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Interaction between Salinity and Original Habitat during Germination of theAnnual Seashore Halophyte Cakile MaritimaMohamed Ali Ghars ab; Ahmed Debez a; Chedly Abdelly a
a Laboratoire d'Adaptation des Plantes aux Stresses Abiotiques (LAPSA), CBBC, Technopole de Borj-Cedria,Hammam-Lif, Tunisia b Pierre and Marie Curie University-Paris, PCMP, Ivry-Sur-Seine, France
Online Publication Date: 01 November 2009
To cite this Article Ghars, Mohamed Ali, Debez, Ahmed and Abdelly, Chedly(2009)'Interaction between Salinity and Original Habitatduring Germination of the Annual Seashore Halophyte Cakile Maritima',Communications in Soil Science and PlantAnalysis,40:19,3170 — 3180
To link to this Article: DOI: 10.1080/00103620903261684
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Interaction between Salinity and Original Habitatduring Germination of the Annual Seashore
Halophyte Cakile Maritima
Mohamed Ali Ghars,1,2 Ahmed Debez,1 and Chedly Abdelly1
1Laboratoire d’Adaptation des Plantes aux Stresses Abiotiques (LAPSA), CBBC,
Technopole de Borj-Cedria, Hammam-Lif, Tunisia2Pierre and Marie Curie University-Paris, PCMP, Ivry-Sur-Seine, France
Abstract: The impact of salinity (0–400 mM NaCl) on the germination of four
Tunisian accessions (Tabarka, Mahdia, Sfax, and Jerba) of the halophyte Cakile
maritima was assessed. Moderate salinity (50–150 mM NaCl) slightly inhibited the
germination of Sfax, Mahdia, and Jerba seeds, since more than 75% of the sown
seeds germinated. Salt adverse impact was more pronounced in Tabarka seeds,
which showed significantly less germination capacity, even under salt-free
conditions (40%). Although increasing salinity drastically inhibited the germina-
tion in Tabarka, Sfax was the most tolerant accession, especially at 200–300 mM
sodium chloride (NaCl). Assessing germination kinetics using a mathematical
model indicated that high salinity impaired and delayed the germination process.
Such an effect resulted from the combination of osmotic and toxic components,
especially at the greatest concentrations (300–400 mM NaCl). These findings
point out that the successful establishment of this halophyte at the earliest
ontogeny stages is both accession- and salt-dependent.
Keywords: Cakile maritima, germination, halophyte, salinity, variability
Received 18 January 2008, Accepted 18 January 2009
Address correspondence to Chedly Abdelly, Laboratoire d’Adaptation des
Plantes aux Stresses Abiotiques, CBBC, Technopole de Borj-Cedria BP 901,
Hamman-Lif, 2050, Tunisia. E-mail: chedly.abdelly@cbbc.rnrt.tn
Communications in Soil Science and Plant Analysis, 40: 3170–3180, 2009
Copyright # Taylor & Francis Group, LLC
ISSN 0010-3624 print/1532-2416 online
DOI: 10.1080/00103620903261684
3170
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INTRODUCTION
Halophytes are native flora of saline environments that can overcome the
ion and osmotic imbalances caused by high sodium chloride (NaCl)
concentrations via a complex set of salt-adaptation mechanisms (Byrt
and Munns 2008). The mechanisms enabling halophytes to cope with salt
presence are complex, as they take place concomitantly at physiological,
biochemical, and molecular levels (Flowers and Colmer 2008).
Investigating the salt response of halophytes not only enables the
progress in the elucidation of the fundamental bases of their performance
but also benefits agriculture because soil salinity significantly limits plant
productivity of most of the crops.
Germination is a critical stage in the development and life cycle of
many plants; it ensures the reproduction and consequently controls the
dynamics of the population (Radosevich, Holt, and Ghersa 1997). Seed
germination can be divided into three phases: imbibition, increased
metabolic activity, and initiation of growth, which loosely parallel the
triphasic water uptake of mature dry seeds (Finch-Savage and Leubner-
Metzger 2006). Imbibition is a physical phenomenon driven by the
extremely low matric potential of dry seeds and is not subject to
physiological control (Bewley and Black 1985). Several uncontrolled
factors may influence the germination process in arid natural environ-
ments, particularly the presence of salt in soil (Ashraf et al. 2008). Salt
and water stresses may reduce germination notably by (i) limiting water
absorption by the seeds (Dodd and Donovan 1999; Ashraf and Foolad
2005), (ii) reducing the mobilization of stored reserves (Soltania,
Gholipoor, and Zeinali 2006; Voigt et al. 2008), and (iii) directly
affecting the structural organization or synthesis of proteins in
germinating embryos (Ramagopal 1990). These processes could be
affected by both the ionic and the osmotic components of salt stress,
although the relative importance of each component is still a matter of
debate. Indeed, the nature of salt impact may differ among and even
within a given species (Dodd and Donovan 1999; Hanslin and Eggen
2005). It may also depend on the salt type (Tobe, Li, and Omasa 2004).
Seeds of most halophytes are sensitive to elevated salinity during
germination and early seedling establishment (El-Keblawy and Al-
Rawai 2005; Gorai and Neffati 2007).
Cakile maritima is an annual plant (Clausing, Vickers, and Kadereit
2000) usually found in drift line habitats where it is exposed to seawater
and spray and profit from increased nitrogen (N) availability associated
with microalgal litter (Pakeman and Lee 1991a, 1991b). The fruits
(siliques) are dimorphic, consisting of upper and lower parts usually
containing one viable seed each (Payne and Maun 1981). The fruits have
a good floating ability because of the presence of an aerenchyme in the
Interaction between Salinity and Original Habitat during Germination 3171
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pericarp (Rodman 1974), enabling the long-distance dispersal of this
species (Ghars et al. 2006). The main objectives of this study were to
compare the impact of increasing salinity (0–400 mM NaCl) on the
germination aptitude and the seed viability of four Tunisian accessions
of C. maritima harvested from different Mediterranean bioclimatic
stages.
MATERIALS AND METHODS
Seed Harvest and Experimental Conditions
Though classified as mediterranean, Tunisian climate covers multiple
bioclimatic stages, from the humid (northern) to the saharan stages
(southern). Yet, the semi-arid stage prevails in the main part of the
country. In the present study, four coastal sites were selected from the
north to the south of the country as following: Tabarka (humid, mean
annual precipitation 1500 mm), Mahdia (semi-arid with temperate
winter, mean annual precipitation 200–700 mm), and Sfax and Jerba
(arid with temperate winter, mean annual precipitation 100–200 mm).
Mature siliques of C. maritima were harvested between August and
October and kept at 4 uC until the beginning of the experiments. Seeds
were germinated in Petri dishes (25 seeds per each and three replicates per
treatment) in the dark at 20 uC for 2 weeks under increasing salinities (0,
50, 100, 150, 200, 300, and 400 mM NaCl). Ungerminated seeds under
salinity were then transferred to distilled water for 7 days to assess their
viability.
Germination Kinetics
The germination kinetics was assessed using a mathematical model, based
on the assumption that the germination process has two steps: latency of
duration (t0) during which the seeds acquire the aptitude to germinate,
followed by the germination itself. After the latency, the probability (k)
of germination per unit of time is the same for all the seeds and constant
with time. The formal translation of this model is
Y tð Þ~Ymax 1ze{k t{t0ð Þ� �
where Y(t) represents the number of germinated seeds at the time t, Ymax
is the plateau reached by y(t) and corresponds to the number of viable
seeds, and k is related to the time for germination of 50% of the viable
seeds with T50% 5 t0 + ln(2) / k.
3172 M. A. Ghars, A. Debez, and C. Abdelly
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Statistical Analysis
A two-way analysis of variance (ANOVA), with the accession (A) and
salinity (S) as factors, and their interaction (A 6 S) was performed for
the whole data set using the SPSS-10 (SPSS, Inc., Chicago) statistical
program. The Duncan post-hoc test was used when significant differences
were found among salt treatments.
RESULTS
The two-way ANOVA revealed a significant effect of A, S, and their
interaction (A 6 S) on seed germination (Table 1). For all the studied
accessions, germination of seeds was significantly reduced under
increasing salinity (Figure 1). Sfax, Jerba, and Mahdia seeds showed
the greatest germination rates on distilled water (.90%), whereas
Tabarka accession displayed the lowest value (40%). Moderate salinity
(50–150 mM NaCl) had no significant effect on seed germination of Sfax,
Jerba, and Mahdia accessions, because more than 75% of the seeds sown
were able to germinate (Figure 1). In contrast, Tabarka was much more
salt-sensitive. Higher salinities strongly inhibited the germination process,
but Sfax accession was relatively more tolerant (28%). In contrast, Jerba,
Mahdia, and Tabarka were the most salt-sensitive (0%).
Concerning the germination kinetics, significant effects of S, A, and
their interaction (A 6 S) were also observed. The only effect within
moderate salinity range (50–150 mM NaCl) was a decrease in the
germination rate (k), which was associated with an increase in T50%, the
time for 50% germination. At 200 mM NaCl, the different parameters
declined significantly as compared to the control. At greater NaCl
concentrations, germination was almost suppressed for the four studied
accessions (Table 2).
Table 1. Results of a two-way analysis of variance of seed germination
parameters by salinity (S) and accession (A)
Parameter Salinity (S) Accession (A) Interaction S 6 A
Observed germination (%) 236.09 107.48 7.15
Ymax 256.37 126.38 8.04
k 129.32 1.72 2.95*
T50% 103.4 18.41 2.76
t0 76.35 8.42 4.71
Germination recovery (%) 25.91 15.55 4.70
Note. Numbers are F values.
*Nonsignificant at 0.05.
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Germination recovery percentages were lower than those recorded
for the control, except for Sfax seeds pretreated with 200 and 300 mM
NaCl (70% and 93% germination recovery in distilled water, respectively)
(Table 3). Thus, NaCl did not alter seed viability, and the inhibition of
germination was mainly attributable to unfavorable osmotic conditions.
The toxic effect of NaCl was observed for the remaining accessions with
three salt concentrations used (200, 300, and 400 mM NaCl), but only at
the greatest concentration for Sfax seeds. In the previous germination
data, there were a significant effects due to S, A, and A 6 S.
DISCUSSION
Germination is a critical step in the halophyte life cycle, especially for
annuals (Katembe, Unger, and Mitchell 1998; Khan and Gul 2008). Our
results indicate that the germination of C. maritima seeds is accession and
salt-dependent. This process was delayed in the presence of NaCl and
markedly impaired at NaCl concentrations exceeding 150 mM. Similar
trends have been reported for several species of Atriplex (Debez, Chaibi,
and Bouzid 2001; Khan, Zaheer Ahmed, and Hameed, 2006; Redondo-
Gomez et al. 2007) and for other halophytes (Liu et al. 2006; Meloni,
Gulotta, and Martinez 2008; Redondo-Gomez et al. 2008). Although
moderate salt treatment inhibited germination without damaging the
seeds, high salinity was toxic. Hence, the salt-enforced dormancy of
Figure 1. NaCl effect on the germination of C maritima. The symbols are the
observed numbers of germinated seeds, expressed as percentage of sown seeds.
The lines were calculated using the equation [Y(t) 5 Ymax(1 + e2k(t2t0))] and
parameter values of Table 1. Means of three replicates ¡ SE.
3174 M. A. Ghars, A. Debez, and C. Abdelly
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C. maritima seems to be due to the combination of (i) the low water
potential of the medium, preventing seed imbibition (Sosa et al. 2005)
and (ii) the harmful impact of Na+ and Cl2 ions. The salt-related osmotic
impact has been documented in halophytes such as Limonium stocksii
(Zia and Khan 2004), Suaeda physophora, Haloxylon ammodendron, and
Table 2. Parameters of seed germination kinetics as a function of salinity and
the accession
NaCl (mM) Ymax k T50% t0
Jerba
0 100.33 ¡ 0.41 0.94 ¡ 0.04 2.05 ¡ 0.28 0.74 ¡ 0.03
50 96.00 ¡ 6.66 0.58 ¡ 0.14 1.50 ¡ 0.40 1.36 ¡ 0.34
100 84.00 ¡ 9.65 0.71 ¡ 0.01 2.14 ¡ 0.31 0.97 ¡ 0.02
150 74.33 ¡ 14.11 0.77 ¡ 0.00 2.53 ¡ 0.77 0.87 ¡ 0.03
200 44.67 ¡ 19.39 0.70 ¡ 0.12 2.23 ¡ 0.41 1.03 ¡ 0.18
300 24.00 ¡ 3.33 0.83 ¡ 0.06 4.47 ¡ 0.32 0.87 ¡ 0.02
400 0.32 ¡ 0.03 0.12 ¡ 0.02 8.63 ¡ 0.32 7.30 ¡ 0.28
Mahdia
0 95.33 ¡ 6.15 0.82 ¡ 0.14 2.17 ¡ 0.38 0.87 ¡ 0.14
50 85.67 ¡ 4.27 0.87 ¡ 0.09 2.77 ¡ 0.11 0.78 ¡ 0.06
100 87.33 ¡ 5.33 0.70 ¡ 0.06 3.47 ¡ 0.30 1.00 ¡ 0.09
150 79.67 ¡ 6.15 0.60 ¡ 0.10 2.63 ¡ 0.14 1.03 ¡ 0.06
200 47.33 ¡ 5.57 0.65 ¡ 0.04 4.43 ¡ 0.35 1.17 ¡ 0.12
300 8.33 ¡ 4.27 0.67 ¡ 0.46 6.23 ¡ 2.33 2.79 ¡ 3.31
400 0.31 ¡ 0.03 0.17 ¡ 0.02 8.80 ¡ 0.18 7.50 ¡ 0.40
Sfax
0 99.67 ¡ 0.53 0.94 ¡ 0.04 1.73 ¡ 0.03 0.76 ¡ 0.02
50 91.33 ¡ 1.07 0.92 ¡ 0.04 1.97 ¡ 0.05 0.96 ¡ 0.35
100 83.67 ¡ 10.95 0.56 ¡ 0.11 2.23 ¡ 0.37 1.33 ¡ 0.49
150 85.00 ¡ 5.62 0.62 ¡ 0.10 2.80 ¡ 0.67 1.14 ¡ 0.21
200 70.33 ¡ 5.94 0.61 ¡ 0.09 3.12 ¡ 0.30 1.14 ¡ 0.21
300 22.00 ¡ 0.92 0.83 ¡ 0.04 4.43 ¡ 0.72 0.85 ¡ 0.06
400 0.28 ¡ 0.06 0.20 ¡ 0.02 8.63 ¡ 0.51 7.13 ¡ 0.14
Tabarka
0 41.67 ¡ 10.18 0.95 ¡ 0.05 2.57 ¡ 0.85 0.73 ¡ 0.04
50 64.33 ¡ 5.33 0.92 ¡ 0.03 2.79 ¡ 0.11 0.76 ¡ 0.03
100 28.00 ¡ 5.62 0.68 ¡ 0.02 2.73 ¡ 0.46 1.02 ¡ 0.02
150 37.67 ¡ 5.33 0.73 ¡ 0.21 3.47 ¡1.21 1.05 ¡ 0.23
200 3.93 ¡ 0.87 0.45 ¡ 0.42 6.17 ¡ 2.4 4.12 ¡ 2.91
300 0.43 ¡ 0.07 0.18 ¡ 0.02 8.76 ¡ 0.13 6.90 ¡ 0.24
400 0.20 ¡ 0.06 0.15 ¡ 0.04 9.03 ¡ 0.14 7.30 ¡ 0.28
Notes. Ymax is the number of viable seeds (percentage of sown seeds), k is the
probability for germination per time unit, and t0 is the latency time. The time for
50% germination (T50%) is given by t0 + ln (2) / k. The values of Ymax, t0, and k
were determined by fitting Eq. (1) to the observed data for germination kinetics.
Means of three replicates ¡ SE.
Interaction between Salinity and Original Habitat during Germination 3175
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H. persicum (Song et al. 2005), Prosopis strombulifera (Sosa et al. 2005),
and Crithmum maritimum (Atia et al. 2006). Interestingly, seeds of C.
maritima studied accessions displayed variable response patterns to salt
treatments. It has been suggested that salt-tolerance variability at the
germination stage is of prime importance, because it may be exploited for
the selection of the most tolerant cultivars (Epstein et al. 1980). This
variability is likely related to the different geographical origins of the
seeds and may confirm the existence of polymorphism of the species. The
influence of geographical origin on seed germination has also been found
in other species (Debez, Chaibi, and Bouzid 2001; Tobe, Li, and Omasa
2000; Cavalcanti, de Andrade, and Soares 2007).
The fact that moderate salt pretreatment did not affect seed viability
could be of vital significance for the ecophysiology of C. maritima.
Indeed, this result may indicate that C. maritima would be able to
produce viable seed banks when salinity levels are high and that these
seeds would germinate early in the spring, after salt leaching from the soil
surface by the winter rains (Ungar 1995). This hypothesis should be
checked with long salt treatment of seeds to document the mortality
kinetics of seeds in various conditions of salt and humidity. This property
is commonly regarded as a means of resistance to salinity (Keiffer and
Ungar 1997). Germination recovery is a common trait described in
several halophytes such as Atriplex centralasiatica (Liu et al. 2006),
Halostachys caspica (Tobe, Li, and Omasa 2006), Phragmites karka
(Zehra and Khan 2007), C. maritimum (Meot-Duros and Magne 2008),
and Halocnemum strobilaceum (Qu et al. 2008). In C. maritima, this
ability to germinate after salt exposure appeared to be variable according
to the accession. In the case of Tabarka, Jerba, and Mahdia, high salinity
(400 mM NaCl) was toxic to seed germination, whereas Sfax accession
appeared to tolerate high NaCl levels and germinate at acceptable levels
when salinity was alleviated. This toxic effect of high salinity on seed
germination has also been reported on several halophytes, including
Atriplex halimus (Debez, Chaibi, and Bouzid 2001), H. recurvum, S.
fruticosa, and T. maritima (Khan and Ungar 1997), and Salsola affinis
(Wei et al. 2008).
Table 3. Variability of the seed germination recovery (%) in C. maritima
NaCl (mM) Jerba Mahdia Sfax Tabarka
200 47.78 ¡ 12.5 45.19 ¡ 8.3 70.00 ¡ 24.4 37.71 ¡ 14.9
300 0 66.25 ¡ 4.2 93.75 ¡ 07.1 16.11 ¡ 6.9
400 0 0 27.84 ¡ 10.9 0
Notes. Seeds that failed to germinate after 2 weeks of exposure to increasing
salinity were transferred for 7 days in pure water before determining their
germination percentage. Means of three replicates ¡ SE.
3176 M. A. Ghars, A. Debez, and C. Abdelly
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As a whole, this study showed significant effects of salinity, original
habitat, and their interaction on the germination process. In all
accessions, seed germination was reduced with increasing salinity because
of combined toxic and ionic effects. Sfax accession was more salt tolerant
than the other accessions, whereas Tabarka accession displayed the
lowest germination rates, even under salt-free conditions. The theoretical
model may be effective in simulating and predicting the germination
pattern of further species dealing with such environmental constraints.
ACKNOWLEDGMENTS
Mohamed Ali Ghars is indebted to the French Ministry of Foreign
Affairs (French Embassy, Tunis) for an AUF fellowship. The con-
structive contribution of Professor Claude Grignon (Biochimie et
Physiologie moleculaire des Plantes, Institut de Biologie Integrative
des Plantes, Ecole Nationale Superieure d’Agronomie/Institut National
de la Recherche Agronomique, Montpellier, France) is gratefully
acknowledged.
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