Next Article in Journal
Implementation of Mitigation Measures to Reduce Phosphorus Losses: The Vestre Vansjø Pilot Catchment
Next Article in Special Issue
Cereal Production Trends under Climate Change: Impacts and Adaptation Strategies in Southern Africa
Previous Article in Journal
Modified Over-the-Row Machine Harvesters to Improve Northern Highbush Blueberry Fresh Fruit Quality
Previous Article in Special Issue
Growth, Yield Performance and Quality Parameters of Three Early Flowering Chia (Salvia hispanica L.) Genotypes Cultivated in Southwestern Germany
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 9
Issue 1
10.3390/agriculture9010014
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Glassworts: From Wild Salt Marsh Species to Sustainable Edible Crops

by
Danilo Loconsole
*,
Giuseppe Cristiano
and
Barbara De Lucia
Department of Agro-Environmental and Territorial Science (DISAAT), University of Bari, “Aldo Moro”, Italy Via Amendola 165/A, 70120 Bari, Italy
*
Author to whom correspondence should be addressed.
Agriculture 2019, 9(1), 14; https://doi.org/10.3390/agriculture9010014
Submission received: 7 December 2018 / Revised: 31 December 2018 / Accepted: 2 January 2019 / Published: 8 January 2019
(This article belongs to the Special Issue Options for Agricultural Adaptation to Climate Change)
Browse Figures
Versions Notes

Abstract

:
Halophytes are naturally adapted in saline environments, where they benefit from the substantial amounts of salt in the growth media. The need for salt-tolerant crops increases as substantial percentages of cultivated land worldwide are affected by salinity. There are few protocols, guidelines, or trials for glasswort (Salicornia (L.) and Sarcocornia (Scott), belong to the Amaranthaceae) field cultivation. The high salt tolerance and content in bioactive compounds make glassworts one of the most important candidates for future use both for fresh and processed food, due to their functional and health properties. This review describes the glassworts respect to their biodiversity and the most important factors affecting propagation, salt tolerance traits, agro-techniques and yields, food uses and nutraceutical properties.

Graphical Abstract

1. Introduction

The depletion of natural resources due to human activity, global change, and the increasing population have led to a great reduction in arable lands along with salinization of the soil and unavailability of freshwater. Only cultivating conventional crops that have a low tolerance to salinity and drought is therefore not recommended in the future [1]; new sustainable crops, with low inputs and strong abiotic tolerance, are thus needed.
Halophytes need a high-salt soil composition to develop properly [2,3]; their salt tolerance is related mainly to the ability to control ion uptake and the vacuolar compartmentalization of Na+, K+, and Cl−, in order to maintain the osmotic balance between vacuoles and cytoplasm by the synthesis of osmotic active molecules [4,5].
Today edible halophytes are one of the most interesting groups of plants as they can be cultivated in marginal areas with seawater, or in saline areas near the sea, in beginning a potential cash crop [6].
Examples of edible halophytes include purslane (Portulaca oleracea L., [7]), marine fennel (Crithmum maritimum L., [8]), ice plants (Mesembryanthemum cristallinum L., [9]), Mediterranean saltworts (Salsola soda L., [10]), and glassworts (Salicornia (L.) and Sarcocornia (Scott), [11]).
This review describes the glassworts in respect to their biodiversity and the most important factors affecting propagation, salt resistance traits, agro-techniques and yields, food uses, and nutraceutical properties.
Glassworts: Salicornia (L.) and Sarcocornia (Scott) genus (Amaranthaceae, subfam. Salicornioideae), are divided into succulents which are annual, and edible halophytes which are perennial.
They are a difficult taxonomy because of the richness of the microspecies, subspecies, hybrids, and varieties. Kadereit et al. [12] found that Salicornia and Sarcocornia were separated from each other near the Middle Miocene (14.2–9.4 mya); however, actual lineages were diversified during the Early Pleistocene (1.4–1.8 mya).

2. Habitat and Apulian Biodiversity

Salicornia and Sarcocornia develop mainly in sandy or muddy saltmarshes that are flooded by the tide, in mudflats, sandflats, and sometimes in open saline areas. Salicornia is found around much of the coastline of Europe from the Arctic to the Mediterranean, as well as on the shores of both the Black Sea and Caspian Sea; it is also present sporadically where inland salines occur across Europe [13].
Annual Salicornia species have a much wider distribution than Sarcocornia in the Northern hemisphere and in South Africa. They are absent from South America and Australia [12]. Table 1 shows the origin of some species belonging to Salicornia and Sarcocornia genus [12,14,15,16].
In south of Italy (Apulia Region), S. europaea L., known as common sea asparagus, is a characteristic pioneer species of the association Thero-Salicornietea [17]; the brackish lakes of Lesina (Figure 1) and Varano (Foggia Province) are rich in this wild plant species, that colonize damp and brackish soils, flooded by the tide for most of the year and dry during the warmer seasons [18]. There are S. glauca Delile and Sarcocornia fruticosa (L.) A.J. Scott too.
In the south of Apulia, the “Torre Guaceto” coastal lagoon (Province of Brindisi—Figure 2) is a National Natural Reserve characterized by a wide number of halophyte plants; among these, Sarcocornia fruticose is one particular example. In the province of Taranto, “Salina dei monaci”, Sarcocornia sp. grows in globe-like shrubs (Figure 3). It is richly branched, with long sterile shoots (in the current year) and fertile shoots (from the previous year) with leaves small and green. In the Province of Lecce, “Le Cesine” another glasswort was found by [19] on cliffs, where the salinity is the same as the sea: Sarcocornia fruticosa L.

3. Morphological Characteristics

As glassworts are characterized by an extremely reduced morphology, they can grow prostrate, erect, or branched [13]. Figure 4a shows that the leaves are very small and the assimilatory surface is composed of succulent branches with cylindrical internodes [20]. Axillary buds on the main stem develop into primary branches which produce secondary ones [21]. Annual species are usually green, but in autumn, near the end of the cycle, the stems turn red. In Salicornia spp. flowers are aggregated in a dense terminal, spike-like thyrses composed of three flowers: one central and two lateral (Figure 4b). In Sarcocornia, these are placed in horizontal rows [12]. Glassworts differ from all other Amaranthaceae since the seeds that lack perisperm [22]. The Salicornia seed is small, ellipsoid, dark (Figure 4c) and is characterized by heteromorphism: i.e., seeds from the same plant have a difference in size, color, or shape [23]. In S. europaea L. there is a wide variation in size: 0.4–0.9 mm [24,25]. Heteromorphism is also widespread in Asteraceae and Amaranthaceae [26,27] and is the result of an adaptation to desert environments, because each seed morph germinates under different conditions [28,29,30,31].

4. Propagation

Propagation can be carried out by both gamic and agamic techniques.

4.1. Gamic Propagation

Halophytes usually inhabit extreme soil parameters. This implies that seeds need strategies in order to overcome these situations: dormancy under hypersaline conditions and germination at high salinity levels [32].
Dormancy starts during the late autumn and ends with seed germination of glassworts in late April–early May [33]. The main advantage of germination in early spring is the abundance of water which involves low salt concentrations, ideal for germination. S. europaea (L.) and Spergularia marina (L.) have two or more different seed morphs and each seed has a different dormancy and salt tolerance [25,34,35]. In fact, the lateral seeds of S. europaea (L.) are more dormant than the central seeds (which are more salt tolerant), in order to maintain a long-term soil seed bank [25]. Orlovsky et al. [36] found that the germination of large seeds was three to four times higher than small seeds in the control and under 0.5–2% salt (both NaCl and 2NaCl + KCl + CaCl2). This high dormancy typical of smaller seeds can be partly broken with chloride or sulfate salts (concentrations of 0.5 to 2%).
In order to overcome the dormancy period in specialized nurseries, seeds need to undergo a cold stratification: T = 5 °C for 30 days in the dark. Aghaleh et al. [37] and Lv et al. [38] reported that Salicornia seeds were exposed to sunlight and salinity using 30:70 or 50:50 seawater:freshwater. This phase ended in 14 days, leading to appropriate seedlings (Figure 4d).
The percentage and rate of germination decreased as salinity increased which is true for both seed morphs [36]. Although there is a greater success of germination under freshwater, halophytes can also germinate at high saline concentrations: for example, S. europaea can germinate at 600 mM NaCl [39,40].
Ungar [34] found that treatments with GA3, play an important role in overcoming salt stress-induced dormancy in Salicornia, Suaeda, and Spergularia.
Several authors have described the recommended environmental parameters of germination: T = 15–25 °C day/5–20 °C night (never under 5 °C and over 30 °C); light = 12–16 h day/8–12 h night [38,39]. The germination phase is not only affected by salt concentration, but also by the salt type: Orlovsky et al. [36] found that large seeds have a good germination under NaCl between 0.5 and 2%, Na2SO4 and 2NaCl + KCl + CaCl between 0.5 and 3%, and 2Na2SO4 + K2SO4 + MgSO4 between 0.5 and 5%. Small seeds are stimulated by chloride salts under 0.5–1%, and sulfate salts under 0.5–3%.

4.2. In Vitro Propagation

In vitro propagation of S. bigelovii and S. europaea was studied [41,42] but “in vitro” culture system of succulent halophytes was not very successful so far. Lee et al. [41] developed in vitro propagation of S. bigelovii using the shoot tip culture method but the regeneration rate was very low; however, Shi et al. [42] established a method of S. europaea regeneration from mature embryos. Tissue culture of succulent halophytes using a mature embryo is not promising because of the microscopic size and non-availability of explants throughout the year.
Joshi et al. [43] found that in Salicornia brachiata an efficient shoot proliferation was observed with combinations BA (8.9 μM) + NAA (5.37 μM) + NaCl (500 mM) and BA (13.3 μM) + NAA (5.37 μM) + NaCl (250 mM) indicating that NaCl is required for the micropropagation.

5. Cultivation

5.1. Growth

Glassworts, in North Apulia, are typically cultivated from February–March to August–September in the acidic marshes near the brackish lake of Lesina, Cagnano Varano, and San Nicandro Garganico in open fields [44]. In Israel, Salicornia is grown using nests or greenhouses in soil, floating systems or plastic sheets [45] with perlite, dune sand, coconut fiber, or a commercial substrate mixed with sand (1:1 v:v) [46]. Singh et al. [3] showed that production (fresh and dry biomass) of S. dolichostachya moss, in hydroponic cultivation, was higher than plants grown in sand media; on the other hand, hydroponic cultivation can lead to chlorosis events.
Gunning [45] reported that Salicornia plants were fertilized with a nutrient solution (30:50 or 50:50 seawater:freshwater) with a N:P:K = 14:10:27 to achieve high yields.
A notable amount of biomass for S. ramosissima woods was achieved using artificial seawater containing 257 mM NaCl [3]; on the other hand, Rozemaa et al. [47] found that growth was depressed at low salt concentrations. Regarding irrigation, Singh et al. [48] showed that cultivation of S. brachiata in a greenhouse using reverse osmosis reject water with and without fluorine ion could be a sustainable solution for reject water management.
The main problem related to wild species introduced to cultivation, is the prevalence of non-commercial characteristics due to genetic diversity, for example, production homogeneity. Besides breeding programmes, with plant growth promoting bacteria (PGPB) could be an alternative in order to increase production. Bashan et al. [49], found that S. bigelovii increase production (height and weight) when inoculated with some PGPB, i.e., Azospirillum halopraefrens; A. brasilense (two different strains); Vibrio aestuarianus + V. proteolyticus; Bacillus licheniformis + Phyllobacterium spp. It is worth underlining that the cultivation of Salicornia could be beneficial in order to increase soil fertility, due to the presence of rhizobacteria in its roots [50].
In Apulia, harvesting, in open field, takes place in July–August; in Israel in August–September, and it is carried out manually in order to maintain the high quality of the final product; only fresh and tender parts can be sold. Salicornia can be collected several times during the year in greenhouses: The harvest can be repeated every two or three weeks (depending on the level of development). Plants are cut above 5 cm from the ground at a height of 10–15 cm [51]. This repeated harvesting enables the same plant to be cut from three to four times depending on the level of growth. The yield can reach 10–15 tons per hectare.

5.2. Flowering

Under natural conditions, when the day length decreases, the reproductive phase of glassworts begins with a differentiation in terminal fruiting spikes [52]. The optimal day length is different for high latitude and short latitude plants: in fact, northern glassworts (S. europaea) need 18 or more hours to prevent flowering; for S. bigelovii, 13 h are enough [51]. Flowering induction has many negative effects on both the production (intense decrease in growth) and production of non-saleable shoots and nutraceutical properties [51]. For perennial Sarcocornia, flowering can be controlled with a repeating harvesting regime [51]. Based on the results of Ventura and Sagi [46], nutrition management can also be used for flowering control. The regulation of Mo and N-NO3 can prevent the reproductive stage, in fact, ammonium fertilization promotes flowering in S. bigelovii. In addition, the sowing date can be useful in preventing flowering: Seeds planted in November or December repress the reproductive stage; whereas, planting in January results in inhibition, because during the growing cycle, the day length increases [51].

5.3. Salinity Tolerance, Water Relations, and Gas Exchange

Glassworts are salt-tolerant species: Redondo-Gòmez et al. [21] showed that S. fruticosa has a considerable salt tolerance, compared with other halophytes, resulting in the greatest growth with 510 mM NaCl treatment. Similar results, regarding the optimal salt concentrations, have been achieved for different genotypes: for Salicornia persica Akhani, e.g., 200 mM NaCl [53]; 200 mM NaCl for S. brachiata [54]; 170–340 mM NaCl for S. europaea, S. bigelovii, S. herbacea, and S. brachystachya [55]. The photosynthetic apparatus of S. fruticosa also appears capable of tolerance prolonged high external salt exposure, suggesting plasticity.
The main salt tolerance responses of plants relate to an increased leaf thickness. Katschnig et al. [56] found that leaf succulence and diameter in S. dolichostachya were higher when plants were grown in 300 mM NaCl of nutrient solution compared to other treatments grown in from 0 to 500 mM NaCl. This is due to an increased accumulation of Na+ and Cl− ions in the vacuoles [57], which leads to a reduced leaf surface area and consequently an increased water use efficiency. In saline environments, in order to ensure the water uptake, a low water potential in the cells is needed [56]. Beside Na+ and Cl− ions, organic compounds such as glycine betaine are stored in the cytoplasm in order to guarantee a water potential equilibrium in the cells [58]. Organic solute as malate dehydrogenase can also act as an enzyme that stabilizes at high salt concentrations [59]. Jolivet et al. [60] also found that glycine betaine inhibits the betacyanins efflux when present in the external medium along with the oxalates. Glycine betaine is perhaps the main organic compound with osmoregulation properties for Salicornia spp. [61].
Another mechanism used to maintain a better water uptake is gas exchange regulation: Stomata conductance generally decreases for halophytes as a reaction to increasing salt concentrations. At high salt concentrations, as reported by Ayala and Oleary [62] for S. bigelovii, stomata conductance decreases, consequently the carbon dioxide fixation and transpiration rate also decrease, in order to obtain the best efficiency in terms of water use.

6. Bioactive Compounds

Halophytes can be used for many commercial purposes: Not only as fresh and processed foods, but also in terms of their high salt content, as biofuel, high nutritional oilseed, medical raw materials, as well as nutraceutical and functional foods [63,64].
Chenopodiaceae members are known to contain high amounts of crude proteins, sulfur, and minerals [65], which favor glasswort as an edible plant. Salicornia, developed in extremely saline environments, produces antioxidative metabolites, which are desirable in the human diet. Simple and complex sugars, alcohols, quaternary amino acid derivatives, tertiary amines, and sulfonium compounds are also useful for human nutrition, and are found on these plants [45].
Guil et al. [66] showed that sea asparagus has high levels of ascorbic and dehydroascorbic acids (more than 100 mg 100 g−1), as well as carotenoids (5 mg 100 g−1). S. bigelovii also show high content of β-carotene (15.9 mg 100 g−1 of fresh weight), and a high amount of vitamin A [67]. Both Salicornia and Sarcocornia showed a high content of polyphenols (1.2 and 2.0 mg GAE g−1 of fresh weight, respectively) [51]. Kang et al. [68] found that the freshwater cultivation of Salicornia had a higher phenolic and flavonoid content, than seawater cultivation.
Due to the specific biochemical composition of Salicornia seeds, they are very good for human health. The main molecules include linoleic (75.6%) and oleic acids (13.0%); in addition to palmitic, linoleic and stearic acids [63]. Proteomic analysis has also revealed a high protein content of the seeds [69]. Considering the main components, palmitic acid, tetracosanol, and octacosanol showed significant levels [70]. Octacosanol is a high-molecular-weight aliphatic alcohol and belongs to cholesterol-lowering drugs such as polycosanol [71].
In addition, the leaves of Salicornia are also a good source of fatty acids such as linoleic and oleic acids [72]. Finally, the presence of selenium has also been detected; which is an important micronutrient both for growth and has good antioxidant effects [73].
The Salicornia genus has antimicrobial, anti-tumor, antioxidant, and anti-inflammatory properties [74].
Abiotic stress, including salt stress, leads to the production of reactive oxygen species in the plants, which damage cellular membranes and enzymatic activity [75]; to combat salt-oxidative stress, antioxidative enzymes and small antioxidant molecules are produced. These molecules give medicinal properties to halophyte plants, which are used for several treatments for chronic disease, including diabetes, cancer [74]. Polysaccharides from S. herbacea at 0.5–4 mg mL−1 have been found to be antiproliferation of human colon cancer HT-29 [76]. Another study found that pentadecylferulate from S. herbacea has an antioxidant effect and, an anti-cancer response to human hepatocellular liver carcinoma HepG2 and human lung adenocarcinoma epithelial A549 cells [77]. The methanol extract of S. herbacea has shown antibacterial activities, mediated by interference with cytochrome and several enzymes [78]. Osteoporosis is a bone disorder, caused by a higher bone adipogenesis (differentiation of stem cells into mature adipocytes): S. herbacea extract has been found to inhibit adipogenesis [69].
Besides the health properties of Salicornia, there are also some negative aspects: Chenopodiaceae members are known to contain a high oxalate content, which could be harmful to consumers [65].

7. Food Uses

The edible parts of glassworts have tender leaves and shoots can be used in a fresh salad, or boiled like spinach without salt, and then coated with extra virgin olive oil (Figure 5). The color, after cooking, resembles seaweed, and the flavor and texture are similar to young spinach or asparagus. Sea asparagus is often used as an accompaniment to fish or seafood [45].
S. europaea L. is currently included in the list of traditional Apulian vegetables.
In Hawaii, it is often blanched and used as a topping for salads or as an accompaniment for fish [79]. The seeds of S. bigelovii can be used to make edible oil; however, it is not always edible because it contains saponins, which can be toxic. S. brachiata is used as fodder for cattle, sheep, and goats [80]. In Sri Lanka, it is used to feed donkeys [81].
In India, shoots can also be transformed into beverages such as nuruk (fermentation starter), makgeolli (Korean rice wine), or vinegar [82,83]. One study found that Salicornia enhances fermenting microbe propagation and improves vinegar quality [84]. Other authors have found that these plants can be used as a source of salt for several dishes. Indeed, S. herbacea powder can be transformed into spherical granules, which may be used as NaCl [85].

8. Conclusions

In the last few years, interest in halophytes cultivation has increased; however, scientific papers and multiple large scale experiments are very limited. There are few protocols for glassworts field cultivation and few guidelines for small cultivations or trials.
The high salt tolerance and content in bioactive compounds makes glassworts one of the most important candidates for future use both for fresh and processed food, due to their functional and health properties.

Author Contributions

D.L., G.C., and B.D.L. have contributed equally to the work reported.

Funding

This research received no external funding.

Acknowledgments

Thanks to Vivai Aurora Soc. Cop. di Fiorentino Guerriero (San Nicandro G.co, Foggia, Italy) for the seeds providing.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Slama, I.; Abdelly, C.; Bouchereau, A.; Flowers, T.; Savouré, A. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. 2015, 115, 433–447. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Ramani, B.; Reeck, T.; Debez, A.; Stelzer, R.; Huchzermeyer, B.; Schmidt, A.; Papenbrock, J. Aster tripolium L. and Sesuvium portulacastrum L.: Two halophytes, two strategies to survive in saline habitats. Plant Physiol. Biochem. 2006, 44, 395–408. [Google Scholar] [CrossRef] [PubMed]
  3. Singh, D.; Buhmann, A.K.; Flowers, T.J.; Seal, C.E.; Papenbrock, J. Salicornia as a crop plant in temperate regions: Selection of genetically characterised ecotypes and optimization of their cultivation conditions. AoB Plants 2014, 6. [Google Scholar] [CrossRef] [PubMed]
  4. Sagi, M.; Savidov, N.A.; L’vov, N.P.; Lips, S.H. Nitrate reductase and molybdenum cofactor in annual ryegrass as affected by salinity and nitrogen source. Physiol. Plant 1997, 99, 546–553. [Google Scholar] [CrossRef]
  5. Flowers, T.J.; Colmer, T.D. Salinity tolerance in halophytes. New Phytol. 2008, 179, 945–963. [Google Scholar] [CrossRef]
  6. Jouyban, Z. The effects of salt stress on plant growth. TJAS 2012, 2, 7–10. [Google Scholar]
  7. Petropoulos, S.A.; Karkanis, A.; Martins, N.; Ferreira, I.C.F.R. Edible halophytes of the Mediterranean basin: Potential candidates for novel food products. Trends Food Sci. Technol. 2018, 74, 69–84. [Google Scholar] [CrossRef]
  8. Montesano, F.; Gattullo, C.; Parente, A.; Terzano, R.; Renna, M. Cultivation of potted sea fennel, an emerging mediterranean halophyte, using a renewable seaweed-based material as a peat substitute. Agriculture 2018, 8, 96. [Google Scholar] [CrossRef]
  9. He, J.; Qin, L.; Chong, E.L.C.; Choong, T.W.; Lee, S.K. Plant growth and photosynthetic characteristics of Mesembryanthemum crystallinum grown aeroponically under different blue-and red-LEDs. Plant Sci. 2017, 8, 361. [Google Scholar] [CrossRef]
  10. Karakas, S.; Cullu, M.A.; Dikilitaş, M. Comparison of two halophyte species (Salsola soda and Portulaca oleracea) for salt removal potential under different soil salinity conditions. Turk. J. Agric. For. 2017, 41, 183–190. [Google Scholar] [CrossRef]
  11. Ventura, Y.; Eshel, A.; Pasternak, D.; Sagi, M. The development of halophyte-based agriculture: Past and present. Ann. Bot. 2014, 115, 529–540. [Google Scholar] [CrossRef] [PubMed]
  12. Kadereit, G.; Ball, P.; Beer, S.; Mucina, L.; Sokoloff, D.; Teege, P.; Yaprak, A.E.; Freitag, H. A taxonomic nightmare comes true: Phylogeny and biogeography of glassworts (Salicornia L., Chenopodiaceae). Taxon 2007, 56, 1143–1170. [Google Scholar] [CrossRef]
  13. Davy, A.J.; Bishop, G.F.; Costa, C.S.B. Salicornia L. Salicornia pusilla J. Woods, S. ramosissima J. Woods, S. europaea L., S. obscura P.W. Ball & Tutin, S. nitens P.W. Ball & Tutin, S. fragilis P.W. Ball & Tutin and S. dolichostachya Moss. J. Ecol. 2001, 89, 681–707. [Google Scholar]
  14. Yaprak, A.E. Sarcocornia obclavata (Amaranthaceae) a new species from Turkey. Phytotaxa 2012, 49, 55–60. [Google Scholar] [CrossRef]
  15. Steffen, S.; Ball, P.; Mucina, L.; Kadereit, G. Phylogeny, biogeography and ecological diversification of Sarcocornia (Salicornioideae, Amaranthaceae). Ann. Bot. 2015, 115, 353–368. [Google Scholar] [CrossRef] [PubMed]
  16. Fuente, V.; Rufo, L.; Rodriguez, N.; Sánchez-Mata, D.; Franco, A.; Amils, R. A study of Sarcocornia A.J. Scott (Chenopodiaceae) from Western Mediterranean Europe. Plant Biosyst. 2016, 150, 343–356. [Google Scholar] [CrossRef]
  17. Pignatti, S. Flora d’Italia, 2nd ed.; Edagricole: Bologna, Italy, 2017; Volume 216, pp. 261–267. (In Italian) [Google Scholar]
  18. Corbetta, F. Lineamenti della vegetazione macrofitica dei laghi di Lesina e di Varano. G. Bot. Ital. 1970, 104, 165–191. (In Italian) [Google Scholar] [CrossRef]
  19. Di Pietro, R.; Dibitonto, P.; Garziano, G.; Sciandrello, S.; Wagensommer, R.P.; Medagli, P.; Tomaselli, V. Preliminary results of floristic and vegetation surveys in three coastal humid areas in the Puglia region (southern Italy). Lazaroa 2009, 30, 99. [Google Scholar]
  20. Castroviejo, S.; Lanz, M.; Lpez Gonzlez, G.; Montserrat, P.; Muoz Garmendia, F.; Paiva, J.; Villar, L. Flora Iberica: Plantas Vasculares de la Peninsula Iberica e Islas Baleares; CSIC: Madrid, Spain, 1990; Volume 2, pp. 526–531. [Google Scholar]
  21. Redondo-Gómez, S.; Mateos-Naranjo, E.; Davy, A.J.; Fernández-Muñoz, F.; Castellanos, E.M.; Luque, T.; Figueroa, M.E. Growth and photosynthetic responses to salinity of the salt-marsh shrub Atriplex portulacoides. Ann. Bot. 2007, 555–563. [Google Scholar] [CrossRef]
  22. Shepherd, K.; Macfarlane, T.; Colmer, T. Morphology, anatomy and histochemistry of Salicornioideae (Chenopodiaceae) fruits and seeds. Ann. Bot. 2005, 95, 917–933. [Google Scholar] [CrossRef]
  23. Ball, P.W. Salicornia L., in Flora of North America: North of Mexico (4): Magnoliophyta: Caryophyllidae, Part 1; Editorial Committee of the Flora of North America, Oxford University Press: Oxford, UK, 2004; ISBN 978-0-19-517389-5. [Google Scholar]
  24. Grouzis, M.; Berger, A.; Heim, G. Polymorphisme et germination des graineshez trois especes annuelles du genere Salicornia. OEC Plant 1976, 11, 41–45. [Google Scholar]
  25. Philipupillai, J.; Ungar, I.A. The effect of seed dimorph-ism on the germination and survival of Salicornia europaea L. populations. Am. J. Bot. 1984, 71, 542–549. [Google Scholar] [CrossRef]
  26. Harper, J.L. Population Biology of Plants; Academic Press: New York, NY, USA, 1977. [Google Scholar]
  27. Imbert, E. Ecological consequences and ontogeny of seed heteromorphism. Perspect. Plant Ecol. Syst. 2002, 5, 13–36. [Google Scholar] [CrossRef]
  28. Song, J.; Fan, H.; Zhao, Y.; Du, X.; Wang, B. Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquat. Bot. 2008, 88, 331–337. [Google Scholar] [CrossRef]
  29. Gul, B.; Ansari, R.; Flowers, T.; Khan, M. Germination strategies of halophyte seeds under salinity. Environ. Exp. Bot. 2003, 92, 4–18. [Google Scholar] [CrossRef]
  30. Wang, F.; Xu, Y.; Wang, S.; Shi, W.; Liu, R.; Feng, G.; Song, J. Salinity effects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol. Biochem. 2015, 95, 41–48. [Google Scholar] [CrossRef]
  31. Ameixa, O.; Marques, B.; Fernandes, V.S.; Soares Amadeu, M.; Calado, R.; Lilleb, A.I. Dimorphic seeds of Salicornia ramosissima display contrasting germination responses under different salinities. Ecol. Eng. 2016, 87, 120–123. [Google Scholar] [CrossRef]
  32. Ungar, I.A. Seed banks and seed population dynamics of halophytes. Wetl. Ecol. Manag. 2001, 9, 499–510. [Google Scholar] [CrossRef]
  33. Khan, M.A.; Ungar, I.A. Influence of salinity and temperature on the germination of Haloxylon recurvum. Ann. Bot. 1996, 78, 547–551. [Google Scholar] [CrossRef]
  34. Ungar, I.A. Salinity, temperature and growth regulator effects on seed germination of Salicornia europaea L. Aquat. Bot. 1977, 3, 329–335. [Google Scholar] [CrossRef]
  35. Okusanya, O.T.; Ungar, I.A. The effects of time of seed production on the germination response of Spergularia marina. Physiol. Plant 1983, 59, 335–342. [Google Scholar] [CrossRef]
  36. Orlovsky, N.; Japakova, U.; Zhang, H.; Volis, S. Effect of salinity on seed germination, growth and ion content in dimorphic seeds of Salicornia europaea L. (Chenopodiaceae). Plant Div. 2016, 38, 183–189. [Google Scholar] [CrossRef]
  37. Aghaleh, M.; Niknam, V.; Ebrahimzadeh, H.; Razavi, K. Effect of salt stress on physiological and antioxidative responses in two species of Salicornia (S. persica and S. europaea). Acta Physiol. Plant. 2011, 33, 1261–1270. [Google Scholar] [CrossRef]
  38. Lv, S.; Jiang, P.; Chen, X.; Fan, P.; Wang, X.; Li, Y. Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiol. Biochem. 2012, 51, 47–52. [Google Scholar] [CrossRef] [PubMed]
  39. Keiffer, C.H.; Ungar, I.A. The effect of extended exposure to hypersaline conditions on the germination of five inland halophyte species. Am. J. Bot. 1997, 84, 104–111. [Google Scholar] [CrossRef]
  40. Muscolo, A.; Panuccio, M.; Piernik, A. Ecology, Distribution and ecophysiology of Salicornia europaea L. In Sabkha Ecosystems. Volume IV: Cash Crop Halophyte and Biodiversity Conservation; Khan, M.A., Böer, B., Öztürk, M., Al Abdessalaam, T.Z., Clüsener-Godt, M., Gul, B., Eds.; Springer Publication: Dordrecht, The Netherlands, 2014; pp. 233–240. [Google Scholar]
  41. Lee, C.W.; Glenn, E.P.; O’Leary, J.W. In vitro propagation of Salicornia bigelovii by shoot-tip cultures. HortScience 1992, 27, 472. [Google Scholar]
  42. Shi, X.L.; Han, H.P.; Shi, W.L.; Li, Y.X. NaCl and TDZ are two key factors for the improvement of in vitro regeneration rate of Salicornia europaea L. J. Integr. Plant Biol. 2006, 48, 1185–1189. [Google Scholar] [CrossRef]
  43. Joshi, M.; Mishra, A.; Jha, B. NaCl plays a key role for in vitro micropropagation of Salicornia brachiata, an extreme halophyte. Ind. Crop Prod. 2012, 35, 313–316. [Google Scholar] [CrossRef]
  44. Urbano, M.; Tomaselli, V.; Bisignano, V.; Veronico, G.; Hammer, K.; Laghetti, G. Salicornia patula Duval-Jouve: From gathering of wild plants to some attempts of cultivation in Apulia region (southern Italy). Genet. Resour. Crop Evol. 2017, 64, 1465–1472. [Google Scholar] [CrossRef]
  45. Gunning, D. Cultivating Salicornia europaea (Marsh Samphire); Daithi O’ Murchu Marine Research Station & University College Cork: Dublin, Ireland, 2016; pp. 1–50. [Google Scholar]
  46. Ventura, Y.; Sagi, M. Halophyte crop cultivation: The case for Salicornia and Sarcocornia. Environ. Exp. Bot. 2013, 92, 144–153. [Google Scholar] [CrossRef]
  47. Rozemaa, J.; Schatb, H. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ. Exp. Bot. 2013, 92, 83–95. [Google Scholar] [CrossRef] [Green Version]
  48. Singh, A.; Sharma, S.; Shah, M.T. Successful cultivation of Salicornia brachiata—A sea asparagus utilizing RO reject water: A sustainable solution. Int. J. Waste Resour. 2018, 8, 322. [Google Scholar] [CrossRef]
  49. Bashan, Y.; Moreno, M.; Troyo, E. Growth promotion of the seawater irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp. Biol. Fertil. Soils 2000, 32, 265–272. [Google Scholar] [CrossRef]
  50. Reddy, M.P. Bromide tolerance in Salicornia brachiata Roxb, an obligate halophyte. Water Air Soil Pollut. 2009, 196, 151–160. [Google Scholar] [CrossRef]
  51. Ventura, Y.; Wuddineh, W.A.; Shpigel, M.; Samocha, T.M.; Klim, B.C.; Cohen, S.; Shemer, Z.; Santos, R.; Sagi, M. Effects of day length on flowering and yield production of Salicornia and Sarcocornia species. Sci. Hortic. 2011, 130, 510–516. [Google Scholar] [CrossRef]
  52. York, J.; Lu, Z.; Glenn, E.P.; John, M.E. Daylength affects floral initiation in Salicornia bigelovii Torr. Plant Biol. 2000, 41–42, (Abstract). [Google Scholar]
  53. Ahmad, S.; Sima, N.; Mirzaei, H.H. Effects of sodium chloride on physiological aspects of Salicornia persica growth. J. Plant Nutr. 2013, 36, 401–414. [Google Scholar] [CrossRef]
  54. Parida, A.K.; Jha, B.J. Physiological and biochemical responses reveal the drought tolerance efficacy of the halophyte Salicornia brachiata. J. Plant Growth Regul. 2013, 32, 342–352. [Google Scholar] [CrossRef]
  55. Cooper, A. The effects of salinity and waterlogging on the growth and cation uptake of salt marsh plants. New Phytol. 1982, 90, 263–275. [Google Scholar] [CrossRef]
  56. Katschnig, D.; Broekman, R.; Rozema, J. Salt tolerance in the halophyte Salicornia dolichostachya Moss: Growth, morphology and physiology. Environ. Exp. Bot. 2013, 92, 32–42. [Google Scholar] [CrossRef]
  57. Jennings, D.H. Halophytes succulence and sodium in plants—A unified theory. New Phytol. 1968, 67, 899. [Google Scholar] [CrossRef]
  58. Storey, R.; Wyn Jones, R.G. Responses of Atriplex spongiosa and Suaeda monoica to salinity. Plant Physiol. 1979, 63, 156–162. [Google Scholar] [CrossRef] [PubMed]
  59. Pollard, A.; Wyn Jones, R.G. Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta 1979, 144, 291–298. [Google Scholar] [CrossRef] [PubMed]
  60. Jolivet, Y.; Larher, F.; Hamelin, J. Osmoregulation in halophytic higher plants-the protective effect of glycine betaine against the heat destabilization of membranes. Plant Sci. Lett. 1982, 25, 193–201. [Google Scholar] [CrossRef]
  61. Gorham, J.; Hughes, L.L.; Wynjones, R.G. Chemical composition of salt-marsh plants from Ynys-mon (Anglesy) - the concept of physiotypes. Plant Cell Environ. 1980, 3, 309–318. [Google Scholar] [CrossRef]
  62. Ayala, F.; Oleary, J.W. Growth and physiology of Salicornia bigelovii Torr. at suboptimal salinity. Int. J. Plant Sci. 1995, 156, 197–205. [Google Scholar] [CrossRef]
  63. Liu, X.G.; Xia, Y.G.; Wang, F.; Sun, M.; Jin, Z.J.; Wang, G.T. Analysis of fatty acid composition of Salicornia europaea L. seed oil. Food Sci. 2005, 2, 42. [Google Scholar]
  64. Fan, P.; Nie, L.; Jiang, P.; Feng, J.; Lv, S.; Chen, X.; Bao, H.; Guo, J.; Tai, F.; Wang, J.; et al. Transcriptome analysis of Salicornia europaea under saline conditions revealed adaptive primary metabolic pathways as early events to facilitate salt adaption. PLoS ONE 2013, 8, e80595. [Google Scholar] [CrossRef]
  65. Norman, H.C.; Masters, D.G.; Barrett-Lennard, E.G. Halophytes as forages in saline landscapes: Interactions between plant genotype and environment change their feeding value to ruminants. Environ. Exp. Bot. 2013, 92, 96–109. [Google Scholar] [CrossRef]
  66. Guil, J.L.; Rodriguez-Garcia, I.; Torija, E. Nutritional and toxic factors in selected wild edible plants. Plant Food Hum. Nutr. 1997, 51, 99–107. [Google Scholar] [CrossRef]
  67. Lu, D.; Zhang, M.; Wang, S.; Cai, J.; Zhou, X.; Zhu, C. Nutritional characterization and changes in quality of Salicornia bigelovii Torr. during storage. Food Sci. Technol. 2010, 43, 519–524. [Google Scholar] [CrossRef]
  68. Kang, S.; Kim, M.R.; Chiang, M.; Hong, J. Evaluation and comparison of functional properties of freshwater-cultivated glasswort (Salicornia herbacea L.) with naturally-grown glass- wort. Food Sci. Biotechnol. 2015, 24, 2245–2250. [Google Scholar] [CrossRef]
  69. Patel, S. Salicornia: Evaluating the halophytic extremophile as a food and a pharmaceutical candidate. Biotech 2016, 6, 104. [Google Scholar] [CrossRef] [PubMed]
  70. Isca Vera, M.S.; Seca Ana, M.L.; Pinto Diana, C.G.A.; Silva, H.; Silva Artur, M.S. Lipophilic profile of the edible halophyte Salicornia ramosissima. Food Chem. 2014, 165, 330–336. [Google Scholar] [CrossRef] [PubMed]
  71. Liu, Y.; Zuo, P.; Zha, X.; Chen, X.; Zhang, R.; He, X.; Liu, C. Octacosanol enhances the proliferation and migration of human umbilical vein endothelial cells via activation of the PI3K/Akt and MAPK/Erk pathways. Lipids 2015, 50, 241–251. [Google Scholar] [CrossRef]
  72. Simopoulos, A.P. Omega-3 fatty acids and antioxidants in edible wild plants. Biol. Res. 2004, 37, 263–277. [Google Scholar] [CrossRef]
  73. Mishra, A.; Patel, M.K.; Jha, B. Non-targeted metabolomics and scavenging activity of reactive oxygen species reveal the potential of Salicornia brachiata as a functional food. J. Funct. Foods 2015, 13, 21–31. [Google Scholar] [CrossRef]
  74. Ksouri, R.; Ksouri, W.M.; Jallali, I.; Debez, A.; Magné, C.; Hiroko, I. Medicinal halophytes: Potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit. Rev. Biotechnol. 2012, 32, 289–326. [Google Scholar] [CrossRef]
  75. Zhu, J.K. Plant salt tolerance. Trends Plant Sci. 2001, 6, 66–71. [Google Scholar] [CrossRef]
  76. Ryu, D.S.; Kim, S.H.; Lee, D.S. Anti-proliferative effect of polysaccharides from Salicornia herbacea on induction of G2/M arrest and apoptosis in human colon cancer cells. J. Microbiol. Biotechnol. 2009, 19, 1482–1489. [Google Scholar] [CrossRef] [PubMed]
  77. Wang, X.; Min, Z.; Yuhui, Z.; Hui, W.; Tianxing, L.; Zhihong, X. Pentadecylferulate, a potent antioxidant and antiproliferative agent from the halophyte Salicornia herbacea. Food Chem. 2013, 141, 2066–2074. [Google Scholar] [CrossRef] [PubMed]
  78. Essaidi, I.; Zeineb, B.; Ahmed, S.; Hayat, B.H.K.; Hervé, C.; Naoki, A.; Abdelfatteh, E.O.; Mohamed, M.C.; Nabiha, B. Phytochemical investigation of Tunisian Salicornia herbacea L., antioxidant, antimicrobial and cytochrome P450 (CYPs) inhibitory activities of its methanol extract. Food Control 2013, 32, 125–133. [Google Scholar] [CrossRef]
  79. Temple, J. Tasting Hawai’i with Moloka’i Chef James Temple: The Other Asparagus … Sea Asparagus. Available online: http://www.tastinghawaii.com/2013/11/the-other-asparagus-sea-asparagus.html (accessed on 21 November 2018).
  80. Narasimha Rao, G.M.; Reddi, B. Distribution and density of Salicornia brachiata (a potential halophyte) in Godavari Estuary. IJBPAS 2013, 2, 974–979. [Google Scholar]
  81. El Shaer, H.M. Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region. Small Rumin Res. 2010, 91, 3–12. [Google Scholar] [CrossRef]
  82. Song, S.H.; Lee, C.; Lee, S.; Park, J.M.; Lee, H.J.; Bai, D.H.; Yoon, S.S.; Choi, J.B.; Park, Y.S. Analysis of microflora profile in Korean traditional nuruk. J. Microbiol. Biotechnol. 2013, 23, 40–46. [Google Scholar] [CrossRef] [PubMed]
  83. Kim, E.; Chang, Y.H.; Ko, J.Y.; Jeong, Y. Physicochemical and microbial properties of the Korean traditional rice wine, Makgeolli, supplemented with banana during fermentation. Prev. Nutr. Food Sci. 2013, 18, 203–209. [Google Scholar] [CrossRef] [PubMed]
  84. Seo, H.; Jeon, B.Y.; Yun, A.; Park, D.H. Effect of glasswort (Salicornia herbacea L.) on microbial community variations in the vinegar-making process and vinegar characteristics. J. Microbiol. Biotechnol. 2010, 20, 1322–1330. [Google Scholar] [CrossRef]
  85. Shin, M.G.; Lee, G.H. Spherical granule production from micronized saltwort (Salicornia herbacea) powder as salt substitute. Prev. Nutr. Food Sci. 2013, 18, 60–66. [Google Scholar] [CrossRef]
Agriculture 09 00014 g001 550
Figure 1. Salicornia europaea fuund at Lesina lagoon (Province of Foggia, Apulia, Italy).
Figure 1. Salicornia europaea fuund at Lesina lagoon (Province of Foggia, Apulia, Italy).
Agriculture 09 00014 g001
Agriculture 09 00014 g002 550
Figure 2. Sarcocornia sp. seeds gathered from Torre Guaceto (Province of Brindisi, Apulia, Italy).
Figure 2. Sarcocornia sp. seeds gathered from Torre Guaceto (Province of Brindisi, Apulia, Italy).
Agriculture 09 00014 g002
Agriculture 09 00014 g003 550
Figure 3. Adult plants of Sarcocornia sp. were harvested from Saline dei Monaci (Province of Taranto, Apulia, Italy).
Figure 3. Adult plants of Sarcocornia sp. were harvested from Saline dei Monaci (Province of Taranto, Apulia, Italy).
Agriculture 09 00014 g003
Agriculture 09 00014 g004 550
Figure 4. Salicornia europaea: (a) cylindric and succulent stem; (b) spike-like inflorescence; (c) seeds; (d) seedlings.
Figure 4. Salicornia europaea: (a) cylindric and succulent stem; (b) spike-like inflorescence; (c) seeds; (d) seedlings.
Agriculture 09 00014 g004
Agriculture 09 00014 g005 550
Figure 5. Apulian traditional dish: boiled Salicornia with extra-virgin olive oil and garlic.
Figure 5. Apulian traditional dish: boiled Salicornia with extra-virgin olive oil and garlic.
Agriculture 09 00014 g005
Table
Table 1. Origin of some species belonging to Salicornia and Sarcocornia genus [12,14,15,16].
Table 1. Origin of some species belonging to Salicornia and Sarcocornia genus [12,14,15,16].
GenusSpeciesSubspeciesOrigin
Salicorniaeuropaea L. (Syn: S. herbacea L., S. brachystachya G. F. W. Mayer, S. ramosissima J. Woods, S. patula Auct.)europaeaFrom southern Spain to northern Scandinavia
disarticulataAtlantic coasts of Netherlands and southern England.
marshalliiAtlantic coasts of Brittany and the Netherlands
S.perennans WilldperennansNorth Africa and the Mediterranean region to the Baltic Sea and White Sean Asia to Yakutsk (Siberia), Japan, and Korean Peninsula
altaicaAltai Mountains (Russia, Mongolia)
S.procumbens Sm.procumbensMediterranean and Atlantic coasts from Morocco to Scandinavia, inland occurrences in Turkey and Ukraine
freitagiiTurkey (Anatolia)
pojarkovaeCoasts of the White Sea (Russia) and Barents Sea (Norway)
heteranthaEndemic in southeast European Russia (Rostov Oblast)
S.persica AkhanipersicaIran
iranicaEastern Mediterranean and Southwest Asia
S.dolichostachya Moss South of Italy (Apulia), Northern European Russia: White Sea coast
S.glauca Delile (Syn: s. macrostachya Moric) South of Italy (Apulia)
S.bigelovii Torrey Gulf of Mexico, Atlantic coast up to Maine, S California
Sarcocorniaalpini Lag. Iberian peninsula
S.carinata Fuente, Rufo & Sánchez Mata Spain
S.fruticosa L. Coasts of the Mediterranean Sea and Atlantic (France)
S.hispanica Fuente, Rufo & Sánchez-Mata Southeastern Iberian peninsula
S.lagascae Fuente, Rufo & Sánchez-Mata Mediterranean coasts of the Iberian peninsula
S.obclavata Yaprak Turkey
S.perennis Miller Atlantic and Mediterranean coasts in West and South Europe and North Africa
S.pruinosa Fuente, Rufo & Sánchez-Mata Atlantic coasts of France, Spain, and Portugal

Share and Cite

MDPI and ACS Style

Loconsole, D.; Cristiano, G.; De Lucia, B. Glassworts: From Wild Salt Marsh Species to Sustainable Edible Crops. Agriculture 2019, 9, 14. https://doi.org/10.3390/agriculture9010014

AMA Style

Loconsole D, Cristiano G, De Lucia B. Glassworts: From Wild Salt Marsh Species to Sustainable Edible Crops. Agriculture. 2019; 9(1):14. https://doi.org/10.3390/agriculture9010014

Chicago/Turabian Style

Loconsole, Danilo, Giuseppe Cristiano, and Barbara De Lucia. 2019. "Glassworts: From Wild Salt Marsh Species to Sustainable Edible Crops" Agriculture 9, no. 1: 14. https://doi.org/10.3390/agriculture9010014

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop