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Although they represent only 2% of terrestrial plant species, halophytes are present in about half the higher plant families and represent a wide diversity of plant forms. Despite their polyphyletic origins, halophytes appear to have evolved the same basic method of osmotic adjustment: accumulation of inorganic salts, mainly NaCl, in the vacuole and accumulation of organic solutes in the cytoplasm. Differences between halophyte and gly-cophyte ion transport systems are becoming apparent. The pathways by which Na and Cl enters halophyte cells are not well understood but may involve ion channels and pinocytosis, in addition to Na and Cl transporters. Na uptake into vacuoles requires Na/H antiporters in the tonoplast and H ATPases and perhaps PPi ases to provide the proton motive force. Tonoplast antiporters are constitutive in halophytes, whereas they must be activated by NaCl in salt-tolerant glycophytes, and they may be absent from salt-sensitive glycophytes. Halophyte vacuoles may have a modified lipid composition to prevent leakage of Na back to the cytoplasm. Becuase of their diversity, halophytes have been regarded as a rich source of potential new crops. Halophytes have been tested as vegetable, forage, and oilseed crops in agronomic field trials. The most productive species yield 10 to 20 ton/ha of biomass on seawater irrigation, equivalent to conventional crops. The oilseed halophyte, Sali-cornia bigelovii, yields 2 t/ha of seed containing 28% oil and 31% protein, similar to soybean yield and seed quality. Halophytes grown on seawater require a leaching fraction to control soil salts, but at lower salinities they outperform conventional crops in yield and water use efficiency. Halophyte forage and seed products can replace conventional ingredients in animal feeding systems, with some restrictions on their use due to high salt content and antinutritional compounds present in some species. Halophytes have applications in recycling saline agricultural wastewater and reclaiming salt-affected soil in arid-zone irrigation districts.
Content may be subject to copyright.
Critical Reviews in Plant Sciences,
18(2):227–255 (1999)
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Salt Tolerance and Crop Potential of Halophytes
Edward P. Glenn and J. Jed Brown
Environmental Research Laboratory, 2601 East Airport Drive, Tucson, Arizona 85706
Eduardo Blumwald
University of Toronto, Toronto, Ontario, Canada, M5S 3B2
Although they represent only 2% of terrestrial plant species, halophytes are present in about half the
higher plant families and represent a wide diversity of plant forms. Despite their polyphyletic origins, halophytes
appear to have evolved the same basic method of osmotic adjustment: accumulation of inorganic salts, mainly
NaCl, in the vacuole and accumulation of organic solutes in the cytoplasm. Differences between halophyte and gly-
cophyte ion transport systems are becoming apparent. The pathways by which Na
and Cl
enters halophyte cells
are not well understood but may involve ion channels and pinocytosis, in addition to Na
and Cl
transporters. Na
uptake into vacuoles requires Na
antiporters in the tonoplast and H
ATPases and perhaps PP
ases to provide
the proton motive force. Tonoplast antiporters are constitutive in halophytes, whereas they must be activated by
NaCl in salt-tolerant glycophytes, and they may be absent from salt-sensitive glycophytes. Halophyte vacuoles may
have a modified lipid composition to prevent leakage of Na
back to the cytoplasm.
Becuase of their diversity, halophytes have been regarded as a rich source of potential new crops. Halophytes
have been tested as vegetable, forage, and oilseed crops in agronomic field trials. The most productive species yield
10 to 20 ton/ha of biomass on seawater irrigation, equivalent to conventional crops. The oilseed halophyte,
cornia bigelovii
, yields 2 t/ha of seed containing 28% oil and 31% protein, similar to soybean yield and seed qual-
ity. Halophytes grown on seawater require a leaching fraction to control soil salts, but at lower salinities they
outperform conventional crops in yield and water use efficiency. Halophyte forage and seed products can replace
conventional ingredients in animal feeding systems, with some restrictions on their use due to high salt content and
antinutritional compounds present in some species. Halophytes have applications in recycling saline agricultural
wastewater and reclaiming salt-affected soil in arid-zone irrigation districts.
salt stress, saline water irrigation, seawater crops, osmotic adjustment, sodium uptake.
In 1980 it was predicted that genetic manip-
ulation would lead to breakthroughs in crop
production on saline water such that ordinary
crops like barley and tomato could be grown on
seawater (Epstein et al., 1980). However, re-
cent assessments have been gloomy. One re-
view points out that from 1980 to 1995 over
300 papers a year were published on mecha-
nisms of salt tolerance in higher plants, yet few-
er than a dozen salt-tolerant cultivars were
released, offering only slight improvement over
the parent lines (Flowers and Yeo, 1995). In
fact, it has been questioned whether any culti-
vars bred for salt tolerance have been commer-
cially successful. Farmers are still better off
planting yield-selected rather than salt-selected
lines in salty soils (Richards, 1992). Two lead-
ing biochemists who take a molecular approach
to salt-tolerance research called for a moratori-
um on further plant breeding until the molecu-
lar genetics are better understood (Bohnert and
Jensen, 1996); a leading breeder who takes a
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tion of this material without the consent of the publisher is prohibited.
physiological approach responded that molecu-
lar biologists project “...the optimism of blue
skies researchers advertising their wares” (re-
ply by Flowers in Bohnert and Jensen, 1996).
Almost all our modern crops are derived
from glycophytes, plants apparently lacking the
genetic basis for salt tolerance, and they have
received the most research attention. All sides
now call for a better understanding of how nat-
urally adapted plants (halophytes) handle salts.
Study of halophytes can be instructive from
three perspectives. First, the mechanisms by
which halophytes survive and maintain produc-
tivity on saline water can be used to define a
minimal set of adaptations required in tolerant
germplasm. This knowledge can help to focus
the efforts of plant breeders and molecular biol-
ogists working with conventional crop plants
(Bohnert et al., 1995; Glenn et al., 1997b; Niu
et al., 1995; Rausch et al., 1996; Serrano, 1996;
Serrano and Gaxiola, 1994; Zhu et al., 1997).
Second, halophytes grown in an agronomic set-
ting can be used to evaluate the overall feasibil-
ity of high-salinity agriculture, which depends
on more than finding a source of tolerant germ-
plasm (Glenn et al., 1997a; Miyamoto, 1996;
Miyamoto et al., 1996; Rhoades, 1993; van
Schilfgaarde, 1993). Third, halophytes may be-
come a direct source of new crops (Aronson,
1989; Boyko and Boyko, 1959; Boyko, 1966;
Somers, 1975; Choukr-Allah et al., 1996;
Glenn et al., 1991, 1997a; Llerena, 1994;
O’Leary, 1994; Squires and Ayoub, 1994). Af-
ter briefly considering the diversity of halo-
phytes, we review the current understanding of
halophyte salt-tolerance mechanisms and their
relevance to efforts to improve crop plants and
the status of halophyte agronomy.
Halophytes are considered to be rare plant
forms that arose separately in unrelated plant
families during the diversification of an-
giosperms (O’Leary and Glenn, 1994); in this
they resemble epiphytes, saprophytes, xero-
phytes, aquatics, and marsh plants (Kremer and
VanAndel, 1995). No comprehensive list of
halophyte species exists, due partly to the prob-
lem of defining the lower salt-tolerance limit at
which a plant should be considered a halophyte.
Aronson (1989) compiled a partial list of halo-
phytes containing 1560 species in 550 genera
and 117 families. His list was drawn from liter-
ature reports and interviews with researchers as
part of a program to assemble a world halo-
phyte collection to screen for new crops (Aron-
son et al., 1988). He used a broad definition of
halophyte that included any plant that was re-
portedly more tolerant than conventional crops,
for which the upper salt content of irrigation
water was taken to be 5 g/l total dissolved solids
(TDS) (85 m
as NaCl) (Ayers and Wescott,
1989). However, his list only included plants
that had potential as food, forage, fuelwood, or
soil stabilization crops.
Based on a comparison of Aronson’s en-
tries with the known number of species in se-
lected halophytic genera, Le Houerou (1993)
estimated that Aronson’s list probably included
20 to 30% of the terrestrial halophytic flora,
which would then reach 5000 to 6000 species,
or 2% of world angiosperm species. Of the spe-
cies in the list, 57% came from just 13 families.
The largest number of halophyte species are in
the Chenopodiaceae; over half of its 550 spe-
cies are halophytic. The three superfamilies,
Poaceae (grasses), Fabaceae (legumes), and
Asteraceae (composites), also have large num-
bers of halophytes, although they represent
fewer than 5% of the species in these families.
These families proliferated through radiative
evolution into many diverse niches, including
saline habitats, during the early evolution of an-
giosperms. Flowers et al. (1977) plotted the oc-
currence of halophytes in the major orders of
flowering plants in a dendogram showing prob-
able relationships between orders. Halophytes
occurred throughout the dendogram in both
primitive (e.g., Laurales, Nymphales) and ad-
vanced (Asterales, Orchidales) orders.
In keeping with their multiple origins, halo-
phytes differ widely in their degree of salt tol-
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erance (Flowers et al., 1977; Ungar, 1991).
Aronson’s (1989) list can be viewed as a pyra-
mid, with the base consisting of several thou-
sand species exhibiting modest tolerance,
narrowing toward the top to perhaps a few doz-
en species capable of high production on sea-
water. At the low end of the salt-tolerance
scale, some crop plants such as sugar beet (
, Chenopodiaceae), date palm (
, Arecacea) and barley (
, Poaceae) can be cultivated on irriga-
tion water approaching 5 g/l TDS (Ayers and
Wescott, 1989) and are sometimes considered
halophytes. At the upper end, species such as
Salicornia bigelovii
(Chenopodiaceae) can
yield as much biomass and seed as convention-
al crops even when the soil solution exceeds
70 g/l TDS (1.3
as NaCl, twice seawater sa-
linity) (Glenn et al., 1991, 1997). The continu-
ous nature of the salt-tolerance gradient extends
downward through the glycophytes as well,
eventually reaching the most sensitive crops
such as rice and bean, which are harmed by 20
to 50 m
NaCl (Greenway and Munns, 1980).
Halophytes also differ widely in their ap-
parent adaptations to handle salts (Ungar,
1991). Classification schemes have been con-
structed that attempt to match morphological
and physiological characters to specific halo-
phyte habitats or growth strategies. Le Houerou
(1993) reviewed three schemes that divided
halophytes into 4 types based on the degree of
salt tolerance, 5 types based on ecological asso-
ciations, and 12 types based on edaphic factors.
However, these classification systems have lit-
tle predictive value. For example, a recent study
attempted to correlate leaf anatomy with zona-
tion of 13 halophytes along a transect in a salt
marsh in Jordan (Weiglin and Winter, 1991).
The purpose was to determine if species with
xeromorphic leaves were distributed differently
than those with mesomorphic leaves; the spe-
cies along the transect differed as well in pho-
tosynthetic pathway (C
or C
), degree of
succulence, and numerous other traits, and
were variously classified as euhalophytes (true
halophytes), psuedohalophytes (salt avoiders),
or crinohalophytes (salt excretors). All combi-
nations of plant types coexisted at 9 of the 11
stations along the transect, and the authors con-
cluded there was no correlation between posi-
tion in the marsh and leaf morphology or any of
the other traits measured in this study.
Earlier studies reported that salt marsh
halophytes can be divided into physiotypes
based on their shoot water content and tendency
to accumulate ions, but the physiotype concept
could not be used to predict salt tolerance or zo-
nation in the marsh (Albert and Popp, 1977;
Storey et al., 1977; Gorham et al., 1980). Salt
excretion is a well-known example of contrast-
ing traits; black mangroves (
have well-developed salt glands that appear to
function in salt tolerance by allowing the plant
to excrete excess salts onto the leaf surface; yet,
the equally salt-tolerant red mangroves (
spp.) excrete no salt at all (Popp et al.,
The taxonomic diversity of halophytes rais-
es the possibility that salt tolerance might be in-
troduced into crop plants through wide crosses
(Epstein et al., 1980). Crops with salt-tolerant,
wild relatives include wheat (related to
and other wild members
of the Triticeae) (Gorham and Wyn-Jones,
1993), barley (related to sea oats,
) (Aronson, 1989), tomato (related
to wild, salt-tolerant tomatoes, including
persicum cheesmanii
L. pimpinellifolium
(Asins et al., 1993), and fodderbeet (
Beta vul-
, related to seabeet,
B. vul-
) (Rozema et al., 1993). The
feasibility of transferring salt tolerance be-
tween species has been demonstrated for
wheat, a glycophyte. A gene (+Knal) for en-
hanced K
discrimination was transferred
from bread wheat (
Triticum aestivum
) to duram
wheat (
T. turginsum
) using conventional cross-
ing, with the hybrid plants exhibiting slightly
improved salt tolerance (Dvorak et al., 1994).
Similarly, salt tolerance genes from
were expressed in hexaploid wheat
(Schachtman et al., 1992). However, the hope
for improving salt tolerance in large steps
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through glycophyte-halophyte crosses has so
far not been fulfilled, attributed to the multigen-
ic nature of halophyte salt tolerance (Flowers
and Yeo, 1995).
Given their diverse origins, any trait that
turns out to be universally present in halophytes
should be suspected to represent convergent
evolution of an essential trait for salt tolerance.
Such a trait should be singled out for scrutiny as
a candidate for eventual transfer from halo-
phytes to glycophytes (Bohnert et al., 1995;
Niu et al., 1995; Serrano, 1996; Zhu et al.,
1997). We attempt to identify such traits in the
next section. Also by their diversity, halophytes
offer a rich source of germplasm to search for
new crops as well as useful genes. At least a
few species might be expected to have desirable
crop characteristics that can be enhanced
through conventional breeding to make them
useful for agriculture. Halophytes have the ad-
vantage of being preadapted to salt tolerance,
which has proven so difficult to introduce into
glycophytes (O’Leary, 1994).
A. Physiology of Halophyte Salt
In contrast to the situation with glyco-
phytes, for which salt tolerance mechanisms
are still vigorously debated (Wyn Jones and
Gorham, 1986; Munns, 1993; Neumann, 1997),
a clear picture of the physiology of halophyte
salt tolerance has emerged, and several key en-
zyme systems and genetic control mechanisms
have been identified. The basic nature of halo-
phyte salt tolerance was described in a 1977 re-
view article (Flowers et al., 1977) that is still
widely cited, although it has been updated
(Flowers and Yeo, 1986, 1988). Halophytes use
the controlled uptake of Na
(balanced by Cl
and other anions) into cell vacuoles to drive wa-
ter into the plant against a low external water
Dicotyledonous halophytes generally accu-
mulate more NaCl in shoot tissues than mono-
cotyledonous halophytes (especially grasses),
which led early researchers to characterize the
former as “includers” and the latter as “exclud-
ers” (Greenway, 1968; Ahmad et al., 1981a,b).
The enhancement of exclusion mechanisms
still appears to be the principal strategy of re-
searchers trying to improve the salt tolerance of
grains (Ashraf, 1994; Dvorak et al., 1994; Ru-
bio et al., 1995; Schachtman et al., 1992; Yeo,
1994), even though Greenway corrected his
earlier characterization of grasses as strict ex-
cluders in 1980 (Greenway and Munns, 1980).
Studies of
Spartina alterniflora
(Bradley and
Morris, 1991),
Leptochloa fusca
(Jeschke et al.,
Sporobolus viginicus
(Blits and Gal-
lagher, 1991; Marcum and Murdoch, 1992),
barley (Fricke et al., 1996),
spp. (Er-
dei and Kuiper, 1979) and
spp. (Nai-
doo, 1994) show that grasses and other
monocotyledonous halophytes use Na
into leaves for osmotic adjustment, as do dicot
halophytes. Because of their lower cell vacu-
olar volume and leaf water content, grasses do
not need as much Na
uptake per unit of growth
as typical dicotyledonous halophytes, so they
maintain lower Na:K ratios on exposure to salt,
but with a few exceptions (e.g., Matsushita and
Matoh, 1992) they are not strict excluders
(Glenn, 1987).
B. Performance of Halophytes on a
Salinity Gradient
The central role of Na
uptake in determin-
ing the salt tolerance of halophytes is illustrated
in Figures 1 and 2, which summarize results
from 20 dicotyledenous (Glenn and O’Leary,
1984) and 27 monocotyledonous halophytes
(Glenn, 1987) screened under similar condi-
tions along a salinity gradient. The plants were
assembled from a world collection of species
reportedly exhibiting unusual salt tolerance,
and spanned the range from essentially glyco-
phytic species such as wheat and sunflower to
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Growth of dicotyledenous halophytes and salt-tolerant glycophytes along a salinity gradient in a green-
house screening experiment (Glenn and O’Leary, 1984). Ten species survived only to 0.18 mol/L NaCl (open circles
= less tolerant species) whereas 10 others survived to 0.72 mol/l NaCl (closed circles = more tolerant species). Pan-
els show relative growth rates (RGR); leaf osmotic pressure contributed by Na
, K
, and Cl
; and Na
, K
, water and
Na:K content of leaves. Error bars are SE of means across species.
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Growth of monocotyledenous halophytes and salt-tolerant glycophytes along a salinity gradient in a
greenhouse screening experiment (Glenn, 1987). Fifteen species survived only to 0.18 mol/l NaCl (open circles =
less tolerant species), whereas 12 others survived to 0.54 mol/l NaCl (closed circles = more tolerant species). Panels
show relative growth rates (RGR); leaf osmotic pressure contributed by Na
, K
, and Cl
; and Na
, K
, water and Na:K
content of leaves.
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highly tolerant salt marsh plants such as
. The species are pooled into
two groups on each graph; those that had posi-
tive growth rates up to seawater salinity
(540 m
NaCl or beyond) (= more tolerant) or
those that had positive growth to 180 m
but did not survive on 540 m
NaCl (= less tol-
Growth of the more tolerant dicot halo-
phytes was stimulated by 180 m
NaCl rela-
tive to controls, whereas less-tolerant dicots
and all the grasses grew better on nonsalinized
solution. This is not an absolute division be-
cause grasses and less-tolerant dicots may be
stimulated by salinities lower than 180 m
NaCl (i.e., 25 to 100 m
NaCl) (Ungar, 1991).
Although grasses were not stimulated by NaCl,
the more tolerant grasses species grew as well
as the more tolerant dicots on higher salt solu-
tions. There was no inverse relationship be-
tween growth rate and salt tolerance;
halophytes are not inherently slow-growing, as
is sometimes assumed (Niu et al., 1995). The
more tolerant dicot halophytes and both groups
of grasses were osmoconformers, maintaining
an osmotic pressure in the shoot approximately
2 to 3 times higher than the osmolality of the
external solution. On the other hand, the less-
tolerant dicots did not have the same ability to
osmotically adjust. Na+K (times two to account
for balancing anions) accounted for 80 to 95%
of the cell sap osmotic pressure of both grasses
and dicots at 180 m
NaCl and above, and Na
was higher than K
in shoot tissues of all plant
on saline solutions, with the exception of sun-
flower (
Helianthus annuus
) (Glenn and
O’Leary, 1984) and common reed (
) (Glenn, 1987), which excluded Na
but did not survive above 180 m
NaCl. Thus,
a (nearly) universal trait of salt-tolerant plants
is the ability to accumulate NaCl for osmotic
Comparative studies of halophyte species
within a genus, for example, Plantago (Erdei
and Kupier, 1979), or of genotypes within a
species, such as
Atriplex canescens
(Glenn et
al., 1992; 1994, 1996, 1997),
Armeria maritima
(Koehl, 1997a,b), and
Salsola kali
and Breckle, 1995), also show that halophyte
salt tolerance can be positively correlated with
capacity for Na
uptake into the shoots. This re-
lationship has been studied in detail in acces-
sions of
A. canescens,
a xerohalophyte, adapted
to both drought and salt stress. Growth rates on
saline solutions differed among genotypes and
was strongly (r = 0.88***) correlated with ca-
pacity for Na
accumulation (n = 16 accessions)
and negatively (r = –0.90***) correlated with
capacity for K
uptake (Glenn et al., 1996), the
opposite of findings usually reported for halo-
phytic grasses (Blits and Gallagher, 1991; Je-
schke et al., 1995 — see also Figure 2).
Differences in ion uptake capacity among gen-
otypes were evaluated under nonsaline condi-
tions prior to exposure of plants to a salinity
gradient; hence, differences were not a conse-
quence of salt treatment but were true predic-
tors of performance.
C. Molecular and Genetic Determinants of
Salt Tolerance
The most common view is that functional
salt tolerance requires a series of integrated ad-
aptations involving cellular systems, tissues
and the whole plant (e.g., Cheeseman, 1988;
Leach et al., 1990; Flowers and Yeo, 1995).
Yet, some molecular biologists predict that just
a few basic biochemical tolerance mechanisms,
related through the effects of water-deficit and
osmotic stress on cellular processes, may be
sufficient to confer tolerance (Bohnert et al.,
1995; Serrano, 1996; Serrano and Gaxioloa,
1994; Zhu et al., 1997). They hypothesize that
these mechanisms exist in glycophytes as well
as halophytes but are more highly developed in
adapted species. We test this viewpoint against
what is known about specific tolerance mecha-
nisms of halophytes, particularly those in-
volved in ion homeostasis. The discussion
centers on Na
, but in reality Cl
is the common
balancing anion for Na
, and it plays an equally
important cellular role. Na
has received the
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most attention because of its inhibitory effect
on enzyme activity and because it interferes
with K
uptake and Ca
functions (in glyco-
phytes), whereas Cl
has received much less at-
tention (Cheeseman, 1988).
It has been stated many times that halo-
phyte cytoplasmic enzymes are not adapted to
high salt levels, but there are differences be-
tween halophyte and glycophyte enzymes sys-
tems. For example, translation of wheat germ
mRNA by polysomes extracted from leaves of
halophytes (
Atriplex isatidea
Inula crith-
) had higher K
and Mg
optima than
polysomes from glycophyte leaves (pea, wheat,
rice, and barley), and Na
substituted for K
better in the halophtye than the glycophyte sys-
tems (Flowers and Dalmond, 1993). Interest-
ingly, the extracellular (cell wall) enzymes of
both glycophytes and halophytes are extremely
salt tolerant (Thiyagarajah et al., 1996), sug-
gesting that salt stress exerted through a high
salinity in the apoplastic space may have been
during the evolution of angiosperms.
Although the flux of Na
through the cyto-
plasm of halophyte cells might be high, the con-
centration of Na
in the cystoplasm is
maintained at nontoxic levels (10 to 150 m
M by
different estimates) (Binzel et al., 1988;
Cheeseman, 1988; Flowers et al., 1986;
Fitzgerald et al., 1992) through the operation of
ion translocases at the plasma membrane (to
import Cl
into the cell and to export Na
out of
the cell) and tonoplast (to sequester Na
and Cl
in the vacuole) (Barkla and Blumwald, 1991;
Bennett and Spanswick, 1983; Blumwald and
Poole, 1985a,b; Bluwald and Gelli, 1997;
Churchill and Sze, 1984; Dupont, 1992; Niu et
al., 1995; Pope and Leigh, 1987; Rausch et al.,
1992; Serrano and Gaxiola, 1994; Zhu et al.,
1997). Cell turgor is maintained by storage of
NaCl in the cell vacuole, which contains 90%
or more of cell water. The water potential in the
cystoplasm of halophilic algae and higher
plants is adjusted by the accumulation of organ-
ic solutes (Bohnert et al., 1995; Gorham et al.,
1980; Koehl, 1997; Storey et al., 1977; Rhodes
and Hanson, 1993), which may also function as
osmoprotectants, stabilizing membrane and en-
zyme structures and scavenging free radicals in
a high osmotic environment (Bohnert et al.,
This method of osmotic adjustment re-
quires at least three types of adaptation with re-
spect to ion homeostasis alone: (1) the capacity
for controlled but rapid uptake of Na
and Cl
into cells to support turgor-driven growth; (2)
efficient sequestration of Na
and Cl
into cell
vacuoles; (3) and mechanisms to ameliorate the
effects of excess entry of NaCl into the plant. In
addition, halophytes require the ability to elab-
orate large quantities of compatible osmotica.
We do not treat the role of organic solutes in the
osmotic regulation of halophytes in detail here,
but the subject has been reviewed by others
(Rhodes and Hanson, 1993; Bohnert et al.,
D. NaCl Uptake into Halophyte Cells
Surprisingly little is known about how Na
enters halophyte cells and tissues (Cheeseman,
1988). In glycophytes, two type of leakage are
thought to be responsible for Na
entry into the
plant. In some plants, such as rice, 20% or more
of water entry into the plants is via transpira-
tional bypass flow, by which water travels
through the root in extracellular spaces rather
than in the symplasm, and bypasses the endo-
dermis to enter the transpiration stream directly
(Garcia et al., 1997). If there is greater than
about 50 mM NaCl in the external solution,
enough Na
can be carried to the shoot via by-
pass flow to poison the leaves. In other plants,
such as wheat, transpiration bypass flow is low
(Garcia et al., 1997), but Na
leaks into the
plant via the symplasm of root cortical cells by
competitive binding onto K
transporters or cat-
ion channels (Rubio et al., 1995; Schachtman
and Schroeder, 1994; Schachtman et al., 1991).
This leakage not only allows damaging levels
of Na
to enter the plant, but it depresses K
take. In plants growing at low salinity, internal
concentrations can exceed external concen-
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trations by two orders of magnitude, and in gen-
eral the Cl
concentration in the plant appears to
increase proportionally to the external supply
(Flowers, 1988). Uptake of Cl
appears to be
mediated by the operation of a plasma mem-
brane Cl
symporter in Chara (a green al-
gae) (Sanders, 1980) and perhaps also barley
(Jacoby and Rudich, 1980).
These mechanisms do not seem plausible
for halophytes, at least with respect to Na
try. In the first place, halophytes often have
thick layers of suberin or double layers of
suberized cells at the root endodermis cells to
prevent transpiration bypass flow (Anderson,
1974; Poljakoff-Mayber, 1974; Kramer, 1984).
Direct measurements in Aster tripolium have
shown virtually no penetration of NaCl past the
root epidermis except by uptake into the sym-
plasm (Zimmerman et al., 1992; see also Yeo
and Flowers, 1986, for a discussion of Na
take by Suaeda maritima). Further, cellular Na
and K
uptake apparently are unlinked in halo-
phytes, which maintain steady rates of K
take across wide ranges of external Na
and rate
of Na
uptake (Flowers et al., 1977; Glenn and
Brown, 1997; Glenn et al., 1996; Koehl,
1997a,b; Reimann, 1992; Reimann and Breck-
le, 1993, 1995) (see Figures 1 and 2). Hence, it
is unlikely Na
leaks into halophyte cells via K
Rates of Na
uptake into halophtes can
be extremely high (Yeo and Flowers, 1986;
Cheeseman, 1988). In succulent halo-
phytes such as Suaeda maritima growing at
340 mM NaCl, Na
uptake by roots is
10 mmol/gdw/day, 10 times greater than K
take and probably too rapid for known carrier-
transport processes (Yeo and Flowers, 1986).
Active uptake may not be necessary because
there is an electrochemical gradient of Na
across the cell membrane (Cheeseman, 1988).
Uptake of Na
and Cl
into halophyte cells may
be via gated cation and anion channels, or even
by vesicles (Cheeseman, 1988; Yeo and Flow-
ers, 1986; Kurkova et al., 1992; Kurkova and
Balnokin, 1994). Electron micrographs of four
halophytes growing on 400 mM NaCl showed
pinocytic invaginations on the cell membrane
and vesicular bodies in the vacuoles, which
were interpreted as evidence that ion transport
from the apoplast to the vacuole in above-
ground organs of salt-accumulating halophyte
is carried out by means of pinocytosis (Kurkova
and Balnokin, 1994).
E. Sequestration of NaCl Into Vacuoles
must be actively pumped into the vac-
uole from the cytoplasm due to the low concen-
tration in the cytoplasm, whereas Cl
enter passively via anion channels to balance
electrical charge differences across the mem-
brane (Blumwald, 1987; Dupont, 1992; Barkla
et al., 1994; Rausch et al., 1996; Pantoja et al.,
1990, 1992). Na
uptake into the vacuole ap-
pears to be mediated by Na
-anitporters in
the tonoplast, working in concert with H
Pases and perhaps PP
ases (Rea et al., 1992)
that provide the proton motive force. Much
more work has been done on the H
which have homology with enzymes from other
organisms and therefore were easily cloned
(Dupont, 1992), than with Na
which have been cloned only recently (Apse et
al., 1998; Darley et al., 1998).
Blumwald and Poole (1985a, 1987), work-
ing with red beet and sugar beet, were the first
to describe antiporter activity in the tonoplast of
salt-tolerant higher plants. Tonoplast antiporter
activity has also been identified in roots or
leaves of the halophytes Atriplex nummularia
(Hassidim et al., 1990), Plantago maritima
(Staal et al., 1991), Atriplex gmelini (Matoh et
al., 1989), and Mesembryanthemum crystalli-
num (Barkla et al., 1995), as well as glyco-
phytes such as barley (Garbarino and Dupont,
1988, 1989), cotton (Hassidim et al., 1990), and
sunflower (Ballesteros et al., 1997). In some
species, the vacuolar Na
antiport appeared
to be constitutive, while in others the antiport
was only activated by high NaCl concentra-
tions. Increasing concentrations of NaCl in the
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growth medium of sugar beet cell suspensions
did not change the K
but doubled the V
the antiport (Blumwald and Poole, 1987). An
increase in V
for the antiport with no change
in apparent K
suggested the addition of more
antiport molecules to the tonoplast in response
to NaCl in the growth medium.
A similar increase in Na
antiport activ-
ity has also been reported after the exposure of
Mesembryanthemum crystallinum to high NaCl
concentrations (Barkla et al., 1995; Low et al.,
1996). Similar results were reported in sun-
flower roots (Ballesteros et al., 1997). In some
salt-tolerant glycophytes, NaCl appears to acti-
vate preexisting tonoplast antiport molecules.
In barley roots the operation of a tonoplast
antiport was demonstrated only when
the roots were grown in the presence of NaCl
(Garbarino and Dupont, 1988). The induction
of the antiport activity by salt was very fast and
appeared to be due to the activation of an exist-
ing protein rather than de novo synthesis, be-
cause the induction was observed in the
presence of protein synthesis inhibitors (Gar-
barino and Dupont, 1989).
In Plantago species the vacuolar Na
antiport is present in the salt-tolerant Plantago
maritima, but not in the more salt- sensitive
Plantago media (Staal et al., 1991). The ab-
sence of Na
antiport activity in the tono-
plast of Plantago media may be related to a
general property observed in salt-sensitive
plants (Mennen et al., 1990; Barkla et al.,
1994). As a generality, in salt-tolerant glyco-
phytes NaCl appears to activate pre-existing
tonoplast antiport molecules, whereas in halo-
phytes vacuolar antiports are constantly acti-
vated, even in plants grown in the absence of
NaCl. This observation is consistent with the
physiological data that show that halophytes
rapidly scavenge Na
from the external medium
and sequester it into the leaf cell vacuoles even
at low external levels.
NaCl also induces V-type H
-ATPase ac-
tivity in leaves of salt- treated plants (Ballester-
os et al., 1996; Dupont, 1992; Kirsch et al.,
1996; Low et al., 1996). Failure of V-type H
ATPase activity to respond to NaCl was cited
as a cause of salt sensitivity in cotton seedlings
(Lin et al., 1997); however, NaCl stimulated the
enzyme most in mature rather than immature
sugar beet leaves, which was interpreted as
showing that rapidly growing tissues may al-
ready have maximal expression (Kirsch et al.,
plays an equally important role as Na
in osmoregulation and salt-tolerance (Flowers,
1988). In salt tolerant plants, Cl
is compart-
mentalized in the vacuole in very high concen-
tration (Matile, 1988). Flucuations in cyto-
plasmic and vacuolar Cl
concentrations have
been shown to regulate the transport of other
anions into the vacuole (Martinoia et al., 1987;
Plant et al., 1994). The dissipation of a vacuolar
positive membrane potential (generated by the
activation of the vacuolar H
ATPase and H
pyrophosphatase) by anions revealed the exist-
ence of a uniport that allows Cl
to accumulate
in the vacuole in response to the membrane po-
tential generated by the H
pumps (Bennett and
Spanswick, 1983; Blumwald and Poole, 1985b;
Kastner and Sze, 1987; Pope and Leigh, 1987).
Dissipation of the membrane potential by Cl
was saturable with a K
of 2.3 mM (Kastner
and Sze, 1987).
Tonoplast channels for passive ion move-
ment of varying degrees of specificity are ubiq-
uitous in plant cells, and several distinct types
of channels involved in the transport of Cl
have been identified (Hedrich and Nehr, 1987;
Pantoja et al., 1992; Tyerman, 1992; Plant et
al., 1994). The operation of these channels pro-
vides a uniport mechanism for the transport of
into the vacuole. Because the operation of
the channel could also dissipate anion gradients
established for active transport, one would ex-
pect the channel activity to be tightly controlled
by factors such as membrane potential, Ca
and other ions. For example, intravacuolar Cl
concentrations were shown to regulate the vac-
uolar anion channel activity; high vacuolar Cl
concentrations favored the transport of nitrate
and phosphate into the vacuole, and the influx
of anions into the vacuole was coupled to Cl
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efflux into the cytosol (Plant et al., 1994). In
halophytes (and salt-tolerant glycophytes) cy-
toplasmic Cl
concentrations have been esti-
mated to be in the range of 25 to 150 mM
(Cheeseman, 1988, Flowers et al., 1986). The
concerted action of the two H
pumps would generate a positive-inside vacu-
olar membrane potential of 40 to 80 mV (Blum-
wald, 1987), and this value could be
underestimated if the salt-induced stimulation
of the vacuolar H
ATPase is taken into consid-
eration. Thus, vacuoles from salt-tolerant
plants would be able to accumulate Cl
at con-
centrations ranging from 200 to 1000 mM with-
out expenditure of additional cellular energy.
F. Retention of NaCl in Halophyte
Once inside the vacuole, Na
is potentially
susceptible to leakage back to the cytoplasm
due to the steep concentration gradient between
compartments; such leakage would increase the
rate at which Na
would need to be pumped into
the vacuole in the first place (Maathuis et al.,
1992). Cl
would leak only if the leakage of Na
proceeded to the point that the vacuole was no
longer positively charged with respect to the
cytoplasm. Vacuoles of high purity isolated
from Suaeda maritima had highly saturated fat-
ty acids and other lipid characteristics consis-
tent with minimizing permeability to NaCl, but
the protein content was low and the polypeptide
content differed little from glycophyte tono-
plast membranes (Leach et al., 1990). Further-
more, tonoplast cation channels through which
might leak back to the cytoplasm were
found to be closed at physiological concentra-
tions of Na
when measured in isolated S. mar-
itima vacuoles by the patch-clamp technique
(Maathius et al., 1992). In the absence of leak-
age, a relatively small proportion of tonoplast
ATPase activity would be needed to main-
tain NaCl compartmentation (10% in mature
cells but more in expanding cells) (Maathius et
al., 1992). Hence, salt tolerance may not require
large expenditures of metabolic energy, raising
the possibility that high yields are possible at
high salinity.
G. Role of Plasma Membrane Anitports
and ATPases
At the cellular level, halophytes and glyco-
phytes can export Na
from the cytoplasm to
the extracellular space via plasma-membrane
- antiports, with H
-ATPases operating
at the plasmalemma providing the H
chemical gradient (Dupont, 1992; Niu et al.,
1995). A series of studies on Atriplex nummu-
laria showed evidence for a root plasmalemma
antiporter that had higher activity in plants
grown on 400 mM NaCl compared with con-
trols, whereas cotton root plasmalemma anit-
porter activity was low and not affected by
NaCl (Braun et al., 1986, 1988; Hassidim et al.,
1990). The A. nummularia antiporter was not
saturated by Na
up to 180 mM NaCl. NaCl also
induced a P-type H
-ATPase from cell suspen-
sion cultures of A. nummularia that may supply
energy for the antiporter, and up-regulation was
also observed in roots and leaves of whole
plants (Niu et al., 1993a,b, 1995). These studies
support the hypothesis that halophytes are ca-
pable of expelling Na
from the cell.
The physiological function of these en-
zymes can be questioned because the rate of en-
try of NaCl into halophytes normally appears to
be rate limiting for growth, and these enzymes
would counteract NaCl uptake. A comparison
of P-type H
-ATPase activity in salt-sensitive
and salt-tolerance species of Plantago grown in
the presence or absence of NaCl showed no dif-
ferences between species or treatments and did
not support a role for plasma membrane AT-
Pases in regulating ion transport (Bruggemann
and Jahiesch, 1987, 1988, 1989). A Na
tiporter was induced by salt in the tonoplast but
not the plasma membrane of the salt-tolerant
species (Staal et al., 1991). Other studies
showed that the same type of NaCl stimulation
of P-H
-ATPase occurred in the halophyte,
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Salicornia bigelovii and a salt-sensitive cotton
variety, suggesting that “...the activity of the
PM-ATPase is not the primary determinant in
salt tolerance and activity of the proteins on the
plasma membrane alone may be insufficient to
regulate intracellular Na
levels” (Lin et al.,
Clarification of the role of plasma mem-
brane Na
antiporters and P-H
has come from a detailed study of A. nummu-
laria plants jumped suddenly to 400 mM NaCl
(Niu et al., 1996). The salinity jump induced
plasmolysis of cortical and endodermal root
cells, presumably due to loss of water in re-
sponse to NaCl accumulation in the apoplast;
leaf mesophyll cells also showed ultrastructural
changes, although they did not undergo plas-
molysis. Apparently, the salt shock was miti-
gated in the root and not fully transferred to the
shoot. Labeled RNA probes were infiltrated
into fixed root and leaf tissues and showed the
specific accumulation of mRNA for P-H-AT-
Pase in root tip epidermal cells in the elonga-
tion zone (where first contact with Na
in root endodermal cells in the elongation zone
(where entry of Na
into the stele is controlled);
and in leaf bundle sheath cells (which are in di-
rect contact with water transported to the leaf in
the xylem). Plants on 200 mM NaCl did not
show ultrastructural change or up-regulation of
P-H-ATPase, and 7 days after transfer to
400 mM NaCl, cell structures of plants returned
to normal appearance and mRNA for P-H-AT-
Pase returned to barely detectable levels. Pre-
sumably, the P-H-ATPase levels were up-
regulated to energize increased rates of second-
ary ion transport across the plasma membrane
to control uptake of Na
into cells and tissues
during osmotic adjustment. Long-term adjust-
ment apparently occurred through an increase
in the resistance of the root cells to Na
(mechanism unknown but presumably involv-
ing lower plasma membrane permeability to
NaCl), and the plasmalemma Na
system operated as a short-term mechanism to
bale excess Na
from the cell before such ad-
justment occurred. These molecular studies
support earlier physiological findings on the
rapid adjustment of ion uptake by Suaeda mar-
itima in response to salinity jumps (Clipson,
H. Ancillary Mechanisms of Salt
In addition to the capacity to sequester
NaCl in vacuoles and to produce compatible os-
motica in the cytoplasm, halophytes have a di-
versity of secondary mechanisms to handle
excess salt. At the tissue level, some halophytes
have salt glands (Lipschitz and Waisel, 1982;
Balsamo and Thomson, 1993, 1996), salt blad-
ders (Schirmer and Breckle, 1982; Freitas and
Breckle, 1992), or succulent tissues (Kramer,
1984; Yeo and Flowers, 1986) to handle tempo-
rary imbalances of NaCl entry into the plant.
Although not all halophytes have salt excretion
organs, in those that do 50% or more of the salt
entering the leaf can be excreted (Bradley and
Morris, 1991; Freitas and Breckle, 1992; War-
wick and Halloran, 1992). Salt excretion, in
turn, may perform secondary adaptive roles,
such as light reflection from desert halophytes
(e.g., Atriplex) (Osmond et al., 1980), or re-
moval of excess salt from the root zone in salt
marsh species such as Spartina (excreted salts
are then carried away by the tides) (Bradley and
Morris, 1991). Succulence can be a mechanism
to dilute excess NaCl in the leaf tissues (Kram-
er, 1984), but the opposite phenomenon, reduc-
tion in leaf water content, is also commonly
observed when halophytes are grown at high
salinities; this concentrates NaCl in the cell sap,
reducing the amount of NaCl that must be ab-
sorbed to support osmotic adjustment (Glenn
and O’Leary, 1984; Glenn, 1987).
Halophytes can also increase their water
use efficiency in response to salt, thereby mini-
mizing the amount of water that must be tran-
spired for each unit of growth (Guy et al., 1980;
Guy and Reid, 1986; Ayala and O’Leary, 1995;
Glenn et al., 1997). C
and C
species increase
water use efficiency by lowering their stomatal
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conductance in response to salt, which decreas-
es rates of both photosynthesis and transpira-
tion but not in direct proportion, resulting in an
increase in water use efficiency (Osmond et al.,
1980). Some facultative CAM plants, such as
Mesembryanthemum crystallinum, switch from
to CAM when exposed to salt, which also in-
creases water use efficiency (e.g., Bohnert et
al., 1995; Thomas and Bohnert, 1993); the
switch to CAM is controlled by the growth
stage of the plant and can be induced by other
triggers such as low temperature, in addition to
salinity (Ratajczak et al., 1994).
Nonhalophytes also increase water use effi-
ciency in response to salt stress (Brugnoli and
Bjorkman, 1992; Brugnoli and Lauteri, 1991;
McCree, 1986; McCree and Richardson, 1987;
Osmond et al., 1980; Shalhevet, 1993; Rich-
ards, 1992), and no unique adaptations of the
photosynthetic apparatus have been identified
in halophytes (e.g., Genard et al., 1991). How-
ever, a form of feedback control of stomatal
opening by apoplastic Na
in the leaves has
been identified in the halophyte, Aster tripoli-
um, that has not been found in glycophytes
(Perera et al., 1994, 1995, 1997).
I. Feasibility of Introducing Salt Tolerance
into Glycophytes Through Gene Transfer:
A Gedanken Experiment
Because conventional breeding to improve
salt tolerance does not seem capable of yielding
breakthrough advances, it is appropriate to ask
whether direct transfer of halophyte genes into
glycophytes might work. To our knowledge no
experiments have been conducted, although
glycophyte genes have been transferred into a
halophyte through the gene gun technique (Li
and Gallagher, 1996), so the question is open to
speculation. The metabolic pathways to elabo-
rate compatible osmotica appear to be present
in all plants but may be blocked in glycophytes;
hence, genetic manipulation of the promotor re-
gions might induce these pathways in glyco-
phytes (Bohnert et al., 1995). Could glyco-
phytes then be induced to safely accumulate
NaCl to support rapid growth and osmotic ad-
justment on salt solutions (the opposite target of
conventional breeding programs that empha-
size salt exclusion)?
Imagine a rice plant capable of producing
organic solutes in the cytoplasm and with a
halophyte-type Na
antiport system inserted
into the tonoplast. Sufficient H
ATPase activi-
ty may already be present in glycophyte tono-
plasts. The choice of rice is appropriate because
NaCl enters rice plants in the transpirational by-
pass flow at about the same rate as it is taken up
by halophytes (Garcia et al., 1997; Yeo, 1994);
furthermore, it is an aquatic plant, and halo-
phytism is thought to have evolved first among
coastal hydrophytes (Ungar, 1991). With the
ability to sequester NaCl into vacuoles, excess
NaCl would be absorbed into root and shoot
cells in its passage through the plant, and it is
conceivable that salt tolerance would be vastly
improved by this single modification. Howev-
er, Leach et al. (1990) regarded the capacity of
the halophyte vacuole to retain Na
as an equal-
ly essential adaptation, and this appears to re-
quire alterations in the fatty acid profile of the
membranes in addition to a functional Na
antiporter and H
-ATPases. Doubtless, there
are many genes required for salt tolerance, but
it will still be interesting to test the affect of sin-
gle-gene additions or alterations on glyco-
phytes, if the relevant halophyte genes can be
cloned and transferred to glycophytes (Bohnert
and Jensen, 1996). In the meantime, it may be
possible to develop salt-tolerant crops through
the direct domestication of halophytes.
The Israeli scientists Hugo and Elisabeth
Boyko were the first modern researchers to
attempt to develop high salinity agriculture
(Boyko and Boyko, 1959; Boyko, 1966). They
demonstrated that some crop plants could be
grown on surprisingly high salinity in sandy
soil, and pointed to the possibility of crossing
crop plants such as wheat with salt-tolerant rel-
atives such as Agropyrum, still a topic of
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research interest. Growing plants in lysimeters
made from empty oil drums on the Red Sea
coast, they showed that a Bedouin strain of bar-
ley could complete its life cycle on full-strength
seawater, presaging the findings of Epstein et
al. (1980). While their experiments raised ini-
tial interest in high-salinity agricultural, their
evidence tended to be anecdotal and there was
no immediate follow-up by others. In fact, Boy-
ko concluded (Boyko, 1966) that “Agrotechni-
cal details for economic purposes have to be
worked out...”, an understatement.
Interest revived in the 1970s, with some re-
searchers working toward the development of
salt-tolerant crops through breeding (Epstein et
al., 1980) and others working on the domestica-
tion of wild halophytes (e.g., Somers, 1975;
Felger, 1979), both approaches suggested by
Boyko. A group at Scripps Institute of Technol-
ogy conducted preliminary studies on seawater
irrigation and compiled a list of potentially use-
ful halophyte species (Mudie, 1974), which has
been expanded (Aronson, 1989; National Re-
search Council, 1990). Three research groups
were initially responsible for most of the subse-
quent field trials of halophytes under irrigation:
the Environmental Research Laboratory of the
University of Arizona, USA (Glenn et al.,
1996); the Halophyte Biotechnology Center,
University of Delaware, USA (Gallagher,
1995); and the Institutes for Applied Research,
Ben Gurion University of the Negev, Israel
(Pasternak and Nerd, 1996; Pasternak and San
Pietro, 1985). Malcolm (1996), working in
Australia, and Le Houerou (1996), working in
north Africa, have been most responsible for
conducting field trials of halophytes under dry-
land conditions. Numerous other researchers at
institutions throughout the arid zones are now
considering halophyte trials (Squires and Ay-
oulo, 1994).
Four basic conditions must be met if halo-
phytes are to succeed as irrigated crops: (1)
they must have high yield potential; (2) the irri-
gation requirements must be within the range of
conventional crops and must not damage the
soil; (3) halophyte products must be able to
substitute for conventional crop products; and
(4) high-salinity agriculture must have a role to
play within the existing agricultural infrastruc-
ture. Whether halophytes can meet these condi-
tions depends in part on their performance as
agronomic crops, which in turn is related to
their basic physiology and biochemistry in rela-
tion to salt stress.
A. Yield Potential of Halophytes
While there have been many laboratory
studies carried out on the salt tolerance of halo-
phytes, there have been relatively few field tri-
als set up to simulate agronomic conditions.
Ecological studies, however, have documented
the high-yield potential of salt marsh species
such as Spartina alterniflora, which produces
up to 40 t/ha of biomass in the low intertidal
zone of estuaries (Odum, 1974). Some halo-
phytes complete their entire life cycles on be-
yond-seawater salinities (Troyo-Dieguez et al.,
Glenn and O’Leary (1985) reported yields
ranging from 13.6 to 17.9 t/ha of dry matter for
the most productive halophyte species in a
screening of species carried out in field plots in
a coastal desert environment (Puerto Penasco,
Sonora, Mexico), using 40 g/l seawater as the
irrigation source. These are comparable to
yields obtained from conventional forage crops
such as alfalfa or Sudan grass in desert irriga-
tion districts. The native species outperformed
the exotics, but the list of productive species in-
cluded several plant types: a succulent, annual
plant (Salicornia bigelovii); a perennial grass
(Distichlis palmeri); a prostrate, rhizomatous
plant with succulent leaves (Batis maritima);
and several species of desert saltbush (Atriplex
Subsequent field trials at the same location
confirmed the high-yield potential of halo-
phytes irrigated with seawater. Over 6 years of
field trials, the annual, oilseed halophyte Sali-
cornia bigelovii produced 12.7 to 24.6 t/ha of
biomass (mean = 18.0 t/ha) and 1.39 to 2.46
t/ha of seed (mean = 2.00 t/ha) over a 200-day
growing cycle (Glenn et al., 1991). The seed
contained 31% protein, 28% oil, and only 5%
fiber and 5% ash; the oil was high in polyunsat-
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urated fatty acids, particularly linoleic acid
(74% of total).
Researchers at Ben Gurion University of
the Negev tested 120 halophytes under full sea-
water irrigation (56 dS/m, approximately 34 g/l
TDS) or on 15% seawater (5.5 dS/m) on the
Mediterranean coast of Israel (Aronson et al.,
1988). Seven Atriplex species produced 12.6 to
20.9 t/ha of biomass containing 9.9 to 19.5%
protein on full-strength seawater, not signifi-
cantly lower than the yields on 15% seawater.
Gallagher (1985) obtained yields of 5.2 to 9.5
t/ha of the saltgrass Distichlis spicata under
seawater (30 g/l) irrigation in Delaware, USA,
while Spartina patens yielded 14.4 t/ha when
harvested in July. These are within the range of
yields from conventional forage grasses. The
herbaceous plant Atriplex triangularis, a poten-
tial fresh vegetable crop for human consump-
tion, yielded the equivalent of 21.2 t/ha on a
fresh-weight basis. Zaruyk and Baalbaki (1996)
proposed Inula crithomoides, a perennial halo-
phyte bush, as a forage plant for saline irriga-
tion. From small-scale experiments, they
extrapolated a yield of 4 t/ha of dry biomass on
40 dS/m (24 g/l) seawater.
These reports show that halophytes can
yield as high as conventional irrigated crops
even under full seawater irrigation. However,
the optimal salinity for growth of even the most
tolerant halophytes is reportedly in the range
200 to 340 mM NaCl (11.4 to 19.4 g/l TDS)
(Glenn and O’Leary, 1985; Yeo and Flowers,
1986). Hence, under high-salinity irrigation
halophytes are beyond their growth optimum,
and soil salt levels must be carefully controlled
to avoid further yield reductions. This raises the
question of whether high-salinity agriculture
can ever be practical, even if adequate germ-
plasm is developed.
B. Irrigation Requirements
Boyko believed that the key to irrigating
with seawater was to use high volumes of water
flooded onto very porous soils (Boyko and
Boyko, 1966). In early experiments, Glenn and
O’Leary (1985) used irrigation depths of 18
m/year to grow halophyte crops on seawater,
simulating a tidal regime. This amount of water
is greatly in excess of the amount of water ap-
plied to grow conventional crops on freshwater
and is clearly uneconomical if the water must
be pumped. More recent experiments have at-
tempted to determine the minimum effective
water requirement of halophytes on different
salinities to determine the upper practical salin-
ity limit for saltwater irrigation.
Miyamoto (1995) estimated the optimum
soil salinity for several euhalophyte species
grown under normal irrigation scheduling (al-
lowing 50% soil moisture depletion between
irrigations). The optimal salinity was approx-
imately 20 g/l or less, and growth was observed
to decline rapidly beyond soil salinities of 20 to
30 g/l. Because the salinity of the soil solution
was 2 to 3 times as high as the salinity of the ir-
rigation water, the irrigation water salinity opti-
mum was about 10 g/l. They concluded that
high-salinity water such as seawater required
special measures to ensure the salinity of soil
solution is maintained at levels that do not
greatly inhibit plant growth.
This can be accomplished by leaching —
applying sufficient water so that a portion of the
applied water percolates past the plant root
zone and carries with it excess salt applied in
the irrigation water. The leaching fraction (LF)
is the proportion of the applied water that per-
colates below the plant root zone (Ayers and
Wescott (1985) and is given by the equation:
The higher the leaching fraction, the lower
the salinity of the soil water. However, higher
leaching fractions and associated greater irriga-
tion depths are associated with higher pumping
cost and larger discharges of water to the aqui-
fer or drainage system, which may be a problem
where best management practices must be fol-
lowed (e.g., Glenn et al., 1998). In general,
there is no straight-forward rule to determine
LF even for conventional crops. Ayers and
LF =
Depth of water leached below root zone
Depth of water applied at the surface
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Wescott (1989) estimated the minimum Leach-
ing Requirement (LR) as:
where EC
= salinity of the applied irrigation
water in dS m–
; EC
= average soil salinity tol-
erated by the crop as measured on a soil satura-
tion extract.
However, Miyamoto (1996) cautions that
leaching requirements estimated by simple
steady-state formulas may prove to be exces-
sive with respect to handling drainage water
when irrigating with seawater or high-salinity
water that exceeds the optimum soil salinity for
plant growth.
Glenn et al. (1997) irrigated Salicornia big-
elovii over 2 years in drainage lysimeters set
into a field of the same crop. The lysimeters
were irrigated daily with seawater (40 g/l TDS)
at five irrigation depths, ranging from 50 to
250% of the rate of evaporation from an evapo-
ration pan. The application rates ranged from
0.73 to 3.79 m/year. Biomass yield increased in
direct proportion to the water application rate,
but all irrigation treatments produced a leach-
ing fraction of about 0.35. Increasing the irriga-
tion depth lowered the soil salinity, and resulted
in higher plant growth and water use, and hence
leaching fractions were approximately equal
over all treatments. High yields required that
the soil-moisture salinity be maintained below
75 g/l in the top 15 cm, which constitutes the
root zone for this shallow-rooted species.
Consumptive water use by S. bigelovii was
about the same as conventional biomass crops
grown on freshwater in nearby irrigation dis-
tricts (Figure 3). Hence, the “salt penalty” for
growing crops on seawater is an additional 35%
water requirement to handle excess salts. This
may be a practical penalty to pay in locations
with sandy coastal soils where seawater is the
only large-scale water source that can be ex-
ploited for agriculture. The expense of pump-
ing water is directly proportional to the amount
of lift required, and many irrigation districts use
water from aquifers 100 m or deeper, whereas
seawater along coastal deserts will usually re-
quire lifts of only 10 to 20 m. However, seawa-
ter irrigation also requires daily irrigation when
soil with low water holding capacity (i.e., sand)
is used; precision irrigation equipment, such as
moving booms, must be used for water deliv-
ery, and these must be modified to handle sea-
water. A pilot-scale farm using four center-
pivot booms, each irrigating 50 ha of Salicornia
bigelovii with 44 g/l seawater, has been estab-
lished in Saudi Arabia (Clark, 1994).
Much lower leaching fractions are possible
if the salinity of the water is lower. Glenn et al.
(1998) grew Atriplex nummularia in drainage
lysimeters set in a closed-canopy plot of the
same plant over 3 years in Tempe, Arizona, on
water of 1.15 and 4.10 g/l TDS with no leaching
fraction other than that provided by rainfall
(7.4% of the irrigation volume). Although root
zone, soil-moisture salinities ranged from 17.1
to 58.5 g/l in the lysimeters irrigated with the
4.1 g/l source, compared with only 2.2 to 5.1 g/l
for the low-salinity source, the plants did not
differ in growth rate and outperformed conven-
tional crops in terms of both yield and water use
efficiency (Figure 4). Hence, at least some
halophyte crops grown at salinities above those
that can be used on conventional crops but be-
low the point where yield reductions occur de-
liver a bonus relative to conventional crops.
Grieve and Suarez (1997) extrapolated yields
of 7.4 t/ha per 3-week cutting interval from the
halophyte Portulaca oleracea grown on ap-
proximately 12 g/l TDS water. These studies
refute the notion that halophytes are inherently
slow-growing plants (e.g., Niu et al., 1995).
C. Effect of High Salinity Water on the Soil
Another concern when irrigating with wa-
ter with high sodium concentrations is that in-
filtration problems will result from soil
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dispersion and structural breakdown. The sodi-
um adsorption ratio (SAR) is the most com-
monly used method to assess potential
infiltration problems. The SAR equation is
where concentrations are expressed in molar
Generally, soils are classified as sodic
when the SAR>15, which would virtually pre-
clude the use of high salinity water for irriga-
tion. However, because the electrolyte
concentration in seawater (and dilutions of sea-
water) is high relative to the sodium concentra-
tion, slow infiltration rates are generally not a
hazard for soil under seawater irrigation, even
in susceptible soils (Quirk, 1971).
D. Useful Products from Halophytes
Although some halophytes are traditional
human foods (Felger, 1979), most of the re-
search has concentrated on their value in animal
feeding systems. Animal feeds that can be pro-
duced from halophytes include forage from
dried plant shoots (hay), oil, seed meal, and
grains. Halophytes have mixed characteristics
as forages. On the positive side, they generally
have high protein content, ranging from 10 to
20% of dry matter (Le Houerou, 1996). On the
negative side, they generally have high salt
FIGURE 3. Biomass yield and irrigation requirements of
Salicornia bigelovii
irrigated with seawater (40 g/l TDS) in
a coastal desert environment at Puerto Penasco, Sonora, Mexico, compared with conventional forage crops irrigated
with fresh water in nearby irrigation districts in the United States (Glenn et al., 1997). Each data point is the mean
value from four lysimeters. Data were collected over two growing seasons (four irrigation rates per growing season).
SAR Na Ca Mg=+
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content (15 to 50% salts on the leaf dry matter)
and are a fairly poor energy source (Le Houer-
ou, 1996). Additionally, halophytes can occa-
sionally contain oxalate levels in the toxic
range (Le Houerou, 1996). While many halo-
phyte species have been tested for use as forag-
es, the salt bush genus Atriplex has received the
most attention.
Atriplex species tend to have high protein
content, generally ranging from 12 to 22%
(Glenn et al., 1994; Watson, 1990). Crude pro-
tein of other halophyte species tends to be low-
er, and the protein content of Salicornia
bigelovii straw ranges only from 4 to 6%
(Glenn et al., 1995). However, in halophytes,
estimates of crude protein overestimate the di-
gestible protein content of the plant (O’Leary et
al., 1985). This is because crude protein esti-
mates may include non-protein nitrogen sourc-
es such as quaternary ammonia compounds and
proline, which are used as osmocompatible sol-
utes by halophytes. Normally, these com-
pounds, which can account for about 50% of
the plant nitrogen content, are not digested and
are excreted in the urine and the feces. Howev-
er, Le Houerou (1996) has shown that it is pos-
sible for non-protein nitrogen to be metabolized
when animals have been given sufficient time
to develop rumen bacteria that are capable of
using the non-protein nitrogen so long as there
is sufficient energy in the diet to allow the bac-
teria to metabolize these compounds.
Despite all the aforementioned drawbacks
associated with utilization of halophytes as for-
ages, Swingle et al. (1996) demonstrated that
halophytes could be incorporated into a practi-
cal lamb diet with no effect on growth perfor-
mance. Suaeda esteroa, Atriplex barclayana,
and Salicornia bigelovii straw were compared
with conventional Cynodon dactylon hay (con-
trol) at 30% of the diet. All diets contained 12.5
to 15% protein and 50% grain as an energy
FIGURE 4. Biomass yield and irrigation requirements of
Atriplex nummularia
irrigated with 1 g/l (open circles) or 4
g/l (closed circles) industrial wastewater in Tempe, Arizona, compared with conventional forage crop yields and wa-
ter use in nearby irrigation districts (Glenn et al., 1998). Each data point is the mean value over 3 years of data col-
lection. The linear equation predicts yield (y) based on water use (x).
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source, typical of high-performance fattening
diets for ruminants. The halophyte forages con-
tained a much higher ash content than the Cyn-
odon hay (24 to 34% vs. 5%). Dry matter intake
was higher for lambs fed diets containing halo-
phytes forages than for lambs fed on the grass
control diet. Lambs fed diets containing halo-
phytes consumed more dry matter to compen-
sate for the lower organic matter content of this
diet compared with the control diet. Because of
the increased intake, halophyte-fed lambs were
able to gain at the same rate as the control
lambs, but, as expected, the feed efficiency was
lower and water intake was higher. Carcass
quality of all lambs was excellent and was not
affected by the inclusion of halophyte forages
in the diet. Similar results were obtained with
goats fed Salicornia bigelovii straw at up to
50% inclusion (Glenn et al., 1992). These re-
sults are in contrast to other results (Benjamin
et al., 1992; Nerd and Pasternak, 1992) that re-
ported poor utilization of Atriplex barclayana
as a forage source for sheep at 70% inclusion.
The key to effective utilization of salt-contain-
ing halophyte forage is to keep the forage com-
ponent of the diet less than 50%, so the animals
can compensate for the dilution effect that salt
has on forage energy content by increasing their
rate of intake (Swingle et al., 1996). Fattening
diets generally contain 25 to 50% forage;
hence, they appear to be the most practical
feeding systems in which to use halophyte for-
One of the most promising uses of halo-
phytes may be as seed crops (Somers, 1975;
Felger, 1979; O’Leary, 1988, 1994; Glenn et
al., 1991; Yensen et al., 1988). One justification
for this claim is that unlike the leaves that accu-
mulate large amounts of salts, the seeds of halo-
phytes have a very low salt content, even under
saline irrigation. Halophyte seeds have been
used as grains. Distichlis palmeri seeds were
harvested by the Cocopa Indians of the Colo-
rado River delta region (Felger, 1979; Yensen
et al., 1988). Halophytes can also be grown for
oilseed production. The perennial seashore
mallow (Kosteletzkya virginica) produces a
seed that is 32% protein and 22% lipid (Gal-
lagher, 1985; Poljakoff-Mayber et al., 1994).
Glenn et al. (1991) examined the oil of Salicor-
nia bigelovii seeds and found it similar in calor-
ic value to soybean oil. No difference in growth
rate was found in chickens fed a diet containing
soybean oil at 2% of the total diet as an energy
supplement, and chickens fed a diet where the
soybean oil was replaced by S. bigelovii oil at
2% of the diet. However, there was growth in-
hibition of chickens fed the S. bigelovii seed
meal at 10% or greater inclusion. It is believed
that the growth depression was caused by sa-
ponins. Growth inhibition was reversed when
the S. bigelovii seed meal was supplemented
with cholesterol at 1%, as cholesterol counter-
acts the antigrowth properties of saponins. Sim-
ilar results were found by Attia et al. (1997).
Ruminants are less susceptible to saponins than
poultry, and seed meal from S. bigelovii was
able to replace cottonseed meal as a protein
supplement (10% inclusion rate) with no affect
on animal performance.
E. Role of High-Salinity Tolerant Crops in
The prospect of greening the world’s coast-
al deserts with seawater crops has been the
most cited scenario for highly tolerant crops,
but there are more immediate opportunities for
high-salinity agriculture. There is currently a
need to develop highly salt-tolerant crops to re-
cycle agricultural drainage water, literally riv-
ers of contaminated water that are generated in
arid-zone irrigation districts. This water can be-
come an environmental hazard when dis-
charged into surface waters or placed in
evaporation ponds, through the evapoconcen-
tration and bioaccumulation of toxic elements
(Boyle, 1996; Hothem and Ohlendorf, 1989;
Matsui et al., 1992; Ong and Tanji, 1993; Ong
et al., 1995; Presser, 1994). Perhaps the best so-
lution is to reuse the water near the site of pro-
duction on progressively more salt-tolerant
crops, thereby reducing the amount of water
that must ultimately be disposed (Grieve and
Suarez, 1997; Rhoades, 1993; Rhoades et al.,
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tion of this material without the consent of the publisher is prohibited.
1989; Wescott, 1988). A limitation to the reuse
of such water is the low salt tolerance of the
conventional crops (Rhoades et al., 1989;
Wescott, 1988) and trees (Karajeh et al., 1994;
Karajeh and Tanji, 1994a,b) that have been test-
ed as secondary crops. Halophytes could great-
ly extend the range of options for disposing of
this type of salty water (Riley et al., 1998;
Glenn et al., 1998; Watson and O’Leary, 1993;
Watson et al., 1994; Grieve and Suarez, 1997).
Another use for halophyte crops is to reclaim
saline soils (Keiffer and Ungar, 1997a,b).
Through their capacity for salt uptake, halo-
phyte can reduce the salt content of soil over
time (as long as they are not irrigated with sa-
line water).
Worldwide, approximately 45 to 60 million
ha of irrigated land have been damaged by salt,
representing 20 to 25% of the total irrigated
acreage in the world (Ghassemi et al., 1995).
Reclaiming these lands for conventional crops
is too costly for most countries to afford, but
they could be used to grow halophytes, as is be-
ing attempted in Pakistan, as an example
(Quereshi et al., 1991). As salt marsh plants,
many halophytes are not only salt tolerant but
can thrive in poorly drained soils, which are the
first to become salinized in irrigation districts.
It is sometimes argued that, in the absence of
complete reclamation, halophyte crops could
only postpone the inevitable salting up of such
land (but this would be a benefit by itself). A
counterargument is that marginal land can be
used for sustained halophyte production in cir-
cumstances where unrealistic inputs would be
needed to maintain soil salt levels low enough
for conventional crops.
Halophytes are a diverse group of plants
with varying degrees of actual salt tolerance,
yet they appear to share in common the ability
to sequester NaCl in cell vacuoles as the major
plant osmoticum. This requires at a minimum a
functional Na
antiport system in the tono-
plast and perhaps special membrane properties
to avoid leakage of Na
from the vacuole to the
cytoplasm. They also must accumulate organic
solutes in the cytoplasm to balance the osmotic
potential in the vacuole. The emerging evi-
dence points to specialized properties of halo-
phyte ion transporters compared with
glycophyte enzymes, which allow them to take
up and sequester NaCl with high efficiency.
Halophyte membrane lipids may also be adapt-
ed to prevent salt leakage.
Although NaCl inhibits the growth even of
halophytes at levels approaching seawater sa-
linity, the metabolic cost of salt tolerance is not
so high that plants are unproductive at high sa-
linity. Halophytes grown on seawater can pro-
duce high yields of seed and biomass, and the
irrigation requirements are within the range of
conventional crops. When grown at lower sa-
linities, C
halophytes such as Atriplex nummu-
laria can substantially outperform conventional
crops in yield and water use efficiency.
Current efforts to produce salt-tolerant con-
ventional crops are aimed mainly at increasing
the salt-exclusion capacity of glycophytes.
However, these efforts have not produced
breakthroughs in salt tolerance (Flowers and
Yeo, 1995), as was predicted twenty years ago
(Epstein et al., 1980). Research with halo-
phytes, by contrast, have identified several pro-
spective crop species and have demonstrated
the overall feasibility of high-salinity agricul-
ture, given suitable germplasm. Progress in
producing highly tolerant cultivars of conven-
tional crops may require a change in strategy, to
attempt to introduce halophyte genes directly
into glycophytes (Bohnert and Jensen, 1996).
Such research has not even begun, but the tools
are at least being assembled, including an un-
derstanding of the molecular determinants of
halophyte salt tolerance. In the meantime, the
quickest way forward may be the direct domes-
tication of halophytes, which have already been
used to demonstrate the feasibility of high-sa-
linity agriculture.
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... Halophytes dominate saline coastal areas and inland arid and semi-arid soils, thriving in saline environments (i.e., 200 mM NaCl) where 99% of salt-sensitive plants (i.e., glycophytes) perish due to ion toxicity induced by high salinity [1,2]. In recent years, several halophytes have received significant scientific interest across the world as emerging novel foods, mainly as potential sources of protein, fiber, minerals, trace elements, and phytochemicals. ...
... Protein digestibility (PD) = Cs − Ce (1) Cs and Ce are the final concentrations of primary amines in the sample digesta and empty digesta, respectively. ...
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Halophytes are considered emerging functional foods as they are high in protein, minerals, and trace elements, although studies investigating halophyte digestibility, bioaccessibility, and intestinal absorption are limited. Therefore, this study investigated the in vitro protein digestibility, bioaccessibility and intestinal absorption of minerals and trace elements in saltbush and samphire, two important Australian indigenous halophytes. The total amino acid contents of samphire and saltbush were 42.5 and 87.3 mg/g DW, and even though saltbush had a higher total protein content overall, the in vitro digestibility of samphire protein was higher than the saltbush protein. The in vitro bioaccessibility of Mg, Fe, and Zn was higher in freeze-dried halophyte powder compared to the halophyte test food, suggesting that the food matrix has a significant impact on mineral and trace element bioaccessibility. However, the samphire test food digesta had the highest intestinal Fe absorption rate, whereas the saltbush digesta exhibited the lowest (37.7 vs. 8.9 ng/mL ferritin). The present study provides crucial data about the digestive "fate" of halophyte protein, minerals, and trace elements and increases the understanding of these underutilized indigenous edible plants as future functional foods.
... Halophilic plants have naturally evolved and acquired morphological, physiological, and anatomical features that allow them to persist in and even benefit from saline soils and irrigation water. In addition, because halophytic plants can extract salt from saline soils, they can delay further salinization or even recover certain ions from saline soils, ultimately allowing traditional crops such as alfalfa, wheat or rice to grow (Glenn et al., 1999;Micklin, 2007;Toderich et al., 2010Toderich et al., , 2013. ...
... The world flora is estimated to contain about 2600 species of halophytes, which belong to 550 genera and 120 families (Shamsutdinova et al., Shamsutdinov et al., 2018). More than 760 economically valuable species of halophytes intended for development of highly saline lands, belonging to 34 families and 214 genera, have been described in the Flora of Central Asia (Akzhigitova, 1982;Kurochkina et al., 1986;Toderich et al., 2009) (Glenn et al., 1999, Lyra et al., 2016 Salicornia europaea without irrigation 2.6-3.9 t/ha, when irrigated with mineralized water 7.5-9.6 t/ha dry matter Currently, technologies of growing halophytes in pure and/or mixed plantings and crops are widely used in the Central Asian region to provide continuous year-round green biomass, improve fodder production and feed staff for desert-pasture animal husbandry, as well as to desalinize, improve land quality and stable functioning of arid ecosystems. ...
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Cover photo: © FAO/Maria Konyushkova Food and Agriculture Organization of the United Nations, Nur-Sultan, 2022 III Obligatory reference: Toderich K., KhujanazarovT., Ibraeva M., Toreshev P., Bozayeva J., Konyushkova M.V. and Krenke A.N. 2022. Training Manual. Innovative approaches and technologies for managing salinization of marginal lands in Central Asia. Nur-Sultan, FAO. The consequences of climate change, population growth and global economic crises have a negative impact on the economy as a whole, and especially on the productivity of saline, arid and degraded lands in Central Asia, including Kazakhstan. Under these conditions, a prerequisite for stable, sustainable development and food security is the adoption of integrated, scientific and innovative approaches to the use and management of limited natural resources. This practical manual is based on the webinar ‘Innovative Approaches and Technologies to Combat Salinization of Marginal Lands in Central Asia’, which was held on August 07-12, 2020, in the framework of FAO-GEF project ‘Integrated Natural Resources Management in Drought-prone and Saltaffected Agricultural Production Landscapes in Central Asia (CACILM-2)’. The thematic program of the webinar was built on a modular approach, where the module represents a complete block on the issues of salinization of natural environments, including soil,water, agricultural land, finding approaches and implementing innovative technologies to manage and reduce damage from salinity: ◆ Module 1 – Classification, assessment methods and sustainable management of saline soils ◆ Module 2 – Approaches and best practices to combat salinization and to increase productivity of marginal lands with the use of halophytes ◆ Module 3 – Screening and determination of salt tolerance threshold, outlines of modern breeding and biotechnology in saline and drought conditions ◆ Module 4 – Documentation, benefits and scaling up of best ◆ practices and technologies in biosaline agriculture ◆ Module 5 – Cross-cutting topics (Food Programme and Nutritional Quality, Value Chain Analysis, Integration of Women, etc.) The training manual is designed for practical training sessions at universities as well as trainings organized in Central Asian (CA) countries to enhance the capacity of farmers, water users,livestock producers and decision makers in integrated natural resource management (INRM) in drought-prone and saline agricultural production landscapes of the region, and to scale up the available best practices and advanced experiences. The training manual includes information on proposed modules, covering land quality control and salinity management; technologies for utilization of marginal water resources for fodder production; technologies for growing new drought and salt tolerant traditional and non-traditional (underutilized,fogetten and negected crops); technology for evaluation of adaptive traits of high-yielding genetic lines and varieties, as well as the basics of their primary seed breeding, farm level seed production, technical property control and seed quality. These materials can be used as a basis and adjusted for training activities depending on the target group and prevailing local context. The material aims at capacity building and knowledge development for agricultural students,agricultural workers, local farmers, households interested in biosaline agriculture. It also addresses issues of value chain analysis and planning, gender equality issues, particularly integration and empowerment of women in the development of saline agriculture. The authors and CACILM-2 project partners from almost all Central Asian countries, leading research institutes and non-governmental organizations of Kazakhstan, who had encountered soil salinity issues in their activities, contributed to the preparation of this manual. The authors express special thanks to Makhmud Shaumarov, Olga Grebennikova, Akmaral Sman,Bakhytzhan Duisembekov, Azamat Ershibulov, Sugyeong Kang and Madina Kassenova for their invaluable help and support in developing this manual. The CACILM-2 project also thanks the Ministry of Agriculture of Kazakhstan, in particular the Land Management Committee, the Ministry of Ecology, Geology and Natural Resources of Kazakhstan, as well as the Department of Surveys, Land Monitoring and Research of the State-owned Corporation ‘Government for Citizens’ of the Ministry of Digital Development, Innovation and Aerospace Industry of Kazakhstan for their continued support in the implementation of project activities.
... Additionally, it was demonstrated that Na + /H + antiporters help in the sequestration of salt and enhance salt tolerance (Sneh Lata Singla-Pareek, New Delhi, India). In fact, almost two-and-a-half decades back whilst elaborating the role of Na + /H + antiporters in the salt tolerance of halophytes, Glenn et al. [14] were already reporting on the potential application of halophytes, non-conventional crops, in the remediation of saline-struck soils and wastewater. With the present-day global challenges, this application could contribute to the development of sustainable strategies. ...
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The Indo-German Science and Technology Centre (IGSTC) funded an Indo-German Workshop on Sustainable Stress Management: Aquatic plants vs. Terrestrial plants (IGW-SSMAT) which was jointly organized at the Friedrich Schiller University of Jena, Germany from 25 to 27 July 2022 by Prof. Dr. Ralf Oelmüller, Friedrich Schiller University of Jena, Germany as the German coordinator and Dr. K. Sowjanya Sree, Central University of Kerala, India as the Indian Coordinator. The workshop constituted researchers working in this field from both India and Germany and brought together these experts in the field of sustainable stress management for scientific discussions, brainstorming and networking.
... This may consist of very selectivity toward Na + uptake during absorption, such as in grasses. Because of the lower cell vacuolar volume of grasses and leaf water content, grasses do not need as much Na + uptake per unit of growth, so they maintain lower Na: K ratios on exposure to salt(Glenn et al., 1999). Another explanation is that Na + and Clare absorbed in significant amounts but arereabsorbed from the xylem sap in either the proximal part of the roots (Ratner and Jacoby 1973) or in the shoots (Rains 1969), where these ions are then either stored or retranslocated to the soil (Winter and Preston 1982). ...
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Salinity is a significant osmotic stressor for Citrus, leading to reduction in general health and well-being. Salinity threatens the banana and citrus growing regions in many areas in Egypt and Florida. Ongoing climate change and sea level rise maximize this danger especially in the coastal regions. In this study, we aimed to: A) to develop effective protocols to micropropagate banana and citrus plants to generate true to type germplasm. B) to investigate the efficacy of various approaches to manage abiotic stress. These approaches included: 1) studying the role of silicon nanoparticles (SiO2-NPs) to mitigate osmotic stress in banana and citrus crops. 2) evaluate the performance of a putative new citrus rootstocks produced via conventional breeding under salt stress conditions and citrus greening disease (HLB). 3) investigate the role of AtNPR1 gene in salt stress tolerance mechanism.
... Donc ces espèces peuvent être valorisées directement comme fourrage pour ces espèces animales. Par exemple,Glenn et al. (1999) ont mentionné que S. fruticosa est très appétée surtout par les dromadaires. A son tour, El Shaer (1997) a indiqué que cette espèce est consommée par les chèvres et les moutons aussi et souvent pâturée pendant l'hiver et le printemps. ...
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Halophytes are widespread in the Tunisian marginal saline soils but not widely exploited. This study aims to evaluate the forage quality and chemical composition of three halophytes, native in southern Tunisia : Salicornia emerici Duval-Jouve, Sarcocornia alpini (Lag.) Castrov. et Sarcocornia fruticosa (L.). Dry biomass (MS), organic matter (MO), mineral (MM) and crude protein (PB) contents, in vitro digestibility, ions and anti-nutritional compounds (flavonoids, tannins and saponins) were determined and compared to those of Medicago sativa (L.), considered as reference feeding plant. The obtained results indicate that dry biomass of these halophytes ranges from 10.50% to 18.63% for S. emerici and S. fruticosa, respectively. Compared to S. emerici, both halophytes recorded the highest percentages of organic matter and crude protein and higher concentrations of Na+, K+, Mg2+, Ca2+ and Fe2+. These three halophytes, harvested during the summer period, showed important digestibility percentages (> 70 % MS), exceeding those of alfalfa, and low levels of ADF, ADL and anti-nutritive compounds (condensed tannins, flavonoids and saponins). These findings suggest that the valorization of these native halophytes as fodder is promising, in particular S. alpini and S. fruticosa. This can provide many economic and environmental advantages in drylands.
... Plants can develop complex adaptation mechanisms in response to ionic stress and those used in osmotic stress. Ionic stress is caused by an accumulation of Na + ions in plants, typically in the leaf, at levels beyond the threshold that triggers leaf cell death with chlorosis and leaf necrosis, followed by a decrease in cellular metabolic activity, including photosynthesis (Glenn et al. 1999). Despite high Na + concentrations damaging plants (Parida and Das 2005), some research showed that low salt levels have little effect on growth and physiological function. ...
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The accession of mulberry (Morus sp.) with salinity tolerance unavailable in Indonesia is needed to overcome the problem of marginal land, especially in the saline areas of the country. Therefore, this research aims to determine the accession of salinity tolerance of mulberry from 6 origins in Indonesia based on growth and physiological parameters. The method used was a factorial randomized block design with the first treatment of stem cutting-derived mulberry accession being M1, M2, M3, M4, M5, M6, and M7, while the second was the concentration of NaCl at 0 mM, 40 mM, 60 mM, and 80 mM. The results showed that M2 accession from Bogor was categorized as tolerance to high salt stress, and M1 was classified as sensitive accession. Increasing salt concentration causes a decrease in growth parameters. It also decreased physiological parameters such as leaf and media relative water content while increasing dissolved sugars. Genotypic scores indicate salinity tolerance and the potential number of leaves, while Na+ content and leaf necrosis percentage showed sodium toxicity in the leaf. Therefore, genotypic score, Na+/K+ ratio, and leaf necrosis percentage are the best parameters to select and identify mulberry accession with high salt stress tolerance.
... Soil salinization is a factor affecting plant nutrition and growth processes due to increased osmotic pressure in the soil [2]. Most plants do not tolerate the high concentration of salts in the soil and cannot grow on soils exposed to salt; such plants are called glycophytes [3]. The osmotic effect of salinity causes metabolic changes in plants similar to those associated with water scarcity [4]. ...
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The study of halophytes as sources of phenolic compounds, as well as conditions that further enhance the accumulation of biologically active compounds in them, is of particular interest. In this paper, the effect of different salinity levels (25–500 mM in the form of NaCl) on the content of phenolic compounds and the antioxidant activity of two rare halophyte species Spergularia marina (L.) Griseb. and Glaux maritima L. cultured in vitro was investigated. A species-specific reaction of plants to salinization was established. In G. maritima, the maximum total content of phenolic compounds was observed at 50–100 mM, flavonoids 75–400 mM, and hydroxycinnamic acids 200–300 mM, as well as individual phenolics (protocatechuic acid, catechin, astragalin, hyperoside, rutin, isoquercitrin, and apigenin derivative) at 100–300 mM NaCl. For S. marina, on the contrary, there was a slight decrease in the content of phenolic compounds when NaCl was added to the nutrient medium compared to the control. The content of protocatechuic acid, rosmarinic acid, and apigenin derivative significantly decreased with increased salt stress. The change in antioxidant activity at different salinity levels was also species specific. The maximum values of different groups of phenolic compounds in G. maritima were observed at 50–300 mM NaCl. The cultivation of S. marina without the addition of NaCl and at 500 mM NaCl allowed the production of plants with the highest content of phenolic compounds. The obtained results can be further used in the development of protocols for the cultivation of these plants in vitro in order to induce the biosynthesis of phenolic compounds in them.
... It is also a powerful antioxidant, helping the plant to protect itself against the damage caused by high salt concentrations [27]. In halophytes, osmotic equilibrium is accomplished by accumulating uncostly energy ions, such as Na + and Cl − , and osmolyte solutes with low molecular weight [45]. ...
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Secondary salinization caused by climate change is a growing global problem. Searching for plants that can survive in areas with high salt content and even have decorative value was the focus of our research. Thirty plants of Limonium gmelinii subsp. hungaricum were planted in clear river sand; another thirty plants were planted in Pindstrup, a growing substrate enriched with 40% clay. With the latter, we modeled the natural soil. In addition to the control tap-water treatment, plants received 50, 125, 250, 375, and 500 mM NaCl solution irrigation twice a week. The leaf sizes of plants planted in sand decreased proportionally with the increasing NaCl concentration, and their dry matter content increased. In the clay-containing medium, leaf sizes increased, even at a concentration of 375 mM, although the dry matter content increased only at high concentrations. Carotene content in both media became higher, due to the higher NaCl concentrations, while proline content in the plants grown in sandy media increased, even with the 125 mM concentration. With our present experiment we proved the salt tolerance of the taxon, and even the soil’s great importance in supporting the plant’s salt tolerance.
... The NaCl threshold for halophytes' salinity tolerance and optimal ecophysiological growth condition is in the range of 100 to 200 mM (i.e., 6-12 g L −1 ) NaCl, but differences exist among species, ecotypes, developmental stages, and environments, so that many aspects of their underlying mechanisms remain unclear or unknown, especially under hypersaline conditions [13,19,33]. Many dicotyledonous halophytes show optimal growth in the presence of 50-250 mM NaCl, while monocotyledonous halophytes generally grow optimally in the absence of salt or at low (50 mM or less) NaCl concentrations [13,34]. Here, S. fruticosa maintained the same total DW and biomass partitioning as the control under saline conditions (15 g L −1 or 257 mM NaCl), showing a relevant decrease of the total biomass only after 30 g L −1 NaCl (i.e., 513.3 mM) exposure. ...
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Hypersaline environments occur naturally worldwide in arid and semiarid regions or in artificial areas where the discharge of highly saline wastewaters, such as produced water (PW) from oil and gas industrial setups, has concentrated salt (NaCl). Halophytes can tolerate high NaCl concentrations by adopting ion extrusion and inclusion mechanisms at cell, tissue, and organ levels; however, there is still much that is not clear in the response of these plants to salinity and completely unknown issues in hypersaline conditions. Mechanisms of tolerance to saline and hypersaline conditions of four different halophytes (Suaeda fruticosa (L.) Forssk, Halocnemum strobilaceum (Pall.) M. Bieb., Juncus maritimus Lam. and Phragmites australis (Cav.) Trin. ex Steudel) were assessed by analysing growth, chlorophyll fluorescence and photosynthetic pigment parameters, nutrients, and sodium (Na) uptake and distribution in different organs. Plants were exposed to high saline (257 mM or 15 g L−1 NaCl) and extremely high or hypersaline (514, 856, and 1712 mM or 30, 50, and 100 g L−1 NaCl) salt concentrations in a hydroponic floating culture system for 28 days. The two dicotyledonous S. fruticosa and H. strobilaceum resulted in greater tolerance to hypersaline concentrations than the two monocotyledonous species J. maritimus and P. australis. Plant biomass and major cation (K, Ca, and Mg) distributions among above- and below-ground organs evidenced the osmoprotectant roles of K in the leaves of S. fruticosa, and of Ca and Mg in the leaves and stem of H. strobilaceum. In J. maritimus and P. australis the rhizome modulated the reduced uptake and translocation of nutrients and Na to shoot with increasing salinity levels. S. fruticosa and H. strobilaceum absorbed and accumulated elevated Na amounts in the aerial parts at all the NaCl doses tested, with high bioaccumulation (from 0.5 to 8.3) and translocation (1.7–16.2) factors. In the two monocotyledons, Na increased in the root and rhizome with the increasing concentration of external NaCl, dramatically reducing the growth in J. maritimus at both 50 and 100 g L−1 NaCl and compromising the survival of P. australis at 30 g L−1 NaCl and over after two weeks of treatment.
... Notably, Salicornia plants can accumulate high concentrations of Na + in their photosynthetically active succulent shoots while avoiding ion toxicity 7,9,10 , suggesting highly efficient ion compartmentalization processes in cells through the action of specialized transporters [11][12][13][14] . Moreover, Salicornia growth is promoted by the addition of NaCl 10,15-17 , making it a particularly interesting genus for the study of salinity tolerance. ...
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Salinity remains a major inhibitor of crop production in irrigated and marginal lands. The identification of genes involved in salinity tolerance has been predominantly limited to model plants and crop species. However, plants naturally adapted to highly saline environments can provide key insights into mechanisms of salinity tolerance. Plants of the genus Salicornia grow in coastal salt marshes, and their growth is even stimulated by NaCl - much can be learnt from them. We generated genome sequences of two Salicornia species and studied the transcriptomic and proteomic responses of Salicornia bigelovii to NaCl. Through the generation of subcellular membrane proteomes, we found that SbiSOS1, a homolog of the well-known SALT-OVERLY-SENSITIVE 1 (SOS1) protein, appears to localize to the tonoplast, where it could be involved in mediating Na+ translocation into the vacuole to prevent toxicity in the cytosol. We identified 11 proteins of interest which, when expressed in yeast, altered salinity tolerance. One of these proteins, SbiSALTY, substantially improves yeast growth on saline media. Structural characterization using NMR showed it to be an intrinsically disordered protein and to localize to the endoplasmic reticulum in planta, where it could interact with ribosomes and RNA, potentially stabilizing or protecting them during salt stress. The study and understanding of the molecular mechanisms providing high salinity tolerance in S. bigelovii is likely to provide significant insights for improving salinity tolerance of crop plants.
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Some 120 species of native and introduced plant species have been screened under conditions of seawater irrigation at a site on the Mediterranean coast of Israel. Plants were grown for 2 yr under irrigation with undiluted seawater (ECi 56.0 dS/m) and with 15% seawater (ECi 5.5 dS/m). Results of the initial performance of all species are summarized. Life form, geographic distribution, "plant type' based on primary habitat, and photosynthetic pathway of each species are reviewed in relation to field performance. More detailed data on annual productivity and feed value are presented for 7 species of Atriplex showing promise as fodder. Known and suspected economic uses of some outstandingly successful species are reviewed. -from Authors
Using stereological procedures, a detailed analysis was made from thin section electron micrographs of secreting and nonsecreting salt glands of Frankenia grandifolia (Cham. and Schlecht) and Avicennia germinans (L.) Stem. In F. grandifolia secretory cells, vacuolar volume significantly decreased, while the volume of endoplasmic reticulum increased in secreting glands. Numerous minivacuoles were predominantly located along the periphery of secreting secretory cells, some in apparent fusion with the plasma membrane. No difference was found in mitochondrial volume in the secretory cells between secreting and nonsecreting glands. In A. germinans, there was a significant decrease in vacuolar volume in secreting secretory cells. The volume of the endoplasmic reticulum and mitochondria also increased in these cells. However, no evidence of mini-vacuolar fusion with the plasma membrane was observed. These results indicate that the physical process of secretion may differ between F. grandifolia and A. germinans; in both, however, the ultrastructural observations support the contention that specific structural parameters are correlated with the process of secretion.
Seeds and seedlings of the halophyte Atriplex patula were exposed to 0–2% NaCl to determine the effect of salt stress on germination and growth. Seeds germinated and plants survived and grew in solutions of up to 2.0% NaCl. Both seed germination and dry mass production were negatively affected by increased salinity. Dry mass production declined to 1% of controls and seed germination to 17% of controls in the 2% NaCl treatments, indicating that seeds were less inhibited than growing plants. Also, recovery treatments indicated that high salinity did not permanently injure seeds. Percent ash, and Na⁺ and Cl⁻ ions increased in shoots with each salt increment, while the K⁺ ion content decreased sharply. Atriplex patula is a facultative halophyte, and is limited to low and moderately saline sites because both seed germination and growth are severely reduced at salinities > 1% NaCl.
Sixteen accessions of the xerohalophyte, Atriplex canescens (Pursh.) Nutt., differing in tendency to accumulate Na or K in leaf tissues, were compared for salt tolerance in a greenhouse study. Plants were grown along a salinity gradient from 72 to 2017 mol/m³ NaCl measured in the root zone. Growth rates (RGR) were negatively affected by salinity for all accessions. Initial leaf levels of Na (measured before exposing plants to saline solutions) were positively correlated with subsequent RGR's of accessions on the salinity gradient (r = 0.60 - 0.88, P < 0.05 across salinity levels), whereas initial leaf K levels were negatively correlated (r = -0.68 to -0.85, P < 0.01 across salinity levels). Varieties linearis (S. Wats.) Munz and grandidentatum Stutz & Sanderson had greater tendency for Na accumulation, lower tendency for K, and higher growth rates on saline solutions than var. occidentalis (Torr. & Frem.) Welsh & Stutz accessions. Within var. occidentalis accessions, RGRs were negatively correlated with initial leaf levels of K but not Na. Postexposure leaf Na and K levels were not strongly correlated with RGR's. All accessions responded to salinity by increasing their uptake of Na, which is the primary mechanism of osmotic adjustment to salinity in this species. It is suggested that differences in tendency to accumulate Na or K among A. canescens genotypes are related to their specialization for saline or xeric habitats, respectively.
Desertification (land degradation in arid, semi-arid and dry sub-humid areas resulting mainly from adverse human impacts) is the main environmental problem of dry lands, which occupy more than 40 per cent of the total global land area. The phenomenon threatens about 3.6 billion hectares and currently affects the livelihood of about 900 million people. Thl! world is now losing annually about 1.5 million hectares of total irrigated lands (240 million hectares) due mostly to salinization, mainly in drylands. Salt affected soils are widely distributed throughout the arid and semi-arid regions, and particularly severe in China (7 million ha), India (20 million ha), Pakistan (3.2 million ha), USA (5.2 million ha), as well as Near East, southern Europe and elsewhere. Demands on production have increased the pressure on existing productive land and moved the limits of production onto increasingly marginal lands. Wise land-use practices have yet to be developed for such conditions. The Executive Director of UNEP reported to the Governing Council in February 1992 concerning the "Status of Desertification and Implementation of the United Nations Plan of Action to Comtat Desertification (PACD)". The Report concludes that major efforts to implement the PACD had gJne into supporting measures rather than concrete corrective field operations. Little evidence of progrl!ss was found in irrigated croplands, rainfed croplands or rangelands. It was recommended that every piece of land should be used in keeping with its ecological characteristics, natural capabilities and constraints.