horticulturae
Review
Biological and Agronomic Traits of the Main Halophytes
Widespread in the Mediterranean Region as Potential New
Vegetable Crops
Tiziana Lombardi 1,2 , Andrea Bertacchi 1,2 , Laura Pistelli 1,2,3 , Alberto Pardossi 1,2,3 ,
Susanna Pecchia 1,2,3, * , Annita Toffanin 1,2,3 and Chiara Sanmartin 1,2, *
1
2
3
*
Citation: Lombardi, T.; Bertacchi, A.;
Pistelli, L.; Pardossi, A.; Pecchia, S.;
Toffanin, A.; Sanmartin, C. Biological
and Agronomic Traits of the Main
Halophytes Widespread in the
Mediterranean Region as Potential
New Vegetable Crops. Horticulturae
2022, 8, 195. https://doi.org/
10.3390/horticulturae8030195
Department of Agriculture, Food and Environment, University of Pisa, Via Del Borghetto 80, 56124 Pisa, Italy;
tiziana.lombardi@unipi.it (T.L.); andrea.bertacchi@unipi.it (A.B.); laura.pistelli@unipi.it (L.P.);
alberto.pardossi@unipi.it (A.P.); annita.toffanin@unipi.it (A.T.)
CIRSEC Centre for Climate Change Impact, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy
Interdepartmental Research Center, Nutraceuticals and Food for Health, University of Pisa,
Via del Borghetto 80, 56124 Pisa, Italy
Correspondence: susanna.pecchia@unipi.it (S.P.); chiara.sanmartin@unipi.it (C.S.)
Abstract: Salinity is one of the oldest and most serious environmental problems in the world. The
increasingly widespread salinization of soils and water resources represents a growing threat to
agriculture around the world. A strategy to cope with this problem is to cultivate salt-tolerant crops
and, therefore, it is necessary to identify plant species that are naturally adapted to high-salinity
conditions. In this review, we focus our attention on some plant species that can be considered among
the most representative halophytes of the Mediterranean region; they can be potential resources,
such as new or relatively new vegetable crops, to produce raw or minimally processed (or readyto-eat) products, considering their nutritional properties and nutraceuticals. The main biological
and agronomic characteristics of these species and the potential health risks due to mycotoxigenic
fungi have been analyzed and summarized in a dedicated section. The objective of this review is to
illustrate the main biological and agronomical characteristics of the most common halophytic species
in the Mediterranean area, which could expand the range of leafy vegetables on the market.
Keywords: salt tolerance; Salicornia; Suaeda; Atriplex; Portulaca; novel food; hydroponic cultivation;
mycotoxigenic fungi
Academic Editors: Silvana Nicola,
Katerina Grigoriadou
and Christoph Schunko
Received: 18 January 2022
Accepted: 21 February 2022
Published: 23 February 2022
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4.0/).
1. Introduction
The increasing salinization of both soils and water resources, which is mainly due to
anthropic activity, has created a new interest in salt tolerant plants as potential crops for
saline environments [1,2].
Halophytes are the plants with the highest level of salt tolerance resulting from several
morphological, physiological, and biochemical traits, such as osmotic adjustment; ion
compartmentalization and homeostasis; detoxification of reactive oxygen species; salt
secretion; and other mechanisms that are not yet fully understood [3–5]. Halophytes can
survive in very saline soils and exploit water resources of moderate-to-high salinity. The
optimal salinity for the growth for most halophytes ranges from 50 to 250 mM NaCl;
however, they can grow and produce as much as conventional crops even when irrigated
with seawater, so with a molarity greater than 500 mM [6]. In general, halophytes are highly
versatile plants and, in addition to their role in coastal-area preservation and as valuable
scientific models for the investigation of salt-tolerance mechanisms, their exploitation as
food and non-food crops could be a winning strategy in a salinizing world.
The cultivation of halophytes under greenhouse conditions—either in soil or in a
soil-less system—or in an open field, to produce raw or minimally processed vegetables
Horticulturae 2022, 8, 195. https://doi.org/10.3390/horticulturae8030195
https://www.mdpi.com/journal/horticulturae
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(i.e., ready-to-eat or fresh-cut products), in particular for gourmet cuisine, is of growing
interest [7–9]. The edible parts of these species are appreciated due to their salty taste and
high content in antioxidant compounds and essential nutrients (minerals, vitamins amino
acids and/or fatty acids) [10,11]. Halophytes also contain ingredients of functional foods
and active principles for medicinal supplements [12–15].
In the Mediterranean regions, the most abundant halophytes are found mainly in
medium–high marshy areas; in most cases, these are directly connected to intertidal areas
and are subject to sea water flooding. The floristic composition of these environments is
closely linked to the topography and seasonal fluctuations in salinity, which can reach
very high values—sometimes higher than that of sea water in the period of maximum
evapotranspiration. The hyper-halophilous communities are dominated by therophytes
or chamaephytes, annual or perennial shrubs, or grasses, while the sub-halophilous ones
are characterized by hemicryptophytes and geophytes of different families. Among the
typical plants, we can include many species of Amaranthaceae, such as Salicornia spp.;
Suaeda vera J. F. Gmel. and S. maritima (L.) Dumort.; Halimione portulacoides (L.) Aellen;
Soda inermis Fourr. and Atriplex spp.; and some species of Poaceae such as Puccinellia distans
(Jacq.) Parl., Sporobolus aculeatus (L.) P. M. Peterson, Thinopyrum acutum (DC.) Banfi, and
Hordeum maritimum Huds. These are often associated with other halotolerant species,
including Limbarda crithmoides (L.) Dumort.; Galatella tripolium (L.) Galasso, Bartolucci and
Ardenghi; Artemisia caerulescens L., Juncus spp.; Limonium spp.; and Plantago coronopus L.
The objective of this review is to illustrate the main biological and agronomical characteristics of the most common halophytic species in the Mediterranean area, which could
expand the range of leafy vegetables on the market.
2. Halophytes: Definition and Complexity
Halophytes represent an ancient and remarkable ecological group of annual or perennial plants with very complex features, whose definition and classification are still not
univocal and often controversial [16]. The species belonging to this group are very different from an ecological, morpho–physiological, and taxonomic point of view; therefore,
their definition can be subjective and vary a lot in the literature according to the different
interpretations. However, following the most popular definition used in the literature,
halophytes can be identified as plants that grow naturally, and complete their life cycle in
environments that contain a higher salt content than most plant species can tolerate [17].
The occurrence of halophytism is widespread throughout the plant kingdom and
appears to have evolved several times, lending support to the concept that many glycophytes may have halophyte genes permanently switched off, but under mutagenesis,
may revert to halophytism [18]. In fact, all four plant kingdoms contain members that are
adapted to saline habitats; however, they occur in greater numbers among the thallophytes,
such as red and brown algae, and terrestrial or aquatic spermatophytes. These plants are
mainly distributed in arid or semi-arid inlands and saline wetlands along the tropical and
sub-tropical coasts, as well as in temperate zones [17].
Halophyte plants and their natural habitats have attracted the attention of many naturalists and writers since very remote times. Allusions to salt-tolerant plants in saline soils along
the banks and margins of salty waters date back to the mid-1500s, and data on halophytes
were already very consistent in the 1700s. In Hortus Cliffortianus and Species Plantarum, when
describing plants, Limneo often provides information on the salinity of their habitat [19].
The introduction of the word ‘halophyte’ probably dates to the Russian botanist
Peter Simon Pallas; in the early 1800s, he wrote that species of Salicornia, Salsola, Suaeda
and related plants, all previously included in the Chenopodiaceae and now included
in Amaranthaceae family following APG classification, “must be united under what he
believes is an appropriate name for Halophyta” [20]. In contrast to the term ‘halophyte’, the
name ‘glycophyte’ was proposed by Stocker (1928) [21] for plants growing in soils with
a low salt content. Most cultivated plants are glycophytes. Given the great biodiversity
of these plants and the difficulty in distinguishing between salt-tolerant glycophytes and
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halophytic species, estimating the number of halophyte species and their diffusion is
more difficult.
According to Houérou (1993) [22] and Glenn et al. (1999) [23], there are about
6000 species of terrestrial and marine plants in the world that are classified as halophytes.
These represent 2% of the angiosperms, and some of them are under continuous taxonomic
revision. Of these, approximately 1100 are widespread in the Mediterranean basin, with
a wide range of levels of tolerance to salinity. Actually, it is possible to refer to the online
database of salt-tolerant plants, namely eHALOPH [24], which is constantly updated. It is
based on the records of Aronson (1989) [25] and includes plants that tolerate a soil electrical
conductivity (EC) of at least about 8 dS/m, corresponding to about 80 mM NaCl concentrations [26]. The eHALOPH Halophyte Database currently identifies more than 1500 species
as salt-tolerant, albeit without labelling them as ‘halophyte’. Other authors report a greater
number of halophytic species but, despite the difference, most detailed lists represent only
0.5% of all angiosperms [27].
The complexity of the halophyte group is also linked to the multitude of ecosystems
that species can contribute to from all over the world. These habitats can be either natural
or non-natural, and include semi-deserts, salt meadows, brackish swamps, mangrove
forests, irrigated lands, and even urban areas. Many of the natural habitats are highly
threatened due to both natural and anthropogenic factors, such as urbanization, tourism,
and pollution. The effects of climate change are increasingly adding to the threats to which
natural halophytic habitats and vegetation are exposed. Many saline habitats are likely
to disappear due to rising sea levels, as these communities generally do not have the
ability to relocate to more inland sites. The conservation value of these ecosystems has
recently been assessed in the EU project ‘Red List of habitats’, which are classified as ‘Near
Threatened’ (Arctic coastal salt marsh, and Mediterranean and Black Sea coastal salt marsh),
‘Endangered’ (Baltic coastal meadow) or ‘Vulnerable’ (Atlantic coastal salt marsh) [28]. In
addition, many countries are facing the loss of agricultural soil due to secondary salinization
resulting from irrigation, fertilization, and climate change. Nearly 20% of the total irrigated
land area (45 million hectares) is already affected by salinization [29]. In regions with saline
soils, halophytes could be alternative crops to glycophytes to produce food, forage, and
fibers, and for industrial purposes. Moreover, when halophytes are grown as companion
plants of glycophytes, the negative effect of salinity is alleviated by the uptake of toxic ions
by the former species, as found by Colla et al. (2006) [30] and Karakas et al. 2021 [31].
3. Classification of Halophytes
Halophytes are very peculiar both physiologically and morphologically, and in some
cases, are of great phytogeographic interest. It is, therefore, not surprising that they have
been the subject of many studies in various fields of botany, and still are today.
The survival of halophytes is strongly influenced by the salinity in the root zone or,
sometimes also by salt spray, as this can happen in saline semi-deserts, in brackish marshes,
or on beaches. These types of environments have both negative effects on plants, due to
the high osmotic pressure of the soil solution and the toxic effect of salt, and positive ones,
as it reduces competition with other plants and may prevent diseases and parasites [32].
When a plant’s response to salinity is considered, we usually refer to NaCl, although
halophytes are also strongly influenced by other salts, such as MgSO4 , NaSO4 or KCl.
Halophytes can be also described as plants that survive in environments where the salt
concentration is around 200 mM NaCl or more [33]. For example, the most salt-tolerant
halophytes, such as Suaeda salsa, can complete their life cycle in soils containing 200 to
500 mM NaCl [34]. Many studies have also shown that suitable high salt concentrations
can enhance the growth of halophytes in comparison with low or negligible salinity [35,36].
This is proven at both the morphological and physiological level, with a greater biomass
accumulation and better seed quality [37], and a higher photosynthetic efficiency [38,39].
By contrast, glycophytes have a limited tolerance to salinity, showing significant
reductions in biomass under saline conditions. Among the glycophytes, two types are
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described based on their degree of sensitivity: salt-sensitive and salt-tolerant. Glycopyhytes
include species, such as rice or soybean, that can suffer irreparable damage starting from
very low concentrations (less than NaCl 50 mM), and others, such as barley or beets, that
can tolerate much higher NaCl concentrations (even those close to 200 mM) [3]. From
the morpho–functional point of view, no single factor is of major importance for the
ability to survive at high NaCl salinity. Therefore, there are no peculiar characteristics that
univocally define all the halophytic species, being a very heterogeneous and systematically
complex group. The combination of several mechanisms often enhances the salt tolerance
of individual species [40].
However, the evolution of multiple specific morpho-anatomical adaptations and
functional characteristics is evident, aimed at fighting the saline environment and even
benefiting from it. These adaptations are mostly related to the prevention of leaf water
loss by transpiration, with dilution of the salts absorbed in excess or, in some cases, with
their excretion. These characteristics are found mainly in the leaves and stems, since they
are the plant organs most rigorously exposed to environmental conditions. Among the
most important characteristics may be the reduction or absence of leaves, the abundance
of glandular trichomes or saline glands, the greater development of supporting tissues,
the development of atypical secondary growth, and leaf succulence. Typical succulent
halophytes are, for example, species of Salicornia and Sarcocornia; these are two very
interesting genera that appeared in Eurasia in the Middle Miocene period, and that have
long represented difficulties for taxonomists due to their growth form with very small
leaves and flowers. Although the response of halophytes to the multiple stressors of saline
environments is well known (Figure 1), their classification in relation to the total number of
flowering plants [41] continues to be very uncertain.
Figure 1. Response mechanisms to salinity stress by halophytic plants. Photo credit: Tiziana Lombardi.
As previously anticipated, due to their taxonomic and ecological complexity, even
today, there is no consensus on a univocal definition. It is, therefore, difficult to draw a
complete list of halophyte species, partly due to the problem of defining the lower limit of
salt tolerance at which a plant should be considered a halophyte. Of course, this difficulty
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is reflected at the environmental level, in the vegetational subdivisions and zonation of
communities dominated by halophyte species.
Halophytes are classified in various ways based on multiple factors, such as general
ecological behaviour and distribution; plant growth response to salinity; salt intake rate;
the presence or absence of saline glands, physiotype, etc. [32].
3.1. Response to Internal Salt Content
One of the first proposed classifications for flowering plants was based on their
response to internal salt content, and divides halophytes into salt-regulating or and saltaccumulating types [42]. Based on their internal salt contents, halophytes were later also
classified as excluders versus includers [17].
3.2. Eco-Physiological Aspects
Eco-physiological aspects can be used to differentiate the halophytes in obligate,
facultative, and habitat-indifferent species [17]. This classification is based on what Ingram
introduced in 1957, albeit without any definition of “low”, “moderate”, and “high” salinity.
All three types of halophytes have better growth and development than glycophytes in
saline environments [17].
•
•
•
Obligate halophytes, mostly the Amaranthaceae members, are species with optimal
growth at moderate or high salinity (NaCl 0.1–5%); they cannot grow at lower salinity, as they require salt as part of their nutrition to activate or de-activate several
salt-sensitive enzymes. These species frequently exhibit an activation of these enzymes, both at very low Na+ concentrations (below the physiological optimum) and
at seawater Na+ concentrations (considered excessive).
Facultative halophytes are plants with the ability to grow on salty soils, but their
optimal growth is observed in low-salt or non-saline conditions. Many dicotyledons
such as Aster tripolium, Chenopodium quinoa, Glaux maritima, and Plantago maritima, but
also some Poaceae, Cyperaceae and Juncaceae, belong to this group.
Habitat-indifferent halophytes normally grow on salt-free substrates, but in saline
conditions they thrive better than sensitive species. This group includes the plants
that can live in disturbed or stable habitats. In some of these, such as Festuca rubra,
Agrostis stolonifera and Juncus bufonius, there are significant genetic and morphological
differences between the populations living on salty soils and those on salt-free soils.
3.3. Salt Tolerance
According to their salt tolerance, Chapman (1942) [43] grouped the halophyte under
two groups: (i) eu-halophytes, subdivided into the three subgroups meso-halophytes,
meso-euhalophytes, en-euhalophytes; (ii) and mio-halophytes.
•
•
Eu-halophytes (extreme halophytes) are plants that can grow in seawater or tolerate
more than 200 mM NaCl (up 5%), and occur almost exclusively in environments of
high salinity [26]. Following the eHALOPH database, this group contains 333 species,
members of 70 families of flowering plants. The 75% of eu-halophytes belong to just
19 families. Eu-halophytes are rather rare amongst flowering plants, representing just
0.4% of the 350,699 accepted names in ‘The Plant List’ within 20% of its 642 families.
Some species of Atriplex, Salicornia, Suaeda, and Salsola can be included in this group.
Mio-halophytes are plants that grow in habitats with low levels of salinity (less than
0.5% NaCl).
Much later, Grigore and Toma (2010) [44] proposed a new classification of halophytes,
distinguishing the extreme halophytes from meso-halophytes, and dividing the extreme
halophytes between irreversible and reversible. Thus, based on the analysis of the anatomical features of some taxa and ecological factors, they concluded that succulent Amaranthaceae (e.g., Salicornia europaea, Suaeda maritima, Halimione verrucifera) that grow only in
very salinized environments, are irreversible halophytes. Conversely, reversible halophytes
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(e.g., Atriplex sp., Bassia sp., and Camphorosma sp.) are not strictly related to high salinity,
and are able to pass from highly salinized areas to less salinized soils.
Based on the different mechanism of salt tolerance, halophytes can be further classified
as follows [45]:
•
•
•
Salt-excluding (root-excluding type) are halophytes (also known as pseudo-halophytes)
that protect the shoot from salinity through apoplastic barriers in the roots and interveinal recycling of ions. Mangrove vegetation shows such a type of tolerance.
Salt-excreting (endo- and eso-recretohalophytes) are plants that avoid cellular damage
by releasing excess salts to the outside via specialized structures called salt glands—
such as species of Limonium, Tamarix, Spartina, Avicennia, and Frankenia—or from
epidermal bladders on the leaves, such as species of Atriplex and Chenopodium.
Salt-accumulating are plants able to accumulate salts that are compartmentalized into
vacuoles and used for osmotic adjustment, e.g., Salvadora persica, Sesuvium portulacastrum, Suaeda nudiflora.
3.4. Habitat and Geographical Distribution
The classification based on the habitat and geographical distribution includes hydrohalophytes and xero-halophytes [46]:
•
•
Hydro-halophytes are halophytic plants that need aquatic conditions or wet soil. Species
growing in aquatic environments belong to this group, such as the mangrove forests,
tidal marshes or coastal lagoons, and the brackish marshes of the temperate zone.
Zannichellia palustris and Althenia filiformis are typical hydro-halophytes in the Mediterranean area [47,48].
Xero-halophytes grow in environments with dry soil due to high evapotranspiration.
Most plants living in desert areas and succulents belong to this group. Atriplex
canescens or A. halimus are xero-halophytes that tolerate both salt and drought stress.
4. Mediterranean Halophytes
In the Mediterranean regions, Amaranthaceae are the dominant angiosperm family, with halophyte species such as Salicornia sp., Sarcocornia sp., Suaeda sp., Salsola sp.
and Atriplex sp. They are followed by Poaceae, such as Hordeum sp., Puccinellia sp., and
Sporobolus sp. [25,26]. Halophyte species are mostly found in coastal brackish areas that are
subjected to periodic flooding.
The halophytes reported in Table 1 were selected for this review.
The choice took advantage of both their diffusion and importance at an environmental
level in the Mediterranean regions, and their degree of salt tolerance recognized by the
main international databases such as eHALOPH. The species were then characterized
from a botanical point of view and investigated regarding the availability of data on their
potential as food-crop sources. Some data have also been provided on the distribution
and availability of these species on the Italian territory, with reference to the Tyrrhenian
coasts [49,50] (Figure 2a,b). These areas represent an important germplasm reserve for the
use of local varieties or ecotypes. The species are reported with the scientific and common
name, the type of halophytism, and the edible organs.
For all the species considered, we followed the taxonomic nomenclature reported by
Bartolucci et al. (2018) [51], except for Soda inermis, herein kept as Salsola soda. This is due to
the taxonomic difficulties of not being fully clarified by the Angiosperm Phylogeny Group
classification [52], related to the revisions of the genus Salsola, from which the taxon Soda
was separated with the only species Soda inermis.
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Table 1. List of halophytes selected on the basis of their diffusion in the Mediterranean region and their type of halophytism according to eHALOPH [24].
Botanical Name
Family
Common Name in English, French,
German and Italian
Type of Halophytism
Edible Organs
Atriplex littoralis L. (Syn.: Atriplex patula L. var.
littoralis (L.) A. Gray)
Amaranthaceae
Grassleaf orache, Arroche du littoral,
Strand-meide, Atriplice litorale.
Psammophyte
Leaves
Atriplex prostrata Boucher ex DC (Syn.: Atriplex latifolia
Wahlenb. = Atriplex hastata L. var. prostrata (Boucher ex
DC.) Lange)
Amaranthaceae
Hastate orache, Arroche couché,
Spiess-meide, Atriplice prostata
Eu-halophyte
Meso-hydrohalophile
Leaves
Beta vulgaris L. subsp. maritima (L.) Arcang. (Tuscany,
Sardinia, Sicily)
Amaranthaceae
Sea beet, Bette maritime, Wilde übe, Bietola
marittima
Mio-halophyte
Leaves
Cakile maritima Scop. subsp. maritima
Brassicaceae
Searocket, Roquette de mer, Strandrauke,
Ravastrello di mare
Psammophile
Halo-nitrophilous
Leaves
Halimione portulacoides (L.) Aellen (Syn.:
Atriplex portulacoides L.)
Amaranthaceae
Sea pursiane, Arroche faux-pourpier,
Strand-salzmeide, Porcellana di mare
Eu-halophyte
Hydro-halophyte
Leaves
Portulaca oleracea L. subsp. oleracea
Portulacaceae
Common pursiane, Purcelane,
Portulach, Porcellana
Xero-halophyte
Leaves
Stem
Salicornia perennans Willd. subsp. perennans (Syn.:
Salicornia europaea auct.; Salicornia patula Duval-Jouve).
Amaranthaceae
Grasswort, Salicorne etaleé, Pannonien
glasschmaiz, Salicornia patula
Eu-halophyte
Xero-halophyte
Stem
Salicornia perennis Mill. subsp. perennis (Syn.:
Sarcocornia perennis (Mill.) A.J.Scott subsp. perennis).
Amaranthaceae
Perennial grasswort, Salicorne vivace,
Ausdauernde gliedermeide, Salicornia
radicante
Eu-halophyte
Hydro-halophyte
Stem
Salsola soda L. (Syn: Soda inermis Fourr.)
Amaranthaceae
Monk’s beard, Soude commune,
Soda-salzicraut, Agretto
Eu-halophyte
Leaves
Young stem
Suaeda maritima (L.) Dumort. (Syn.:
Chenopodium maritimum L.)
Amaranthaceae
Sea-blite, Soude maritime, Strand-sode,
Sueda marittima
Eu-halophyte
Mesohydro-halophile
Leaves
Young stem
Suaeda vera J.F. Gmel (Syn.: Suaeda fruticosa (L.) Forssk.
subsp. vera (J.F. Gmel.) Maire & Weiller).
Amaranthaceae
Shrubby sea-blite, Soude vraie, Strauchige
sode, Sueda vera
Eu-halophyte
Halo-nitrophilous
Leaves
Young stem
Horticulturae 2022, 8, 195
The species and subspecies Halimione portulacoides, Salicornia perennans subsp. perennans, Salicornia perennis subsp. perennis, Salsola soda, Suaeda maritima and S. vera are exclusive to brackish areas. A. prostrata, B. vulgaris subsp. maritima, and Portulaca oleracea can be
found in both brackish areas and internal saline soils. Cakile maritima subsp. maritima, and
Atriplex littoralis are halophytes that grow exclusively in dune environments.
The main multidisciplinary traits of the 11 selected species are reported in Appendices A–C.
8 of 32
Figure 2.2.Salt
marshe
vegetation
of Tyrrhenian
coasts (Italy):
Salicornia
communities;
(b)
Figure
Salt
marsh
vegetation
of Tyrrhenian
coasts (a)
(Italy):
(a) perennis
Salicornia
perennis communities;
Salicornia
perennans
communities.
Photo credit:
(b)
Salicornia
perennans
communities.
PhotoAndrea
credit:Bertacchi.
Andrea Bertacchi.
The species and subspecies Halimione portulacoides, Salicornia perennans subsp.
perennans, Salicornia perennis subsp. perennis, Salsola soda, Suaeda maritima and S. vera
are exclusive to brackish areas. A. prostrata, B. vulgaris subsp. maritima, and Portulaca
oleracea can be found in both brackish areas and internal saline soils. Cakile maritima subsp.
maritima, and Atriplex littoralis are halophytes that grow exclusively in dune environments.
The main multidisciplinary traits of the 11 selected species are reported in
Appendices A—C.
5. Halophytes as Potential Novel Crops
The Mediterranean basin is extraordinarily rich in wild, edible halophytes that grow
in both coastal and inland salty areas. The use of wild halophytes for food, and for ethnomedicine, is very ancient. Many plant species have been used traditionally as herbs and
vegetables, and accounts of their uses can often be found in ethnobotanic literature [53–55].
This suggests a high potential for Mediterranean halophytes to undergo exploitation by
the food industry towards the production of new products with functional and healthy
properties, such as beverages, salad mix, microencapsulated oils, food additives, antimicrobial agents, etc. Different parts of halophytes can be consumed, such as the leaves, young
shoots, seeds, flower buds, roots, and fruits.
Examples of wild, edible halophytes belong to the genera Atriplex, Bassia, Beta, Cakile,
Chenopodium, Crithmum, Plantago, Portulaca, Salicornia, Salsola, and Suaeda. Some halophytes
have received attention as potential food sources due to their beneficial effects [7,12,56,57].
To overcome salinity, plants adopt various strategies. A common characteristic of salt
tolerance is the leaf accumulation of L-proline. It is an amino acid commonly synthesized
in the cytosol and stored in the chloroplasts, and its accumulation rises to 80% of the amino
acid pool when plants are exposed to environmental stress [58]. Proline is well known
for its osmoprotectant activity, such as its ability to change cell osmotic pressure, so its
presence helps halophytes to counteract salty soils. Therefore, proline is considered to
play a pivotal role in defense /protective mechanisms, as the scavenging activity against
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reactive oxygen species, to provide stabilization of the cellular membrane and play the role
of a metal chelator [58]. Another compound accumulated by halophytes is glycine betaine,
which interact with macromolecules (proteins, enzymes) and contribute to the mitigation
of salinity stress [59]. Salsola soda (Syn.: Soda inermis) is an example of a glycine betaine
accumulator [60].
Some halophytes are also a good source of nutraceuticals. For instance, Salicornia perennis
(Syn.: Sarcocornia perennis subsp. perennis) is used in the human diet for its nutraceutical
components. S. perennis leaves are rich in proteins (6.9 mg/100 g d.w.), polyunsaturated
fatty acids (PUFA; linolenic acid is about 21% of PUFA), and minerals such as Ca, Mg, Fe and
K [7]. Salicornia ramosissima is used as gourmet food due to the presence of antioxidants as
phenolics compounds, and of α- and γ-tocopherol [7]. Suaeda maritima (Syn.: Chenopodium
maritimum) contains a good amount of Ca, Mg, Fe, Zn, and Cu, which represent up
to 10% of the allowed daily intake (ADI) and are a good source of vitamins such as
beta-carotene and lutein, vitamin A, and vitamin C [11]. Phenolic compounds and/or
derivatives, such as phenolic acids (e.g., gallic acid), phenylpropanoids (e.g., cinnamic acid,
caffeic acid), flavonoids (e.g., quercetin and kaempferol) and lignans, are often present in
Suaeda sp., Sarcocornia sp., and other halophytic species. Suaeda vera might be a valuable
source of phenolic compounds due to its antioxidant, anti-inflammatory, and anticancer
properties [61], as well as bioactive flavonoids, and other beneficial properties. Likewise,
the leaves of S. vera accumulate sugars, especially galactoarabinans, which have a good
antioxidant-activity effect and contribute to cell stability [62].
However, other plants accumulate sugar alcohols (e.g., mannitol, inositol, sorbitol)
to maintain cell homeostasis. The leaves of B. vulgaris spp. maritima contain several
nutraceutical compounds, such as tocopherols, phenols, ascorbic acids, and some fatty acids,
although their consumption could be limited by the presence of malic and oxalic acid [12]. In
Cakile maritima, the leaf content of minerals, vitamins, and amino acids, such as proline and
glycine, increases in response to salt treatment [57,63]. Portulaca oleracea, also named “Global
Panacea” by the World Health Organization, contains 3% carbohydrates, 2% protein, as well
as various vitamins (especially vitamin A) and all the essential minerals. Its leaves are rich
in flavonoids and contain alkaloids, including dopa, dopamine, and noradrenalin. Portulaca
is a good source of Omega-3 fatty acids (α-linolenic acid and linoleic acid), contained
in the leaves, stems and flowers. The presence of various bioactive compounds confers
to Portulaca several pharmacological properties, such as antimicrobial, antioxidant, antiinflammatory, antidiabetic, neuroprotective, antiulcerogenic, and anticancer activity [64].
More information about the biochemical characteristics of the 11 selected species are
illustrated in Appendices A–C.
6. Cultivation of Halophytes in Hydroponic Greenhouse
As potential new vegetable species, halophytes are also candidates for greenhouse
cultivation, which can allow year-round production of high-quality products with an efficient use of resources such as water, fertilizers, and manual labor. In the last three decades,
protected horticulture has developed in many regions, particularly in the Mediterranean
countries (e.g., Spain, Italy, Turkey, and Morocco), where the mild climate during winter
makes it possible to produce many crops in simple structures [65]. The increasing competition arising from the globalization of production and marketing, the greater awareness of
the environmental impacts provoked by intensive cropping systems, the increasing demand
for healthy foods, and the shortage of resources such as water, are forcing greenhouse
growers to apply more sustainable growing techniques. The use of greenhouses with
better climate control and more advanced growing technologies, such as drip fertigation,
hydroponics (or soil-less culture), and integrated control over pests and diseases, are the
most relevant aspects of the development of the greenhouse industry worldwide.
Many soilless growing systems have been designed and tested for greenhouse crop
production. Nowadays, the term “hydroponics” includes all methods and techniques for
cultivating plants without soil in artificial substrates (aggregate culture) or in an aerated
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nutrient solution (liquid or water culture) [66]. Aggregate culture is generally used for row
crops with low crop density and long growing cycles, such as Solanaceae, Cucurbits, and
strawberry, while water culture is adopted for short-cycle and high-density crops such as
leafy vegetables and herbs [66].
We searched SCOPUS for documents on the hydroponic cultivation of halophytic
species using the following search strategy (last access: 15 February 2022): TITLE-ABS-KEY
(halophyte* OR halophytic*) AND (hydroponic* OR aquaponic* OR aquaculture OR soilless). We found 260 research articles published between 1983 and the beginning of 2022;
almost half of these have been published since 2017, demonstrating the recent interest of
plant scientist in this subject. Much attention has been paid to the utilization of these species
in integrated or multitrophic marine aquaponic systems, in which halophytes are cultivated
in undiluted or diluted seawater along with aquatic species such as fish, crustaceans and
seaweeds [67]. In these systems, halophytes play a fundamental role in the bioremediation
of effluents from aquaculture [68].
The halophytes most studied in hydroponics and aquaponics are the following:
Salicornia dolichostachya [69], S. perennans [70,71], S. ramosissima [69,72], S. bigelovii [73],
Sarcocornia neei [74,75], Halimione portulacoides [9,76,77], and Portulaca oleracea [78–82]. The
crop yield observed in some halophytic species grown in soil-less culture is shown in
Table 2, along with other information on growing conditions. We are not aware of any studies conducted on the hydroponic production of the other species selected for this review
(Table 1). The hydroponic techniques mainly used for halophytes are deep culture, floating
system, and sand culture. Singh et al. (2014) [69] found that in Salicornia dolichostachya
and S. ramosissima, the harvestable biomass was greater in hydroponic culture than in
sand culture.
One of the main advantages of a hydroponic system over soil cultivation is that
plant growth rate, and then crop yield, are increased as result of better mineral nutrition
and water uptake. In Israel, under field conditions, Salicornia persica produced 13.4 to
16.0 kg/m2 of fresh biomass in six months when grown under field conditions on sand
dune soil and drip-irrigated with moderate salinity (10 dS/m), or 18.6 kg/m2 when grown
in an unheated greenhouse on coconut fiber-filled sleeves irrigated with moderately saline
aquaculture effluent (EC 4 dS/m) [83]. In Salicornia europaea cultivated for two months in a
floating system in the typical greenhouse climate conditions of summer in Central Italy and
using groundwater or diluted seawater (with salinities ranging between 10 and 30 g/L),
the production of fresh shoots was between 7.10 and 9.78 kg/m2 , depending on the salinity
of the nutrient solution [70].
Small dimensions and fast growth rate make some halophytes good candidates for
the hydroponic production of fresh-cut baby leaves, which are increasingly used for mixed
salads. Baby leaves are young plants harvested two to four weeks after seed germination.
In addition, hydroponic culture allows the improvement of product quality by appropriate
management of the nutrient solution [84]. Tender and very clean leaves and shoots are
generally harvested in hydroponic systems, and this facilitates the washing operation
with minimal processing. There is a growing interest in the fresh-cut baby leaves of halophytes [15], and some studies have demonstrated the good adaptation of purslane [85,86]
and sea fennel [14].
Among soilless growing methods, the floating system is the simplest and most costeffective technique to produce baby leaves at high crop density [86].
Intensive cropping systems, such as greenhouse hydroponics, enhance crop productivity but could affect the produce quality of wild edible plants, particularly as regards their
nutritional, nutraceutical and organoleptic traits [87]. Recently, in a study conducted
with three species of halophytes (Mesembryanthemum nodiflorum, Suaeda maritima and
Sarcocornia fruticosa), harvested from the wild in two different locations in Portugal or
cultivated hydroponically, it was found that cultivated plants are more succulent, and have
fewer fibers and antioxidants than wild plants [11]. Increased succulence is a positive trait
from an organoleptic point of view.
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Table 2. Fresh biomass production of some halophytic species grown in hydroponics under different growing conditions, and at different plant density and salinity
levels of the nutrient solution.
Species
Location
(Country)
Growing Technique
Growing Season
and Environment
Growing Cycle
(Days/Month)
Plant Density
(Plants/m2 )
Salinity Level
Fresh Biomass
(kg/m2 )
Halimione
portulacoides
Portugal
Hydroponics
(floating system)
Growth chamber
10 weeks
110–220
20 g/L NaCl
3.1–5.4
[9]
Halimione
portulacoides
Portugal
Hydroponics
(floating system)
Growth chamber
10 weeks
220
20 g/L NaCl
3.41–5.40
[77]
Portulaca oleracea
Jordan
Soil-less substrate
Unheated
greenhouse,
March–July
5 months
5.5–6.5 dS/m
14.6–26.9
Total yield depended
on genotypes
[80]
Portulaca oleracea
Spain
Hydroponics
(floating system)
Unheated
greenhouse, July
15 days
2.7 dS/m
1.64–2.66
Total yield depended
on genotypes
[78]
Portulaca oleracea
Spain
Microgreens
Growth chamber
4 weeks
0–80 mM NaCl
1.51–1.97
Yield was greater at
higher salinity
[81]
Portulaca oleracea
Canada
Hydroponics
(floating system)
Controlled-climate
greenhouse
26 days
266
0–10 mM NaCl
4.90–5.73
[79]
Portulaca oleracea
Alabama, US
Mixture of Jiffy mix,
sand, and soil
Controlled-climate
greenhouse
60 days
20
Hoagland nutrient
solution
0.54
[82]
Salicornia bigelovii
Canada
Hydroponics
(floating system)
Controlled-climate
greenhouse
28 days
266
6–200 mM NaCl
0.33–1.69
The greatest yield was
found at 200 mM NaCl
[73]
Salicornia
dolichostachya
Germany
Sand culture or
hydroponics (floating
system)
Controlled-climate
greenhouse
42 days
37
257–513 mM NaCl
0.86–1.06
Yield was greater in
floating system than in
sand
[75]
Salicornia europaea
Italy
Hydroponics
(floating system)
Greenhouse,
summer
58 days
60
0–30 g/L (artificial
sea salt)
4.80–9.84
The lowest yield and
the highest yield were
found at salinity of 30
and 10 g/L
[70]
Salicornia
ramosissima
Germany
Sand culture
Hydroponics
(floating system)
5 weeks
-
257–513 mM NaCl
1.06
[69]
Salicornia persica
Israel
Coconut-fiber-filled
sleeves
Unheated
greenhouse
5 months
-
4 dS/m
18.6
[83]
Suaeda glauca
Canada
Hydroponics
(floating system)
Controlled-climate
greenhouse
27 days
266
6–200 mM NaCl
4.02–5.65
2050
Note
The lowest yield was
found at 200 mM NaCl
Reference
[88]
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7. Health Risks Associated with the Consumption of Cultivated Halophytes
For the economic development of halophytic crops, the possible presence of healthhazardous substances must be considered for nitrate and oxalate—which generally accumulate, to a large extent, in species belonging to the Amaranthaceae [89,90]—and Na,
with regard to irrigation with saline water. The risk associated with the presence of heavy
metals and other environmental pollutants is not considered in this review, as this risk is
minimized if halophytes are grown under controlled conditions with safe irrigation water;
this is in contrast with the harvest of these plants in the wild, which is prohibited in most
areas where these species could be collected.
7.1. Nitrates
Nitrate (NO3 − ) may be harmful to human health as it can be converted to nitrite
(NO2 − ) causing methaemoglobinaemia or carcinogenic nitrosamines [89]. According to the
World Health Organization (WHO) and the European Commission’s Scientific Committee
on Food (SCF), the ADI for NO3 − is 3.7 mg/kg b.w. (222 mg for an adult weighing
60 kg), while the USA Environmental Protection Agency (EPA) has set an ADI of about
7.0 mg/kg b.w. The main sources of NO3 − in human diet are drinking water, cured meat
and vegetables; the latter generally provide 30% to 94% of the daily dietary intake of
NO3 − [89].
The European Commission has established maximum limits for the NO3 − content in
some vegetable species marketed for fresh consumption or as frozen products: 3000 mg/kg
f.w. for spinach (Spinacea oleracea); 2000–5000 mg/kg f.w. for lettuce (Lactuca sativa);
and 6000–7000 mg/kg f.w. for rocket salad (Eruca sativa, Diplotaxis sp., Brassica tenuifolia,
Sisymbrium tenuifolium). The limits depend on growing conditions. For instance, the limits
are higher for vegetables grown in the fall–winter season and under cover, compared to
those grown in spring–summer and in an open field. Limits to NO3 − levels have been
set in other European countries for other species [89]. We are not aware of the maximum
NO3 − levels set for the halophytes selected for this review.
Many leafy vegetables easily accumulate NO3 − in their edible tissues under growing
conditions that enhance NO3 − uptake by the roots (e.g., high NO3 − concentration in the
growing medium) while NO3 − reduction is hampered. For instance, low solar radiation
limits leaf photosynthesis and the availability of reducing equivalents (ferredoxin and
NADPH) for NO3 − reduction, and this account for large NO3 − accumulation in plants
grown in winter with abundant nitrogen fertilization. Hydroponic cultivation stimulates
root mineral uptake and can enhance more NO3 − accumulation in leaf tissues compared
to soil cultivation [91]. On the other hand, plant mineral nutrition can be controlled
by the adjustment of the nutrient-solution composition. For instance, nutrient-solution
deprivation [92], or the replacement of NO3 − with Cl− [93], during the last few days of
cultivation can reduce leaf NO3 − content to below the limits set by EU Regulation 2008 [94].
Nitrate accumulation is hampered when plants are grown with high NaCl in the growing
medium due to the competitive interaction between NO3 − and Cl− [95]. In the halophyte
Suaeda salsa (L.), NO3 − reduction and assimilation were stimulated by Cl− application, with
a consequent reduction in leaf nitrogen accumulation [94]. Nitrate content can vary very
much within species and cultivars, and the degree of NO3 − accumulation is associated with
the location of nitrate reductase activity and the plant’s capacity of NO3 − accumulation on
halophytes marketed for human consumption. Recently, Labiad et al. (2021) [14] reported
that NaCl concentration and leaf spray with methyl jasmonate did not affect the NO3 −
concentration of baby leaves of hydroponically grown Crithmum maritimum, which ranged
between 229 and 296 mg/kg f.w. It was calculated that a daily consumption of 100 g of
C. maritimum leaves did not reach the ADI of NO3 − for adult persons. However, the content
of NO2 − was between 453 and 970 mg/kg f.w., and the same daily intake of baby leaves
largely surpassed the ADI for nitrite (3.6 mg, according to SCF) [89].
In a greenhouse experiment with Salicornia europaea, grown in summer in an aerated
water culture with different concentrations (0, 10, 20 and 30 g/L) of a synthetic sea salt
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(Instant OceanTM ), shoot NO3 − content averaged 3397 mg/kg f.w. in the controls and was
much lower in salt-treated plants, with no major differences across salinity levels (the mean
value was 1374 mg/kg f.w.) [70].
7.2. Sodium
Sodium is one of the most abundant elements on earth and in seawater, and along
with Cl− , is by far the dominant ion in saline soils [96]. Halophytes tolerate a high
concentration of Na in the root zone, and some of them require NaCl for optimal growth
and development [97]. Although root control of Na uptake and the excretion of Na salts via
specific organs (such as salt glands) are among the mechanisms of salt tolerance in some
halophytes, most of them are eu-halophytes and accumulate large amounts of Na+ and
other ions; these are compartmentalized in vacuoles for osmotic adjustment. Therefore,
the consumption of halophytes grown in saline conditions originates the risk of excessive
intake of Na. According to the World Health Organization [98], the recommended ADI
of Na for adults is 2 g per day, as greater intake increases the risk of hypertension and
cardiovascular diseases.
In wild plants of Beta vulgaris subsp. maritima, Cakile maritima, Portulaca oleracea and
Salicornia europaea, harvested in the South-East Spain, the Na content of fresh, edible organs
was 171, 308, 42 and 884 mg/100 g f.w., respectively [63]. In Sarcocornia perennis subsp.
perennis; S. perennis subsp. alpini; S. ramosissima; and Arthrocnemum macrostachyum, collected
in the South of Portugal, edible tips contained, respectively, 2049, 1029, 910 and 1393 mg
Na/100 g f.w. [7]. When Halimione portulacoides was grown hydroponically in artificial
seawater (20 g/kg) under non-limited nutrient conditions, at harvest, fresh leaves contained
750 mg Na/100 g f.w. [9]. In the aforementioned study performed by Boni (2020) [70] with
hydroponically grown Salicornia europaea, the shoot Na content was 471, 1299, 1672 and
1806 mg/100 g f.w. at salinity level of 0, 10, 20 and 30 g/L, respectively. Therefore, when
halophytes harvested in the wild or cultivated with high sodium concentration in the
growing medium are consumed, much attention must be paid not to exceeding the ADI
recommended by the WHO. On the other hand, dried halophytes such as Salicornia spp.
and Halimione portulacoides can replace Na salts to produce low-Na foods [99,100].
7.3. Oxalate
Oxalate is an anti-nutritional factor contained in many foods, although those rich in
oxalate, such as some vegetables, generally play a minor role in human diet [101]. Oxalate
can bind to several minerals, thus reducing their bioavailability in humans. Oxalate can
reduce the availability of Ca due to the formation of an insoluble complex that is contained
in the most urinary stones of kidney. Almost all the species considered in this review
(Table 1) belong to Amaranthaceae, which includes some vegetables naturally rich in
oxalates such as spinach, Swiss chard, and mangold [102]. A general guideline from the
American Dietetic Association is to restrict the daily intake of oxalate to 40–50 mg/day [103].
Among the species considered for human consumption, undoubtedly, the most investigated
halophyte is purslane, as it is a good source of omega-3 fatty acids, amino acids, and
vitamins. However, this species also contains high concentrations of antinutritional factors,
such as NO3 − and oxalate [104]. The oxalate content found in hydroponically cultivated
purslane ranges from 800 mg/kg f.w. [105] to more than 6000 mg/kg f.w. [106], and it has
been known to reach 7700 mg/kg f.w. in plants collected in the wild [107]. With such
high contents, a few grams would be enough to exceed the maximum recommended daily
intake of oxalates. In purslane, the oxalate content depends on the genotypes [106,108],
nitrogen nutrition [105,109], and harvesting stage [110]. Decreasing the nitrogen supply
and the NO3 /NH4 ratio in the culture solution has been known to reduce the oxalate
content of stems and/or leaves of purslane grown in hydroponics [105,106,110]. Carvalho
et al. (2009) [108] found a reduction in the oxalate content of purslane leaves when NaCl
was added to the hydroponic solution. In a recent work with purslane microgreens,
cultivated in a growth chamber under different light conditions, oxalic content significantly
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decreased when plants were illuminated with red and blue, or red, blue, and far-red LEDs.
The nutrient solution contained 80 mM NaCl, compared with the controls grown under
fluorescent light with a NaCl-free nutrient solution [81].
7.4. Mycotoxigenic Fungi and Mycotoxins in Edible Halophytes: A Potential Health Risk?
The parts of the halophyte plants used for nutrition could become potential natural
sources of mycotoxins, if contaminated by mycotoxigenic fungal species.
Mycotoxins are a series of secondary metabolites produced by a variety of filamentous
fungi that can grow on a diversity of crops and are associated with important morbidity
and mortality in humans and animals, as well as with major economic losses. Exposure to
mycotoxins can occur by inhalation, dermal contact, and primarily by ingestion. Because of
their low molecular weight, thermostability and wide spectrum of toxicity, the management
of the contamination of food and feed with mycotoxins is problematic [111]. Moreover, it
is important to note that climate change is expected to significantly increase mycotoxin
production by fungi [112].
A very large number of mycotoxins (>300) has been identified in agricultural products; correspondingly, mycotoxigenic species can be found in all major taxonomic groups,
but the most important are produced by many species of the genera Aspergillus, Penicillium,
Alternaria, and Fusarium [113]. Of the great number of known mycotoxins, only a few are
commonly found in fruits and vegetables: aflatoxins (produced by several Aspergillus species);
ochratoxin A; patulin and citrinin (by Penicillium and Aspergillus species); alternariol and derivatives (by Alternaria species); and trichothecin (by Trichothecium roseum) [114,115].
Mycotoxins rarely cause outbreaks via fresh food, but they are still a risk factor for
foodstuffs of plant origin [116]. The contamination of fruits and vegetables with fungi
that produce mycotoxins can occur in the field, at harvest and during transportation, and
in storage. The presence of fungi on fresh products does not always lead to mycotoxin
contamination but reveals that there is a potential risk, because many environmental factors
can trigger the formation of mycotoxins [114]. Mycotoxins produced on fresh products
may be found in their host tissues even after the fungal mycelium has been eliminated.
This is critical for the safety of consumers, since apparently healthy parts can be used as
ready-to-eat fresh products or dried food preparations [117,118]. In this regard, careful
attention should be paid to the composition of the mycoflora on the edible parts, and to the
presence of mycotoxigenic fungi.
Many scientific papers report the presence of endophytic fungal populations inhabiting several species of halophytes. Endophytic fungi generally reside within plants without
causing any disease symptoms and have gained the attention of many researchers for their
ability to produce bioactive metabolites [119–121]. However, recent findings highlight
the possible contribution of endophytic strains in differentiating new lineages with an
uneven mycotoxin assortment during the exploration of new ecological contexts [122].
Thirumalai et al. (2020) [123] pointed out the importance of investigating the endophyte
community of leafy vegetables, especially those with a longer shelf life, for their mycotoxin production.
Therefore, against this background, the data relating to the endophytic, and/or mycotoxigenic fungal species reported on the halophytes described, have been presented in
Appendices A–C. The examples confirm that representative fungal genera containing mycotoxigenic species have been frequently reported on halophytes. Therefore, symptomless
infections could cause serious food-safety problems, as the plant can look normal, but it
may contain mycotoxins.
Many mycotoxin-producing fungal species belonging to the Aspergillus and Penicillium
genera have been isolated from low-water-activity environments (aw below 0.8) due to
their adaptive xerotolerance/halotolerance [124,125]. Maciá-Vicente et al. (2008) [126]
found a high occurrence of Aspergillus fumigatus and members of Pleosporales, such as
Alternaria species, in saline environments. Recently, Calabon et al., 2021 [127] reviewed the
fungal biodiversity in salt-marsh ecosystems. They found 486 taxa associated with different
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hosts, of which 95.27% (463) belonged to the phylum Ascomycota, and the Pleosporales was
the largest order with 178 taxa recorded. Moreover, Pleosporales and Alternaria spp. are
known to produce heavily pigmented spores and/or mycelia (especially melanin) that may
protect the fungi in a high-salinity environment (UV radiation, desiccation, and extreme
temperatures) [128].
Interestingly, within the Pleosporales order, some fungal genera have a host and habitat preference and can be found in marine or saline habitats in association with various
kinds of halophytes. The majority of the Neocamarosporium species described so far were
found in association with Atriplex hastata, A. prostrata, Beta vulgaris, Halimione portulacoides,
Salicornia spp., and Salsola sp.; halotolerance seems to be a typical characteristic of this
fungal genus [129,130]. The importance of the problem addressed is confirmed by recent observations of the presence of mycotoxigenic fungi and their mycotoxins in some halophytic
plants [131,132].
Although toxicological assessments and guidelines are in place to curb the impact
of many contaminants on public health, these safeguards cannot be applied to naturally
occurring mycotoxins. For this reason, the health risk posed to the consumer by natural
mycotoxins appears more serious than the health risk posed by man-made pesticides,
preservatives, and other food additives [133,134].
7.5. Pathogenic Bacteria Potentially Associated with Edible Halophytes
To the best of our knowledge, there are no studies on the microbial contamination of
halophytes intended for human consumption. Nevertheless, we can assume that the contamination of halophyte-based food preparation due to bacteria follows the general guidelines
adopted for other vegetables. Bacteria such as Aeromonas spp., Bacillus cereus, Campylobacter spp.,
Clostridium botulinum, Escherichia coli, Listeria monocytogenes, Salmonella enterica, Shigella spp.,
Staphylococcus spp., and Yersinia enterocolitica are generally associated with fresh vegetable
produce. Among these, E. coli, L. monocytogenes and S. enterica have been found to be
responsible of most fresh-produce outbreaks in the United States [135].
The fresh vegetable market, including halophytes, is expanding due to global changes
and to consumer habits being more oriented toward healthier lifestyle choices. On the
other hand, the diffusion of foodborne illness is often associated with the intake of readyto-eat preparations. These are consumed without being exposed to processing treatments,
and pathogen contamination may be uncontrolled as a result. Listeria monocytogenes and
Staphylococcus aureus have been proven to have the ability to survive in different types
of salad over a range of temperatures, depending on the type of preparation and storage
conditions [136]. In fresh-cut vegetables, the microbiological standard for Salmonella spp.
is absence in 25 g of foods [137]; for Listeria monocytogenes, the standard is absence in 25 g
before the food has left the immediate control of the producer, and <100 cfu/g in products
that are placed on the market during their shelf life [137]. Studies on the presence of enteric
pathogens in fresh-cut vegetables indicate that contamination with pathogens occurs
infrequently [138]. However, in a recent study, increased consumption of fresh produce
was correlated with increased outbreaks of microbial infection of these products [139].
The presence of halophyte species in food preparation is desirable to contribute to the
preservation of biodiversity and improving sustainable practices; the development and
application of accurate practices in the preparation and prevention of cross-contamination
are essential to preclude the presence of pathogens.
8. Conclusions and Future Perspectives
Global climate change and soil degradation due to progressive salinization are now
quite evident. In this context, halophytes can be of fundamental importance both for the
restoration of salinized lands, and as a commercial alternative to traditional crops.
Some halophytes (e.g., Portulaca oleracea and Salicornia spp.) are cultivated and consumed as a novel source of nutraceutical components, conferring beneficial effects, such
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as proline. Further compounds that are well represented are phenolic compounds and/or
derivatives, fatty acids, vitamins (tocopherols and ascorbic acid), and some minerals.
For these purposes, multidisciplinary investigations are crucial, starting with the
identification of the species, subspecies and ecotypes, and subsequently characterizing
their ecological, nutritional, and organoleptic properties, for their use as crop plants. This
approach may not always be simple, as the halophytes, especially some members of the
Amaranthaceae, often have high intraspecific morphological and physiological variability.
The cultivation and commercial production of edible halophytes is still in early stages;
in the European market, their consumption is recent, and therefore not covered by any
food-safety regulations. Despite the promising future for multiple uses of edible halophytes,
there is still little knowledge of natural mycotoxin contamination in these plants, and more
investigations are required before conclusions can be drawn on the health risks associated
with their consumption.
Author Contributions: Conceptualization, A.P., L.P., T.L., A.B., A.T., S.P. and C.S.; writing—original
draft, A.P., L.P., T.L., A.B., A.T. and S.P.; review and editing, A.P., L.P., T.L., A.B., A.T., S.P. and
C.S.; supervision, A.P.; funding acquisition, C.S. and A.P. All authors have read and agreed to the
published version of the manuscript.
Funding: This study was conducted in the framework of the project entitled “HALOphytes grown in
saline Water for the production of INnovative ready-to- eat salad-HALOWIN” and funded by the
University of Pisa, “PRA 2020”, grant number PRA_2020_43.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.
Appendix A
The systematic, morphological, and biochemical characteristics of the species considered in the present work (Table 1) are reported below. Nomenclature follows the APG IV
classification system [52].
AMARANTHACEAE Juss.—Dicotyledons, annual or perennial, shrubs, or herbs.
Leaves are simple without stipules, succulent or reduced in some taxa. Small flowers,
bisexual or unisexual, in flower heads or spikes. Simple perianth of 3–5 scary tepals.
Stamens equal in number to the tepals, and alternated with petaloid staminoids. Fruit is
utricle or pyx. Seeds with annular embryo surrounding the mealy albumen. Cosmopolitan.
Appendix A.1. Genus Salicornia L.
The genus Salicornia includes several annual and perennial plants, divided into a series
of diploid and tetraploid species and subspecies [140], difficult to distinguish based on
macroscopic characteristics. The genus name derives from the Latin ‘sal’ (salt) and ‘conus’
(horn), due to the shape of the branches. These plants have articulated stems, succulent and
apparently aphill, with very small flowers (hermaphrodites) that are difficult to observe.
These are normally inserted in terminal racemes consisting of triflorous dicases, inserted at
the axil of leaf-like bracts, in correspondence with each node. In this Appendix, following
updates of Bartolucci et al. (2018) [51], reference is made to subspecies Salicornia perennans
Willd. subsp. perennans, and S. perennis Mill. subsp. perennis. Other authors include the
latter species in the genus Sarcocornia [141,142]. The two species are both diploid (2n = 18).
Appendix A.1.1. Salicornia perennans Willd. subsp. perennans (Syn.: Salicornia europaea auct.;
Salicornia patula Duval-Jouve; Salicornia herbacea (L.).) Eu-halophyte
Botanical traits
Biological form: scapose therophyte.
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Morphological characteristics: Stem 5–40 cm tending to purple with ripening, very
branched at the base. The inflorescence is trifloral with the central flower much larger than
the lateral ones. Mature seeds covered with curved and often hooked hairs.
Habitat: salt marshes, soils muddy clay-asphyxial, basic and hypersaline. S. perennans
is widespread along almost all the Italian coasts. It grows in lagoons and basins subjected
to periodic flooding of seawater and at the edges of the salt flats, along the coasts.
Chorological type: W-Europe (Euri-Medit.)
Flowering period: September–November.
S. perennans tolerates a NaCl concentration of more than 1000 mM, although its optimal
growth has been observed at 200 mM [143]. The plants contain large amounts of minerals,
especially Ca, Mg and iodine (I), and osmolytes such as betaine and choline [144].
Biochemical traits
The plant is cultivated for its oilseed used in human consumption and as a forage crop
in saline coastal environments.
Wang et al. (2021) [145] performed metabolomic characterization of the leaves of
S. europaea, and discovered 694 metabolites involved in the tolerance to salt conditions:
flavonoids, alkaloids and coumarins, and the branched chain amino acids, glucosamine,
maltose, and glucose. At a high salt concentration (500 mM NaCl), the succulence is due
to the Na+ content of the cell, which promotes the osmotic adjustment and increases the
proline and other osmolyte content, maintaining cell turgor [146]. The first investigation
on the effects of salt stress in S. europaea was elucidated in 2009 [147] by looking at the
growth parameters, free proline content, ion accumulation, lipid peroxidation, and several
antioxidative enzymes activities of in vitro plantlets. At high salt concentration (300 mM),
peroxidation of lipid membranes occurs, reflecting free-radical-induced oxidative damage
at the cellular level [148], counteracted by the increase in polyphenol content and enzymatic
scavenger activity (peroxidase and superoxide dismutase). Salicornia shoots are also a good
source of fatty acids such as linoleic and oleic acids [12,54].
The oilseeds of S. herbacea (Syn.: S. perennans) are rich in proteins [149] and linoleic
(75.6%) and oleic acids (13.0%); they also contain a significant amount of palmitic, linoleic,
and stearic acids, as well as tetracosanol, and octacosanol [149]. The composition is very
similar to the composition of safflower oil. The extracts exhibit activity against different
kinds of oxidative stress, inflammation, diabetes, asthma, hepatitis, cancer, and gastroenteritis [150].
Plant mycobiota
The analysis of the fungal community structure in Salicornia europaea in Poland revealed
the presence of nine orders, and among them, the most representative were Pleosporales
(main genus Alternaria) and Eurotiales (including the genera Aspergillus and Penicillium) [151,152].
Pleospora sp., Alternaria alternata, and A. phragmospora were the major endophytes
found in Salicornia europaea in Japan [153].
Lopes et al. (2020) [132] investigated the presence of potentially mycotoxigenic fungi
and the occurrence of aflatoxins (AFB1, AFB2, AFG1, AFG2) and ochratoxin A in fresh and
powdered samples of Salicornia spp. (wild and cultivated) in Portugal. Potentially toxigenic
fungi (Aspergillus flavus, A. fumigatus, A. niger, and Penicillium sp.) were present in most of
the analyzed samples, and relevant levels of AFB1 > 5 µg kg−1 and total aflatoxins (sum of
AFB1, AFB2, AFG1 and AFG2) > 10 µg kg−1 were found in various samples. Ochratoxin
A was not found in any of the samples. It is interesting to note that a sample of Salicornia
supplied by a local producer exhibited very high levels of contamination, but no aflatoxins
were found in the samples grown either in greenhouses or in hydroponic cultivation. The
presence of aflatoxins may not be considered a serious problem for those who consume
Salicornia occasionally; however, this halophyte is widely used as forage [154], which, if
contaminated, could be a risk to both animals and humans.
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Appendix A.1.2. Salicornia perennis Mill. subsp. perennis (Syn.: Sarcocornia perennis (Mill.) A.
J. Scott subsp. perennis). Eu-halophyte
Botanical traits
Biological form: succulent chamaephyte.
Morphological characteristics: Bushy stem 50–60 cm, rooting at the nodes. The inflorescence is 3-flowered with the central flower a little larger than the lateral ones. Mature
seeds covered with short, curved hairs.
Habitat: hypersaline margins of the brackish areas where S. perennans also grows,
often dry in summer.
Chorological type: Medit.-Atlant.
Flowering period: September–November.
Biochemical traits
The halophyte S. perennis contains high levels of proteins (6.9 g/100 g d.w.) and n-3
polyunsaturated fatty acids (PUFA)—particularly linolenic acid (21.1% of total FA)—and
low concentrations of toxic metals, below the limits imposed by the European Commission. The plant is also a good source of minerals, particularly Na (64.1 mg/g d.w.), and
manganese (31.4 mg/g d.w.). Other detected natural minerals include the presence of Ca,
Mg, Fe and K. Leaf extracts show great antioxidant potential due to the content of total
phenols (20.5 mg GAE/g d.w.), carotenoids (280 mg/100 g d.w.), and tocopherols (vitamin E, 1.2 mg/100 g d.w.) [7]. In addition, flavonoids, such as kaempferol and quercetin,
and to a lesser extent, gallic acid and other hydroxy-benzoic acids, have been reported
in Sarcocornia species; the intake of 100 g of edible portions (wet weight) of S. perennis
would cover 71% of said recommended daily dose, to reduce the risk of cardiovascular and
coronary heart disease [7]. Other metabolites, such as pectic polysaccharides, can protect
the immune and reproductive systems of mammals against toxic chemical-inducers of
oxidation reactions. All the cited compounds confer important biological properties, such
as antioxidant, anti-inflammatory, hypoglycemic and cytotoxic activity [6].
Plant mycobiota
Petrini and Fisher (1986) [155] found 32 species of endophytic fungi in apparently healthy
stems from 20 tussocks of Salicornia perennis on a salt marsh at Dawlish Warren, Devon, UK.
The most frequent colonizers belonging to the order Pleosporales were Pleospora salicorniae and
P. bjorlingii, and two species of Stagonospora. Other isolates were Alternaria alternata, A. tenuissima,
Cladosporium tenuissimum, Coniothyrium sp., Hypoxylon bipapillatum, Leptosphaeria sp., Phoma sp.,
Pleospora herbarum and Septoria sp.
Appendix A.2. Genus Suaeda Forssk ex J.F. Gmelin
The Suaeda genus includes about 100 species, mainly halophytes with fat leaves; they
grow in saline and alkaline wetlands and deserts almost all over the world but are primarily
extra-tropical. The species are annuals or perennials, dwarf shrubs or, rarely, trees. The
genus is known to be taxonomically very complicated due to its high polymorphism [156].
The two species Suaeda maritima (L.) Dumort., and S. vera J. F. Gmel, described below,
are both diploid with 2n = 36.
Appendix A.2.1. Suaeda maritima (L.) Dumort. (Syn.: Chenopodium maritimum L.;
Schoberia maritima (L.) C.A. Mey). Eu-halophyte/halo-nitrophilous
Botanical traits
Biological form: scapose therophyte.
Morphological characteristics: A 30–80 cm plant, first glaucous and then, with ripening,
tending to red. Leaves (8–16 mm) with a semi-circular section, the lower opposite, the
others alternate, never pointed. Flowers in glomeruli at the axil of the leaves on the
upper branches.
Habitat: Mainly salty coastal areas, both on sandy soils in the back dune and clayey
soils, where there is an accumulation of organic remains; it is also ecologically useful in
swamp formations due to its ability to trap mud.
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Chorological type: Medit.-Occid.
Flowering period: July–August.
Biochemical traits
Suaeda maritima is a succulent halophyte, suitable for human consumption due to
the high concentrations of proteins, fiber and minerals [11]. The leaves have a pleasant,
salty taste due to the high salt content [157]. S. maritima contains a noticeable content
of various minerals, such as Ca, K, Mg, Fe, Zn and Cu, and the consumption of 20 g
of fresh leaves could represent 2–10% of the recommended daily intake [11,158]). It is
also rich in vitamins. Regarding fat-soluble vitamins, β-carotene represents the most
important provitamin A (9.30–20.7 mg/100 g d.w.). The species also has high content of
lutein (20–89 mg/100 g d.w.) in comparison with other vegetables. These metabolites are
involved in many physiological processes, such as immune response, and the prevention
of vision-degenerative diseases related to age in humans and animals [159]. The content
observed in Vitamin A is 5.39 mg/100 g d.w., showing similar values to those of species
with good sources of vitamin A (e.g., spinach 5.45 mg/100 g d.w.) [11]. S. maritima shows
a content of ascorbic acid (Vitamin C) above that of other vegetables, such as parsley
and broccoli [11,160]. In addition, other antioxidant metabolic compounds, such as total
phenolic, flavonoids and condensed tannin, are detected in S. maritima [11]. The most
representative compounds are chlorogenic acid, cinnamic acid, catechin hydrate, coumaric
acid, luteolin-7-O-glucoside. The results of such work confirmed the direct correlation
between the content of phenolic compound flavonoids, with the antioxidant activity of
the extracts.
The cultivated plants of S. maritima showed a different nutritional profile compared
with wild plants in [11]: leaves had a higher content of moisture, ash, and fiber. High water
content and succulence are the result of a high concentration of osmolyte solutes, such as
proline and glycine betaine, that contribute to the regulation of turgor [157].
Plant mycobiota
The genetic diversity of the fungal endophytes isolated from halophytic plants, sampled from salt marshes located in west and South Korea, was studied using the internal
transcribed spacer (ITS) region as a DNA barcode for the classification of the specimens.
Generic richness and diversity were determined by counting the genera present in the
fungal communities in plant samples. In S. maritima sampled in west Korea, 7 genera and
7 species were found, and the most abundant genera were Alternaria and Cladosporium [161].
In South Korea 11 genera and 21 species were isolates from S. maritima samples and the most
dominant genus was Fusarium, followed by the genera Penicillium and Alternaria [162]. The
endophyte assemblage of S. maritima in India was dominated by Camarosporium palliatum
as indicated by its mean density of colonization [163].
Appendix A.2.2. Suaeda vera J. F. Gmel (Syn.: Suaeda fruticosa (L.) Forssk.;
Suaeda fruticosa (L.) Forssk. subsp. vera (J. F. Gmel.) Maire & Weiller;
Chenopodium fruticosum (L.). Eu-halophyte (Halo-nitrophilous)
Botanical traits
Biological form: nano-phanerophyte.
Morphological characteristics: A plant that can reach one meter in height, with woody,
very branchy and glaucous stems with semi-cylindrical and slightly more pointed leaves
(8–15 mm) than S. maritima.
Habitat: salty and nitrophilous soils, but soils of calanchive and internal marly areas.
Chorological type: Cosmopol.
Flowering period: June–July.
Biochemical traits
The obligate halophyte S. fruticosa is known to increase its content of sugars, protein,
and proline under high salt concentration [164]. Both the leaves and seeds are edible
and used for human consumption. Succulence is one of the mechanisms used by this
species to protect itself from salt stress [164]. Regarding sugars, the composition seems
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related to that of galactoarabinans, by the presence of pectin-like polysaccharides and
neutral monosaccharides (including arabinose, mannose, galactose, rhamnose, glucose,
and xylose). These polysaccharides possess significant potential in antioxidant activity
effect [62]. Other phytochemicals with antioxidant activity—such as phenols, flavonoids,
tannins, proanthocyanidins, and carotenoids—have been isolated from S. fruticosa extracts,
reproducing the therapeutic benefits of these plants, and also used as herbal tea [165]. Alkaloids and saponins have also been detected, to enlarge their phytopharmacological use. S.
fruticosa produces numerous seeds under saline conditions and contains about 25% oil [12],
four saturated fatty acids (11.04%), and six unsaturated fatty acids (89.06%) [166]. These
nutritional components promote the consumption of the leaves and seeds of S. fruticosa
as food and feed. Unsaturated fatty acids (linoleic and oleic acids) confer the ability to
overcome damage to the cell membrane under stress conditions, by controlling the expression of desaturase genes [167]. This plant is used in folk medicine for its hypoglycemic
and hypolipidemic activity [12]; a good anti-inflammatory effect was also detected in
polysaccharide extracts [62]. Interesting anticancer activity against human lung carcinoma
and colon adenocarcinoma cell lines were reported for dichloromethane extracts [168].
Plant mycobiota
Fisher and Petrini (1987) [169] found that Camarosporium spp. (85.3% in stems) and
Colletotrichum gloeosporioides (30% in leaves) endophytically colonized S. fruticosa in England.
Appendix A.3. Genus Salsola L.
Recently, the Salsola genus has been revised with the creation, among others, of the
new taxa Soda (which would therefore include S. soda species as S. inermis). However, the
original classification is still maintained in this review, as the new taxonomic classification
has not yet been fully clarified in APG IV. The species of Salsola are mostly subshrubs,
shrubs, small trees, and rarely, annuals. The leaves are mostly alternate, rarely opposite,
simple, and entire. The bisexual flowers have five tepals and five stamens.
Salsola soda L. (Syn.: Soda inermis Fourr.). Mio-halophyte (halo-nitrophilous)
Botanical traits
Biological form: scapose therophyte.
Morphological characteristics: 20–120 cm tall, often red with ripening; leaves 20–40 mm
long, succulent, opposite and slightly sharp; axillary flowers.
Habitat: salty coastal areas on both sandy soils in the back dune and clayey soils,
where there is an accumulation of organic remains.
Chorological type: Paleotemp.
Flowering period: July–August.
Biochemical traits
S. soda represents a valid alternative crop for saline soils, because of its accumulation and tolerance to very high levels of Na [60]. Therefore, S. soda is considered a
“bio-desalinating companion plant” for tomatoes and peppers in saline soils in the Mediterranean area [60]. Its cultivation can be achieved in different saline (NaCl) concentrations
and in desalinized soils [170]. S. soda (Syn.: S. inermis) is also considered a glycine-betaine
accumulator. Various Salsola species, including the species S. soda, have been examined for
their phytochemical composition, showing the presence of alkaloids, flavonoids, saponins,
coumarins, and sterols [171–173]. The shoots contain flavonoid glycosides and triterpenoid
saponins [174]. In particular, the presence of quercetin 3-O-β-D-glucuronopyranoside
may confer functional nutraceutical and medicinal properties. In fact, shoot extracts have
been found to exhibit hypoglycemic, antioxidant, anti-cholinesterase, and antimicrobial
activity [172,175]. Alkaloids present in the extracts from Salsola species have been evaluated
against Alzheimer’s disease [172].
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Appendix A.4. Genus Atriplex L.
The genus Atriplex, with about 300 species, is the richest in species of the Amaranthaceae family. It has worldwide distribution, occurring on all the continents except
Antarctica. Annual or perennial herbs or shrubs. The inflorescences consist of axillary or
terminal spikes or spicate panicles, or axillary clusters of glomerular flowers. The flowers
are unisexual. Some species are monoecious, others dioecious.
Appendix A.4.1. Atriplex littoralis L. (Syn.: Atriplex patula L. var. littoralis (L.) A. Gray).
Halo-nitrophilous
Botanical traits
Biological form: scapose therophyte.
Morphological characteristics: both 40–120 cm high, with erect angular stem and
lanceolate linear leaf lamina.
Habitat: seacoasts, ruderal and sub-saline habitat.
Chorological type: Europe and Paleotemp.
Flowering period: July–October.
Atriplex littoralis germination and growth are reduced at salinities higher than 1%
NaCl [176]. The plant accumulates salt in the seeds and bracteoles (~40–50%) [177]. In
adult plants, the salt is accumulated in the aerial parts, like other halophytes in the Amaranthaceae.
Biochemical traits
Regarding the 300 species belonging to the Atriplex genus, the species A. littoralis
has not been deeply investigated for phytochemical content and biological activity. The
plant is rich in flavonoids, glycosides, alkaloids, amino acids, minerals, saponins, and
phytoecdysteroids [178].
Plant mycobiota
Some Alternaria species (A. alternata, A. raphani, A. tenuissima), Cladosporium oxysporum,
Fusarium moniliforme and F. tricinctum were found in Atriplex littoralis sampled at various
growth stages from an inland salt marsh in Canada [178,179].
Appendix A.4.2. Atriplex prostrata Boucher ex DC (Syn.: Atriplex hastata L. var. prostrata
(Boucher ex DC.) Lange; Atriplex latifolia Wahlenb.). Halo-nitrophilous
Botanical traits
Biological form: scapose therophyte.
Morphological characteristics: both 40–120 cm high, with erect angular stem and
hastate/triangular leaf lamina.
Habitat: seacoasts, ruderal, and sub-saline habitat.
Chorological type: Europe and Paleotemp.
Flowering period: July–October.
Biochemical traits
Atriplex prostrata is a facultative halophyte. Seed germination has been known to
decrease by 25% at 200 mM NaCl [179]. In saline environments, Na accumulation is
associated with a decrease in the content of K, Ca and Mg, and with reduced plant growth
and photosynthesis [180]. However, some antioxidant enzymes have been known to
increase in the aerial organs while the lignin content decreases [181]. Polyphenol content
has been shown to increase with external salt concentration [182], but different behaviour
of polyamines and ethylene was observed: spermine, putrescine and spermidine content
decreased under saline conditions, while ethylene increased together with proline [183].
Appendix A.5. Genus Halimione Aellen
Monoecious annual or perennial herbs with silvery grey stems and leaves. The leaves
are opposite in the lower part and alternate in the upper part of the plants. The leaf blade
is oblong with entire margins
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Halimione portulacoides (L.) Aellen (Syn.: Atriplex portulacoides L.). Eu-halophyte
Botanical traits
Biological form: chamaephyte.
Morphological characteristics: species up to 80 cm tall has a prostrate stem, often
rooting at the nodes; opposite leaves with lanceolate lamina, up to 60 mm long, with
obtuse apex.
Habitat: salty and clayey coastal areas.
Chorological type: Circumbor.
Flowering period: June–July.
Biochemical traits
H. portulacoides is an obligate halophyte with succulent leaves. The optimal growing
condition was assessed at 200 mM NaCl; however, this species can tolerate up to 1 M
NaCl [184]. Anthocyanins, polyphenols, and proline increases significantly with salinity,
being maximal at 1000 mM NaCl [185]. The activity of superoxide dismutase (EC 1.15.1.1,
SOD), ascorbate peroxidase (EC 1.11.1.11, APX), and glutathione reductase (EC 1.6.4.2, GR)
is significantly stimulated by salinity in the leaves of H. portulacoides, whereas catalase (EC
1.11.1.6, CAT) activity is maximal in the 0–400 mM NaCl range. Leaves contain phenolic
compounds, mostly sulphated flavonoids that confer high antioxidant activity [184].
The salt tolerance of H. portulacoides can be attributed to the leaf waxes containing long
chain chloroalkanes. Recently, the polar lipid profile of leaves has been determined and
classified in over five classes of phospholipids, three classes of glycolipids characterized by
the presence of PUFA (n-3 and n-6 FA), and one class of glycosphingolipids [186].
High productivity and a capacity to grow in soil contaminated by heavy metals also
make this species potentially useful for saline soil reclamation and phytoremediation
purposes, and even as fodder plants [187]. Volatile organic compounds have been detected
in the root exudates [168].
Plant mycobiota
Specific works on fungi associated with H. portulacoides date back to the 1960s [188,189]. In
these studies, different fungi were identified. Mycoflora of leaves of H. portulacoides growing in
two salt marshes showed a high presence of Alternaria tenuis and other Pleosporales, together
with Cladosporium herbarum. More recently, these finding were confirmed by molecular
studies (BOX-PCR fingerprinting, and sequencing of the ITS region of the ribosomal
DNA cluster) performed on 111 isolates obtained from the roots, stems, and leaves of
H. portulacoides; this revealed that 74.5 % belonged to the order Pleosporales [190]
Appendix A.6. Genus Beta L.
This genus consists of annual, biennial, or perennial species. The stems, erect or
procumbent, have alternate leaves, ovate-cordate to rhombic-cuneate; the margins are
mostly entire, with obtuse apex. The inflorescences are long spike-like cymes or glomerules,
and flowers are bisexual.
Beta vulgaris L. subsp. Maritima (L.) Arcang. (Syn.: Beta maritima L.) Mio-halophyte
Botanical traits
Biological form: hemicryptophyte (rarely therophyte).
Morphological characteristics: 20–80 cm tall, with many erect angular stems; flowers
in leafy ears; spatulate leaves up to 220 mm long and with reddened petiole.
Habitat: pebbly coastal soils.
Chorological type: Euri-Medit (Atl.).
Flowering period: June–August.
Biochemical traits
The leaves of Beta vulgaris subsp. Maritima constitute a healthy food against digestive
disorders, burns, throat pains and anaemia [191]. Shoots’ fresh weight is increased with
salinity [192]. Under salt stress, sea beet roots revealed a higher content of Cl− and Na+ ,
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and a lower content of K+ [192]. Mg content is increased in shoots and roots, while Ca is
less affected by salinity.
In a comparative study with other halophytes, B. vulgaris subsp. Maritima showed an
appreciable content of malic acid (51.36 mg/100 g d.w.) and oxalic acid (581 mg/100 g d.w.) [191].
The four chemical structures of tocopherols were detected, but α-tocopherol (vitamin E activity)
was the major component. Total phenols (62 mg/100 g d.w.), total flavonoids (21.6 mg/100 g d.w.),
and vitamin C (20 mg/100 g d.w.) were also present in the leaf extracts, and the antioxidant
activity was significantly correlated with the antioxidant compounds [191]. The basal leaves
contain fatty acids, such as α-linolenic acid, linoleic acid, and palmitic acid. The aerial parts
contain essential oil rich in sesquiterpenes (69.5%) with a prevalence of γ-irone (26.3%) [193]. They
showed antioxidant, cytotoxic, anticholinesterase and anti-tyrosinase activity.
Appendix B
BRASSICACEAE Burnett—Dicotyledons, herbaceous, annual, and perennial, and
shrubs. Leaves without stipules, flowers arranged in racemes, panicles, or corymbus heads
or spikes. Each flower has four petals, set alternating with the sepals, and six stamens.
Fruit is silique or silicle. Cosmopolitan.
Appendix B.1. Genus Cakile Mill.
Annual plants with an erect or decumbent stem. The common species in Europe and
North America grow close to the coast, often in dunes. Their leaves are fleshy. Flowers
are typically pale mauve to white, with petals about 1 cm in length. Each fruit has two
sections, one that remains attached to the adult, and another that falls off for dispersal by
wind or water.
Cakile maritima Scop. subsp. maritima. Halo-nitrophyle (Psammophile)
Botanical traits
Biological form: scapose therophyte.
Morphological characteristics: Stem 10–30 cm tall, often devoid of leaves. Odd-pinnate
divided leaves (max 50 mm long); small lilac flowers; siliqua (10–20 mm) formed by two
superimposed articles, the lower more or less rhombic, the upper conical.
Habitat: sandy coasts, in the dune belt of drift lines.
Chorological type: Medit.-Atl.
Flowering period: January–December.
Biochemical traits
Cakile maritima (Sea Rocket) is a facultative halophyte that tolerates high salt concentration.
Under salinity conditions, fatty acid contents have been detected in the leaves, with ω6 PUFAs as the major fatty acid group (17.88%) [168]. Amino acids—such as GABA, proline
and glycine—and sugar content increased, while the phenolic content decreased, in plants
subjected to high salt concentration [194]. Other metabolites, such as flavonoids, flavonoid
glycosides, sinapic and chlorogenic acid derivatives, are not affected by salinity [57].
Cakile maritima has a high antioxidant capacity and maintains a high content of αtocopherol when exposed to short-term NaCl treatment [195]. The leaves contain high
levels of vitamins, proteins, and minerals [196]. Several minerals (Na, K, Ca, Mg, S) are
detected in leaves—as are micronutrients such as Fe, Zn, and B—depending on salt level
concentrations [57]. The ratio of Ca/P (about 1.0) is considered a good value for good Ca
and P intestinal absorption. Oxalic acid content and the oxalic acid/Ca ratio are high in
C. maritima, while the ratio of K/Na is low [196].
Plant mycobiota
Many mycotoxigenic Alternaria species (e.g., A. alternata, A. mali, A. arborescens) were
isolated from fresh tissues of C. maritima in Tunisia. The Alternaria population showed
that most of the strains (90%) produced at least one of four assessed mycotoxins (alternariol, alternariol methyl ether, tenuazonic acid, and altenuene), sometimes at very high
levels [131].
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Appendix C
PORTULACACEAE Juss.—Monotypic taxon that only contains the genus Portulaca.
Dicotyledons, succulent annual herbs growing flat on the ground. Small, fat leaves. Small
flowers with 2 sepals, 5 to 7 short-lived petals, and typically 6 to 40 stamens (sometimes
more or less). Fruit is capsule. Sub cosmopolitan.
Portulaca oleracea L. subsp. oleracea. Xerophyte
Botanical traits
Biological form: therophyte.
Morphological characteristics: stems are round, thick, succulent and mostly prostrate.
They range in colour from light green to reddish brown. The leaves are alternate or nearly
opposite and sessile along the stems. The leaves are rather thick and succulent. The small,
yellow flowers occur singly or in small, terminal clusters, and consist of five yellow petals
and two green sepals. Fruit is capsule and splits open around the middle.
Habitat: ruderal areas and occasionally in salty soils.
Chorological type: (Sub-Cosmopol.) Cryptogenic.
Flowering period: May–October
Biochemical traits
Portulaca oleracea is an underutilized halophyte plant, already consumed as a vegetable
in a variety of ways around thew world [197]. Nowadays, it is rich in omega-3 and omega-6
fatty acids (ω-3 and ω-6-FAs) as well as proteins, carbohydrates, carotenoids, vitamins
A and C, and minerals [198]. Secondary metabolites are also present in the whole plant
(leaves, stems, and roots) with a high content of phenolic compounds, especially lignans,
which are important for ethno-pharmaceutical use [198]. The extract of this species is
considered a potential source of melanosis-inhibiting compounds, for its diphenol oxidaseinhibiting activity [199]. Recently, microgreens of purslane have been produced under
salinity to emphasize the potentiality of this plant cultivation; the content of total phenolics,
flavonoids, carotenoids, and fatty acids, as well as the total antioxidant capacity content,
are positively affected by salinity in P. oleracea microgreens grown with 80 mM NaCl in the
nutrient solution [81].
Plant mycobiota
Some culturable endophytic fungi of P. oleracea, collected from Hohhot, Inner Mongolia,
belonged to the genera Penicillium and Fusarium [200]. Fusarium solani was the most
common species identified on the roots of P. oleracea, collected from the El-Kharga Oasis
in Egypt. In addition, the entomopathogenic fungus Beauveria bassiana was found in leaf
tissue for the first time in 2021 [201].
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