-stabilised soil water status could
also affect the stability of LA I, INL I or BL I (which
depends on INL I) vs FTSW because the final leaf area and
internode length depend on the timing of water stress in
relation to the development period for each phytomer
(Lecoeur et al. 1995 on pea, Belaygue et al. 1996 on white
clover, Randall and Sinclair 1988 on soybean). Even if
relationships between individual parameters and com-
posite indicators with FTSW may change, the classification
based on the relative sensitivity to water stress between
these individual parameters and composite indicators is
likely to be consistent.
In conclusion, contrasts between vegetative growth
components of Shiraz grapevines in their respective sen-
sitivities to soil water deficits (based on FTSW) have been
identified and quantified. In particular, the parameter of
vegetative development of lateral branches II (LER II)
was sensitive to mild soil water deficit whereas the
parameters of vegetative development and growth of the
phytomers on lateral branches I, LER I, LA I and INL I, or
of the frequency of branching, FB II, were relatively insen-
sitive to FTSW, except for severe water deficit. Two com-
plementary composite indicators were identified from this
analysis. The first was an indicator of growth of branches
I (BL I) and the second was an indicator of branching
intensity on branches I (LN II/LN I). These ‘easy to mea-
sure’ composite indicators were more sensitive to FTSW
than all the individual parameters measured on branches
I and than FB II. They were also more sensitive to FTSW
than Ψp, or even than gs for LN II/LN I which showed a
similar trend as LER II. They can be used to diagnose mild
water deficits (using LN II/LN I) as well as the medium
water deficits (using BL I) required to constrain vegetative
vigour, and thus improve the balance between vineyard
yield and grape quality.
Acknowledgements
Anne Pellegrino received funding from the French
Ministry of Agriculture and the Languedoc-Roussillon
region. We thank Yvan Bouisson, Philippe Naudin, Carla
Machado and Adriano Zago for their technical assistance.
Grateful acknowledgment is also made to my colleagues at
CSIRO Plant Industry (Horticulture Unit) Merbein, and
especially to Dr Rob Walker, for their helpful input during
the final stages of manuscript preparation.

Pellegrino, Lebon, Simonneau & Wery
References
Améglio, T., Archer, P., Cohen, M., Valancogne, C., Daudet F.A.,
Dayau, S. and Cruiziat P. (1999) Significance and limits in the use of
predawn leaf water potential for tree irrigation. Plant and Soil 207,
155–167.
Belaygue, C., Wery, J., Cowan, A.A. and Tardieu, F. (1996)
Contribution of leaf expansion rate, of leaf appearance, and stolon
branching to growth of plant leaf area under water deficit in white
clover. Crop Science 36, 1240–1246.
Bindi, M., Bellesi, S., Orlandini, S., Fibbi, L., Moriondo, M. and
Sinclair T. (2005) Influence of water deficit stress on leaf area devel-
opment and transpiration of Sangiovese grapevines grown in pots.
American Journal of Enology and Viticulture 56, 68–72.
Choné, X., Van Leeuwen, C., Dubourdieu, D. and Gaudillère, J.P.
(2001) Stem water potential is a sensitive indicator of grapevine
water status. Annals of Botany 87, 477–483.
Cifre, J., Bota, J..M., Escalona, J.M., Medrano, H. and Flexas, J.
(2005) Physiological tools for irrigation scheduling in grapevine
(Vitis vinifera L.). An open gate to improve water-use efficiency?
Agriculture, Ecosystems and Environment 106, 159–170.
Delgado, E., Vadell, J., Aguilo, F., Escalona, J.M. and Medrano, H.
(1995). Irrigation and grapevine photosynthesis. In: Photosynthesis:
From Light to Biosphere. Vol. IV. Ed. P. Mathis, pp. 693–696.
Dry, P.R. and Loveys, B.R. (1998) Factors influencing grapevine vigour
and the potential for control with partial rootzone drying. Australian
Journal of Grape and Wine Research 4, 140–148.
Gaudillère, J.P., Van Leeuwen, C. and Ollat, N. (2002) Carbon isotope
composition of sugars in grapevine, an integrated indicator of vine-
yard water status. Journal of Experimental Botany 53, 757–763.
Gubler, W.D., Marois, J.J., Bledsoe, A.M. and Bettiga, L.J. (1987)
Control of Botrytis bunch rot of grape with canopy management.
Plant Disease 71, 599–601.
Hardie, W.J. and Considine, J.A. (1976) Response of grapes to water-
deficit stress in particular stages of development. American Journal
of Enology and Viticulture 27, 55–61.
Hardie, W.J. and Martin, S.R. (2000) Shoot growth on de-fruited
grapevines: A physiological indicator for irrigation scheduling.
Australian Journal of Grape and Wine Research 6, 52–58.
Hsiao, T. (1973) Plant responses to water stress. Annual Review of
Plant Physiology 24, 519–570.
Jackson, D.I. and Lombard, P.B. (1993) Environmental and manage-
ment practices affecting grape composition and wine quality. A
review. American Journal of Enology and Viticulture 44, 409–430.
Jaquinet, A. and Simon, J.L. (1971) Contribution à l’étude de la
croissance des rameaux de vigne. Revue Suisse de Viticulture,
d’Arboriculture et d’Horticulture 3, 131–135.
Jones, H.G. (2004) Irrigation scheduling: advantages and pitfalls of
plant-based methods. Journal of Experimental Botany 55,
2427–2436.
Jun, L. (1994) Effects on growth and yield of rice by control of tiller-
ing through induced mild drought stress. In: The development, test-
ing and application of crop models simulating the potential of pro-
duction of rice. SARP Research Proceedings DLO-WAU-IRRI of the
International Workshop on the Simulation of Potential Production
in Rice. Kumbakonam, Tamil Nudu, Inde. pp. 57–61.
Koundouras, S., Van Leeuwen, C., Seguin, G. and Glories, Y. (1999)
Influence de l’alimentation en eau sur la croissance de la vigne, la
maturation des raisins et les caractéristiques des vins en zone
méditerranéenne (exemple de Némée, Grèce, cépage Saint-Georges,
1997). Journal International des Sciences de la Vigne et du Vin 33,
149–160.
Lebon, E., Pellegrino, A., Lecoeur, J. and Tardieu, F. (2001) Shoot
architectural responses induced by controlled soil water deficit in
vine (Vitis vinifera L. cv. Grenache noir). Proceedings 12th GESCO
Conference, AGRO Montpellier, France. 1, pp. 229–244.
Lebon, E., Dumas, V., Pieri, P. and Schultz, H.R. (2003) Modelling the
seasonal dynamics of the soil water balance of vineyards. Functional
Plant Biology 30, 699–710.
Lebon, E., Pellegrino, A., Tardieu, F. and Lecoeur, J. (2004) Shoot
development in Grapevine (Vitis vinifera L.) is affected by the mod-
ular branching pattern of the stem and intra- and inter- shoot troph-
ic competition. Annals of Botany 93, 263–274.
17550238, 2005, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1755-0238.2005.tb00030.x by Montpellier SupAgro, Wiley Online Library on [21/03/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Vegetative indicators of water stress 315
Lecoeur, J., Wery, J., Turc, O. and Tardieu, F. (1995) Expansion of pea
leaves subjected to short water deficit: Cell number and cell size are
sensitive to stress at different periods of leaf development. Journal
of Experimental Botany 46, 1093–1101.
Lecoeur, J. and Sinclair, T.R. (1996) Field pea transpiration and leaf
growth in response to soil water deficits. Crop Science 36, 331–335.
Lecoeur, J. and Guilioni, L. (1998) Rate of leaf production in response
to soil water deficits in field pea. Field Crops Research 57, 319–328.
Matthews, M.A., Anderson, M.M. and Schultz, H.R. (1987)
Phenologic and growth responses to early and late season water
deficits in Cabernet franc. Vitis 26, 147–160.
Moriana, A. and Fereres, E. (2002) Plant indicators for scheduling irri-
gation of young olive trees. Irrigation Science 21, 83–90.
Pellegrino, A., Wery, J. and Lebon, E. (2002) A water balance model
can be used to evaluate the water stress experienced by a crop in
farmer’s fields: A case study in vineyards in south-eastern France.
Proceedings 7th ESA Conference, Cordoue, Spain. pp. 313–314.
Pellegrino, A. (2003) Elaboration d’un outil de diagnostic du stress
hydrique utilisable sur la vigne en parcelle agricole par couplage d’un
modèle de bilan hydrique et d’indicateurs de fonctionnement de la
plante. PhD Thesis, Ecole Nationale Supérieure Agronomique,
Montpellier, France.
Pellegrino, A., Lebon, E., Voltz, M. and Wery, J. (2004) Relationships
between plant and soil water status in vine (Vitis vinifera L.). Plant
and Soil 266, 129–142.
Randall, H.C. and Sinclair, T.R. (1988) Sensitivity of soybean leaf
development to water deficits. Plant, Cell and Environment 11,
835–839.
Schultz, H.R. and Matthews, M.A. (1988) Vegetative growth distrib-
ution during water deficits in Vitis vinifera L. Australian Journal of
Plant Physiology 15, 641–656.
Schultz, H.R. (2003) Differences in hydraulic architecture account for
near-isohydric and anisohydric behaviour of two field-grown Vitis
vinifera L. cultivars during drought. Plant, Cell and Environment 26,
1393–1405.
Smart, R.E., Dick, J.K., Gravett, I.M. and Fisher, B.M. (1990) Canopy
management to improve grape yield and wine quality – Principles
and practices. South African Journal for Enology and Viticulture 11,
3–17.
Soltani, A,. Khooie, F.R., Ghassemi-Golezani, K. and Moghaddam, M.
(2000) Thresholds for chickpea leaf expansion and transpiration
response to soil water deficit. Field Crop Research 68, 205–210.
Steinberg, S.L., Miller, J.C. and McFarland, M.J. (1990) Dry matter
partitioning and vegetative growth of young peach trees under
water stress. Australian Journal of Plant Physiology 17, 23–36.
Stoll, M., Loveys, B. and Dry, P. (2000) Hormonal changes induced by
partial rootzone drying of irrigated grapevine. Journal of
Experimental Botany 51, 1627–1634.
Tregoat, O., Van Leeuwen, C., Choné, X. and Gaudillère, J.P. (2002)
The assessment of vine water and nitrogen uptake by means of
physiological indicators. Influence on vine development and berry
potential (Vitis vinifera L. cv. Merlot, 200, Bordeaux). Journal
International des Sciences de la Vigne et du Vin 36, 133–142.
Van Leeuwen, C. and Seguin, G. 1994. Incidences de l’alimentation en
eau de la vigne, appréciée par l’état hydrique du feuillage, sur le
développement de l’appareil végétatif et la maturation du raisin
(Vitis vinifera variété Cabernet Franc, Saint-Emilion 1990). Journal
International des Sciences de la Vigne et du Vin 28, 81–110.
Winkler, A.J. and Williams, W.O. (1939) The heat required to bring
Tokay grapes to maturity. Proceedings of the American Society of
Horticultural Science 37, pp. 650–652.
Zahavi, T., Reuveni, M., Scheglov, D. and Lavee, S. (2001) Effect of
grapevine training systems on development of powdery mildew.
European Journal of Plant Pathology 107, 495–501.
Manuscript received: 3 June 2005
Revised manuscript received: 29 July 2005