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DOI: 10.32604/phyton.2022.017778


Germination and Photosynthetic Responses to Salinity and Alkalinity in Avicenna marina Propagules

Abdallah Atia1,2,*, Ahmed Abdallah Hussain3,4 and Barhoumi Zouhaier3,5

1Department of Biology, College of Arts and Science Mahayel Asir, King Khalid University, Abha, 61413, Saudi Arabia
2Research Unit, Nutrition and Nitrogen Metabolism and Stress Protein, Department of Biology, Faculty of Sciences of Tunis, Campus Universitaire El Manar I, Tunis, 1068, Tunisia
3Department of Biology, King Khalid University, Abha, 61413, Saudi Arabia
4Faculty of Science, Abu Haraz, Gezira University, Wed Medani, 21111, Sudan
5Laboratory of Extremophile Plants, Biotechnology Center of Borj Cedria, University Tunis El Manar, Tunis, 1068, Tunisia
*Corresponding Author: Abdallah Atia. Email: atbdllh@yahoo.fr
Received: 06 June 2021; Accepted: 28 October 2021

Abstract: Avicenna marina (Forssk.) Vierh is a halophytic mangrove. The reproductive unit is green and has photosynthetic propagules. Mangroves are naturally exposed to fluctuations in some abiotic factors at the soil surface, including salinity and alkalinity. The objective of this study was to determine the effects of two salts including NaCl and NaHCO3 on germination processes and discuss the relationships between cotyledon photosynthesis and embryo axis growth in A. marina propagules. These propagules came from Al Birk, located on the shoreline of the Saudi Red Sea. The results showed that the studied salts did not affect neither the final germination percentage nor the embryo axis growth. However, rooting and root growth were delayed by both salts at 300 mM and were strongly inhibited by 600 mM NaHCO3. Both NaCl and NaHCO3 reduced the photosynthetic activity. These two salts did not affect the other photosynthetic parameters, including stomatal conductance, net transpiration, and intercellular CO2. Thereafter, the reduction in net photosynthesis was not related to any limitation of stomatal conductance. The early germination phase was independent of cotyledon photosynthesis, whereas rooting and root growth may be limited by reduced photosynthesis under NaCl and NaHCO3.

Keywords: Avicenna marina propagules; cotyledons; embryo growth; germination; photosynthesis; alkalinity; salinity

1  Introduction

Mangroves are halophytic trees and shrubs that grow in the intertidal zone, constituting a specific ecosystem on tropical and subtropical coastlines [1]. They thus play an important role in coastal protection against soil erosion, high wave energy, tidal flooding, and tropical cyclones [2]. The mangrove ecosystem is well known for its biodiversity and provides a habitat for wildlife [3]. Mangroves have several economic and medicinal uses, including fodder for animals such as camels and cattle, and firewood in coastal areas [1]. Secondary compounds from mangrove species have been reported to have antimicrobial, antioxidant, and other beneficial effects on human health [1]. However, scientists suggest that about 33%–44% of mangrove ecosystems may be lost in the future due to an increase in sea level and human impacts [4]. Thus, these areas need urgent protection.

Avicenna marina is the most common species along the Red Sea coast of Saudi Arabia [5] and can be used for mangrove ecosystem restoration [6]. An understanding of the responses of mangrove species to abiotic stress is required to ensure the conservation and management of mangrove ecosystems [7]. In A. marina, salt tolerance during the vegetative stages is assured by several mechanisms, including salt accumulation in leaf cells, stimulation of antioxidative activity, salt exclusion by roots, and salt excretion via salt glands [2,5]. However, the effects of different salts during its germination and early stages of growth are largely unknown.

The propagation of A. marina occurs via propagules (i.e., the fruits). The latter is an oval, heart-shaped, two-valved capsule that is 20–25 mm in diameter, sometimes with an apex that has a short beak. The capsule is well-developed and exendospermous, and the embryo is enveloped by a thin pericarp [8]. The embryo axes and the cotyledons are green and photosynthetic. The propagules of mangroves are naturally exposed to saline seawater. Thus, salinity is the main factor that influences germination and establishment on this species [5,8]. The main ions that compose seawater include the cations Na+, K+, Ca2+, and Mg2+ and the anions Cl, SO42−, CO32−, and HCO3 [9]. The two latter ions increase pH and cause alkaline stress. One study [5] showed that toxic ions (Na+ and Cl) mainly accumulate in the pericarp away from the embryo axes and cotyledons. The same authors suggest that the early development of the embryonic axis inside the propagule before dispersal from the mother plant might help in overcoming high salinity during the germination stage and seedling establishment. However, the salt tolerance mechanisms during germination and early seedling growth in A. marina (Forssk.) Vierh. remain unclear.

In A. marina, the cotyledons are photosynthetic and may contribute to embryo axis growth and early seedling growth. Their role under stress conditions is essential for the success of seedling establishment [10]. We hypothesized that photosynthesis activity may influence germination. However, information on the relationships between photosynthesis, germination, and embryonic axis growth is scarce. Thus, the main goals of this investigation were to (i) determine the effects of two salts, namely NaCl and NaHCO3, on germination and embryo axis growth, (ii) determine the effects of these salts on cotyledon photosynthesis, and (iii) investigate the extent of photosynthetic inhibition by these two salts and its subsequent effects on germination and early seedling growth.

2  Materials and Methods

2.1 Propagule Collection

Propagules were collected in April 2018 from Al Birk (18°11′36″N, 41°32′50″E) on the Saudi Arabian Red Sea shoreline. They were transported in plastic bags to the laboratory at King Khalid University (Abha, Saudi Arabia). Healthy propagules were carefully selected and stored under laboratory conditions for 1 day.

2.2 Germination and Growth Experiment

The propagules of A. marina are crypto-viviparous, whereby the embryo grows but does not rupture the pericarp. Thus, for this experiment, “germination” refers to propagule growth initiation, i.e., radicle elongation. To study propagule germination and embryo growth, an experiment was conducted in a glasshouse with a 14/10 h photoperiod, 27/18°C temperature, and 60/75% relative humidity day/night regime. Surface sterilization of the propagules was achieved by incubation in 2% (v/v) NaOCl for 1 min, followed by rinsing three times for 2 min with distilled water.

For the experiment, 15 propagules were sown in 20-cm-diameter plastic trays (plates) filled with a 3-cm-thick layer of peat-moss/vermiculate (3:1) moistened with 1 L distilled water or a suitable solution containing 300 or 600 mM of NaCl or NaHCO3. To maintain the salinity concentration, the plates were enveloped with transparent plastic films to limit any evaporation.

2.3 Pericarp Rupture Percentage

Pericarp rupture was scored over time, and mean values ± SE were calculated from triplicate plates (N = 3 × 15). The numbers of propagules with ruptured pericarps were counted and recorded after 1, 3, 6, 8, 10, 13, and 15 days.

2.4 Germination Percentage

Germination was scored over time as visible radicle protrusion. Mean values ± SE were calculated from triplicate plates (N = 3 × 15). Germinated propagules were counted and recorded after 1, 3, 6, 8, 10, 13, and 15 days, following which the germination percentage was calculated.

2.5 Rooting and Seedling Growth

Rooting or root initiation refers to the date when the first root appeared following pericarp rupture and radicle emergence. Mean values ± SE were calculated from triplicate plates (N = 3 × 15). Rooting percentage was calculated after 1, 3, 6, 8, 10, 13, and 15 days.

At 15 days of the salinity treatment, after root initiation, the seedlings were harvested. Cotyledons, embryo axes, and roots were separated, and their fresh weights were determined using an electronic balance. Samples were then oven-dried at 70°C for 7 days and re-weighed to determine their constant dry weights.

2.6 Relative Water Content (RWC) Determination

Relative water content was determined as follows: RWC = (fresh weight – dry weight)/(dry weight) [11].

2.7 Gas Exchange Analysis

Photosynthetic parameters (photosynthetic rate, A; stomatal conductance, gs; transpiration, E; internal CO2 concentration, Ci) were measured using a Licor-6400 (Licor, Lincoln, NB, USA) photosynthesis apparatus with a 6400-05 Conifer Chamber. The measurements were performed on the cotyledons under a photosynthetic photon flux density of 350–400 μmol/(m2 s).

To estimate the intrinsic water use efficiency, we used the following ratio: iWUE = A/gs [12].

2.8 Statistical Analyses

A one-way analysis of variance (ANOVA) was used to assess the significant effects of salinity and alkalinity. Homogeneity of variances was achieved with the Levene’s test. Tukey’s test (P <0.05) was used to compare the mean values. Statistical analysis was performed with the statistical package SPSS (version 17.00) for Windows (SPSS Inc., Chicago, IL, USA).

3  Results

3.1 Pericarp Rupture Percentage

Pericarp rupture began one day after sowing and reached 55.6% under the distilled water treatment. Under 300 and 600 mM NaCl, the pericarp rupture percentage was 38%. Under 300 and 600 mM NaHCO3, the pericarp rupture percentages were 24.44% and 46.7%, respectively. After 15 days, the pericarp percentage reached 98.8 under the distilled water and 300 mM treatments, but reached 88.89% under 600 mM NaCl. Under 300 and 600 mM NaHCO3, the pericarp rupture percentages were 95.56% and 93.3%, respectively. Tukey’s test (P <0.05) showed no significant effect of NaCl and NaHCO3 (Figs. 1A and 1B).


Figure 1: Pericarp rupture percentage over time in A. marina propagules under (A) saline and (B) alkaline stress. (means of 3 replicates ± SE). Means with different letters are significantly different at P <0.05

3.2 Germination Percentage

Germination began by radicle emergence at 3 days after sowing either under distilled water or salt and alkaline stress. The salt and alkaline stress delayed germination but did not affect the final germination percentage. For instance, after 6 days, the germination percentages were 71.1%, 44.4%, and 42.2% under H2O, 300, and 600 mM NaCl, respectively. Tukey’s test (P <0.05) indicated a significant effect of NaCl (Fig. 2A). Under 300 and 600 mM NaHCO3, the germination percentages were 40% and 48.9%, respectively. Tukey’s test (P <0.05) showed no significant effect of NaHCO3 (Fig. 2B). After 15 days, the germination percentage reached 95.6% under distilled water, but was 88.9% and 84.4% under 300 and 600 mM NaCl, respectively (Fig. 2A). Under alkaline stress, the germination percentage reached 93.3% under either 300 or 600 mM NaHCO3 (Fig. 2B). Tukey’s test (P <0.05) showed no significant effects either under NaCl or NaHCO3 (Figs. 2A, 2B).


Figure 2: Germination percentage over time in A. marina propagules under (A) saline and (B) alkaline stress. (means of 3 replicates ± SE). At each time point, means with different letters are significantly different at P <0.05

3.3 Rooting

Rooting began 6 days after sowing under distilled water, and the rooting percentage reached 24.4%. Salt and alkaline stress delayed the rooting process. For instance, under 600 mM NaCl, the rooting percentage reached only 8.9% at 6 days after sowing and 0% under alkaline conditions. The rooting percentage reached 17.8% and 13.3% under 300 and 600 mM NaHCO3, respectively.

After 15 days, the rooting percentage was 71.1% under distilled water and reached 62% under both 300 and 600 mM NaCl concentrations. Under 300 mM NaHCO3, the rooting percentage was 53.3%, and no rooting occurred under 600 mM NaHCO3. Tukey’s test (P <0.05) indicated significant effects of both salts (NaCl and NaHCO3) on this parameter (Figs. 3A and 3B).


Figure 3: Rooting percentage over time in A. marina propagules under (A) saline and (B) alkaline stress. (means of 3 replicates ± SE). Means with different letters are significantly different at P <0.05

3.4 Seedling Growth

No significant effects of 300 and 600 mM NaCl or NaHCO3 on cotyledon growth were found (Table 1). Embryo axis growth was not significantly affected by these salts according to Tukey’s test (P <0.05) (Table 1). Root growth was not affected by NaCl concentration but was significantly reduced under 300 mM NaHCO3 (P <0.05).


3.5 Relative Water Content

Both NaCl and NaHCO3 salts decreased the water content in the cotyledon tissues. Tukey’s test (P <0.05) showed significant effects of the two salts on this parameter (Table 1). However, no significant effects of the two salts on water content in the embryo axis were noted according to Tukey’s test (P <0.05) (Table 1). Relative water content significantly increased under 300 and 600 mM NaCl and 300 mM NaHCO3 according to Tukey’s test (P <0.05) (Table 1).

3.6 Cotyledon Gas Exchange

One-way ANOVA showed that salinity had a significant effect on photosynthetic activity (A). (F = 5.141; P =0.02). One-way ANOVA also indicated that alkalinity had a significant effect on A (F = 7.854; P =0.005) (Fig. 4A). gs was not significantly affected by 300 and 600 mM NaCl compared to the control (Fig. 4B). Under the NaHCO3 treatments, only 600 mM resulted in significantly higher gs as compared to the control (Fig. 4B) (F = 1.567; P =0.241).


Figure 4: Effect of saline and alkaline stress on photosynthetic parameters in A. marina cotyledons under (A, net photosynthetic rate; gs, stomatal conductance; E, transpiration; Ci, internal CO2 concentration; iWUE, intrinsic water use efficiency) (means of 5 replicates ± SE). Means with different letters are significantly different at P <0.05

The transpiration (E) measurement showed no significant effect of NaCl (F = 3.095; P=0.075) or NaHCO3 (F = 3.217; P =0.069) (Fig. 4C). Internal CO2 (Ci) measurement showed no significant effect of both concentrations of NaCl (F = 1.211; P =0.325) or NaHCO3 (F = 2.740; P =0.097) (Fig. 4D).

The intrinsic water use efficiency was not significantly reduced by either NaCl concentrations compared to the control (F = 3.076; P =0.076) (Fig. 4E). For NaHCO3, a significant reduction was recorded under 600 mM compared to the control (Fig. 4E) (F = 5.063; P =0.021), as also determined by Tukey’s test (P <0.05) (Fig. 4E).

4  Discussion

This work aimed to determine the effects of salt and alkaline stress on propagule germination and photosynthetic activity in the cotyledons of A. marina. In this species, the reproductive unit is green and possesses photosynthetic propagules. This mangrove is a salt-tolerant species during the vegetative stages, though salt and alkaline stress can affect early seedling growth. We were therefore interested in whether photosynthesis reduction under NaCl and NaHCO3 in A. marina cotyledons affects propagule germination and early seedling growth.

4.1 Effect of Salt and Alkaline Stress on Germination and Seedling Growth

The optimum germination of A. marina propagules (95.56%) was obtained under distilled water (Figs. 1A and 1B). However, alkaline and saline conditions did not significantly reduce germination. This suggests that A. marina, which grows along coastlines, has developed special mechanisms to tolerate high alkaline and saline conditions during the germination process. In halophytic plants, including mangroves, rapid germination leads to fast seedling establishment [13]. Both rapid propagule germination and mangrove growth are important. The propagules of A. marina are viviparous and therefore lose their viability rapidly [14]. However, the germination capacity of other mangrove species was found to decrease under high salt concentrations, as reported for Avicennia officinalis (L.) [2]. In the two physiographic types of Avicennia schaueriana Stapf and Leechm. ex Moldenke, the germination percentages were 45.1%, and 76.4% under low salinity, and germination was inhibited under higher salinity [15]. The same result was obtained for Laguncularia racemosa (L.) [14]. Thus, we suggest that the high germination capacity of A. marina under high salt and alkaline stress may explain why it is considered a dominant mangrove species along several coastlines throughout the world.

NaCl delayed rooting and root development, whereas a higher concentration of NaHCO3 completely inhibited root development. In plants, the rapid elongation of the roots is primarily the result of the massive expansion of young cells produced by ongoing division in the meristem tissues. Excessive salinity has been reported to inhibit both root cell production and cell expansion [16]. Alkaline treatment has serious adverse impacts on root growth and is accompanied by marked ROS accumulation in the roots [17]. Excess ROS accumulation under various stressors is a major cause of cellular damage. In rice, the exogenous application of procyanidins, which are antioxidants, significantly alleviated alkalinity-induced cellular damage and improved alkalinity-induced reductions in seedling growth [17]. Thus, we can speculate that in A. marina, alkaline stress causes ROS accumulation and inhibits rooting and root growth by altering hormone growth metabolism. For instance, in Brassica rapa, salt induced a high level of ROS accumulation, which resulted in perturbations to auxin metabolism by modifying both the biosynthesis of IAA and its catabolism, thereby causing root growth inhibition [18].

4.2 Effect of Salt and Alkaline Stress on Photosynthesis

The propagules of A. marina have a high total sugar concentration in comparison with the seeds of other halophytes [5]. Some authors suggest that the high sugar content in the propagules prevents water loss and increases viability. Soluble sugar accumulation is a sign of adaptation to salinity in plants [19,20]. Plants accumulate sugar via photosynthesis. In viviparous propagules, the germination process occurs in the mother plant before dissemination. Since the embryo cotyledons are photosynthetic, they act as the source of photo-assimilates for the early growth phase of seedlings. In the current experiment, the photosynthetic activity in the A. marina cotyledons was significantly reduced by saline and alkaline stresses compared to the control (Fig. 4A). This was accompanied by rooting inhibition and root growth reduction under NaHCO3, but embryo axis growth was not affected. By contrast, the water content in the cotyledons and the growth of the embryo axis were not affected by the two salt treatments. Instead, we detected a significant increase in the water content of the roots. Thus, the root growth inhibition caused by alkaline stress resulted from the accumulation of toxic ions and not from the water status alteration. In the propagules of A. marina, toxic ions, including Cl and Na+, accumulated in the coat, while K+ accumulation was observed in the cotyledons and embryonic axis, which maintained a high K+/Na+ ratio [5]. Thus, we suppose that the low toxic ion accumulation and the high sugar accumulation in the A. marina cotyledons allowed this species to maintain normal embryo axis growth even under high saline and alkaline stresses. It is suggested that the large reserved mass in the folded cotyledons of A. marina propagules sustains embryo growth and seedling establishment under salinity [5]. Such high reserve accumulation is noteworthy when compared to some other halophyte seeds. For instance, sugar accumulation in the propagules of A. marina was about 3-fold higher than in the seeds of Halophyrum mucronatum (L.) Stapf [21] and 75-fold higher than in the seeds of Kochia indica Wight [22]. The high sugar content in the A. marina propagules is considered as an avoidance mechanism that reduces water loss from the propagules by the high ambient osmotic pressure [5]. However, we suggest that sugar accumulation not only prevents water loss but also allows embryo axis growth under seawater when the photosynthetic activity is reduced under alkaline and saline stresses.

Stomatal conductance was not affected by the two NaCl concentrations and 300 mM NaHCO3, but it was stimulated by 600 mM NaHCO3. Thus, the reduction in photosynthesis activity was not related to the limitation of stomatal conductance. The impairment of photosynthetic enzyme activities and reduction in chlorophyll and carotenoid contents and/or chloroplast ultrastructure alteration could explain the reduced photosynthetic activity by salt and alkaline stresses [5,23]. A decline in photosynthetic activity was also observed in A. marina [8] and two other mangrove species, including Kandelia candel (L.) Druce and Bruguiera gymnorhiza (L.) Lam. [24]. The same feature was also observed in some other halophytes, such as Aeluropus littoralis (Gouan) Parl. [25]. By contrast, in other halophytes, such as Cakile maritima Scop. [26], Sesuvium portulacastrum (L.), Tecticornia indica (Willd.) K.A.Sheph. & Paul G.Wilson [23], and Limoniastrum guyonianum [27], salinity stimulated photosynthetic activity. On the contrary, it is well-known that photosynthesis diminution is accompanied by conductance and internal CO2 concentration (Ci) reductions. This was not the case in the present study. By contrast, in Chenopodium quinoa cultivated under saline conditions, photosynthetic activity was not affected, although stomatal conductance was severely reduced [28].

The Ci is used to determine the assimilation ability of mesophyll cells for CO2 [29]. In this study, although the two tested salts decreased photosynthesis, there was no effect on Ci. The same result was found in 14 barley genotypes [28] and in Polygonum arenastrum [30]. To explain these results, it has been suggested that Ci remains steady or increases at very low gs values (<5 mmol H2Om–2 s–1), whereas Ci generally decreases under full to intermediate conductance conditions [31]. This behavior has been observed in rice under salinity [32] and barley under water stress [33]. This result confirmed that salt did not affect stomatal conductance, and thus the reduction in photosynthesis rate could be explained by the decrease in the activity of certain enzymes. Intrinsic water use efficiency (iWUE) exhibited similar trends as photosynthesis rate. Its reduction under high saline and alkaline stresses was because of a decline in the net photosynthetic rate rather than stomatal conductance since the latter remained constant under stress conditions [25]. The persistence of stomatal conductance led to constant transpiration since the latter occurs via stomatal conductance.

5  Conclusion

In conclusion, a reduction in photosynthesis did not alter the early germination phases under saline and alkaline stresses, whereas alkaline stress caused rooting inhibition, root growth reduction, and altered seedling establishment.

Funding Statement: This research was supported by King Khalid University (KKU), Award No. R.G.P. 1/114/40, Abha, Saudi Arabia.

Conflicts of Interest: The authors declare that they have no conflicts of interest to report regarding the present study.


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