Scientia Horticulturae 178 (2014) 145–153

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Responses of Mediterranean ornamental shrubs to drought

stress and recovery
Stefania Toscano, Domenica Scuderi ∗ , Francesco Giuffrida, Daniela Romano
Department of Agricultural and Food Science (DISPA), University of Catania, Via Valdisavoia 5, 95123 Catania, Italy

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to evaluate the differences in the mechanisms that are involved in the resis-
Received 29 May 2014 tance of ornamental species to drought stress resulting from a regular suspension and recovery of the
Received in revised form 5 August 2014 water supply. Plants of five ornamental shrubs [Callistemon citrinus (Curtis) Skeels (Callistemon), Lau-
Accepted 14 August 2014
rus nobilis L. (Laurus), Pittosporum tobira (Thunb.) W.T. Aiton (Pittosporum), Thunbergia erecta (Benth.)
Available online 22 September 2014
Anderson (Thunbergia) and Viburnum tinus L. ‘Lucidum’ (Viburnum)] were subjected to two consecutive
cycles of suspension/rewatering (S-R) and compared with plants that were watered daily (C). The relative
Keywords:
water content (RWC), leaf water potential ( ), net photosynthetic rate (A), transpiration rate (E) and sto-
Water stress
Biomass
matal conductance (Gs) parameters were monitored during the experiment. The five species that were
Gas exchange investigated exhibited different responses to drought stress. At the end of the experimental period, S-R
Photosynthesis treatment had no effect on dry weight in all species, except Pittosporum. In Pittosporum, drought stress
Water relations reduced total plant biomass by 19%. Drought stress induced alterations in shrubs, including decreases in
the shoot dry matter and increases in the root to shoot ratio, strongly affecting Callistemon and Pittospo-
rum. All species adapted to water shortages using physiological mechanisms (RWC and water potential
adjustment, stomatal closure and reductions in photosynthesis). Following rewatering, the species fully
recovered and thus can be considered appropriate for green spaces in the Mediterranean environment.
However, Laurus and Thunbergia seem to be less sensitive to drought stress than the other species.
© 2014 Elsevier B.V. All rights reserved.

1. Introduction knowledge is useful for the establishment of tools to improve sus-

tainable green areas. The high number of ornamental plants that are
Water deficits are considered the main limiting factor for plant used in Mediterranean areas (Romano, 2004) allows for the isola-
growth in the Mediterranean region during the summer because of tion of suitable genotypes that are able to cope with environmental
the high levels of solar radiation and high temperatures (Di Castri, stresses. All this has led to increased interest in the study of orna-
1981). However, the global climate changes that this region has mental plant responses to water deficits in urban and suburban
experienced during the last several decades have led to signifi- landscape environments.
cantly increased water shortages throughout the year (IPCC, 2007; Plant responses to drought are multiple and interconnected
Wang et al., 2007). Thus, the issues that are linked to water short- (Efeoğlu et al., 2009) and their capacities to adapt to this stress may
age are of interest to landscape management, and the area of green vary considerably within genera and species (Sánchez-Blanco et al.,
sustainability is becoming increasingly relevant. The possibility 2002; Torrecillas et al., 2003). Mediterranean species have devel-
of isolating specific plants that are resistant to particular abiotic oped physiological and morphological adaptations to water stress
stresses is currently being studied (Franco et al., 2006) because this (Dickson and Tomlinson, 1996), including the regulation of gas
exchange (Moriana et al., 2002), osmotic adjustment (Chartzoulakis
et al., 1999), the development of leaf protective structures (i.e.,
hairs, thick cuticles and schlerenchymatic cells), leaf modifica-
Abbreviations: A, net photosynthetic rate; ANOVA, analysis of variance; DW, tions (i.e., inclination variations, increased thicknesses and reduced
dry weight; E, transpiration rate; Gs , stomatal conductance; RWC, relative water surface areas) (Castro-Díez et al., 1998; Gratani and Bombelli,
content; S-R, cycle suspension/rewatering; SLA, specific leaf area; R/S, root/shoot
2000; Karabourniotis, 1998) and more extensive root systems
ratio.
∗ Corresponding author at: Via Valdisavoia 5, 95123 Catania, Italy. (Malinowski and Belesky, 2000). Numerous morphological adap-
Tel.: +39 95 234322. tations to water stress involve the aerial portions of plants. Leaf
E-mail addresses: domenica.scuderi@gmail.com, dscuderi@unict.it (D. Scuderi). growth is the most sensitive plant process to water deficits

http://dx.doi.org/10.1016/j.scienta.2014.08.014
0304-4238/© 2014 Elsevier B.V. All rights reserved.
146 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153

(Bradford and Hsiao, 1982; Hsiao, 1973; Jones, 1985). The verti-
cal orientations of the leaves allow the plants to reduce the radiant
energy that is intercepted (Pereira and Chaves, 1993). The specific
leaf area, which is often used as an indirect indicator of leaf thick-
ness, is reported to be reduced under drought conditions (Liu and
Stützel, 2004; Marcelis et al., 1998). The reduction of the specific Fig. 1. Timeline for suspension/rewatering (S-R) treatments used in experiment.
leaf area is assumed to be a way to improve water use efficiency Plants were irrigated daily to container capacity or subjected to suspension/
rewatering treatment [Start trial (T0), 7 days no water (S1), 7 days daily irrigation
(WUE) (Craufurd et al., 1999; Wright et al., 1994) because thicker (R1), 7 days no water (S2), 14 days daily irrigation (R2)].
leaves usually have higher densities of chlorophyll and proteins
per unit leaf area and thus have greater photosynthetic capacities
per unit leaf area than thinner leaves (Liu and Stützel, 2004). The W.T. Aiton (Pittosporum), Thunbergia erecta (Benth.) Anderson
specific leaf area was shown to be reduced in Asteriscus maritimus (Thunbergia) and Viburnum tinus L. ‘Lucidum’ (Viburnum)], from
following water stress as a direct consequence of reduced leaf areas commercial nursery, were transplanted into 3.3-L pots (one plant
(Rodríguez et al., 2005). Similar results were found for Eragrostis per pot) that were filled with a mixture of sand (75%), silt (18%) and
curvula, Oryza sativa, Abelmoschus esculentus and Asteriscus mar- clay (7%). Six-month-old plants were watered daily to pot capacity
itimus following water stress, and significantly decreased total leaf (determinated by gravimetric method) at regular intervals prior to
areas were observed (Rucker et al., 1995; Shubhra et al., 2003). the initiation of the treatments using a drip irrigation. The initial
Several authors have found frequent increases in the root- biomasses of the plants were 69.3 g plant−1 (Callistemon), 180.6 g
shoot ratios in plants under water stress (Blum, 1996; Zwack and plant−1 (Laurus), 172.6 g plant−1 (Pittosporum), 145.6 g plant−1
Graves, 1998), which has been considered to be an adaptive strategy (Thunbergia) and 38.4 g plant−1 (Viburnum). After 30 days, 30
(Bargali and Tewari, 2004; Guo et al., 2007; Li et al., 2008) because plants from each species were subjected to two consecutive cycles
a larger investment in roots improves the absorption of water. of suspension/rewatering (S-R), while another 30 plants from each
Reduced photosynthesis is one of the main consequences of species were watered daily (C). For every cycle in the S-R treatment,
water stress (Hsiao and Acevedo, 1974; Huang, 2004) and is related the water suspension lasted for 7 days, after which the plants were
to stomatal closure, which is implemented by the plant to reduce rewatered to pot capacity for another 7 days. After the second water
water loss through transpiration (Nayyar and Gupta, 2006; Yang suspension cycle, S-R treatment plants were maintained under the
et al., 2006). However, the duration and speed of the stomatal clo- same conditions as the control plants for 14 days (Fig. 1).
sure vary depending upon the species (Schulze and Hall, 1982). The mean air temperatures, relative humidity levels and global
Evergreen trees have adopted mechanisms to cope with the typ- radiation levels during the experimental periods were recorded on
ical conditions of the Mediterranean, including the ability to endure a data logger (CR 1000; Campbell Scientific Ltd., Loughborough, UK).
water limitation and to recover after rainfall (Galmés et al., 2007). The maximum and minimum temperatures were 22.6 and 18.2 ◦ C,
Further, lemon plants respond to water stress and rewatering by respectively, and the mean relative humidity levels ranged from 60
developing drought avoidance mechanisms, such as stomatal clo- to 68%. The total radiation levels ranged from 8.2 to 11.6 MJ m−2 .
sure, leaf rolling and partial defoliation (Ruiz-Sànchez et al., 1997).
Efeoğlu et al. (2009) demonstrated that the relative water content 2.2. Data collection
in maize was significantly reduced under drought stress conditions
but significantly increased during the recovery period, reaching the On days 37 (S1), 44 (R1), 51 (S2) and 64 (R2) (Fig. 1) of the exper-
levels of the control plants. Other authors (Sánchez-Blanco et al., imental period, the midday relative water content (RWC) and the
2002) have shown that plants of Cistus albidus and C. monspeliensis midday leaf water potential ( ) were measured between 12:00 and
that experienced water stress and recovery have developed differ- 14:00 (solar time). The RWC were measured on fully opened leaves.
ent avoidance mechanisms, for example, C. albidus limits growth Five leaf discs that were 10 mm in diameter were excised from the
and cell expansion, while C. monspeliensis reduces photosynthetic interveinal areas of each plant. For each replicate, 30 discs were
processes. pooled, and their fresh weights (FW) were determined. They were
Water stress could limit plant vegetative growth, performance floated on distilled water in Petri dishes for 4 h to regain turgid-
and also the survival of shrubs and trees (Fernández et al., 2006), ity and then the turgid tissue was quickly blotted to remove excess
and consequently, the selection of drought-tolerant plants may water and reweighed [turgid weight (TW)]. The samples were dried
be considered a strategy for the improvement of landscape man- at 80 ◦ C for 24 h to determine the dry weights (DW) (Rouphael et al.,
agement (Niu et al., 2008). However, information regarding the 2008). The RWC were calculated according to Jones and Turner
responses of some ornamental species in Mediterranean environ- (1978):
ments to short-term water stress is still lacking. Thus, the aim of RWC% = (FW − DW/TW − DW) ∗ 100
this study was to evaluate differences in the mechanisms that are
involved in the resistance of ornamental species to water stress The leaf water potential were estimated according to Scholander
as a result of a regular suspension and recovery of the water sup- et al. (1965) using a pressure chamber (PMS Model 1000, Instru-
ply. These different mechanisms were studied in five ornamental ment Company, Albany, Oregon, USA). The leaves were removed
shrubs that are commonly used in Mediterranean landscapes. with a sharp blade near the petiole bases and immediately tested.
On days 30 (T0), 37 (S1), 44 (R1), 51 (S2) and 64 (R2) (Fig. 1) of the
experimental period, the net photosynthetic rate (A), transpiration
2. Material and methods rate (E) and stomatal conductance (Gs) were measured on mature,
fully expanded leaves using a CO2 /H2 O IRGA (LCi, ADC Bioscientific
2.1. Plant materials, growing conditions and experimental Ltd., Hoddesdon, UK). The measurements were carried out in clear
treatments conditions from 10:00 to 13:00 (solar time). All of the photosynthe-
sis measurements were performed on outer, fully expanded leaves
The experimental trial was carried out in an unheated green- that were sampled from branches that were located in the middle
house that was located in Catania, Italy (37◦ 30 N 15◦ 06 E 20 m a.s.l.). of the canopy.
The five ornamental shrubs [Callistemon citrinus (Curtis) Skeels At the end of the experiment, nine pots per treatment (three
(Callistemon), Laurus nobilis L. (Laurus), Pittosporum tobira (Thunb.) per replication) were randomly chosen for the measurement of
 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153 147

the following parameters: dry weight production and partition- reduction in the leaf area of 49% (Fig. 3). In Pittosporum, S-R treat-
ing, leaf number, leaf characteristics (unit area, specific leaf area, ment reduced leaf area by 40%; however, this reduction was not
chlorophyll content) and root length. Plants that were located at the related to reduced leaf numbers but rather related to reduced leaf
borders of blocks were not harvested. The dry weights (DW) were size (unit leaf area) (Fig. 3). Similar to Pittosporum, S-R treatment
obtained by drying the weighed samples in a thermoventilated also reduced leaf area (∼22%) and leaf size (∼19%) in Viburnum but
oven at 70 ◦ C to constant weights. Root lengths were determined not leaf number (Fig. 3).
by Newman’s modified line intersect method (Newman, 1966). The effect of S-R treatment on leaf RWC at different times during
The chlorophyll content was determined using a SPAD-502 chloro- the experiment varied among species. In Laurus and Thunbergia, S-
phyll meter (Minolta Camera Co., Osaka, Japan). As proposed by R treatment decreased leaf RWC by 30 and 27%, respectively, but
Wang et al. (2005), a calibration curve was plotted considering only during the first drought event (Fig. 4B and D). In contrast, S-
the relationship between the SPAD values and the chlorophyll R treatment decreased leaf RWC in all other species, during both
content as extracted according to Moran and Porath (1980). drought events (Fig. 4A, C and E). During the first drought event
The following equation was used to obtain the chlorophyll con- (S1), leaf RWC in Callistemon, Pittosporum and Viburnum plants
tent (␮g cm−2 ): chlorophyll (␮g cm−2 ) (Callistemon) = 2.567 SPAD decreased by 21, 55 and 9%, respectively, compared with the con-
index–123.8 (R2 = 0.765***); chlorophyll (␮g cm−2 ) (Laurus) = 0.958 trol. However, during the second drought event, S-R treatment had
SPAD index–13.74 (R2 = 0.761***); chlorophyll (␮g cm−2 ) (Pit- less effect on leaf RWC, although they were significant, by 3% in
tosporum) = 0.929 SPAD index–20.58 (R2 = 0.759***); chlorophyll Callistemon, by 16% in Pittosporum and by 4% in Viburnum. At the
(␮g cm−2 ) (Thunbergia) = 0.787 SPAD index–4.960 (R2 = 0.744***); end of the second rewatering period (R2), S-R treatment had no
chlorophyll (␮g cm−2 ) (Viburnum) = 0.932 SPAD index–13.66 influence on the leaf RWC in any species (Fig. 4).
(R2 = 0.844***) (n = 30). The leaf areas were determined using a leaf For all species, the S-R treatment decreased leaf water poten-
area meter (Delta-T Devices Ltd, Cambridge, UK). The specific leaf tial during each drought event compared to controls (Fig. 4). The
area (SLA) were calculated as the ratio of the leaf area to the leaf lowest values were measured during first drought event (S1). Dur-
dry weight. ing the first drought event, the S-R treatment reduced leaf water
potential by 44% in Callistemon, 52% in Laurus, 38% in Pittospo-
rum, 50% in Thunbergia and 100% in Viburnum. During the second
2.3. Statistics
drought event, the S-R treatment reduced leaf water potential by
8% in Callistemon, 28% in Laurus, 39% in Pittosporum, 14% in Thun-
The experiment was conducted as a randomised complete block
bergia and 13% in Viburnum compared to controls (Fig. 4F–L). At
design with three replicates (the species were randomized within
the end of the second recovery period (R2), the S-R treatment had
blocks); each experimental unit consisted of ten plants. The statis-
no influence on leaf water potential in any species similar to the
tical analyses were performed using CoStat version 6.311 (CoHort
trend observed with the RWC.
Software, Monterey, CA, USA). Data were subjected to a two-way
The net photosynthesis (A) rates in the control plants were at
analysis of variance (ANOVA), to determine the effects of drought
beginning of the trial (T0), on average, 6.7 ␮mol CO2 m−2 s−1 (Cal-
stress and species as main effect and their interaction. The means
listemon), 6.0 ␮mol CO2 m−2 s−1 (Laurus), 5.4 ␮mol CO2 m−2 s−1
were compared using the Student–Newman–Keuls test (P ≤ 0.05).
(Pittosporum), 5.7 ␮mol CO2 m−2 s−1 (Thunbergia) and 6.0 ␮mol
The interactions, when significant, are presented separately in the
CO2 m−2 s−1 (Viburnum).
figures.
During the first suspension (S1), the S-R treatment reduced A by
Leaf RWC, leaf water potential and leaf gas exchange data were
64% in Callistemon, by 67% in Laurus, by 87% in Pittosporum, by 54%
subjected to one-way variance (ANOVA) at each data (T0, S1, R1,
in Thunbergia and by 81% in Viburnum. During the first recovery
S2 and R2) to determine the effects of stressed and control plant
(R1), Thunbergia and Viburnum maintained the values below of
for each species. Pair-wise comparisons were done using Student’s
the control plants (by 28 and 32%, respectively). During the second
t-test for means of samples with unequal variances.
drought event (S2), the S-R treatment reduced photosynthesis by
57% in Callistemon, by 67% in Laurus, by 80% in Pittosporum and by
3. Results 77% in Viburnum (Fig. 5).
Transpiration (E) was lower in S-R-treated plants of all species
At the end of the experiment, the S-R treatment only altered during drought events (S1 and S2); in Thunbergia instead the
total plant dry weight of Pittosporum (Table 1; Fig. 2). The S-R treat- decrease was not significant throughout the experiment. In all
ment reduced total dry weight of Pittosporum by ∼66 g (19%). These species, S-R treatment had no influence on E during recovery
modifications were a consequence of a 27% reduction in the shoot periods (R1 and R2) (Fig. 5).
dry weights (Fig. 2). The first S-R treatment reduced Gs by 54% in Callistemon, 70% in
In all species, S-R treatments increased the root-to-shoot ratio Laurus, 100% in Pittosporum and 83% in Viburnum (Fig. 5). During
(Table 1). Root/shoot ratio (R/S) differed among treatment from the second period of S-R, the reduction were similar in Pittosporum
0.55 (control plants) to 0.71 (stressed plants). Among the species, and Viburnum (by 100 and 83%), while in Laurus the reduction level
in the mean of the treatments, R/S varied from 0.18 of Viburnum reached 100%. S-R treatment had no influence on Gs in Thunbergia
to 0.96 of Laurus. In all species, root length increased among treat- plants at all times of the experiment.
ment from 71.2 cm g−1 (control plants) to 94.2 cm g−1 (stressed
plant). Among the species, in the mean of the treatments, root
length varied from 52.5 cm g−1 in Pittosporum to 128.2 cm g−1 in 4. Discussion
Thunbergia.
The SLA and leaf chlorophyll content in all species were unaf- The study of stress/recovery responses is instrumental for
fected at the end of the second rewatering cycle (Table 2). achieving a better understanding of the mechanisms underlying
The effect of S-R treatment on leaf numbers and leaf areas dif- the abilities of plants to adapt to different environments and cli-
fered among species (Table 2). The S-R treatment had no influence matic conditions (Sapeta et al., 2013). Our results indicate that
on the number of leaves, total leaf area or leaf size (unit leaf area) the shrubs that were used in this experiment employ various
in Laurus or Thunbergia (Fig. 3). The S-R treatment decreased the mechanisms, such as the differential partitioning of dry matter
number of leaves in Callistemon by 32% (Fig. 3) and resulted in a between roots and shoots parts, the reduction of the number and
148 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153

Table 1
Total and shoot dry weights, root/shoot ratio and root length in five species of ornamental shrubs (Callistemon citrinus, Callistemon; Laurus nobilis, Laurus; Pittosporum tobira,
Pittosporum; Thunbergia erecta, Thunbergia; Viburnum tinus ‘Lucidum’, Viburnum) grown in containers.

Species Treatment Total dry weight (g plant−1 ) Shoot dry weight (g plant−1 ) Root/shoot ratio (g g−1 ) Root length (cm g−1 )
c d a
Callistemon 118.6 62.7 0.88 68.3c
Laurus 282.5a 144.3b 0.96a 79.7b
Pittosporum 298.7a 212.7a 0.40c 52.5d
Thunbergia 196.1b 116.3c 0.66b 128.2a
Viburnum 76.4d 64.9d 0.18d 84.8b
C 202.9a 131.6a 0.55b 71.2b
S-R 185.8b 108.7b 0.71a 94.2a
a
Significance
Treatment (T) * *** ** ***
Species (S) *** *** *** ***
T × Sb * *** n.s. n.s.

Plants were irrigated daily to container capacity (C) or subjected to suspension/rewatering treatment (S-R treatment: 7 days no water, 7 days irrigation, 7 days no water, 14
days irrigation). Values are means for main effects of species (S) and irrigation treatment (T).
a
n.s. = not significant; *,**,*** represent significance of main effects and interactions at 0.01 < P < 0.05, 0.001 < P < 0.01 and P < 0.001, respectively, from ANOVA. The values
in the same column followed by the same letter are not significantly different at P≤0.05 (Student–Newman–Keuls).
b
The data concerning significant interactions are presented separately.

Fig. 2. Effects of water treatments on the total dry weights (g plant−1 ) and shoot dry weights (g plant−1 ) in five species of ornamental shrubs (Callistemon citrinus, Callistemon;
Laurus nobilis, Laurus; Pittosporum tobira, Pittosporum; Thunbergia erecta, Thunbergia; Viburnum tinus ‘Lucidum’, Viburnum) grown in containers. Plant were irrigated daily
to container capacity (C) or subjected to suspension/rewatering treatment (7 days no water, 7 days irrigation, 7 days no water, 14 days irrigation). Columns denoted with the
same letters are not significantly different, as determined by Student–Newman–Keuls (P≤0.05 test).

Table 2
Leaf number, total plant leaf area, unit leaf area, specific leaf area (SLA) and chlorophyll content in five species of ornamental shrubs (Callistemon citrinus, Callistemon; Laurus
nobilis, Laurus; Pittosporum tobira, Pittosporum; Thunbergia erecta, Thunbergia; Viburnum tinus ‘Lucidum’, Viburnum) grown in containers.

Species Treatment Leaf Total Unit SLA Chlorophyll

(n.plant−1 ) leaf area leaf area (cm2 g−1 ) content
(cm2 plant−1 ) (cm2 plant−1 ) (␮g cm−2 )

Callistemon 1370.7a 3626.7d 2.7e 87.1c 49.4a

Laurus 541.9c 6218.1b 11.9b 81.6c 31.9c
Pittosporum 1155.8b 10827.9a 9.2c 87.0c 21.0d
Thunbergia 1311.6a 6919.0b 5.4d 168.5a 42.9b
Viburnum 127.2d 4751.5c 39.4a 117.7b 37.5c
C 999.1a 7416.9a 14.7a 106.8 36.6
S-R 803.8b 5520.3b 12.7b 110.0 37.5
Significancea
Treatment (T) *** *** *** n.s n.s.
Species (S) *** *** *** *** ***
T × Sb ** *** *** n.s n.s

Plants were irrigated daily to container capacity (C) or subjected to suspension/rewatering treatment (S-R treatment: 7 days no water, 7 days irrigation, 7 days no water, 14
days irrigation). Values are means for main effects of species (S) and irrigation treatment (T).
a
n.s. = not significant; *,**,*** represent significance of main effects and interactions at 0.01 < P < 0.05, 0.001 < P < 0.01 and P < 0.001, respectively, from ANOVA. The values
in the same column followed by the same letter are not significantly different at P≤0.05 (Student–Newman–Keuls).
b
The data concerning significant interactions are presented separately.

size of leaves and leaf area, stomatal closure, declines in Gs and A, the short duration of our experiment, the effects of the alterations in
that allow them to tolerate repeated cycles of drought. Our results irrigation appear to involve both morphological and physiological
are similar to those by Zollinger et al. (2006), who reported that parameters.
different mechanism of drought avoidance (declines in Gs, Pn and Growth and photosynthesis are the primary processes that are
s) were found in six ornamental herbaceous perennials. Despite affected by drought stress (Chaves and Oliveira, 2004). The effects of
 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153 149

Fig. 3. Interactive effects of water treatments and species on the leaf numbers (n◦ plant−1 ), the total leaf areas (cm2 plant−1 ) and unit leaf areas (cm2 plant−1 ) in five species
of ornamental shrubs (Callistemon citrinus, Callistemon; Laurus nobilis, Laurus; Pittosporum tobira, Pittosporum; Thunbergia erecta, Thunbergia; Viburnum tinus ‘Lucidum’,
Viburnum) grown in containers. Plant were irrigated daily to container capacity (C) or subjected to suspension/rewatering treatment (7 days no water, 7 days irrigation, 7
days no water, 14 days irrigation). Columns denoted with the same letters are not significantly different, as determined by Student–Newman–Keuls (P≤0.05 test).

the suspension/rewatering treatment led to differences in shrubs, water deficits did not significantly affect the relative chlorophyll
including decreased shoot dry matter in S-R treatment plants. The concentrations in the leaves. Lack of detectable change in chloro-
negative impact of suspension in irrigation strongly affected Callis- phyll concentrations may have been due to the relatively short
temon and Pittosporum but not Laurus, Viburnum or Thunbergia. duration of the experiment. Other authors have demonstrated that
These results support previous studies that indicated that reduced the leaf chlorophyll concentrations of Carrizo citrange plants were
biomass production is a result of lower water availability (Shao not affected by relatively short-term salinity or drought-stress
et al., 2008; Mugnai et al., 2009); in our study, Callistemon and Pit- treatments (Pérez-Pérez et al., 2007).
tosporum were less tolerant to water stress conditions compared In our study, plants were able to survive the water shortages
to the other ornamental shrubs studied. mainly due to altered physiological mechanisms. In fact, the adap-
Root-to-shoot ratio increased in plants suffering from water tation of plants to water stress most commonly involves stomatal
shortages. This response is attributable to the development of closure, reduced photosynthesis rates and the adjustment of the
bigger roots systems in relation to shoot biomass in accordance water potential (Ludlow, 1980).
with previous reports, which suggested that the shoot growth is Many studies have shown that when plants are subjected to
inhibited relatively more than root growth as a consequence of drought, leaves exhibit large reductions in their relative water
reducing water loss (Monneveux and Belhassen, 1996). Increased content and water potential (Kyparissis et al., 1995; Scarascia-
root-to-shoot ratios have been frequently observed in plants under Mugnozza et al., 1996). This dehydration is often reversible (Efeoğlu
drought conditions (Blum, 1996; Zwack and Graves, 1998) to et al., 2009). In fact, in our study, the RWC values were significantly
reduce water consumption (Wu et al., 2008) and increase water reduced under stress conditions but noticeably increased during
absorption (Nicholas, 1998). This result was confirmed by increased recovery, reaching values that were similar to those of the con-
root lengths allowed the plants to improve their absorbent sur- trol plants. It has been suggested that increases in stomatal and
faces. Through this mechanism of avoidance, the plants adapt to osmotic sensitivities following an initial drought episode may help
the stress without changing their shoot biomasses. In other species, plants better tolerate repeated episodes of drought (Williams et al.,
such as Callistemon and Pittosporum, this ratio also increased as a 2000). This was confirmed by our results, in which we revealed use-
result of reductions in the shoot dry weight. Additionally, Nayyar ful knowledge regarding the mechanisms by which select species
and Gupta (2006) showed that water deficits affect the shoot parts, are able to better tolerate repeated episodes of drought. In fact,
particularly the photosynthetic apparatus. although the RWC was significantly reduced in the first suspension,
Water deficit not only decreased shoot dry weights but also in correspondence of the second suspension, the differences among
decreased leaf area. These reductions may be due either to reduced stressed plants and control were small and sometimes not signifi-
leaf numbers or leaf size. According to Mugnai et al. (2009), deficit cant. The reductions measured in the second suspension were only
irrigation reduces the leaf area in Callistemon citrinus. This was also more pronounced for Pittosporum and Viburnum. However, at the
confirmed by Álvarez and Sánchez-Blanco (2013) in Callistemon cit- end of the stress period, all of the species fully recovered the leaf
rinus, in which the reduced leaf areas were attributed to decreased water status with RWC values similar to control plants.
leaf numbers. The midday leaf water potential were markedly different
Drought stress reduced leaf area in Pittosporum and Viburnum between the control and stressed plants, although the latter recov-
similar to the effects of drought in Cistus monspeliensis and C. albidus ered leaf water potential values similar to control plants at the end
(Sanchez-Blanco et al., 2002). In our study, Pittosporum and Vibur- of the recovery period. Water stress has been shown to influence
num, which were subjected to drought-recovery cycles, reduced the sensitivity of photosynthetic apparatus photoinhibition (Ferrar
leaf area at the end of the trial. This response is attributed to an and Osmond, 1986; Osmond, 1994; Osmond and Chow, 1988). In
avoidance mechanism that allowed the minimisation of water loss addition to affecting stomatal closure, drought stress reduced gas
through stomatal closure in addition to the reduction of carbon exchange in the plants by limiting the transpiration and photosyn-
assimilation in whole plants and consequently plant growth (Bañon thetic rates. A previous study showed that the reduction of water
et al., 2006). stress from −1.0 to −2.0 MPa results in smaller cells and less devel-
Chlorophyll is one of the main chloroplastic components that oped leaves; thus, the photosynthetic areas are reduced (Medrano
was employed in sustaining photosynthesis, and the relative et al., 2002). This occurred in Callistemon, which exhibited
chlorophyll concentration is positively correlated with the pho- reduced leaf numbers, and Viburnum, which showed decreased leaf
tosynthesis rate (Guo and Li, 1996). Flexas and Medrano (2002) size.
reported that water stress reduces green leaf colour in C3 plants Lenzi et al. (2009) demonstrated that the net photosynthesis of
due to chlorophyll degradation. However, our study indicated that drought stressed oleanders recovered levels equivalent to control
150 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153

Fig. 4. Relative water content (RWC, %) and water potential (, MPa) of leaves in five species of ornamental shrubs (Callistemon citrinus, Callistemon; Laurus nobilis, Laurus;
Pittosporum tobira, Pittosporum; Thunbergia erecta, Thunbergia; and Viburnum tinus ‘Lucidum’, Viburnum) grown in containers. Plant were irrigated daily to container capacity
for the species in the control () or subjected to suspension/rewatering treatment () (7 days no water, 7 days irrigation, 7 days no water, 14 days irrigation). Their absence
indicates that the size was less than the symbol. The vertical bars indicate the S.E. of the means. The asterisks depict statistically significant differences between control and
stressed plants at each date (S1, R2, S2 and R2) for each species. Significance values were obtained from a t-test for means of samples with unequal variances.
 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153 151

Fig. 5. Net photosynthesis (A), transpiration (E) rates and leaf conductance (Gs) in five species of ornamental shrubs (Callistemon citrinus, Callistemon; Laurus nobilis, Laurus;
Pittosporum tobira, Pittosporum; Thunbergia erecta, Thunbergia; Viburnum tinus ‘Lucidum’, Viburnum) grown in containers. Plants were irrigated daily to container capacity
for the species in the control () or subjected to suspension/rewatering treatment () [7 days no water (S1), 7 days irrigation (R1), 7 days no water (S2), 14 days irrigation
(R2). The vertical bars represent the S.E. of the means. Their absence indicates that the size was less than the symbol. The asterisks depict statistically significant differences
between control and stressed plants at each date (T0, S1, R2, S2 and R2) for each species. Significance values were obtained from a t-test for means of samples with unequal
variances.
152 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153

plants at the end of drought stress. Further, the recovery of the pho- stem xylem characteristics in two Pistacia (Anacardiaceae) species along a cli-
matic gradient. Flora 193, 195–202.
tosynthetic rates following water stress depends on the intensity
Chartzoulakis, K., Patakas, A., Bosabalidis, A.M., 1999. Changes in water relations,
of the stress (Sapeta et al., 2013). The recovery of photosynthe- photosynthesis and leaf anatomy induced by intermittent drought in two olive
sis may be fast and complete following moderate stress, but the cultivars. Environ. Exp. Bot. 42, 113–120.
recovery after severe stress is progressive and slow and sometimes Chaves, M.M., Oliveira, M.M., 2004. Mechanisms underlying plant resilience
to water deficits: prospects for water-saving agriculture. J. Exp. Bot. 55,
incomplete (De Souza et al., 2004; Flexas et al., 2006; Miyashita 2365–2384.
et al., 2005). Following rehydration, when the stomata reopened, Craufurd, P.Q., Wheeler, T.R., Ellis, R.H., Summerfiled, R.J., Williams, J.H., 1999. Effect
the photosynthesis rates in the stressed plants increased to those of temperature and water deficit on water-use efficiency, carbon isotope dis-
crimination, and specific leaf area in peanut. Crop Sci. 39, 136–142.
of the control plants for all of the species in our study. This sug- De Souza, R.P., Machado, E.C., Silva, J.A.B., Lagôa, A.M.M.A., Silveira, J.A.G., 2004.
gests that both the dark and light reactions of photosynthesis were Photosynthetic gas exchange, chlorophyll fluorescence and some associated
not damaged during the stress period (Lenzi et al., 2009). It should metabolic changes in cowpea (Vigna unguiculata) during water stress and recov-
ery. Environ. Exp. Bot. 51, 45–56.
be noted that the transpiration rates in all of the species follow- Di Castri, F., 1981. Mediterranean-type shrublands of the world, in: Di Castri, F.,
ing the recovery period were similar to those of the control plants. Goodall, D.W., Specht, R.L. (Eds.), Mediterranean-Type Shrublands. Elsevier,
A rapid recovery after stress condition can be correlated with a Amsterdam, pp. 1–52.
Dickson, R.E., Tomlinson, P.T., 1996. Oak growth, development and carbon
greater physiological tolerance to drought and this proves that the
metabolism in response to water stress. Ann. Sci. Forest. 53, 181–196.
plants had activated improved adaptive mechanisms of avoidance Efeoğlu, B., Ekmekçi, Y., Çiçek, N., 2009. Physiological responses of three maize cul-
which allows the plant to regain full turgor more efficiently. This is tivars to drought stress and recovery. South Afr. J. Bot. 75, 34–42.
Fernández, J.A., Balenzategui, L., Bañón, S., Franco, J.A., 2006. Induction of drought
in line with results that were obtained by Momen et al. (1992) in
tolerance by paclobutrazol and irrigation deficit in Phyllirea angustifolia during
relation to Quercus wislizenii plants. the nursery period. Sci. Hort. 107, 277–283.
These results have allowed us to obtain useful information Ferrar, P.J., Osmond, C.B., 1986. Nitrogen supply as a factor influencing photoinhi-
regarding the responses of some shrubs to suspension/rewatering bition and photosynthetic acclimation after transfer of shade-grown Solanum
dulcamara to bright light. Planta 168, 563–570.
cycles. All of the species that were examined were able to employ Flexas, J., Medrano, H., 2002. Drought-inhibition of photosynthesis in C3 plants:
both morphological and physiological mechanisms to adapt to stomatal and non-stomatal limitations revisited. Ann. Bot. 89, 183–189.
water stress and recovery when the stress was over. Drought stress Flexas, J., Bota, J., Galmés, J., Medrano, H., Ribas-Carbó, M., 2006. Keeping a posi-
tive carbon balance under adverse conditions: responses of photosynthesis and
reduced allocation to aboveground structures (dry weight, leaf respiration to water stress. Physiol. Plant. 127, 343–352.
area and leaf number), and increased root growth (dry weights Franco, J.A., Martínez-Sánchez, J.J., Fernández, J.A., Bañón, S., 2006. Selection and
and root lengths), allowed the plants to survive the suspension nursery production of ornamental plants for landscaping and xerogardening in
semi-arid environments. J. Hort. Sci. Biotechnol. 81 (1), 3–17.
period. The effects of drought on Callistemon, Pittosporum and Galmés, J., Flexas, J., Savé, R., Medrano, H., 2007. Water relations and stomatal char-
Viburnum almost exclusively involved aboveground growth. The acteristics of Mediterranean plants with different growth form and leaf habits:
Laurus and Thunbergia plants appear to be more tolerant of drought responses to water stress and recovery. Plant Soil 290, 139–155.
Gratani, L., Bombelli, A., 2000. Correlation between leaf age and other leaf traits in
compared to the other species, increased root development as an
three Mediterranean maquis shrub species: Quercus ilex, Phillyrea latifolia and
adaptive mechanism. Measurement of physiological parameters Cistus incanus. Environ. Exp. Bot. 43, 141–153.
allow further separation amongst species in their drought. Dur- Guo, P., Li, M., 1996. Studies on photosynthetic characteristics in rice hybrid proge-
nies and their parents. I. Chlorophyll content, chlorophyll-protein complex and
ing the suspension period, E, A, Gs and  values decreased in
chlorophyll fluorescence kinetics. J. Trop. Subtrop. Bot. 4, 60–65.
all species. However, Laurus and Thunbergia showed similar RWC Guo, S.W., Chen, G., Zhou, Y., Shen, Q.R., 2007. Ammonium nutrition increases pho-
values between the stressed plants and control plants during the tosynthesis rate under water stress at early development stage of rice (Oryza
second suspension period. Both of these species also had a more sativa L.). Plant Soil 296, 115–124.
Hsiao, T.C., 1973. Plant responses to water stress. Ann. Rev. Plant Physiol. 24,
highly developed root systems. The ability of Thunbergia plants to 519–570.
tolerate periods of drought stress was also demonstrated by the Hsiao, T.C., Acevedo, E., 1974. Plant responses to water deficits, water use efficiency,
trend in transpiration, which increased during the first drought and drought resistance. Agr. For. Metereol. 14, 59–84.
Huang, B., 2004. Recent advances in drought and heat stress physiology of turfgrass:
event without being influenced by the second drought event. a review. Acta Hort. 661, 185–192.
IPCC, 2007. Summary for policymakers of climate change 2007: the physical science
basis. Contribution of Working Group I to the Fourth Assessment Report of the
Acknowledgments Intergovernmental Panel on Climate Change. Cambridge, Cambridge University
Press.
The research Responses of Mediterranean ornamental shrubs to Jones, H.G., 1985. Partitioning stomatal and non-stomatal limitations to photosyn-
thesis. Plant Cell Environ. 8, 95–104.
drought stress and recovery was supported by the research project Jones, H.G., Turner, N.C., 1978. Osmotic adjustment in leaves of sorghum in response
PRIN 2009. Molecular, physiological and morphological aspects of to water deficits. Plant Physiol. 61, 122–126.
ornamentals response to sub-optimal water resources and ionic Karabourniotis, G., 1998. Light-guiding function of foliar sclereids in the evergreen
sclerophyll Phillyrea latifolia: a quantitative approach. J. Exp. Bot. 49, 739–746.
stress founded by the Italian Ministry of University and Research Kyparissis, A., Petropoulou, Y., Manetas, Y., 1995. Summer survival of leaves in a
and marked by grant number 2009BW3KL4 002. soft-leaved shrub (Phlomis fruticosa L., Labiates) under Mediterranean field con-
ditions: avoidance of photoinhibitory damage through decreased chlorophyll
contents. J. Exp. Bot. 46, 1825–1831.
References Lenzi, A., Pittas, L., Martinelli, T., Lombardi, P., Tesi, R., 2009. Response to water
stress of some oleander cultivars suitable for pot plant production. Sci. Hortic.
Álvarez, S., Sánchez-Blanco, M.J., 2013. Changes in growth rate, root morphology and 122, 426–431.
water use efficiency of potted Callistemon citrinus plants in response to different Li, W.X., Oono, Y., Zhu, J., He, X.J., Wu, J.M., Iida, K., Lu, X.Y., Cui, X., Jin, H., Zhu,
levels of water deficit. Sci. Hort. 156, 54–62. J.K., 2008. The Arabidopsis NFYA5 transcription factor is regulated transcrip-
Bañon, S., Ochoa, J., Franco, J.A., Alarcón, J.J., Sánchez-Blanco, M.J., 2006. Hardening tionally and posttranscriptionally to promote drought resistance. Plant Cell 20,
of oleander seedlings by deficit irrigation and low air humidity. Environ. Exp. 2238–2251.
Bot. 56 (1), 36–43. Liu, F., Stützel, H., 2004. Biomass partitioning, specific leaf area, and water use effi-
Bargali, K., Tewari, A., 2004. Growth and water relation parameters in drought- ciency of vegetable amaranth (Amaranthus spp.) in response to drought stress.
stressed Coriaria nepalensis seedlings. J. Arid Environ. 58, 505–512. Sci. Hort. 102, 15–27.
Blum, A., 1996. Crop responses to drought and the interpretation of adaptation. Plant Ludlow, M.M., 1980. Adaptive significance of stomatal responses to water stress,
Growth Regul. 20, 135–148. in: Turner, N.C., Kramer, P.-J. (Eds.) Adaptation of Plants to Water and High
Bradford, K.J., Hsiao, T.C., 1982. Physiological responses to moderate water stress, Temperature Stress. Wiley, New York, pp. 123–128.
in: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (Eds.), Physiological Plant Malinowski, D.P., Belesky, D., 2000. Adaptations of endophyte-infected cool-season
Ecology. II. Water Relations and Carbon Assimilation. Encyclopedia of Plant grasses to environmental stresses: mechanisms of drought and mineral stress
Physiology. New Series Vol. 12B, Springer-Verlag, Berlin, pp. 264–324. tolerance. Crop Sci. 40, 923–940.
Castro-Díez, P., Villar-Salvador, P., Pérez-Rontomé, C., Maestro-Martínez, M., Marcelis, L.F.M., Heuvelink, E., Goudriaan, J., 1998. Modelling biomass production
Montserrat-Martí, G., 1998. Leaf morphology, leaf chemical composition and and yield of horticultural crops: a review. Sci. Hort. 74, 83–111.
 S. Toscano et al. / Scientia Horticulturae 178 (2014) 145–153 153

Medrano, H., Escalona, J.M., Bota, J., Gulías, J., Flexas, J., 2002. Regulation of photo- Ruiz-Sànchez, M.C., Domingo, R., Savè, R., Biel, C., Torrecillas, A., 1997. Effects of
synthesis of C3 plants in response to progressive drought: stomatal conductance water stress and rewatering on leaf water relations of lemon plants. Biol. Plant.
as a reference parameter. Ann. Bot. 89 (SPEC. ISS.), 895–905. 39 (4), 623–631.
Miyashita, K., Tanakamaru, S., Maitani, T., Kimura, K., 2005. Recovery responses of Sánchez-Blanco, M.J., Rodríguez, P., Morales, M.A., Ortuño, M.F., Torrecillas, A.,
photosynthesis, transpiration, and stomatal conductance in kidney bean follow- 2002. Comparative growth and water relation of Cistus albidus and Cistus
ing drought stress. Environ. Exp. Bot. 53, 205–214. monspeliensis plants during water deficit conditions and recovery. Plant Sci. 162,
Momen, B., Menke, J.W., Welker, J.M., 1992. Tissue water relations Quercus wis- 107–113.
lizenii seedlings: drought resistance in a California evergreen oak. Acta Oecol. Sapeta, H., Costa, J.M., Louren, T., Maroco, J., van der Lindee, P., Oliveira, M.M., 2013.
13, 127–136. Drought stress response in Jatropha curcas: growth and physiology. Environ. Exp.
Monneveux, P., Belhassen, E., 1996. The diversity of drought adaptation in wide. Bot. 85, 76–84.
Plant Growth Regul. 20, 85–92. Scarascia-Mugnozza, G., de Angelis, P., Matteucci, G., Valentini, R., 1996. Long-term
Moran, R., Porath, D., 1980. Chlorophyll determination in intact tissues using N,N- exposure to elevated (CO2 ) in a natural Quercus ilex L. community: net photo-
dimethylformamide. Plant Physiol. 65, 478–479. synthesis and photochemical efficiency of PSII at different levels of water stress.
Moriana, A., Villalobos, F.J., Fereres, E., 2002. Stomatal and photosynthetic responses Plant Cell Environ. 19, 643–654.
of olive (Olea europaea L.) leaves to water deficits. Plant Cell Environ. 25, Scholander, P.F., Bradstreet, E.D., Hemmingsen, E.A., Hammel, H.T., 1965. Sap pres-
395–405. sure in vascular plants. Science 148, 339–346.
Mugnai, S., Ferrante, A., Petrognani, L., Serra, G., Vernieri, P., 2009. Stress-induced Schulze, E.D., Hall, A.E., 1982. Stomatal responses, water loss and CO2 assimilation
variation in leaf gas exchange and chlorophyll a fluorescence in Callistemon rates of plants in contrasting environments, in: Lange, O.L., Nobel, P.S., Osmond,
plants. Res. J. Biol. Sci. 4 (8), 913–921. C.B., Ziegler, H. (Eds.), Physiological Plant Ecology. II. Water Relations and Carbon
Nayyar, H., Gupta, D., 2006. Differential sensitivity of C3 and C4 plants to water deficit Assimilation. Encyclopedia of Plant Physiology New Series 12B. Springer, Berlin,
stress: association with oxidative stress and antioxidants. Environ. Exp. Bot. 58, pp. 181–230.
106–113. Shao, H.B., Chu, L.Y., Jaleel, C.A., Zhao, C.X., 2008. Water-deficit-stress-induced
Newman, E.I., 1966. A method of estimating the total length of roots in a sample. J. anatomical changes in higher plants. Compt. Rend. Biol. 331, 215–225.
Appl. Ecol. 3, 139–145. Shubhra, V., Dayal, J., Goswami, C.L., 2003. Effect of phosphorus application on
Nicholas, S., 1998. Plant resistance to environmental stress. Curr. Opin. Biotechnol. growth, chlorophyll and proline under water deficit in clusterbean (Cyamopsis
9, 214–219. tetragonoloba L. Taub). Indian J. Plant Phys. 8, 150–154.
Niu, G., Rodrigues, D.S., Mackay, W., 2008. Growth and physiological response to Torrecillas, A., Rodriguez, P., Sanchez-Blanco, M.J., 2003. Comparison of growth,
drought stress in four oleander clones. J. Am. Soc. Hort. Sci. 133, 188–196. leaf water relations and gas exchange of Cistus albidus and C. monspelien-
Osmond, C.B, 1994. What is photoinhibition: some insights from comparisons of sis plants irrigated with water of different NaCl salinity levels. Sci. Hort. 97,
shade and sun plants, in: Baker, N.R., Bowyer, J.R. (Eds.), Photoinhihition of Pho- 353–368.
tosynthesis: From Molecular Mechanisms to the Field. BIOS Scientific Publishers Yang, X., Chen, X., Ge, Q., Li, B., Tong, Y., Zhang, A., Li, Z., Kuang, T., Lu, C., 2006.
Ltd., Oxford, pp. 1–24. Tolerance of photosynthesis to photoinhibition, high temperature and drought
Osmond, C.B., Chow, W.S., 1988. Ecology of photosynthesis in the sun and shade: stress in flag leaves of wheat a comparison between a hybridization line and its
summary and prognostications. Aust. J. Plant Physiol. 15, 1–9. parents grown under field conditions. Plant Sci. 171, 389–397.
Pereira, J.S., Chaves, M.M., 1993. Plant water deficits in Mediterranean ecosys- Wang, Q., Chen, J., Stamps, R.H., Li, Y., 2005. Correlation of visual quality grading and
tems, in: Smith, J.A.C., Griffiths, H. (Eds.), Plant Responses to Water SPAD reading of green-leaved foliage plants. J. Plant Nutr. 28, 1215–1225.
Deficits—From Cell to Community. BIOS Scientific Publishers Ltd., Oxford, Wang, Y., Zhou, G., Wang, Y., 2007. Modelling responses of the meadow steppe
pp. 237–251. dominated by Leymus chinensis to climate change. Clim. Change 82, 437–452.
Pérez-Pérez, J.G., Syvertsen, J.P., Botía, P., García-Sánchez, F., 2007. Leaf water rela- Williams, M., Rosenqvist, E., Buchhave, M., 2000. The effect of reducing production
tions and net gas exchange responses of salinized Carrizo citrange seedlings water availability on the post-production quality of potted miniature roses (Rosa
during drought stress and recovery. Ann. Bot. 100 (2), 335–345. × hybrida). Postharvest Biol. Technol. 18, 143–150.
Rodríguez, P., Torrecillas, A., Morales, M.A., Ortuño, M.F., Sánchez-Blanco, M.J., 2005. Wright, G.C., Nageswara, R.C., Farquhar, G.D., 1994. Water-use efficiency and carbon
Effects of NaCl salinity and water stress on growth and leaf water relations of isotope discrimination in peanut under water deficit conditions. Crop Sci. 34,
Asteriscus maritimus plants. Environ. Exp. Bot. 53, 113–123. 92–97.
Romano, D., 2004. Strategie per migliorare la compatibilità del verde orna- Wu, F., Bao, W., Li, F., Wu, N., 2008. Effects of drought stress and N supply on
mentale con l’ambiente mediterraneo, in: Pirani, A. (Ed.), Il verde in the growth, biomass partitioning and water-use efficiency of Sophora davidii
città. La progettazione del verde negli spazi urbani. Edagricole, Bologna, seedlings. Environ. Exp. Bot. 63, 248–255.
pp. 363–404. Zollinger, N., Kjelgren, R., Cerny-Koenig, T., Kopp, K., Koenig, R., 2006.
Rouphael, Y., Cardarelli, M., Colla, G., 2008. Yield mineral composition, water rela- Drought responses of six ornamental herbaceous perennials. Sci. Hort. 109,
tions, and water use efficiency of grafted mini-watermelon plants under deficit 267–274.
irrigation. Hort. Sci. 43 (3), 730–736. Zwack, J.A., Graves, W.R., 1998. Leaf water relations and plant development of
Rucker, K.S., Kvien, C.K., Holbrook, C.C., Hook, J.E., 1995. Identification of peanut three freeman maple cultivars subjected to drought. J. Am. Soc. Hort. Sci. 123,
genotypes with improved drought avoidance traits. Peanut Sci. 22, 14–18. 371–375.