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Article

Salinity Tolerance Mechanism of Crithmum maritimum L.: Implications for Sustainable Agriculture in Saline Soils

by
Bihter Colak Esetlili
1,*,
Lale Yildiz Aktas
2,
M. Tolga Esetlili
1,
Tugba Oztekin
2,
Cenk Ceyhun Kılıc
3 and
Yusuf Kurucu
1
1
Department of Soil Science and Plant Nutrition, Faculty of Agriculture, Ege University, Bornova 35100, Izmir, Turkey
2
Department of Biology, Faculty of Science, Ege University, Bornova 35100, Izmir, Turkey
3
Bayındır Vocational Training School, Ege University, Bayindir 35840, Izmir, Turkey
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(18), 8165; https://doi.org/10.3390/su16188165
Submission received: 29 July 2024 / Revised: 7 September 2024 / Accepted: 13 September 2024 / Published: 19 September 2024
(This article belongs to the Special Issue Advances in Sustainable Agricultural Crop Production)
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Abstract

:
Edible halophytes are attracting attention due to their potential for agriculture in saline and marginal areas. The salt tolerance mechanism was analyzed in Crithmum maritimum L., based on ionic, osmotic, and redox homeostasis strategies under salt stress. The methodology involved growing C. maritimum seeds in pots under controlled greenhouse conditions and exposing them to different NaCl concentrations (0, 100, 200, and 300 mM) for five months. High salinity levels decreased plant length and biomass, but the shoot-to-root length and biomass ratio increased significantly. Photosynthetic pigments (chlorophyll and carotenoids) were quantified using spectrophotometric analysis, while macro- and micro-nutrient contents were determined via the Kjeldahl method, flame photometry, and atomic absorption spectrophotometry. Osmolyte accumulation, including proline and glycine betaine, was analyzed using specific biochemical assays, and antioxidant enzyme activities (SOD, CAT, and POX) were measured to assess redox homeostasis. Photosynthetic pigments in C. maritimum leaves slightly increased at 100 mM NaCl, but significantly declined at 200 and 300 mM NaCl. A high Na content in the shoots indicated no restriction in mineral uptake in the roots. Nitrogen and phosphorus slightly decreased under high salinity. The cation content in the shoots varied: potassium decreased, while calcium and magnesium increased with salinity, although the Mg+2/Na+ and K+/Na+ ratios showed similar declining patterns. The micro-nutrients iron and manganese increased in the shoots, while copper remained unchanged. The content of osmolytes proline and glycine betaine significantly increased under the 200 and 300 mM NaCl treatments. Antioxidant enzyme activities (SOD, CAT, and POX) decreased at 100 and 200 mM NaCl, but were strongly induced at 300 mM NaCl. The total antiradical activity of the leaves increased with higher salinity levels. Our results indicated that the facultative halophyte characteristics of C. maritimum emerged after exposure to 200 mM NaCl. Increased calcium content may be a key factor in salinity tolerance. We concluded that C. maritimum employs strong osmotic adjustment and redox homeostasis mechanisms, making it a promising candidate for cultivation in saline environments.

1. Introduction

Globally, around 20% of cultivated land is impacted by soil salinization [1], and this figure is expected to rise to 50% by 2050 [2]. To meet the food demand of a growing population, efforts are being made towards the cultivation of new edible and stress-tolerant plants. Halophytes are possible candidates for agriculture in saline and/or extreme areas [3].
Crithmum maritimum L. is a wild edible plant that is considered a promising alternative crop for saline habitats in sustainable agriculture. This perennial, edible halophytic plant is typically found in salt marshes, rock crevices, and sandy areas along the Mediterranean and Atlantic coastlines [4]. Crithmum maritimum L. is one of the most studied halophytes of the Apiaceae family due to its extensive area of growth and use. In different coastal regions of the Mediterranean, the plant parts are used in food or beverages due to having high essential oil and essential fatty acid contents [5,6]. Furthermore, its medicinal value (diuretic, digestive, laxative, and purgative properties) and high antioxidant capacity have been reported [7,8].
We examined 123 articles, using the WOS platform, which were published between 2014 and 2024 and were directly related to C. maritimum. The analysis of articles revealed a significant research interest in C. maritimum, extending gradually across various subject headings over the last several years. The predominant focus areas have been secondary metabolites, followed by food/edible uses, and agricultural potential (Figure 1). The insights gained from these studies have indicated that there is limited research on the physiology of sea fennel.
Crithmum maritimum is a facultative halophyte plant that differs from euhalophytes by having no salt exclusion mechanism and no salt hair/bladders, Kranz anatomy, or bulliform cells in the leaves, although it has some degree of succulence [9,10]. The classification of halophytes varies based on the salt content in their habitats or the plant response to salinity. Facultative halophytes can grow in both saline and non-saline conditions and exhibit salt stress responses only under high-salinity conditions [11]. This is an important agricultural advantage of the C. maritimum plant compared to euhalophytes that require a certain amount of NaCl in the field. Although salt tolerance dynamics in facultative halophytes are species-specific, general discrimination has emerged due to salt excretion ability or the lack thereof [12]. Under salinity conditions, plants initially encounter osmotic stress, followed by disruption of ion homeostasis. The combined effect of these stresses leads to oxidative stress. After recognition of salt stress, salt-tolerant plants may activate signal transduction pathways to accumulate substances for osmoregulation, to maintain ionic and redox homeostasis [13]. Determining the characteristics of the salt tolerance mechanism of C. maritimum is essential.
There is limited research describing the specific features of the salt stress response and tolerance mechanism of C. maritimum, the subsequent salt effect on mineral nutrient uptake and partition and growth parameters, and the impact of such stress on osmotic and redox homeostasis [14,15,16]. These studies revealed that C. maritimum tolerates moderate salt stress but experiences significant physiological and biochemical changes at high NaCl concentrations.

2. Materials and Methods

2.1. Materials

Crithmum maritimum L. seeds were collected in September 2020 from their natural saline habitat near the Aegean Sea, specifically in Ahmetbeyli, Menderes, Izmir, Türkiye (Figure 2). Crithmum maritimum is a perennial, 25–50 cm tall, herbaceous plant that grows spontaneously on calcareous rock cracks. The seeds were collected from the rock cracks and cavities where they grow. Seeds of C. maritimum collected from their natural habitats were subjected to germination tests under controlled laboratory conditions. The results demonstrated a remarkable germination rate, with approximately 93% of the seeds successfully germinating at an average temperature of 21 °C. This high germination percentage underlines the species potential for successful propagation in controlled environments, which could be essential for conservation and cultivation efforts.

2.2. Experimental Design

This study was conducted as a pot experiment in the greenhouses of the Department of Soil Science and Plant Nutrition, using a randomized experimental design with four replications. A total of 16 pots were used (4 NaCl doses × 4 replicates × 1 plant = 16 pots), with each pot containing 1 kg of soil (dry weight) sieved through a 2 mm mesh.
Critimum maritimum seeds, approximately 0.40 cm in size, collected from their natural habitat were subjected to germination tests under controlled laboratory conditions. The results demonstrated a remarkable germination rate, with approximately 93% of the seeds successfully germinating at an average temperature of 21 °C. Two seedlings from each germinated seed were selected and transferred to pots containing 1 kg of soil. The pots were irrigated with distilled water until the plants emerged to the surface. Before the experiment began, the soil was analyzed for its physical and chemical characteristics (Table 1).
The pH and water-soluble salts were measured in a 1:1 (w/v) soil-to-distilled water suspension using a pH meter and EC meter. Organic matter content was assessed through wet oxidation with K2Cr2O7, following the method proposed by [16,17,18]. The calcium carbonate (CaCO3) content was determined volumetrically using a Scheibler calcimeter [18]. The texture contents were assessed following the methods outlined by [18]. In the soil analysis, total N was measured using the Kjeldahl method, and available phosphorus (P) was determined using the Olsen method, which is effective for assessing P availability in soils with a neutral to alkaline pH. Potassium (K), sodium (Na), calcium (Ca), and magnesium (Mg) were extracted using 1 N NH4OAc, a method widely used for the assessment of exchangeable cations. For measurement of the micro-nutrients, iron (Fe), copper (Cu), zinc (Zn), and manganese (Mn) were extracted using 1 N DTPA, which effectively chelates these elements, providing a measure of their bioavailable forms in the soil. Plant-extractable/-available contents of P, K, Ca, Mg, Na, Fe, Zn, Mn, and Cu in the soil were measured according to [17,18] (Table 1).
Sodium chloride was applied to one-month-old seedlings via the irrigation water at different concentrations (0, 100, 200, and 300 mM). The NaCl concentration in the experimental soil was around 12.5 mM NaCl. The NaCl solutions were renewed once a week over the course of 5 months. The experiments were carried out in controlled conditions in a greenhouse, maintained at a temperature of 25 ± 5 °C. From 20 April 2021 to 26 November 2021, radiation energy within the greenhouse was manually gauged every 30 min between 10:00 and 16:00, the period of maximum daylight efficacy. This measurement was carried out using a Lux Meter HP-8818 (Zhuhai Holdpeak instrument Co., Ltd., Guangdong, China) device, and the results were averaged and evaluated in Lux × 10 units. The minimum and maximum recorded values during the growth period of C. maritimum ranged between 222 and 1056 Lux × 10. After 5 months of exposure to NaCl, the plants were harvested, with the roots and shoots collected separately.

2.3. Photosynthetic Pigments Analysis

The analysis of photosynthetic pigments (chlorophyll and carotenoids) of fresh leaves of C. maritimum was carried out following the procedure outlined by [19]. A small quantity of the leaf sample (0.10 g) was homogenized in 80% acetone (v/v), and the extract was filtered using Whatman No.1 filter papers. The absorption spectra of the filtrate were then spectrophotometrically assessed at 663, 646, and 470 nm wavelengths (Thermoscientific, Waltham, MA, USA). Chlorophyll a, b, and the total carotenoid content were determined using the equation proposed for 80% acetone [19].

2.4. Growth Parameters and Macro- and Micro-Nutrient Analysis

Crithmum maritimum seedlings were harvested and weighed from each pot to ascertain the fresh biomass yield (FBY) and shoot and root length [20]. In preparation for macro- and micro-nutrient analysis, fresh samples collected from each plot were rinsed with distilled water. The samples were kept at 65 ± 5 °C for a period of 48 h to dry. These samples were subsequently ground in readiness for analyzing the plant nutrients. The nitrogen (N) content was gauged using a variation of the Kjeldahl method [21]. We employed dry ash extracts to colorimetrically determine the phosphorus (P) content using the vanadomolybdophosphoric yellow color method [22]. The quantities of potassium (K), calcium (Ca), and sodium (Na) were ascertained using a flame photometer, while the amounts of magnesium (Mg), iron (Fe), zinc (Zn), manganese (Mn), and copper (Cu) were measured using an atomic absorption spectrophotometer [20].

2.5. Determination of Osmolytes

Measurement of the proline content, as outlined by [23], was carried out in this study. A proportion (2 mL) of the extract derived from grinding 0.3 g of the fresh leaf material with 10 mL of 3% (w/v) sulfosalicylic acid was combined with 2 mL of acetic acid and 2 mL of ninhydrin reagent. The reaction mixture was placed in a water bath (95 ± 5 °C) for 1 h and subsequently treated with 4 mL of toluene. The absorbance of the toluene phase was measured at 518 nm. The results were expressed as moles per gram of fresh mass.
To quantify the content of glycine betaine (GB), 0.05 g of plant leaves was extracted at room temperature with liquid nitrogen and 1 mL of distilled water. Overnight, the extract was incubated at 4 °C. The specimens were spun in a centrifuge at 4500 rpm at a temperature of 4 °C for 30 min. The supernatant was kept at −20 °C for storage. The samples were injected into a high-performance liquid chromatograph system (HPLC) using an Ace C18 (25 cm × 4.6 mm × 5 m) column and a 200 nm UV detector after being diluted 1/10 with water [23].

2.6. Antioxidant Enzyme Activities

Crithmum maritimum leaf samples (1 g) were homogenized with 0.1 M 50 mL K-phosphate buffer, including 2 mM EDTA, 10% (w/v) glycerol, 1 mM phenylmethanesulfonyl fluoride (PMSF), and 2% (w/v) polyvinylpyrrolidone to obtain the superoxide dismutase, catalase, and peroxidase enzyme activities, as well as total soluble protein content determination. The homogenate was centrifuged at 12,000× g for 30 min at 4 °C. The supernatant was then used for the enzyme and protein experiments. The method in [24] was used to measure the total soluble protein content of the leaf extract, and bovine serum albumin (BSA) was used as a standard.
Superoxide dismutase (SOD) activity was measured using the method in [25,26], with slight modifications. For the test, 25 µL of the enzyme sample was added into 50 mM potassium buffer (pH 7.4), and the freshly prepared reaction mixture contained 1 mM EDTA, 0.62 mM NBT, and 0.98 mM NADH. A microplate reader (SpectraMax 250 Molecular Devices, San Jose, CA, USA) was used for constant monitoring of the NBT reduction. The 50% inhibition of the initial rate of NBT was defined as one enzyme unit.
Catalase (CAT) activity was measured by monitoring H2O2 absorption at 240 nm. Potassium phosphate (0.05 M, pH 7.0) buffer with 3% (w/v) H2O2 was added to 0.20 mL of plant extract, to a total 3 mL volume. A 3 min kinetic measurement was used to capture the decline in the mixture’s absorbance [27].
Peroxidase (POX) activity was assessed based on the oxidation of 3.3 diaminobenzidine tetrahydrochloride (DAB). The plant extract (0.20 mL) was added to the reaction mixture containing sodium phosphate citrate buffer (0.15 M, pH 4.4), 0.4 M DAB, 0.05 g of gelatin, and 6% (w/v) H2O2. A 3 min kinetic measurement captured the increase in absorbance [28].

2.7. Antiradical Activity

A 2,2 diphenyl-1-picrylhydrazil radical (DPPH) assay was used to measure the antiradical activity, or the capacity to scavenge free radicals, with certain adjustments made in accordance with a prior study [27]. A total of 0.1 g of plant material and 80% ethanol (1 mL) were homogenized. The homogenate was centrifuged for 15 min at 4 °C at 9000× g rpm. After 50 µL of supernatant and 1.95 mL of DPPH were mixed, the decrease in absorbance at 515 nm was measured [29,30].

2.8. Statistical Analysis

Statistical evaluations were performed utilizing the SPSS Statistics 20.0 software, adhering to a randomized block design, with a comparison of significant means. The Least Significant Difference (LSD) test was employed to determine the statistical significance of the variations in the treatments at p < 0.05.

3. Results and Discussion

One-month-old C. maritimum seedlings were exposed to different NaCl concentrations for 5 months. During the growth period in the greenhouse, it was observed that the growth stimulation of C. maritimum seedlings required optimum temperature limits of 25 ± 5 °C on average. Even at the highest concentration of 300 mM NaCl, no indications of toxicity, such as necrotic or chlorotic lesions on the leaves, were detected. NaCl-treated seedlings and plants did not show any wilting or dehydration symptoms on the leaves (Figure 3).

3.1. Growth Parameters

A significant decrease in shoot length was observed with an increasing salinity level. While the root length was maintained at a moderate salinity level, it significantly declined at concentrations of 200 and 300 mM NaCl (43.75 and 59.37%). Salinity caused a reduction in shoot biomass, except in the 200 mM NaCl treatment. Root biomass was not affected by salinity; however, it was significantly decreased by 51.15% in the 300 mM NaCl treatment (Table 1). Growth parameter evaluation indicated that biomass production and partitioning among the above- and below-ground organs were significantly influenced by different NaCl levels. The shoot-to-root ratio for both length and biomass significantly decreased at 100 mM NaCl exposure, but the ratios significantly increased at 200 and 300 mM NaCl compared to the control.
The control and moderate salinity groups exhibited a 0.71 and 0.59 shoot-to-root length ratio, respectively. In contrast, a higher salinity level caused an enhancement in shoot length over root length, reaching a ratio of 1:1. Biomass production exhibited a similar trend in the control and 100 mM groups (3.60 and 3.21 S/R biomass ratio, respectively); however, the shoot-to-root biomass ratio was substantially higher, reaching 3.88 and 4.45 in the 200 and 300 mM NaCl treatments, respectively (Table 2).
The root-to-shoot ratio is used to evaluate the overall plant growth dynamics. A high root-to-shoot ratio typically indicates limited availability of water or nutrients, particularly nitrogen and phosphorus, as plants allocate more resources to root development to access scarce nutrients in the soil [31]. Consistent with soil conditions, halophytes showed a more significantly altered shoot-to-root length and biomass than non-halophytes under salinity. The ratio also differs among halophyte plants based on tolerance level, reflecting their adaptation, survival, and habitat modification abilities [32]. The shoot-to-root ratio of C. maritimum was found to be higher under the 200 and 300 mM NaCl applications when compared to the 100 mM NaCl application. This indicated better adaptation to saline environments and the ability to direct assimilates in the shoots.
Consistent with our findings, the researchers in [33] recorded high salinity tolerance, as reflected by constant values in growth rates, at 200 mM NaCl in Crithmum maritimum. Our data aligned with previous studies on C. maritimum by [34,35], which reported that salt stress positively affects the aerial parts by increasing the fresh weight while reducing the root biomass. The researchers in [36] suggested that sea fennel requires salt in the growth medium; however, our data showed that C. maritimum can grow under non-saline conditions as well (Figure 3).
Different studies have reported a reduction in the growth of C. maritimum at 200 mM NaCl [14,15]. Our data showed not only reduced growth but also increasing shoot growth over root growth, indicating that the tolerance level to salinity is related to the partition of organ development. Our results, when evaluated together with previous reports, revealed that the salinity tolerance level of C. maritimum may vary depending on ecotypes, trial conditions, duration of salinity treatment, and plant age [32,33,34,35].

3.2. Photosythetic Pigments

The total chlorophyll content (Chl) of C. maritimum leaves was significantly decreased by 37.3% and 46.9%, respectively, when the NaCl concentrations (200 and 300 mM) were higher (Figure 4). Carotenoids (Car) are fundamental pigments of the photosynthetic antenna complex and antioxidant defense mechanism of chloroplasts. The carotenoid content exhibited a similar trend in response to high salinity levels as the chlorophyll content. Severe salinity levels of 200 and 300 mM NaCl resulted in a substantial decline in the leaf Car contents by 67.9 and 73.2%, respectively, in comparison to the control plants.
The relationship between salinity levels and pigment content can be used to understand a plant’s stress tolerance and adaptation. While moderate salinity levels generally do not significantly impact the photosynthetic capacity of plants, high salinity levels can substantially reduce pigment content and, consequently, photosynthetic performance [37]. The pigment results in our study were in accordance with the growth parameters, indicating that a moderate (100 mM) salinity level did not have any impact on the photosynthetic capacity and biosynthesis reactions of Crithmum maritimum. Previous reports noted that salinity can lead to a reduction in plant growth, even in halophytes, due to reduced carbon fixation [37]. The researchers in [38] reported a decrease in the chlorophyll content of C. maritimum seedlings when treated with 85 mM and higher NaCl concentrations (85–512 mM) for six weeks. In contrast, our study showed that leaf Chl and Car levels were still higher at 100 mM NaCl after 5 months than in the control group. These results indicated the elevated salt tolerance of the Aegean coast ecotype. The identified differences may be attributed to species diversity, climate, and geographical conditions.

3.3. Ion Homeostasis: Macro- and Micro-Nutrient Contents

Macro- and micro-nutrient deprivation is commonly experienced by plants grown in saline environments due to the osmotic restrictions and their competitive take-up and transport in plants. The macro- and micro-elements in the roots and shoots of C. maritimum are shown in Table 3 and Table 4.
The Na+ content of the root and shoot tissue gradually increased with an increasing NaCl concentration. The sodium content was increased in the roots by around 144% (300 mM NaCl); however, the increase reached 234% in the shoots. Thus, this study revealed that C. maritimum is a Na+ includer and uptaken Na+ cannot be restricted to the roots; it is significantly transferred to and accumulated in the shoots. The nitrogen content remained at the control level in the roots, while it slightly (significant at p < 0.05) decreased in the shoots, regardless of the salinity level (27.17%). A significant increase in the P content in the roots was also not observed in the shoots, as shown by a gradual decrease in the P content of the shoots with an increasing salinity level (24.39% at 300 mM NaCl). Maintaining a relatively high N and P content in the shoots may restrict nutrient imbalances under salinity stress conditions. High salinity levels (200 and 300 mM) caused a significant decrease (of up to 13.18%) in the root K+ content, which was more prominent in the aerial parts at up to 33.05% at the highest NaCl level. Like the values of K+ in the shoots, the K+/Na+ ratio was significantly reduced in the NaCl-treated plants, with minor differences at the different NaCl concentrations.
Unlike K+, salinity exposure leads to different responses in other cationic minerals like Mg+2 and Ca+2. The magnesium content in the roots remained at the control level with the highest NaCl concentration, yet it slightly increased in both the 100 and 200 mM NaCl conditions. Salt stress can affect Mg+2 uptake and content, which in turn can indirectly impact the levels of chlorophyll and other photosynthetic pigments. However, if the Mg+2 levels in plants are maintained, the structural integrity of chlorophyll and other pigments can be preserved [39,40]. The magnesium content of the shoots showed a very distinct pattern in comparison to the K+ content; it profoundly increased by up to 30.76% with an increasing salinity level compared to the control. However, a decline in the Mg+2/Na+ ratio exhibited similar patterns as the K+/Na+ ratio. The discrepancy between the exact value of the mineral nutrients and cation/Na+ ratios reflects the importance of Na+ dominance to the occupation of cation channels. Among the cation/Na+ ratios in aerial tissue, the highest reduction rate was found for K+. Facultative halophytes can balance the Na+/K+ ratio under salt stress. They can compartmentalize Na+ in vacuoles and distribute K+ effectively [10].
The calcium content in the roots reduced with an increasing salinity level, whereas the shoots exhibited the opposite profile, with a substantial increase in the Ca+2 content under severe salinity conditions. The Ca+2 content of C. maritimum shoots increased by 7.8 and 15.89% after exposure to 200 and 300 mM NaCl, respectively. The Ca+2 content of C. maritimum roots decreased by 39%, 50%, and 78.38% after exposure to 100, 200, and 300 mM NaCl, respectively.
In contrast to our findings, the researchers in [35] reported a lower leaf Ca+2 content for C. maritimum in their 150 mM NaCl treatment when compared to the control. Other studies have also reported a low Ca+2 content in the shoots of plants under salinity stress [41,42].
To the best of our knowledge, the selective transfer of Ca+2, which was indicated by the inverse relationship of the Ca+2 content between the roots and shoots, was not significant to the salinity tolerance of Critimum maritimum. This may be attributed to the importance of high Ca+2 accumulation in the shoots for the stimulation of the salt tolerance signal transduction pathway of Critmum maritimum. The Ca+2 content of sea fennel was first reported in [43]. In this comparative study of the nutritional value of some halophytes, the researchers reported that the Ca+2 concentration (8.5 mg kg−1, fresh weight) of sea fennel was much higher than the other halophytes in the study. The significant differences between halophyte plants in terms of Ca+2 content may be a critical factor limiting plant growth. Consequently, an increase in the Ca+2 content could be one of the most dependable factors contributing to the salinity tolerance of Critimum maritimum. As a strategic response to manage salt-affected agricultural ecosystems, the addition of Ca+2 to soils could significantly alleviate the dysfunctions induced by salt stress in plants (Figure 5).
Salinity exposure caused an increase in the Fe, Mn, and Cu micro-nutrients in the roots of C. maritimum. The highest value was found for Fe of up to 38.59 in the 200 mM NaCl treatment. As in the roots, the Fe, Mn, and Cu micro-nutrients increased in the shoots, with the highest content measured in the 200 mM NaCl group. However, the slight changes in Cu content in the shoots were not statistically significant. The only exception among the studied micro-nutrients was Zn; while the Zn content of the roots slightly decreased, the reduction rate of the Zn content in the shoots reached 60.49% in the 300 mM NaCl treatment (Table 4).
Micro-nutrients such as Mn, Fe, Zn, and Cu play various roles in managing salt stress in plants. Salt stress can inhibit the uptake of micro-nutrients such as Fe and Zn in plants [39]. This can affect the synthesis of photosynthetic pigments and overall plant health. Their roles include reducing ion toxicity, maintaining water balance, enhancing nutrient uptake and assimilation, and reducing oxidative stress. In this context, we observed that increased salinity particularly reduced Zn uptake in Crithmum maritimum. Increased salt stress also negatively impacts the synthesis of photosynthetic pigments [12,44]. Plants can develop various adaptation strategies and mechanisms to increase Fe uptake under salt stress conditions [39]. Therefore, it is important to conduct comprehensive studies to identify the adaptation strategies of Crithmum maritimum in relation to Fe uptake.

3.4. Osmotic Homeostasis: Proline and Glycine Betaine Accumulation

The proline content of C. maritimum leaves decreased by 58.82% after exposure to 100 mM NaCl. It increased by 316.12 and 214.25% after exposure to 200 and 300 mM NaCl, respectively, in comparison to the control plants (Figure 6A). Glycine betaine (GB) is a quaternary ammonium compound which accelerates the recovery of photosystem II from photoinactivation [45]. This osmolyte may also stimulate a H2O2-dependent increase in both the expression and the activity of antioxidant enzymes [46]. The osmolyte GB content was significantly elevated due to increased NaCl (200 and 300 mM) by around 101.41 and 123.64%, respectively, in comparison to the 100 mM NaCl plants (Figure 6B). The findings indicated that the threshold value was a 200 mM NaCl concentration, at which C. maritimum triggers response mechanisms like osmolyte accumulation. Under highly saline environments, the plant appears to act as an osmotic adjuster, and 200 and 300 mM saline applications trigger osmolyte proline build-up in the plant as a defense reaction. Parallel to our results, the researchers in [47] showed that C. maritimum had higher levels of proline accumulation at a higher salt concentration (300 mM) in comparison to 100 mM NaCl, indicating an effective osmotic adjustment mechanism of the plant against increasing salt levels in the soil. Gradual increases in GB levels may indicate that this osmolyte is one of the basic contributors to osmotic adjustment, along with proline, to overcome salinity stress. The impact of the GB level on the osmoprotection of C. maritimum leaves was also reported in [38].

3.5. Redox Homeostasis: Antioxidant Enzymes and Antiradical Activity

Antioxidant enzymes (SOD, CAT, and POX) are the main defense enzymes against oxidative stress. The enzyme activities in C. maritimum leaves remained almost the same in the 100 mM NaCl treatment; however, a slight reduction was found in peroxidase activity (37.63%) in the leaves in comparison to the control plant leaves. In contrast to the low-concentration salt treatment, the 200 mM salt treatment substantially reduced the activities of SOD, CAT, and POX by 28.95, 45.45, and 54.37%, respectively (Figure 7). A severe salinity stress impact was observed in the 300 mM NaCl treatment, which caused an increase in the antioxidant enzyme activities by 112.91% for SOD, 63.64% for CAT, and 69.97% for POX.
The direct impacts of salinity often lead to a variety of secondary effects, including oxidative stress. This is marked by the build-up of reactive oxygen species (ROS), such as H2O2, O2−, and OH−, which can potentially damage lipids, proteins, and nucleic acids [48]. To mitigate the harmful effects of ROS, plants produce antioxidative enzymes like superoxide dismutase, catalases, and peroxidases, which enhance ROS detoxification. The increase in antioxidant enzyme activities is regarded as a basic regulation process in salinity tolerance. C. maritimum plants can invoke their antioxidant defense mechanism under high saline concentrations to avoid oxidative stress damage to the cells.
The SOD enzyme may limit the activation of other antioxidant enzymes due to scavenging the superoxide radicals and the precursors of most ROS. Salinity stress results in the production of superoxide anions via the Mehler reaction in chloroplasts, and over-reduction of the ubiquinone pool in the mitochondria [49]. Superoxide anions are converted to H2O2 by catalase and peroxidases. Among the antioxidant enzymes, superoxide dismutase (SOD) exhibits a higher level of activity in halophytes compared with glycophyte plants [50].
The researchers in [14] found declines in the SOD, CAT, and POX activities of C. maritimum under the highest salinity level (200 mM) in their study, which was consistent with our data. However, our data showed that an increasing salt concentration in the soil (300 mM) stimulated antioxidant defense mechanisms by enhancing the activities of all three enzymes. Similar results were reported for higher catalase activity in 256–427 mM NaCl treatments than in the control plants of Critimum maritimum [38]. The induced antioxidant enzyme activities, in company with antiradical activity and osmolyte accumulation at the highest NaCl concentration, may be considered part of the enhanced salinity tolerance of the plant.
The antiradical activity of C. maritimum leaves showed a similar trend in antioxidant enzyme activities. However, increasing NaCl concentrations increased the antiradical potential of the leaves by around 73.43 and 101.41% after exposure to 200 and 300 mM NaCl, respectively, in comparison to the control. After the threshold value of 100 mM, we can hypothesize that high salinity stress activates several antioxidant chemicals in C. maritimum, especially phenols and/or flavonoids. In accordance with our results, the strong antioxidant and/or antiradical capacity of C. maritimum leaves has been reported for various ecotypes in previous studies [7,34,51], suggesting that it is based on the high phenolic content of the plant.
Halophytes are plants that can grow in marginal soils, where other crop plants cannot be grown. However, to ensure their sustainable production, the correct growing systems must be chosen. Our results showed that the plant activates different components of tolerance mechanisms based on salinity thresholds. At a 200 mM NaCl concentration, osmoregulation is activated by accumulating proline and glycine betaine to cope with water uptake restriction and metabolic disorders. Depending on the increasing salinity (>200 mM), while the Na concentration in the roots increases, growth continues. However, there is a C. maritimum sustainable production potential, especially in places affected by soil infertility, with a salt content of up to 200 mM. Our findings showed that ambient temperature particularly influences growth performance, but increased salinity also has an effect on plant growth and defense components. It is recommended that genotype differences in terms of the response to salinity should be evaluated to determine their usability as a functional production model and/or alternative product for certain locations with saline conditions.

4. Conclusions

The ability of C. maritimum to maintain ionic, osmotic, and redox homeostasis makes it a promising alternative crop for cultivation in salt-affected soils, with significant promise for contributing to sustainable agricultural practices. As a halophytic plant, C. maritimum could be an excellent candidate for the implementation of a circular halophyte mixed farming system relying on the selective transfer of ions from the roots to the shoots. It is recommended that future research should focus on the development of mixed farming systems which integrate C. maritimum with other crops. Such systems could explore the synergistic benefits of using halophytes in crop rotation or intercropping systems, with the aim of improving soil health and productivity. This approach could be employed for the desalination or enhancement of saline regions.

Author Contributions

Conceptualization, B.C.E. and L.Y.A.; methodology, B.C.E., M.T.E. and L.Y.A.; validation, B.C.E. and L.Y.A.; formal analysis, T.O. and B.C.E.; investigation, M.T.E.; resources, Y.K.; data curation, B.C.E., L.Y.A. and C.C.K.; writing—original draft preparation, B.C.E. and L.Y.A.; writing—review and editing, B.C.E., L.Y.A., M.T.E. and T.O; visualization, T.O. and L.Y.A.; supervision, Y.K. and C.C.K.; project administration, Y.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data reported in manuscript are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Analysis of 123 articles on Crithmum maritimum published between 2014 and 2024 based on subject headings from WOS database.
Figure 1. Analysis of 123 articles on Crithmum maritimum published between 2014 and 2024 based on subject headings from WOS database.
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Figure 2. Distribution of Crithmum maritimum populations across the study area, highlighting the Aegean Sea coast at Ahmetbeyli, Menderes, Izmir, Türkiye.
Figure 2. Distribution of Crithmum maritimum populations across the study area, highlighting the Aegean Sea coast at Ahmetbeyli, Menderes, Izmir, Türkiye.
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Figure 3. Growth phenotype of Crithmum maritimum under 300 mM NaCl stress for 5 months.
Figure 3. Growth phenotype of Crithmum maritimum under 300 mM NaCl stress for 5 months.
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Figure 4. Effects of salinity on total chlorophyll and carotenoid contents of Crithmum maritimum treated with 0 (control), 100, 200, and 300 mM NaCl for 5 months. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
Figure 4. Effects of salinity on total chlorophyll and carotenoid contents of Crithmum maritimum treated with 0 (control), 100, 200, and 300 mM NaCl for 5 months. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
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Figure 5. Effect of different salt treatments on Ca+2 content of Crithmum maritimum shoots and roots. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
Figure 5. Effect of different salt treatments on Ca+2 content of Crithmum maritimum shoots and roots. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
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Figure 6. Effect of different salt treatments on proline (A) and glycine betaine (B) contents of C. maritimum leaves. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
Figure 6. Effect of different salt treatments on proline (A) and glycine betaine (B) contents of C. maritimum leaves. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
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Figure 7. Effect of different salt treatments on antioxidant enzyme activities (SOD (A), CAT (B), POX (C)) and antiradical activity (D) of Crithmum maritimum leaves. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
Figure 7. Effect of different salt treatments on antioxidant enzyme activities (SOD (A), CAT (B), POX (C)) and antiradical activity (D) of Crithmum maritimum leaves. Values are expressed as means standard deviation; different letters represent significant differences at p < 0.05, as per the results of the LSD test.
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Table 1. Physical and chemical properties of the soil used in the pot experiment.
Table 1. Physical and chemical properties of the soil used in the pot experiment.
TexturepHEC
µS/cm		CaCO3NtotalOM
%
Sandy loam6.9410153.320.0221.48
Available (mg kg−1)
PKNaCaMgFeZnMnCu
8.4025027672110313.404.340.60
Table 2. Effects of salt stress on some growth parameters of Crithmum maritimum.
Table 2. Effects of salt stress on some growth parameters of Crithmum maritimum.
NaCl
(mM)		Shoot Length
(cm)		Root Length
(cm)		Shoot/Root Length RatioFresh Shoot Biomass (g)Fresh Root Biomass (g)Shoot/Root Biomass Ratio
023.00 a*32.00 a0.71 a18.74 a5.20 a3.60 c
10021.30 b35.67 a0.59 b16.76 b5.21 a3.21 c
20019.30 c18.00 b1.10 c19.68 a5.07 a3.88 b
30014.30 d13.00 c1.10 c11.31 c2.54 b4.45 a
SD3.6110.070.243.501.190.52
LSD0.051.293.700.031.970.340.25
* p < 0.05: Means in the same column followed by different letters are significantly different.
Table 3. Effects of salt treatments on leaf and root macro-nutrients of Crithmum maritimum.
Table 3. Effects of salt treatments on leaf and root macro-nutrients of Crithmum maritimum.
NaCl
(mM)		N (%)P (%)K (%)Mg (%)Ca (%)Na (%)
RootShootRootShootRootShootRootShootRootShootRootShoot
02.775.29 a*0.22 b0.41 a1.82 b3.63 a0.51 b0.39 c0.074 a0.86 c0.16 d0.29 d
1002.974.82 b0.27 a0.37 a1.89 a2.97 b0.59 a0.46 b0.045 b0.84 c0.27 c0.63 c
2003.194.26 c0.28 a0.31 b1.74 c2.64 c0.58 a0.51 a0.037 c0.93 b0.33 b0.78 b
3002.834.17 c0.26 a0.31 b1.58 d2.43 d0.51 b0.48 ab0.016 d1.00 a0.39 a0.97 a
SD0.2050.1520.0140.0270.020.0440.0030.020.0170.0220.0230.03
LSD0.050.438 ** 0.3660.0300.0490.0460.0930.0400.0530.0060.0250.0490.063
* p < 0.05: Means in the same column followed by different letters are significantly different. ** Not significant.
Table 4. Effects of salt treatments on root and shoot micro-nutrients of Crithmum maritimum.
Table 4. Effects of salt treatments on root and shoot micro-nutrients of Crithmum maritimum.
NaCl
(mM)		Fe (mg kg−1)Mn (mg kg−1)Zn (mg kg−1)Cu (mg kg−1)
RootShootRootShootRootShootRootShoot
0285 d*125 b18 b33 c4.10 a10.81 a6.35 c6.65
100429 a116 b19 ab32 c3.70 ab7.20 c7.70 a6.10
200395 b148 a21 a46 a3.27 b8.87 b7.20 ab7.59
300376 c123 b20 ab37 b3.89 a4.27 d6.80 bc5.74
SD4.794.51.41.70.230.500.370.24
LSD0.0510.589.523.143.960.571.370.720.59
* Different letters represent significant differences at p < 0.05, as per the results of the LSD test.
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Colak Esetlili, B.; Yildiz Aktas, L.; Esetlili, M.T.; Oztekin, T.; Kılıc, C.C.; Kurucu, Y. Salinity Tolerance Mechanism of Crithmum maritimum L.: Implications for Sustainable Agriculture in Saline Soils. Sustainability 2024, 16, 8165. https://doi.org/10.3390/su16188165

AMA Style

Colak Esetlili B, Yildiz Aktas L, Esetlili MT, Oztekin T, Kılıc CC, Kurucu Y. Salinity Tolerance Mechanism of Crithmum maritimum L.: Implications for Sustainable Agriculture in Saline Soils. Sustainability. 2024; 16(18):8165. https://doi.org/10.3390/su16188165

Chicago/Turabian Style

Colak Esetlili, Bihter, Lale Yildiz Aktas, M. Tolga Esetlili, Tugba Oztekin, Cenk Ceyhun Kılıc, and Yusuf Kurucu. 2024. "Salinity Tolerance Mechanism of Crithmum maritimum L.: Implications for Sustainable Agriculture in Saline Soils" Sustainability 16, no. 18: 8165. https://doi.org/10.3390/su16188165

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