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Article

Effects of Chloride and Sulfate Salts on Seed Germination and Seedling Growth of Ballota hirsuta Benth. and Myrtus communis L.

by
Mohammed Dadach
1,
Muhammad Zaheer Ahmed
2,
Arvind Bhatt
3,
Emanuele Radicetti
4 and
Roberto Mancinelli
5,*
1
Ecology and Environment Research Laboratory, Faculty of Nature and Life Sciences, Bejaia University, Targua Ouzemour, Bejaia 06000, Algeria
2
Dr. M. Ajmal Khan-Institute of Sustainable Halophyte Utilization (MAK-ISHU), Faculty of Science, University of Karachi, Karachi 75270, Pakistan
3
Lushan Botanical Garden, Chinese Academy of Sciences, Jiujiang 332900, China
4
Department of Chemical, Pharmaceutical and Agricultural Sciences (DOCPAS), University of Ferrara, 44121 Ferrara, Italy
5
Department of Agricultural and Forestry Sciences (DAFNE), University of Tuscia, 01011 Viterbo, Italy
*
Author to whom correspondence should be addressed.
Plants 2023, 12(22), 3906; https://doi.org/10.3390/plants12223906
Submission received: 18 October 2023 / Revised: 9 November 2023 / Accepted: 15 November 2023 / Published: 20 November 2023
(This article belongs to the Special Issue Seed Biology at the System Level)
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Abstract

:
Soil salinity is a well-known abiotic factor affecting the germination and seedling growth of various plant species. Therefore, we evaluated the effects of different chloride salts (NaCl, KCl and MgCl2) and sulfate salts (Na2SO4, K2SO4 and MgSO4) on the seed germination and early seedling growth of two important ethnomedicinal shrubs of North Africa and the Mediterranean basin (Ballota hirsuta and Myrtus communis). Seeds of these species were subjected to five salinity levels (0–100 mM) and incubated at 20 °C under a light regime (12 h photoperiod). Both species demonstrated their highest germination percentage under control conditions (i.e., without salinity). However, as salinity levels increased, the germination percentages for both species decreased, regardless of the type of salt used. Cations appeared to be more determinative than the anions in regulating the seed germination of both species. M. communis seeds displayed greater sensitivity to sodium (Na+) salts, especially when accompanied with chloride (Cl−) anions. At the higher salt concentrations (75 and 100 mM), Na+ salts had a more pronounced inhibitory effect on M. communis seedling growth compared to potassium (K+) and magnesium (Mg2+) salts. Conversely, Mg2+ salts were more detrimental to seedling growth in B. hirsuta. Based on our results, it can be concluded that both of these species are able to tolerate a moderate level of salinity. Overall, B. hirsuta may be a promising choice for rehabilitating the soils dominated by chloride salts, while M. communis could be utilized for restoring sulfate-dominated soils.

1. Introduction

Soil salinization has become a major global problem which negatively affects plant growth and establishment by interfering with various physiological processes due to osmotic stress and ionic imbalance [1]. Generally, salt-affected soils are categorized into three groups (i.e., saline, sodic and saline–sodic soils) based on the type and extent of salts present. Total soluble salts (measured by electrical conductivity, EC), water potential and pH are mainly used to characterize salt-contaminated soils [2]. Saline soils pose a significant challenge due to the prevalence of soluble salts, particularly sulfate (SO42−) and chloride (Cl−) salts. Additionally, the adverse impact of salinity can be exacerbated when the soil contains a high concentration of sodium (Na+) [3]. High evaporation, which greatly exceeds precipitation in arid and semi-arid regions, leads to the accumulation of salts on the soil surface that results in irreversible alterations in the soil’s physicochemical properties and which ultimately hampers plant growth and survival [4,5].
Selection of salt-resistant species is considered to be the first and most important step for reclaiming salt-affected land. Therefore, understanding salinity tolerance at early growth phases (i.e., seed germination and seedling establishment stages) could be an effective screening method to identify suitable species for the phytoremediation of degraded saline lands [6]. Seed germination and seedling establishment are considered to be the most critical phases in a plant’s life cycle because they play a pivotal role in determining the species survival, especially under unfavorable conditions [7]. Salinity exerts a negative influence on seed germination by disrupting enzymatic activities, interfering with protein metabolism and impeding the mobilization of the seed’s reserves [8]. Moreover, the presence of excessive amounts of salt in soil decreases growth by compromising the ability of seedlings to take up water (osmotic stress) and/or altering cellular ion homeostasis (ionic stress). Excessive accumulation of Na+ and Cl− in the plant tissues leads to severe ion imbalance that results in an alteration in the stomatal regulation, disruption of the chlorophyll biosynthesis and inactivation of plant growth hormones; all these circumstances subsequently affect seedling establishment [9,10].
Sodium chloride is widely used to test salinity tolerance during the seed germination and seedling establishment stages because of its prevalence in the inland and coastal soils of the arid and semi-arid regions [11]. However, sometimes many other ions such as K+, Mg2+, Ca2+, SO42− and CO32− may exist in higher quantities as compared to Na+ and Cl− [12,13]. The presence of certain cations (i.e., Na+, K+, Ca2+ and Mg2+) and their accompanying anions (e.g., Cl−, NO3− and SO42−) also severely affects germination and plant development [14]. Furthermore, it has been documented that various salt agents may have differing effects during the germination and seedling establishment stages, and these effects can vary depending on the species. For example, Lavandula stoechas seeds exhibited better tolerance to MgCl2 compared to other dissolved salts [15]. On the other hand, Artemisia herba-alba seeds displayed greater susceptibility to MgCl2 when compared to NaCl, CaCl2 and Na2SO4 [6]. A similar trend in salt tolerance was observed for Chenopodium glaucum [16] and Zygophyllum simplex [17] during seed germination.
North Africa is suffering from frequent and prolonged drought events and thus it is considered to be the third most salt-affected region after the Middle East and Australia [18]. Saline soils in North African countries are primarily characterized by the presence of various chloride- and sulfate-based salts, although NaCl is the prominent soluble salt (>50%) in these countries. Moreover, the principal cation components in the North African soils are Na+ and Mg2+ [6]. The expansion and sustainability of plant populations depends on successful seed germination and subsequent seedling establishment. However, different salt types can have varying effects on plants. Therefore, we investigated the effects of different chloride and sulfate salts on the seed germination and seedling establishment of two medicinally important species.
Ballota hirsuta Benth. (Family of Lamiaceae) is a perennial, low-growing sub-shrub, native to the Mediterranean region. It is commonly found in a variety of habitats, including open forests, rangelands, plains, and low-elevation mountainous areas within the semi-arid zones of North Africa and southern Europe [19]. A previous study indicated that B. hirsuta seeds exhibited a remarkable germination capacity across a wide temperature range (5 to 30 °C) under controlled laboratory conditions. However, salinity (using NaCl) and drought stress (simulated by polyethylene glycol) severely restricted seed germination [20]. The flavonoids (viz., quercetin-3-glucodide and luteolin-7-rutinoside) found in this plant have been employed in the treatment of various health conditions [21]. In Algeria, this species is known as “Merouit” and is traditionally utilized for the treatment of bruises, injuries and rheumatic pain [22]. Recently, 43 essential oil compounds have been identified in B. hirsuta, rendering it a valuable candidate for cosmetic applications [23]. Harsh climatic conditions and anthropogenic pressures are the main factors disturbing various B. hirsuta populations in their natural habitat [24].
Myrtus communis L. (Family of Myrtaceae) is a small perennial tree, native to the Mediterranean region and North Africa and now widely naturalized in many regions, such as in South America, Northwestern Himalaya and Australia. This species is commonly found in coastal areas, inland hills and open fields, and its growth habits can vary from a small tree to a large shrub depending on environmental conditions, genetic plasticity and growth patterns [25,26]. Moreover, this species is regarded as a promising and adaptable species that could effectively fit into transitional production strategies on a large scale in moderately saline lands of the Mediterranean region [26]. In folk medicine, M. communis is employed for its antiseptic, anti-inflammatory, disinfectant and hypoglycemic properties and also used to cure many diseases such as lung disorder, stomach pains, cough and poor appetite [27]. Moreover, this species is very aromatic due to the high essential oil content in its leaves, and it is mainly utilized in the production of perfume and cosmetic products [28]. Evidence shows that various factors such as soil salinity, prolonged drought and land-clearing activities are severely affecting the growing area of M. communis [15].
The concept of large-scale cultivation of underutilized plants, particularly medicinal ones, as part of non-conventional agricultural practices, has emerged as an innovative and sustainable strategy. This approach aligns with the principles of promoting clean agro-biodiversity and ensuring food and nutrition security for disadvantaged and marginalized populations, especially in developing countries. Furthermore, implementing such practices in marginal land is reported to contribute to achieving various sustainable development goals, including crop diversification, improved health and well-being, decent employment, poverty reduction and the conservation of natural resources [29]. Consequently, promoting the propagation of neglected crops, including medicinal plants, stands as a critical measure to enhance nutritional security and ecological resilience while minimizing adverse effects on food production.
Studies examining the impact of various salts on seed germination and seedling establishment, particularly concerning medicinal plants native to North Africa and the Mediterranean region, have been relatively underexplored despite their significant importance [15,30]. Therefore, the aim of this study was to examine the effects of chloride salts (NaCl, KCl and MgCl2) and sulfate salts (Na2SO4, K2SO4 and MgSO4) on seed germination and seedling establishment of B. hirsuta and M. communis. The outcome of this investigation will lead to understanding of the innate response of these species during their early life phases when they face salinity, and hence could be used for optimizing their cultivation in salt-affected soils.

2. Results

2.1. Salt Stress Effect on Germination Parameters

The analysis of variance (ANOVA) indicated a significant effect of salt types (S) and salt concentrations (SCs) on all seed germination attributes of B. hirsuta, with the exception of the synchrony index (Syn), which was not affected (p > 0.05). Notably, the interaction between S and SC significantly influenced the final germination percentage (FGP), decreasing germination percentage (DGP) and uncertainty (Unc) (Table 1). A similar pattern was observed in the case of M. communis, with the exception of Unc. In this species, the interaction between S and SCs did not show a significant effect (Table 2).
Both species, B. hirsuta and M. communis, exhibited their highest germination percentages under control conditions (without salinity), achieving 85% and 90%, respectively (Table 3 and Table 4). The seed germination percentage of both the species decreased with increasing salinity concentration, irrespective of S. However, the effects of different types of salts on the seed germination appeared to be species-specific. Specifically, M. communis consistently maintained a germination percentage exceeding 14% at a concentration of 100 mM, regardless of the S. In contrast, none of the B. hirsuta seeds were able to germinate at 100 mM when exposed to K2SO4, MgSO4 and MgCl2 (Table 3).
Germination percentage of M. communis seeds was lower than 50% at 75 mM (DGP < 50%) under all the tested S. However, at 100 mM, the decline in germination percentage followed the order MgSO4 > MgCl2 > Na2SO4 = KCl = K2SO4 > NaCl. In the case of B. hirsuta, a germination percentage of less than 50% (DGP < 50%) was observed prior to reaching 75 mM for Na2SO4, K2SO4 and MgCl2. At 100 mM, the decline in germination percentage followed this order NaCl > Na2SO4 > KCl > K2SO4 = MgCl2 = MgSO4.
Salt stress extended the time of 50% germination (T50) and reduced germination speed (GSP) in both species, although a significant (p < 0.05) increase in mean germination time (MGT) was found only in the case of M. communis (Table 3 and Table 4). The exposure of seeds to 100 mM of different Cl− and SO42− salts significantly (p < 0.05) reduced the Unc, except with NaCl and KCl for B. hirsuta and MgSO4 for M. communis. The Syn was higher for B. hirsuta as compared to M. communis, although Syn appeared to be unaffected by salinity concentration (Table 3 and Table 4).
The coefficient of determination (R2) displayed a strong correlation between FGP and S with linear regression values ranging between 0.993 and 0.868 for B. hirsuta and 0.996 to 0.954 for M. communis. The slope of regression line was −0.86 and −0.78 in the case of seeds treated with K2SO4 and NaCl for B. hirsuta and M. communis, respectively, indicating that the maximum reduction in germination percentage with each 1 mM increase in salt was approximately 0.86% for B. hirsuta and 0.78% for M. communis, respectively (Figure 1 and Figure 2).

2.2. Salt Stress Effect on Seedling Growth

Seedling growth traits of B. hirsuta were significantly (p < 0.05) affected by S and SC. The two-way ANOVA analysis confirmed that the interaction of S and SC had a significant (p < 0.05) effect on hypocotyl length (HL), radicle length (RL), seedling tolerance index (STI) and seedling vigor index (SVI) (Table 1). A similar pattern was observed for M. communis, with the exception of RL and STI (Table 2).
Increasing SC significantly decreased the seedling growth (both HL and RL), salinity tolerance and vigor indexes in both the species, except in B. hirsuta, where the low concentration (25 mM) of K+ and Mg2+ salts (either with Cl− or SO42−) improved HL only (>3 cm as compared to the control 2.96 cm) (Table 3). Hypocotyl growth of M. communis was severely inhibited in Na2SO4 (0.25 cm at 100 mM vs. 1.50 cm in the control), while the root growth was severely inhibited in K2SO4 (0.32 cm at 100 mM vs.1.26 cm in the control) (Table 4). However, seedling growth (both HL and RL) of B. hirsuta decreased in the following order of salts KCl > NaCl > Na2SO4 > K2SO4 > MgCl2 > MgSO4.

3. Discussion

Understanding the effect of salinity during germination and seedling establishment is hypothetically essential for screening salt-resistant species that could be used for developing an effective cultivation strategy in areas affected by salinity. Encouraging the cultivation of medicinally important species is a plausible practice that will contribute to (1) reducing the pressure on wild populations, (2) assisting conservation actions, (3) meeting the demands of therapeutic uses and (4) increasing local peoples’ livelihoods [31,32].
Soil salinization is one of the major problems in North African and Mediterranean regions. Therefore, emphasis should be placed on restoring the native vegetation [33]. Selecting salt-resistant native plants with substantial economic and ecological potential could be among the innovative techniques to utilize these species for restoration/rehabilitation purposes.
In this study, B. hirsuta and M. communis showed a remarkable tolerance to different kinds of chloride- and sulfate salts during the germination stage. Seeds of both species were able to germinate even at 100 mM salinity, with the exceptions being MgCl2, K2SO4 and MgSO4 for B. hirsuta seeds. This level of tolerance during the germination stage is higher than the salinity tolerance capacity reported in the majority of glycophytes [34]. These findings are consistent with previous studies conducted on different Mediterranean glycophytic species such as Artemisia herba–alba [6], Marrubium vulgare [30], L. stoechas [15] and Cistus monspeliensis [35]. Generally, both the glycophytes and halophytes exhibited optimum germination in the absence of salt [36,37,38,39]. However, the suppressive effects of chloride and sulfate salts are less detrimental to the germination of halophytes [11].
Overall, increasing salinity levels hinder the germination capacity and homogeneity (i.e., increase asynchronized germination) in glycophytes and halophytes. In the present study, exposing seeds to different types of salts adversely affected the germination speed, with the slowest germination speed seen at the highest salinity level. These results are consistent with a previous study, in which NaCl, CaCl2, MgCl2 and Na2SO4 were found to significantly delay germination speed in M. vulgare [30]. Similarly, reductions in germination percentage and germination speed have been shown in Zygophyllum album seeds when treated with different levels (0 to 400 mM) of NaCl, CaCl2 and Na2SO4 [40]. Usually, seeds tend to maintain dormancy under salinity, which in turn contributes to reducing germination speed as well as germination percentage [41]. Delaying the germination under salinity conditions could be a bet-hedging strategy that may allow these seeds to remain persistent (i.e., fail to germinate while still viable) in soil seed banks until the occurrence of precipitation events that dilute the salinity and create suitable opportunities for germination and seedling establishment, especially in arid and semi-arid bio-climates [13,42]. Likewise, decreased germination homogeneity under salinity implies that seeds extend their germination period over time, thereby increasing the likelihood of some seedlings surviving challenging conditions (such as drought and salinity). This is in contrast to higher germination homogeneity, which leads to a simultaneous emergence of the entire seedling cohort.
Chloride appears to have a more pronounced inhibitory effect on the germination of M. communis compared to sulfate. Conversely, B. hirsuta seeds exhibited the opposite response. Previous studies revealed that Cl− is metabolically more toxic than SO42− during seed germination in various species such as Haloxylon ammodendron, Halogeton glomeratus and Lepidium latifolium [11,12]. Usually, seed cells can easily uptake Cl− either passively (following electrochemical potential gradient) or actively (via symporters or antiporters) that eventually contribute to hampering the germination fitness [43]. Moreover, chloride’s strong capacity to destabilize and alter the structure of primary and secondary metabolites, resulting in reduced osmotropic properties, leads to a subsequent accumulation of reactive oxygen species [44]. The toxicity of chloride arises via interference with its nutritive roles [45]; however, most of the Cl− targeted molecules are still unknown and thus deserve further investigation. The higher seed germination of B. hirsuta in the presence of Cl− may be attributed to the role of this anion in facilitating water uptake, which is crucial for successful radicle emergence. In our case, Cl− salts appeared to be less inhibitory in both species at the seedling growth phase, which might be attributed to the role of Cl− as a micronutrient [46], especially in the oxygen-evolving complex system of photosynthesis [47]. Sulfate is an essential macronutrient with different functions in plant metabolism and cell homeostasis. Sulfate is present in a reduced form in amino acids, lipids and proteins [48]. The assimilation of sulfate in plants occurs through H+/SO42− cotransporters [49] and is facilitated by adenosine-5′-phosphosulfate reductase [50]. In the present study, it is likely that the germination of B. hirsuta was influenced by the presence of accompanying cations, which reduced the solubility of SO42− in water [51].
The effects of cations on seed germination and seedling growth were species-specific, depending on both the type of cation and species. For example, B. hirsuta seeds exhibited a reduction in germination percentage in the following order of cations: Na+ > K+ > Mg2+, whereas M. communis seed germination declined in the order of Mg2+ > K+ > Na+. A similar toxic effect of Mg2+ was observed during the germination of H. glomeratus, L. latifolium and Peganum harmala seeds [11], while Na+ showed a severe toxic effect during the germination of Chenopodium quinoa [52] and L. stoechas seeds [15]. We hypothesize that seed germination is primarily influenced by cations due to their regulatory roles in various processes of metabolism, as well as their ability to interact with various stress-responsive signaling molecules [53]. For example, Mg2+ is one of the essential mesoelements that play a pivotal role in various physiological functions within plants. It interferes with a wide range of post-germination processes (e.g., chlorophyll biosynthesis and carbon fixation) due to its interrelated roles (i.e., cofactor and activator of a number of enzymes) [54]. However, the precise mechanisms by which Mg2+ regulates seed germination remain unclear. Both deficiency and excess of Mg2+ can induce stress and cause a disturbance in enzymes associated with carbohydrate metabolism, such as ructose-1,6-bisphosphatase and GDPD-glucose pyrophosphorylase [55]. Myrtle seeds are reported to contain fatty acids [56]. The higher tolerance of M. communis seeds to Mg2+ is presumably related to the role of this ion in stimulating lipase activity, particularly in high-oil seeds [11]. Consequently, myrtle oily seeds exhibited better performance in the presence of MgCl2 and MgSO4 in the growth medium.
Seeds subjected to higher doses of salts (75 and 100 mM) exhibited remarkable detrimental effects on seedling growth capacity. However, seeds treated with 25 mM did not show any toxic effects on seedling growth (i.e., high hypocotyl and radical lengths). The majority of dissolved salts, except NaCl and Na2SO4, demonstrated a promotion of B. hirsuta seedling growth at 25 mM. This growth promotion at the lowest concentration could be attributed to magnesium and potassium, which serve as two essential macronutrients involved in various physiological functions. For example, Mg2+ is a crucial divalent ion that plays a key role in stomatal movement (opening/closing), regulation of key photosynthetic enzymes and modulation of protein biosynthesis [54]. On the other hand, K+ is required by plants to accomplish many vital functions, such as (i) transport of organic metabolites, (ii) protein synthesis, (iii) maintenance of appropriate cellular pH, (iv) regulation of osmotic balance and (v) cell extension [57]. Moreover, B. hirsuta and M. communis seeds/seedlings exhibited a relatively high tolerance to Na+ salts, indicating their adaptability to cope with this potentially toxic ion. The capacity for rapid and robust seedling growth under high osmotic potential are beneficial adaptive characteristics that enable the development of a deep root system, allowing these species to access deeper soil horizons, thus increasing the likelihood of seedling survival even in the presence of salt.

4. Materials and Methods

4.1. Seed Harvesting Site

Mature seeds of B. hirsuta (Figure 3A) were collected during their natural dispersal in July 2022 from a naturally growing population situated near Sidi Bel Abbes city in Algeria (34°57′44.42″ N, 0°51′48.88″ E; 683 m above sea level). The seed collection site experiences a semi-arid climate with annual mean thermal amplitude of ≈20 °C (2.5 °C (minimum) and 35.5 °C (maximum)). Precipitation is erratic and limited (<220 mm per annum), occurring mostly during winter (Figure 4A).
The ripe berries (blue-black capsules) of M. communis (Figure 3B) were collected in October 2021 from a naturally growing population located near Béjaia city in Algeria (36°44′54.07″ N, 5°01′23.67″ E; 73 m above sea level). This area is characterized by a sub-humid climate, with annual rainfall slightly exceeding 600 mm and an average temperature of about 18.5 °C (Figure 4B). Precipitation mainly occurs during autumn and winter.
After being brought to the laboratory, the seeds were manually separated from the fruits, air-dried and subsequently stored in brown paper bags at 20 °C until the start of the experiment (ca. 3 months after collection).

4.2. Effect of Different Salts on Seed Germination

Seeds with uniform size, color and shape were used for the germination trials. To break both physical and physiological dormancy in M. communis seeds, they were subjected to a 1-month stratification period at 4 °C, followed by soaking in 250 ppm GA3 for 24 h [58]. Seeds of both species were surface-sterilized using 0.50% sodium hypochlorite for 10 min and subsequently washed thrice with deionized water to avoid fungal attacks. Seeds were sown in 9 cm Petri dishes lined with two disks of filter paper (Whatman No. 1) and moistened with 7 mL of different concentrations (0, 25, 50, 75 and 100 mM) of chloride (NaCl, KCl and MgCl2) and sulfate (Na2SO4, K2SO4 and MgSO4) salts. These concentrations were selected based on preliminary experiments on these species [20,26]. Four replicates of 25 seeds each were used for each treatment. Petri dishes were sealed with parafilm and placed in a seed incubator set at a constant temperature of 20 °C and 12 h photoperiod. The incubator was fitted with cool-white fluorescent tubes (≈25 µmol m−2 s−1); optimal conditions for the germination for most of the Mediterranean species [59]. Germinated seeds were counted every 48 h up to the 30-day period. Seeds were considered germinated with the emergence of the radicle (≥2 mm) [60].

4.3. Determination of Seed Germination Attributes

Germination data were used to determine the final germination percentage (FGP), mean germination time (MGT), germination speed (GSP), uncertainty (Unc) and synchrony (Syn), as described by Lozano-Isla et al. [61]:
F G P = F i n a l   p o r t i o n   o f   e m e r g e d   s e e d s T o t a l   n u m b e r   o f   s e e d s × 100
M G T = ∑ i = 1 k t i n i ∑ i = 1 k n i × 100
G S P = ∑ i = 1 k n i ∑ i = 1 k n i X i × 100
U n c = − ∑ i = 1 k f i l o g 2 f i ,   being   f i = n i ∑ i = 1 k n i
S y n = ∑ C n i , 2 N ,   being   c n i , 2 = n i ( n i − 1 ) 2   and   N = ∑ n i ( ∑ n i − 1 ) 2
where ni is the number of seeds germinated at the ith time, ti is the number of days from the beginning of the germination test to the ith observation, Xi is the period of germination experiments, k is the final day that germination was scored, fi is the relative germination frequency and Cni,2 is the number of seeds germinated at the ith time interval.
Decline in germination percentage (DGP) was calculated with the following equation [62]:
D G P = F G P   i n   c o n t r o l − F G P   i n   s t r e s s f u l   c o n d i t i o n F G P   i n   c o n t r o l × 100
Lower DGP values indicate higher salt resistance.
The time of 50% germination (T50) was determined using the following formula [63]:
T 50 = T i + ( N 2 − N i ) ( T j − T i ) N j − N i
N is the total number of emerged seeds, and Ti and Tj are the time which seeds took to reach the adjacent counts of Ni and Nj, respectively, where Ni < N/2 < Nj.
The definition of each seed germination trait, as reported by Lozano-Isla et al. [61] and Ranal and Santana [64], are provided in Table 5.

4.4. Determination of Seedling Growth Parameters

From each Petri plate, a random selection of five seedlings was sampled to evaluate growth parameters. The lengths of hypocotyls and radicles were individually measured at the end of germination experiments (after 30 days) using a graduated ruler.
The seedling tolerance index (STI) was determined using the following equation [65]:
S T I = m e a n   r a d i c l e   l e n g t h   i n   s t r e s s f u l   c o n d i t i o n m e a n   r a d i c l e   l e n g t h   i n   d i s t i l l e d   w a t e r × 100
Seedling vigor index (SVI) was calculated by using the formula suggested by Abdul-Baki and Anderson [66]:
S V I = m e a n   h y p o c o t h y l   l e n g t h + m e a n   r a d i c l e   l e n g t h × 100

4.5. Statistical Analysis

Germination and seedling growth data underwent arcsine transformation to ensure homogeneity of variance before performing an ANOVA. A two-way ANOVA was used to determine the differences among the effects of S, SC and their interaction on various dependent variables related to seed germination (FGP, MGT, GSP, Unc, Syn, DGP, T50) and seedling growth (HL, RL, STI and SVI). Subsequently, a pairwise Tukey’s (HSD) post hoc test (p ≤ 0.05) was conducted to determine the significant differences between means. Statistical analyses were carried out using IBM SPSS Statistics (version 22.0, SPSS Inc., Chicago, IL, USA). Additionally, linear regression analysis was performed to evaluate the coefficient of determination (R2) between the FGPs and different SCs for both the tested species.

5. Conclusions

We investigated the impact of different chloride (NaCl, KCl and MgCl2) and sulfate (Na2SO4, K2SO4, MgSO4) salts on the seed germination of B. hirsuta and M. communis. Despite the negative effects of salt stress, both species demonstrated resilience by successfully germinating even under higher salinity levels, reaching up to 75 mM. Chloride-based salts significantly inhibited the seed germination of M. communis compared to sulfate salts, while the response in B. hirsuta was the opposite. Milder salt concentrations, particularly those composed of Mg2+ and K+ at 25 mM, promoted seedling growth in B. hirsuta. Conversely, seedling growth in M. communis was more hindered by Na+ salts compared to K+ and Mg2+ salts. In general, chloride salts of Na+ and K+ were found to be less inhibitory than sulfate salts, while MgCl2 exhibited greater toxicity than MgSO4 for both of our studied species. Based on our findings, we proposed that both hold promise as salt-resistant glycophytes, making them valuable candidates for enhancing livelihoods and contributing to the restoration of North African and Mediterranean saline lands.

Author Contributions

Conceptualization, M.D. and M.Z.A.; methodology, M.D.; software, M.D.; validation, A.B., E.R. and R.M.; formal analysis, M.D.; investigation, M.D.; resources, M.D. and M.Z.A.; data curation, M.D., M.Z.A., A.B., E.R. and R.M.; writing—original draft preparation, M.D., M.Z.A. and A.B.; writing—review and editing, A.B., E.R. and R.M.; visualization, M.D., M.Z.A. and R.M.; supervision, A.B. and R.M.; project administration, E.R. and R.M.; funding acquisition, E.R. and R.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

All relevant data are within the paper.

Acknowledgments

We sincerely thank the editors and the anonymous reviewers, whose insightful comments and suggestions improved the quality of this manuscript. This work was certified by the Ministry of Higher Education and Scientific Research (D.G.R.S.D.T., Algeria).

Conflicts of Interest

The authors declare no conflict of interest.

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Plants 12 03906 g001
Figure 1. Linear regression analysis of final germination percentages of B. hirsuta seeds treated with different concentrations of chloride and sulfate salts.
Figure 1. Linear regression analysis of final germination percentages of B. hirsuta seeds treated with different concentrations of chloride and sulfate salts.
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Plants 12 03906 g002
Figure 2. Linear regression analysis of final germination percentages of M. communis seeds treated with different concentrations of chloride and sulfate salts.
Figure 2. Linear regression analysis of final germination percentages of M. communis seeds treated with different concentrations of chloride and sulfate salts.
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Plants 12 03906 g003
Figure 3. (A) Plant of Ballota hirsuta (a), flower (b) and seeds (c); (B) plant of Myrtus communis (a), flower (b) and seeds (c).
Figure 3. (A) Plant of Ballota hirsuta (a), flower (b) and seeds (c); (B) plant of Myrtus communis (a), flower (b) and seeds (c).
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Plants 12 03906 g004
Figure 4. Last six-year climatic data (annual precipitations and mean temperatures) of Sidi Bel Abbes (A) and Béjaia (B) provinces (Source—Algerian National Meteorological office).
Figure 4. Last six-year climatic data (annual precipitations and mean temperatures) of Sidi Bel Abbes (A) and Béjaia (B) provinces (Source—Algerian National Meteorological office).
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Table 1. Results of two-way ANOVA (mean squares, F ratio and p value) testing the influences of salts (S), concentrations (SCs) and their interactive effect (S × SC) on seed germination patterns and early seedling growth of B. hirsuta.
Table 1. Results of two-way ANOVA (mean squares, F ratio and p value) testing the influences of salts (S), concentrations (SCs) and their interactive effect (S × SC) on seed germination patterns and early seedling growth of B. hirsuta.
Source of Variation
Dependent VariablesSalt (S)Concentration (SC)S × SC
Mean SquaresF Ratiop ValueMean SquaresF Ratiop ValueMean SquaresF Ratiop Value
FGP354.744.3380.00214,172.71173.310.000341.144.170.000
DGP501.903.270.01119,472.32196.940.000479.943.140.000
MGT0.585.620.0001.3713.290.0000.151.440.153
GSP87.347.380.000170.0214.360.00018.521.560.108
T502.033.180.01412.5019.600.0000.711.100.374
Unc0.485.940.0002.3028.760.0000.232.850.001
Syn0.031.580.1800.051.790.0850.020.880.605
HL6.5841.100.00023.20144.990.0001.126.980.000
RL7.4438.380.00066.68344.420.0000.964.930.000
STI2740.1635.040.00024,127.54308.500.000347.504.440.000
SVI47,780.3414.780.0001,449,784.25448.500.0009273.342.860.001
FGP: final germination percentage; DGP: decreasing germination percentage; MGT: mean germination time; GSP: germination speed; T50: time to reach 50% of final germination; Unc: uncertainty; Syn: synchrony; HL: hypocotyl length; RL: radicle length; STI: seedling tolerance index; SVI: seedling vigor index.
Table 2. Results of two-way ANOVA (mean squares, F ratio and p value) testing the influences of soluble salts (S), concentrations (SCs) and their interactive effect (S × SC) on seed germination patterns and early seedling growth of M. communis.
Table 2. Results of two-way ANOVA (mean squares, F ratio and p value) testing the influences of soluble salts (S), concentrations (SCs) and their interactive effect (S × SC) on seed germination patterns and early seedling growth of M. communis.
Source of Variation
Dependent VariablesSalt (S)Concentration (SC)S × SC
Mean SquaresF Ratiop ValueMean squaresF Ratiop ValueMean SquaresF Ratiop Value
FGP14,224.70437.240.000316.909.740.00078.152.400.005
DGP17,320.08409.800.000387.199.160.00096.402.280.007
MGT23.2457.700.0001.533.800.0050.521.300.215
GSP90.7480.760.0005.865.220.0001.751.560.094
T5090.5632.600.00017.226.200.0003.841.380.166
Unc2.4334.120.0000.192.660.0310.040.600.894
Syn0.036.640.0000.011.050.3960.000.440.978
HL3.0265.180.0000.510.840.0000.102.200.010
RL1.5430.010.0000.254.780.0010.061.070.399
STI8531.3411.380.0001849.842.460.042391.580.520.946
SVI154,656.5198.000.0008836.1611.320.0001921.542.460.004
FGP: final germination percentage; DGP: decreasing germination percentage; MGT: mean germination time; GSP: germination speed; T50: time to reach 50% of final germination; Unc: uncertainty; Syn: synchrony; HL: hypocotyl length; RL: radicle length; STI: seedling tolerance index; SVI: seedling vigor index.
Table 3. Seed germination patterns and seedling growth features of B. hirsuta in response to different concentrations of chloride- and sulfate-based salts.
Table 3. Seed germination patterns and seedling growth features of B. hirsuta in response to different concentrations of chloride- and sulfate-based salts.
SaltsSC
(mM)		FGP
(%)		DGP
(%)		MGT
(Days)		GSP
(%)		T50
(Days)		UncSyn
(bit)		HL
(cm)		RL
(cm)		STISVI
Control085a0a2.46a40.75a3.22a1.20a0.50a2.96ab5.25a100a770.80a
NaCl2565b23.52b2.44a41.42a3.58a1.14a0.52a2.74ab4.34a82.74a460.50b
5054b36.47c2.72a37.15a4.10ab1.30a0.40a2.30ab3.00b57.06b284.68c
7554b36.47c3.02a33.47ab4.80ab1.56a0.32a1.74bc2.06b39.28c209.50d
10040c52.94c3.08a33.25ab5.00b0.96ab0.30a0.62c0.58cd11.02d48.58e
KCl2578a8.24ab2.45a40.85a3.45a1.18a0.50a3.56a3.68ab70.56ab560.62ab
5048bc45.88c2.55a39.77a3.76a1.16a0.50a3.22a2.88b55.65b286.48c
7546bc43.5c2.56a39.12a3.97a1.12a0.44a3.08a2.66b51.42b283.50c
10020d76.47d3.68a28.82b6.70b1.15a0.41a2.66ab2.44b46.83b102.04e
MgCl22576a10.58ab2.31a43.30a3.38a1.26a0.62a3.52a2.55b49.30b462.58b
5072ab15.30ab2.58a39.36a3.98a1.22a0.46a1.26bc1.04c19.67c168.14d
7534c60cd2.50a40.55a3.98a1.11a0.46a0.32cd0.32d6.15d23.38f
1000e100e---0b-0d0d0d0g
Na2SO42572ab15.29b3.06a33.08ab4.90ab1.80a0.54a2.14b2.62b49.80b306.62c
5057b32.94c3.12a32.05ab5.00b1.64a0.36a0.74c0.38cd7.42d64.44e
7542c50.58c3.57a28.10b5.82b1.44a0.33a0.25d0.36cd6.76d26.48f
10025d70.58d3.70a27.04b6.52b0.80b0.28a0.14d0.24d4.64d9.46g
K2SO42574a12.94ab2.42a40.75a3.60a1.14a0.48a3.28a3.56b67.88ab501.02b
5042c50.58c2.84a41.26a4.62ab1.50a0.30a1.60dc1.34c25.34c133.42d
7530c64.70cd2.92a35.30ab4.84ab1.30a0.27a0.50cd0.48cd9.28d27.10f
1000e100e-34.62ab-0b-0d0d0d0g
MgSO42585a0a2.61a38.30a4.08ab1.32a0.42a3.42a2.72b51.70b522.98b
5068b20.02b2.58a41.14a4.50ab1.21a0.48a0.76c0.90c17.36cd113.56e
7546bc45.88c2.61a38.39a5.06b1.36a0.38a0.44cd0.28d5.28d34.88f
1000e100e---0b-0d0d0d0g
SC: salt concentration; FGP: final germination percentage; DGP: decreasing germination percentage; MGT: mean germination time; GSP: germination speed; T50: time to reach 50% of final germination; Unc: uncertainty; Syn: synchrony; HL: hypocotyl length; RL: radicle length; STI: seedling tolerance index; SVI: seedling vigor index; NaCl: sodium chloride; KCl: potassium chloride; MgCl2: magnesium chloride; Na2SO4: sodium sulfate; K2SO4: potassium sulfate; MgSO4: magnesium sulfate. Values sharing the same letter are not significantly different (p ≤ 0.05, Tukey’s test).
Table 4. Seed germination patterns and seedling growth features of M. communis in response to different concentrations of chloride- and sulfate-based salts.
Table 4. Seed germination patterns and seedling growth features of M. communis in response to different concentrations of chloride- and sulfate-based salts.
SaltsSC (mM)FGP (%)DGP (%)MGT (Days)GSP
(%)		T50
(Days)		UncSyn
(bit)		HL (cm)RL (cm)STISVI
Control090a0a5.71a17.52a10.48a2.22a0.26a1.50a1.26a100a251.32a
NaCl2574b17.52b5.89a17.02a9.78a2.30a0.19a1.22b0.84b70.92b153.68b
5054c41.17c6.26a15.96ab11.06a2.28a0.17a1.16b0.72b63.28bc100.36c
7530d67.72d6.98ab14.68bc12.39a2.04a0.16a0.82c0.61b55.06c41.64d
10014e83.72e7.12ab14.05bc12.50a1.25b0.13a0.60c0.56b52.38c17.56f
KCl2584a7.25a6.2a16.34ab10.75a2.48a0.16a1.94a1.30a111.80a272.48a
5067b26.35b6.90ab14.64bc12.22a2.61a0.16a1.50a1.20a103.26a177.82b
7540c54.42c7.64b13.10cd14.04b2.31a0.13a0.82c0.90ab77.98b71.56d
10020d78.06e8.39b11.97d16.16b1.44b0.13a0.50cd0.50b41.40c20.66f
MgCl22562bc32.35c5.86a17.04a10.85a2.76a0.18a1.46a1.14a92.16ab160.52b
5050c45.59c6.24a16.08ab11.06a2.30a0.18a1.02b0.88ab68.75b86.26cd
7534d61.66d7.40ab13.52c13.94ab2.00ab0.15a0.90bc0.72b77.38b62.58d
10022e74.96d9.21b11.08d18.00c1.37b0.13a0.31d0.48bc43.15c17.74f
Na2SO42565b27.80b6.00a16.68a9.94a2.40a0.15a0.96bc0.78b67.86b113.82c
5052c42.70c6.72a14.94bc11.08a2.24a0.17a0.82c0.75b65.48b82.14c
7536d60.14d8.02b12.42c15.34b2.30a0.14a0.58cd0.50b41.46c39.38e
10018e79.45de9.16b10.94d17.55bc1.52b0.12a0.25d0.36c32.7411.12f
K2SO42565b27.92b6.28a15.92ab11.06a2.45a0.16a1.18ab1.02ab83.52ab142.75b
5046c48.62c7.22ab14.00bc13.68ab2.24a0.15a0.90bc0.60b53.58c70.14d
7530d66.20d7.82b12.86c14.44b2.10a0.14a0.66c0.44bc32.82d33.42e
10020e78.00e8.52b11.75d16.16b1.64b0.13a0.35d0.32c28.08d13.6f
MgSO42585a5.80a6.90ab14.52bc12.52a2.74a0.20a1.40a1.08a96.42213.24ab
5062bc30.80bc7.16ab13.96bc13.10ab2.55a0.13a1.34a0.92ab77.68141.95b
7536d60.34d7.80ab12.98c15.72b2.20a0.12a1.30ab0.84b72.8277.15d
10030d67.65d9.06b11.28d17.22bc1.80ab0.12a0.86c0.82b68.2549.64e
SC: salt concentration; FGP: final germination percentage; DGP: decreasing germination percentage; MGT: mean germination time; GSP: germination speed; T50: time to reach 50% of final germination; Unc: uncertainty; Syn: synchrony; HL: hypocotyl length; RL: radicle length; STI: seedling tolerance index; SVI: seedling vigor index. NaCl: sodium chloride; KCl: potassium chloride; MgCl2: magnesium chloride; Na2SO4: sodium sulfate; K2SO4: potassium sulfate; MgSO4: magnesium sulfate. Values sharing the same letter are not significantly different (p ≤ 0.05, Tukey’s test).
Table 5. List of the variables along with their meanings used for characterizing germination attributes.
Table 5. List of the variables along with their meanings used for characterizing germination attributes.
VariablesAbbreviation Definition
Final germination percentage FGP Percentage of seeds that successfully germinated
Mean germination time MGTNumber of germinated seeds relative to non-germinated seeds at evaluation time
Germination speed coefficient GSPThe rate of seed germination over a time interval
Germination uncertainty UncAssessment of the variability in the distribution of germination frequencies
Germination synchrony Syn Degree of overlap in germination timing
Decreasing germination percentageDGPExpresses the difference in percentage between control and stressed seed lots
Time of 50% germinationT50The average time required to achieve 50% germination
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MDPI and ACS Style

Dadach, M.; Ahmed, M.Z.; Bhatt, A.; Radicetti, E.; Mancinelli, R. Effects of Chloride and Sulfate Salts on Seed Germination and Seedling Growth of Ballota hirsuta Benth. and Myrtus communis L. Plants 2023, 12, 3906. https://doi.org/10.3390/plants12223906

AMA Style

Dadach M, Ahmed MZ, Bhatt A, Radicetti E, Mancinelli R. Effects of Chloride and Sulfate Salts on Seed Germination and Seedling Growth of Ballota hirsuta Benth. and Myrtus communis L. Plants. 2023; 12(22):3906. https://doi.org/10.3390/plants12223906

Chicago/Turabian Style

Dadach, Mohammed, Muhammad Zaheer Ahmed, Arvind Bhatt, Emanuele Radicetti, and Roberto Mancinelli. 2023. "Effects of Chloride and Sulfate Salts on Seed Germination and Seedling Growth of Ballota hirsuta Benth. and Myrtus communis L." Plants 12, no. 22: 3906. https://doi.org/10.3390/plants12223906

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