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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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