1. Introduction
Soil salinization is known to be one of the long-term impacts of major tsunamis, such as the 2004 Indian Ocean tsunami in Indonesia [1] and the 2011 Tohoku-oki tsunami in Japan [2]. The increase in soil salinity following a tsunami affects crop production for several years, even after several hundred millimeters of rainfall has occurred to leach out the salts [1]. Saltwater damage to agricultural lands was so severe that crops could not be grown on large parts of the tsunami-inundated farmland even two years after the disaster [2]. Actionable strategies to reduce the impact of seasalt on crop production are required to ensure sustainable food production worldwide [3].
Soil salinization is not only caused by tsunamis but is also driven by global climate change, which has significantly impacted the salinization of agricultural lands, particularly in arid, semi-arid, and coastal areas [4]. Salinity-induced yield losses due to land degradation have substantial economic impacts on agriculture, raising food security concerns [5], with an estimated economic cost reaching up to USD 27 billion per year [6]. Nearly half of the agricultural land available worldwide is located in arid or semi-arid regions, and 108 million hectares out of the 1.4 billion hectares of agricultural lands are affected by excessive salt concentrations [7].
In Bangladesh, the area of saline soil increased from 1% to 33% between 1990 and 2015, primarily due to seawater intrusion in coastal areas [8]. Global climate change may accelerate saltwater intrusion into fertile soils as a result of sea level rise, and excessive groundwater extraction in dry regions could also increase soil and groundwater salinity. It is estimated that about 600 million people living in coastal zones around the world could be affected by salinization [9].
Research in basic biology aimed at elucidating the mechanisms of salt tolerance in plants has long been conducted with model plants, using multiple approaches, including physiology [10], genomics [11], and molecular breeding [10]. Although our understanding of Na+-induced plant adaptive responses at the molecular level has greatly advanced [10], unfortunately, such efforts are not yet readily applicable to practical agriculture in the field.
Plants of the Vigna genus hold significant agricultural importance, particularly in Asia. The most well-known species in this genus include Vigna radiata (mung bean), Vigna unguiculata (cowpea or black-eyed pea), and Vigna angularis (adzuki bean). These legume crops offer a range of benefits for sustainable agriculture and food security [12]. They are a valuable source of plant-based protein, which is critical in regions where meat and dairy consumption is low. Mung beans and cowpeas, in particular, contribute significantly to the diet in many countries, helping to address malnutrition [13,14].
Vigna plants have the ability to fix atmospheric nitrogen through a symbiotic relationship with nitrogen-fixing Rhizobium bacteria in their root nodules. This nitrogen fixation enriches the soil with nitrogen, reducing the need for synthetic fertilizers and promoting sustainable crop rotation practices [15,16]. Growing Vigna species as part of a crop rotation system helps improve soil fertility and supports the health of subsequent crops [17].
Despite their agricultural significance, these Vigna plants cannot be cultivated in salinized soil regions due to their classification as glycophytes sensitive to salt stress [16]. Numerous studies have shown that the germination and growth of V. radiata are severely hindered by salt stress, with experimental evidence demonstrating such effects at 200 mM NaCl [18,19]. Under these conditions, various physiological and biochemical parameters indicate significant damage to the plants [18,19,20]. Although differences in salt stress sensitivity have been observed among varieties and genotypes [21,22], no salt-tolerant V. radiata species capable of thriving under conditions equivalent to seawater (~600 mM NaCl) has been reported to date.
Vigna marina, referred to as the wild beach bean [23], beach cowpea [24], or dune bean [25], naturally grows in coastal areas across tropical and subtropical regions in the Pan-Pacific [25] and Africa [26]. Its natural habitat in seawater-front areas has made the high salt tolerance of V. marina a topic of significant interest in plant research. In laboratory studies, the salt tolerance of V. marina has primarily been evaluated using NaCl solutions. However, its tolerance to seawater—a critical aspect of foundational knowledge for practical applications—has not yet been experimentally demonstrated. This study aims to highlight the remarkable seawater tolerance of V. marina through side-by-side comparative experiments with V. radiata and V. angularis as negative reference species. The findings establish V. marina as a highly seawater-tolerant Vigna species, positioning it as a promising candidate for addressing crop production challenges caused by soil salinization resulting from seawater intrusion in agricultural lands.
2. Materials and Methods
2.1. Plant Materials
The seeds of Vigna marina were collected from sandy beaches on Okinawa Island, a subtropical coral island in Japan. After collection, the seeds were separated from the pods, sorted, and air-dried. The seeds were selected based on specific criteria: uniform size, color, and collection date. The selected seeds were stored in a desiccator at room temperature. For seed sterilization, 2.5 mL of sodium hypochlorite was diluted in 25 mL of sterile distilled water and then mixed with 0.1% Tween 20. The seeds were immersed in this sterilization solution for 5 min. After sterilization, the solution was removed, and the seeds were rinsed three times with sterile distilled water. The seeds of Vigna radiata and Vigna angularis were purchased from a commercial supplier.
2.2. Seed Floating Experiments
Due to the natural variability in seawater composition caused by geographical, physical, and biological factors, artificial seawater was used as the experimental medium to ensure consistency and reproducibility in the experiments. The seeds of V. marina, V. radiata, and V. angularis were incubated in aquarium tanks containing 9 L of artificial seawater (Japan Bio-Chemicals, Tokyo, Japan) for one month. The room and water temperatures were both maintained at 26 °C. The light intensity was set to 50 μmol m−2 s−1, with a 12 h photoperiod. The seeds were incubated for durations of 1, 2, 3, 4, 5, 6, 7, 14, and 30 days, with untreated seeds serving as the control. A total of 1000 seeds were used for each species.
2.3. Seed Germination Experiments
To break the dormancy of V. marina seeds, a pinhole was made to create a tiny pore in each seed. The treated seeds were then transferred to Petri dishes containing a single sheet of Whatman No. 1 filter paper moistened with 10 mL of sterilized distilled water. The seeds were incubated in a growth chamber with a light intensity of 50 μmol m−2 s−1 and a 12 h photoperiod at 25 °C. The number of germinated seeds was recorded daily, and the final germination percentage was calculated after 7 days. Three replicates were used in these experiments. The germination of seeds of V. marina (with pores), V. radiata, and V. angularis was used for comparison.
2.4. Seedling Growth Experiments
The seeds of the three legumes were sterilized with the solution described above and germinated in Petri dishes containing a single sheet of Whatman No. 1 filter paper moistened with 10 mL of distilled water for 48 h. The germinated seeds were transferred to plastic pots (5.5 cm in diameter) filled with 240 g of sand and watered daily with 20% Hoagland’s solution. After two leaves had fully expanded, healthy seedlings of similar size were transferred to new plastic pots (one seedling per pot) containing 240 g of sand.
The seedlings were incubated in a growth chamber under non-photoinhibitory light intensity (35 μmol m−2 s−1), a 12 h photoperiod, and a temperature of 25 °C. Relative humidity was maintained at 80% to prevent excessive evaporation from the medium.
The seedlings were watered daily with equal amounts of 100% artificial seawater (Japan Bio-Chemicals). Since artificial seawater does not contain nitrate ions, 0.2 mM sodium nitrate was added to simulate coastal seawater and provide a nitrogen source for plant growth. After harvesting, the plants were washed with distilled water and air-dried for 10 min. The seedlings were then separated into leaves, stems, and roots, and their fresh weights were measured. Dry weights were determined after drying each part at 80 °C for 48 h.
2.5. Chlorophyll a Fluorescence Measurement
Seedlings with two fully expanded leaves were used to monitor photosynthetic activity during seawater irrigation treatment. The effects of seawater irrigation on photosynthetic activity were assessed using the maximum quantum yield of Photosystem II (Fv/Fm), which was quantified with a FluorCam 700 MF imaging fluorometer (Photon Systems Instruments, Drásov, Czech Republic) as previously described [27]. Prior to chlorophyll fluorescence measurements, the plants were dark-adapted for 15 min. Measurements were taken daily for up to 7 days during the seawater irrigation treatment.
3. Results
3.1. Natural Habitat of Vigna marina
Vigna marina (Burm.) Merrill, also known as marine bean, beach pea, coastal cowpea, or dune bean, is a pan-tropical coastal legume widely distributed across northeastern Australia [28], India [29], Africa [26], Southeast Asia [30], and the Ryukyu Archipelago, including Okinawa, Japan [31]. Figure 1A shows a typical natural habitat of V. marina in Okinawa. V. marina forms colonies on sandy beaches near the shoreline. Generally, V. marina communities are located closest to the sea among native coastal plants, where seawater washes the coastal sands (Figure 1B), creating an oligotrophic or nitrogen-poor environment.
In Okinawa, V. marina flowers and bears seeds throughout the year (Figure 1C), but the peak blooming period occurs during the rainy season in June. As a leguminous plant, V. marina develops root nodules (Figure 1D,E) that harbor nitrogen-fixing bacteria along with leghemoglobin (Figure 1F). In polluted or eutrophic areas, these nodules are rarely found, and other non-nitrogen-fixing coastal plant species, such as Ipomoea gracilis, tend to dominate the habitat. Therefore, the presence of V. marina with root nodules in the field can serve as an indicator of a clean and oligotrophic environment.
3.2. Seawater Tolerance of Seeds
V. marina is a pan-tropical coastal plant known for its sea-dispersal capability [31]. Remarkably, the seeds of V. marina have been recorded to float in saltwater for up to 25 years while retaining their germination ability [25]. Figure 2 compares the seawater tolerance of seeds from three Vigna species: V. marina, V. radiata, and V. angularis. Although their morphology and size are similar (Figure 2A), there is a significant difference in the air space within the seeds. The seeds of V. marina, encased in a thick seed coat, form a large central cavity (Figure 2B). The large air space likely contributes to the buoyancy of V. marina seeds in seawater (Figure 2C). In contrast, the seeds of V. radiata and V. angularis are not buoyant and sank immediately to the bottom of the seawater tank (Figure 2D,E).
Most V. marina seeds maintained buoyancy for a long time in seawater (Figure 3A). Even after long immersion, such as for 30 days, V. marina exhibited 100% germination (Figure 3B,C). In contrast, the germination ability of V. radiata and V. angularis decreased with prolonged seawater immersion (Figure 3B). This confirms that the seeds of V. marina are extremely tolerant to long-term exposure to seawater. With its high buoyancy and conserved germination capacity after long-term seawater immersion, Vigna marina can achieve a wide distribution through ocean current seed dispersal, a significant characteristic of sea-dispersed species [31,32].
3.3. Seawater Tolerance of Seedlings
Figure 4 compares the seawater tolerance of seedlings from three Vigna species. V. radiata and V. angularis were susceptible to watering with seawater. Even on the first day, symptoms of damage were observed in their leaves and stems (Figure 4). In contrast, V. marina was unaffected by seawater. This was confirmed by monitoring their fresh and dry weights during cultivation (Figure 5). The increase in both fresh and dry weights indicated that V. marina continued to grow even with seawater supplementation. In contrast, both V. radiata and V. angularis showed a decrease in both fresh and dry weights with extended seawater treatment, presumably due to dehydration and degradation leading to death. Similar trends were observed with high concentrations of cations and anions (Figures S1 and S2), supporting significant tolerance of salt stress of V. marina.
3.4. Seawater Tolerance of Photosynthetic Activity
The results in Figure 5 indicate that V. marina can grow even in the presence of seawater. To verify its photosynthetic growth, we investigated changes in the photosynthetic activity of leaves among V. marina, V. radiata, and V. angularis. Pulsed amplitude modulation (PAM) chlorophyll a fluorescence measurement is a non-destructive method for monitoring the photosynthetic activity of intact plants. The quantum yield of Photosystem II, which is reflected in the chlorophyll a fluorescence parameter Fv/Fm, has been widely used to evaluate physiological damage to photosynthesis under various environmental stresses. Figure 6 compares the Fv/Fm values of the three Vigna species during seawater treatment. Consistent with plant growth (Figure 5), Fv/Fm did not change in V. marina, whereas it decreased in both V. radiata and V. angularis with extended days of seawater treatment. The photosynthetic measurements also confirm that V. marina is extremely tolerant to seawater.
4. Discussion
4.1. V. marina as a Seawater-Tolerant Legume Plant
Focusing on agriculture in areas affected by seawater intrusion, we have demonstrated the seawater tolerance of seeds, germination, growth, and photosynthesis in V. marina through a side-by-side comparison with V. radiata and V. angularis. The results clearly indicate that V. marina is a highly seawater-tolerant Vigna species, consistent with expectations based on its natural habitat (Figure 1) and supported by previous studies using NaCl solutions [25,28,30,31,33,34,35].
Maintaining photosynthetic activity is a key indicator of tolerance or resistance to abiotic and environmental stresses in plants [36]. The chlorophyll a fluorescence parameter Fv/Fm, which represents the ratio of variable-to-maximum fluorescence after dark adaptation, is widely used to assess the maximum quantum yield of Photosystem II (PSII) [37,38,39]. This parameter is particularly valuable for evaluating the integrity of the photosynthetic machinery under stress conditions [37], including NaCl stress [40,41].
Figure 6 clearly illustrates that the photosynthetic activity of V. marina remains unaffected by seawater, whereas V. radiata and V. angularis exhibit significant damage under the same conditions. The observed resistance in V. marina, as indicated by Fv/Fm, aligns with recent studies utilizing Y(II)—a measure of the actual quantum yield of PSII under light-adapted conditions—which reported NaCl tolerance in V. marina at concentrations up to 200 mM [35]. Therefore, it can be concluded that the photosynthetic machinery of V. marina demonstrates high seawater tolerance.
4.2. Difference Between NaCl and Seawater Tolerance
In plant science, the terms salt tolerance [42], salinity tolerance [11,43], NaCl tolerance [44], and seawater tolerance (this study) are often used synonymously to describe a plant’s ability to survive and grow under high salt content. However, these terms carry different connotations depending on the types and composition of salts involved, as well as the specific environmental conditions [44,45].
To simulate seawater conditions, solutions of NaCl at concentrations of 600 mM (full-strength seawater), 300 mM (half-strength), or 200 mM (one-third strength) are often applied to assess salt stress tolerance in plant [35]. Halophytes—plants adapted to saline environments—are experimentally distinguished from glycophytes (salt-sensitive plants) primarily by their tolerance to NaCl [46]. It is important to note that in addition to NaCl, seawater contains high concentrations of sulfate ions (SO42−), the second most abundant anion in seawater, after Cl−, approximately at 30 mM [47,48]. This adds complexity to seawater stress, as plants must manage not only Na+ and Cl− ions but also SO42−.
On land, sulfur is supplied through rainfall containing sulfurous compounds from oceans or volcanic activity [49]. Generally, sulfur availability is limited in inland soils, requiring plants to actively take up sulfur using specialized sulfate transporters (SULTRs) that mediate H+ and SO42− co-transport [50]. Sulfur-containing fertilizers, along with nitrogen fertilizers, are therefore crucial for crop production, with much of the research emphasis placed on sulfur deficiency [51]. Recent studies suggest that, in addition to reactive oxygen species (ROS), which are involved in salt-induced plant damage [11,52,53,54], reactive nitrogen species (RNS) and reactive sulfur species (RSS) also play roles in cellular damage and intercellular signaling in plants and other organisms [11,55]. While small amounts of these reactive molecules act as signaling agents, their excessive accumulation can cause cellular damage or death [55]. In plants, the toxic gas hydrogen sulfide (H2S), a primary source for RSS, can be generated from SO42− during sulfur assimilation in chloroplasts [49].
Sulfur toxicity has historically been overlooked in agricultural research, as sulfur is considered an essential nutrient for crop production. However, in addition to NaCl tolerance, seawater tolerance may also require the ability to cope with high concentrations of sulfate ions, a significant source of potentially cytotoxic RSS. Further research focusing not only on NaCl tolerance but also on tolerance to sulfur toxicity is needed to uncover the molecular mechanisms underlying the seawater tolerance of V. marina.
4.3. V. marina as a Strong Candidate for Addressing Crop Production Challenges
V. marina demonstrates significant potential as a candidate for addressing crop production challenges [30,56], particularly in environments affected by seawater intrusion, such as those impacted by tsunami disasters. In addition to its resilience to salt stress, V. marina exhibits strong tolerance to heat and drought in hot, sandy beach environments, making it broadly suitable for regions facing multiple abiotic stresses.
Adaptability breeding is essential for developing cultivars suited to diverse climates. Recent insights from its draft genome sequence and identified quantitative trait loci (QTLs) provide valuable information to guide future breeding efforts [29]. Due to its ocean current-driven seed dispersal ability, the wild species of V. marina may have adapted to diverse local environments, resulting in high genetic diversity [28,56]. Further surveys of this wild species across tropical and subtropical coastal areas are needed to explore its genetic variability [32,57,58]. Encouragingly, V. marina grows during the winter in subtropical Okinawa, where January, the coldest month, has an average minimum temperature of 15 °C. This suggests its potential for cultivation in temperate regions. In this context, V. marina, which has naturally adapted to a subtropical climate, is distinct from tropical wild species or subspecies and may serve as a unique platform for both conventional and molecular breeding approaches, as well as for genome editing technologies [5,52].
Conceptualization, H.Y.; investigation, A.S. and S.P.N.; writing—original draft preparation, A.S. and H.Y.; writing—review and editing, S.P.N. and R.F.N. All authors have read and agreed to the published version of the manuscript.
Not applicable.
The data presented in this study are available on request from the corresponding author.
We thank Shinya Hara, Yoshimitsu Shima, Yuko Ota, Michiyo Tokashiki, Wataru Akao, and Ji Dasol for their technical support.
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 1. Vigna marina growing in the field. (A) Overview of a V. marina habitat. (B) V. marina growing on the seashore with abundant coral skeletons. (C) Yellow flowers and mature bean pods. (D) A seedling growing in the field. (E) Root nodules. (F) Transverse section of the nodules showing reddish leghemoglobin.
Enlarge this image.Figure 2. Seeds of three Vigna species. (A) Seeds of V. marina, V. radiata, and V. angularis (from left to right). (B) Transverse sections of three Vigna species: V. marina, V. radiata, and V. angularis (from left to right). (C) Floating seeds of V. marina in a seawater tank. (D) Sunk seeds of V. radiata. (E) Sunk seeds of V. angularis.
Enlarge this image.Figure 3. Seawater tolerance of three Vigna species. (A) Floating test in seawater for the three Vigna species. (B) Germination ability of the three Vigna species after seawater treatment. (C) Photographs of the germination of V. marina after immersion in seawater for the indicated number of days. Bars represent SD (n = 3).
Enlarge this image.Figure 4. Effect of seawater supplementation on seedlings of three Vigna species. The seedlings were watered with seawater daily. The numbers indicated in the photos represent the number of days under treatment. White bars indicate a scale of 1 cm.
Enlarge this image.Figure 5. Changes in fresh and dry weight of seedlings from three Vigna species during seawater treatment. (A) Total fresh weight changes. (B) Total dry weight changes. Bars represent the standard deviation (SD), with n = 3.
Enlarge this image.Figure 6. Effects of seawater treatment on photosynthetic activity in three Vigna species. (A) Changes in Fv/Fm values in V. marina. (B) Changes in Fv/Fm values in V. radiata. (C) Changes in Fv/Fm values in V. angularis. White open circles indicate the Fv/Fm values of leaves from seedlings watered with distilled water. Colored filled circles represent the values from seedlings subjected to seawater treatment. In general, an Fv/Fm value near 0.8 serves a criterion for undamaged photosynthesis. A decrease in Fv/Fm suggests inhibition or impairment of photosynthesis. Bars represent SD (n = 3).
Supplementary Materials
The following supporting information can be downloaded at:
References
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