Touchette 2007 Journal of Experimental Marine Biology and Ecology

Journal of Experimental Marine Biology and Ecology 350 (2007) 194 215
www.elsevier.com/locate/jembe
Seagrass-salinity interactions: Physiological mechanisms

used by submersed marine angiosperms for a life at sea
Brant W. Touchette
Center for Environmental Studies and Department of Biology, Campus Box 2625, Elon University, Elon, NC 27244, USA
Received 2 April 2007; received in revised form 18 May 2007; accepted 29 May 2007
Abstract
Due to the nature of coastal and estuarine systems, seagrasses must be able to tolerate short-term salinity fluctuations including
both hyposaline and hypersaline conditions. Salt tolerance can be achieved, in part, through vacuolar ion sequestering (mostly Na+,
K+, and Cl) and cytosolic osmolyte accumulation (K+ and organic osmolytes), with differences in cellular ion levels attributed to
selective ion flux and ion partitioning between the cytoplasm and vacuole (with lower cytoplasmic-to-vacuolar ratios favoring
higher cellular Na+ concentrations). The hydrophilic nature of organic compounds such as organic acids, soluble carbohydrates,
and free amino acids allow them to serve as osmoprotectants and low-molecular-weight chaperones which diminishes the
inhibitory effects of potentially harmful ions on metabolic processes. Nevertheless, some carbohydrate studies on seagrasses have
shown decreased soluble sugar content with increased salinities. During salt stress, carbohydrates are likely converted to other
organic compounds that would better facilitate osmotic adjustment in these plants. This is further supported by observed decreases
in sucrose-P synthase (a key enzyme involved in sucrose synthesis) activities in seagrass exposed to higher salinities. While
modifications in ion flux and organic solute levels often follow changes in environmental salinities, these adjustments are relatively
slow (hours to days). Therefore, the initial response to sudden salinity change will include rapid alterations in turgor pressure driven by
water flux in the direction of the osmotic gradient. The rate of water movement depends largely on the hydraulic conductivity of the
plasmalemma and the elastic properties of the cell wall (bulk elastic modulus; ). Observations on cell wall elasticity indicate that
some seagrasses maintain fairly rigid walls (high values), thereby limiting the amount of water influx during hypoosmotic stress.
Although high would be beneficial to open-water coastal plants living in relatively stable saline environments, in estuaries where
salinities fluctuate considerably over shorter intervals, high could promote flaccid cells with no turgor pressure during
hyperosmotic conditions. Hypo- and hyperosmotic conditions also inhibit photosynthesis in seagrasses. Decreases in photosynthesis
have been attributed to declines in chlorophyll content, changes in chloroplast ultrastructure, disruptions of electron flow through
photosystems, and inhibitions of key photosynthetic enzymes. The uptake of nutrients can also be strongly influenced by salinity.
High affinity Na+-dependent nutrient transport systems (for NO3 , H2PO4 , and HPO2
4 ) which benefit from the inwardly driving force
for Na+ have been observed in seagrasses. Nitrate reductase, the key enzyme involved in nitrate reduction/ assimilation, also has
elevated activities at higher salinities which would agree with Na+-dependent NO3 transport. While our basic understanding of how
seagrasses survive in saline environments is increasing, it still lags well behind marine algae and terrestrial halophytes. It is likely that
further investigations will reveal unique physiological adaptations that have not been observed in other plants.
2007 Elsevier B.V. All rights reserved.
Keywords: bulk elastic modulus; carbon metabolism; ion transport; nutrients; osmolytes; osmotic adjustment; photosynthesis; respiration
Tel.: +1 336 278 6185; fax: +1 336 278 6258.

E-mail address: btouchette@elon.edu.
0022-0981/$ - see front matter 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2007.05.037
B.W. Touchette / Journal of Experimental Marine Biology and Ecology 350 (2007) 194215
1. Introduction
Seagrasses are highly productive submersed marine
angiosperms that grow in shallow coastal and estuarine
waters, providing critical habitat for numerous finfish,
shellfish, waterfowl, and herbivorous mammals (Phillips
and Meez, 1988; Klumpp et al., 1989). Substantial
declines in seagrass habitat have been reported worldwide, mostly attributed to light reductions from algal
overgrowth, sediment loading, and sediment resuspension
(Harlin, 1993; Morris and Tomasko, 1993). Processes
including direct physiological responses to nutrient
enrichment (Touchette and Burkholder, 2000a) and
altered salinity regimes have also contributed to the
disappearance of seagrass meadows (Zieman et al., 1999;
Rudnick et al., 2005). Clearly, salinity is a major
environmental component that can influence the structure
and function of seagrass communities (Montague and
Ley, 1993). Studies conducted on these marine angiosperms suggest that most species have optimal growth
195
between 30 and 40 psu, although a few species have

enhanced growth in brackish waters (e.g. Zostera
capensis; Table 1). Seagrasses can tolerate short-term
salinity fluctuations, as necessitated by the nature of
coastal and estuarine environments which are often
susceptible to changes in natural (freshwater inflows,
hurricanes) and anthropogenic (wastewater disposal,
desalination plants, and modified watersheds) freshwater
inputs (Adams and Bate, 1994; Tomasko and Hall, 1999;
Torquemada et al., 2005; Thorhaug et al., 2006). Due to
the interplay between fresh and marine waters, estuaries
tend to be more osmotically variable (salinities can range
between 0 and 35 psu, but can also reach 70 psu in
hypersaline embayments; Walker and McComb, 1990)
than near-shore coastal environments (with slight declines
of 3 psu following unusually high rainfall; Barbour, 1970;
McConnaughey, 1978; Kraemer et al., 1999). Therefore
seagrasses in estuarine environments are likely to be better
adapted to rapid and substantial salinity changes in
comparison to near-shore coastal species.
Table 1
Salinity preferences in seagrasses
Species
Productivity/plant size
Amphibolis antarctica
Amphibolis antarctica
Halophila johnsonii
Ruppia cirrhosa
Ruppia maritima
Thalassia testudinum
Zostera capensis
Zostera marina
Photosynthesis
Halophila engelmannii
Halophila johnsonii
Halophila ovalis
Ruppia maritime
Ruppia maritima
Zostera marina
Zostera marina
Zostera muelleri
Zostera nana
Other
Amphibolis antarctca
Ruppia cirrhosa
Ruppia maritima
Ruppia maritima
Zostera capensis
Salinity preference (psu)
Salinities tested (psu)
Determined by
Reference
42
42
30
0
20
30
20 to 40
40
15
22
35 to 64
35 to 65
0 to 60
0 to 75
0 to 60
15 to 40
0 to 70
0 to 60
0 to 75
22 and 32
Productivity
Leaf production
Leaf production
Total plant mass
Productivity
Productivity-field
Leaf area
Productivity
Total plant mass
Productivity
Walker (1985)
Walker and McComb (1990)
Torquemada et al. (2005)
Adams and Bate (1994)
Berns (2003)
Zieman (1975)
Kahn and Durako (2006)
Berns (2003)
Kamermans et al. (1999)
25
40
9 to 52
17 to 35
20
30 to 40
40
31
22
35
32
5 to 35
0 to 60
0 to 88
0 to 35
0 to 40
0 to 70
0 to 60
0 to 93
22 and 32
0 to 140
0 to 65
Photosynthetic rates
Photosynthetic efficiency
Fluorescence
O2 production; electrodes
O2 production; Winkler
Dawes et al. (1987)

Torquemada et al. (2005)
Ralph (1998)
Lazar and Dawes (1991)
Murphy et al. (2003)
Berns (2003)
Biebl and McRoy (1971)
Kamermans et al. (1999)
Kerr and Strother (1985)
Ogata and Matsui (1964)
35 to 42
10 to 20
0 to 15
0 to 10
20 to 40
30 to 40
35 to 65
0 to 30
0 to 30
0 to 70
0 to 70
10 to 50
Plant survival
Natural occurrence
Germination; N.C. ecotype
Germination
Plant survival
Natural occurrence
Walker and McComb (1990)

Koch and Dawes (1991)
Data are sorted by evaluation technique (i.e., productivity or plant size, photosynthesis, and other) and include seagrass species, estimated salinity
preference (psu), range of salinities evaluated, technique used to determine preference, and reference.
196
Salinity fluctuations can alter important plant biochemical and physiological processes, which in turn,
can influence plant metabolism, growth, development,
and reproduction (McMillan and Moseley, 1967; Zieman,
1975; Walker and McComb, 1990; Ramage and Schiel,
1998; Vermaat et al., 2000; Torquemada et al., 2005).
While our understanding of salt tolerance in terrestrial
halophytes and marine algae has progressed considerably over the last decade, our comprehension of
basic physiological mechanisms involving salt tolerance in seagrasses remains incomplete. Therefore
the purpose of this review is to synthesize what is
known about plant-salinity interactions in seagrasses
including ion transport and accumulation, osmotic adjustment, photosynthetic and respiratory responses,
nutrient acquisition, and carbon metabolism. Due to
a number of gaps in our basic understanding of salt
tolerance in seagrasses, I have also invoked key physiological principles from other marine macrophytes
(including marine algae) and terrestrial halophytes to
build upon existing knowledge of seagrass-salinity
interactions.
2. Plant-salinity relations
Arguably, one of the greatest obstacles for vascular
marine plants to overcome is high salinities. Seawater is
more than 3% salt, with molarities of major ions ranging
from 540 mM for Cl-, 460 mM for Na+, and 50 mM Mg+.
For most angiosperms, elevated environmental salinities
can promote both hyperionic and hyperosmotic stress,
with consequential decreases in growth and development
and increases in plant mortality (Mahajan and Tuteja,
2005). Elevated environmental salinities will generate
lower water potentials, making it increasingly difficult for
plants to acquire water and nutrients from the environment (Munns, 2002; Larcher, 2003; Touchette, 2006;
Fig. 1). While physiological responses to saline stress are
remarkably similar to drought stress as increased
environmental salts effectively pull water away from
plant tissues comparisons between salinity stress and
desiccation should be made with some caution. Both
increased salinity and desiccation will increase cellular
ion concentrations, however the ratios of different ions in
plant tissues will be dissimilar. That is, the proportion of
Fig. 1. Whole-plant water relations in seagrass during hypo- and hypersaline conditions. Illustrations show initial water flux for plants acclimated to
35 psu and undergoing hyposaline (10 psu) conditions (left panel), and plants acclimated 15 psu and undergoing hypersaline (40 psu) conditions
(right panel). Water flux, as indicated by arrows, moves from high to low water potentials (). Leaf, sheath, rhizome, and root osmotic potentials (o)
were estimated from Halodule wrightii (collected from a euryhaline estuary) using a vapor-pressure osmometer (see Fig. 2). Vapor-pressure
measurements were converted to MPa according to the empirical equation (MPa = (0.173 [0.0269 mmol Kg 1]) 0.10) described by Rumbaugh
(1991). The degree of water flux will depend greatly on the hydraulic conductivity of the cell membrane and the elastic properties of the cell wall.
different ions will remain constant during dehydration but

will change markedly during salinity stress due to
selective ion uptake (Kirst, 1989).
In halophytes, vacuolar ion sequestering and cytosolic
osmotically-active solute (osmolytes) accumulation are
used to generate high intracellular osmotic pressure
(Flowers et al., 1977). In Halodule wrighii, Ruppia
maritima, Thalassia testudinum, and likely most other
seagrasses, steady-state plant tissues are hyperosmotic
relative to their external environment (Fig. 2; Berns,
2003; Kahn and Durako, 2006). Consequently, marine
plants must be able to balance Na+ and Cl fluxes used
for maintaining osmotic equilibrium while preventing the
accumulation of these toxic ions within the cytoplasm.
Moreover, many emergent halophytes have salt-secreting
glands that effectively remove excess salt from plant
tissues (Liphschitz and Waisel, 1974; Hansen et al.,
1976), however such structures are apparently lacking in
seagrasses (Jagels, 1973; Murphy et al., 2003).
197
3. Ion flux and ion balance

Salt-damage on plants (as outlined by Mahajan and
Tuteja, 2005) can be derived from four basic physiological processes: (i) loss of ionic equilibrium as the influx of
Na+ lowers cellular membrane potentials followed by the
accumulation of Cl down an electrochemical gradient,
(ii) disruption of cellular metabolism by Na+ through the
impairment of vital enzymes (Niu et al., 1995), (iii)
loss of osmotic balance following ion accumulation,
resulting in both reduced growth and development, and
(iv) decreased photosynthetic efficiencies and increased
formation of reactive oxygen species (ROS) following
Na+ buildup (Flowers et al., 1977; Greenway and Munns,
1980; Yeo, 1998).
Na+ is of particular concern as the extreme negative
membrane potential in plant cells can support Na+
cytoplasmic concentrations at hundred-fold higher than
levels observed in the natural environment (Carpaneto
Fig. 2. Non-vascular and total osmolality in Halodule wrightii tissues acclimated for six weeks to three different environmental salinities (15, 25, and
35 psu using artificial seawater in greenhouse microcosms). Tissues evaluated include leaves (panel-A), sheath (panel-B), roots (panel-C), and
rhizome (panel-D). Horizontal bars crossing each salinity-pair represent the osmolality of the cultured seawater. Note that tissue osmolality is
maintained well above seawater conditions. Data are presented as means 1 SE (n = 5), with significant differences within each tissue class indicated
by letters (ANOVA). Osmolality measurements were determined using a Wescor Vapor Pressure Osmometer (model 5520; Logan, Utah) according to
Tyerman (1982) and Murphy et al. (2003).
198
Species
Seagrasses
Cymodocea nodosa
Halophila stipulacea
Halophila stipulacea
Posidonia australis
Posidonia oceanica
Posidonia oceanica
Ruppia maritima
Ruppia maritima
Zostera marina
Zostera marina
Zostera marina
Zostera marina
Zostera marina
Zostera marina
Mean 1 SE
Halophytes and Coastal Wetland Plants
Cococarpus erectus
Halocnemum strobilaceum
Halocnemum strobilaceum
Laguncularia racemosa
Rhizophora mangle
Rhizophora mangle
Rhabdadenia biflora
Na+(mg g 1)
K+(mg g 1)
Na+:K+
Tissue type
Salinity (psu)
Reference
20.6a
65.3a
61.2a
1.79.4b
34.3
54.8c
1030
1022
2740
4045
1.54.0
2.55.5
16.0
320 mmol dm 2
300 mmol dm 2
400 mmol dm 2
28.9 10.8
20.4
19.8
15.4
3.610.9
24.3
22.5
1024
1020
16.525.0
24.532.0
1.05.5
2.04.5
32.0
200 mmol dm 2
190 mmol dm 2
100 mmol dm 2
17.6 2.7
1.72
5.61
6.75
1.30
4.14
2.40
2.00
1.81
2.74
2.55
1.50
1.22
0.85
1.60
1.58
4.00
2.7 0.58
Whole plant
Aboveground
Belowground
Leaf
Leaf
Leaf
Leaf
Rhizome
Leaf
Rhizome
Aboveground
Belowground
Shoot and Root/Rhi.
Leaf
Shoot
Root
34 to 38 psu
34 to 38 psu
34 to 38 psu
13 to 57 psu
34 to 38 psu
Seawater
Not provided
Not provided
Not provided
Not provided
3 psu to seawater
3 psu to seawater
9 to 44 psu
Seawater
Seawater
Seawater
Malea and Haritonidis (1995)

Malea (1994)
Malea (1994)
Tyerman et al. (1984)
Malea et al. (1994)
Ledent et al. (1995)
Walsh and Grow (1973)
Lyngby and Brix (1983)
Lyngby and Brix (1983)
Van Diggelen et al. (1987)
Ye and Zhao (2003)
Ye and Zhao (2003)
Ye and Zhao (2003)
2.1d
23.0
155
10.8e
4.6D
8.7e
13.3d
2.7
24.6
1.57
5.6
7.8
13.3
39.1
1.32
3.27
167
1.11
0.58
1.63
167.8
Leaf
Seedlings
Seedlings
Leaf
Leaf
Leaf
Leaf
2.5 to 20 psuh
0.00 M NaCl
0.68 M NaCl
10 psui
2.5 to 20 psu
10 psui
2.5 to 20 psu
Vilarrubia (2000)
Pujol et al. (2001)
Pujol et al. (2001)
Medina et al. (1995)
Vilarrubia (2000)
Medina et al. (1995)
Vilarrubia (2000)
Table 2
Sodium and potassium levels (mg g 1 dry weight, unless otherwise noted) observed in different plant groupings (seagrasses, halophytes and coastal wetland plants, marine algae, and terrestrial plants)
6.9e
230.0e
7.0e
46.0e
46.1 22.6
60.6
17.5
16.6
14.6
18.4 5.3
0.19
22.3
0.71
5.33
18.67 15.0
Leaf
Leaf
Root
Root
42.7f
54.7f
38.2f
36.3f
14.6
19.3
70.6f
39.5 7.3
31.8
43.2
115.8
35.0
70.2
112.2
86.9
70.7 13.4
2.28
2.15
0.56
1.77
0.35
0.29
1.38
1.25 0.32
Whole
Whole
Whole
Whole
Whole
Whole
Whole
0.50
0.32 g
0.15g
0.30
0.42f
1.40
0.40
0.15
0.45 0.14
2.25
24.3
24.0
1.55
4.24
1.95
1.91
0.41
7.57 3.63
0.38
0.02
0.01
0.32
0.17
1.22
0.35
0.62
0.38 0.14
Leaf
Shoots
Fruit
Leaf
Tubers
Leaf
Leaf
Leaf
plant
Plant
plant
plant
plant
plant
plant
0.0 mmol/dm3 NaCl

1000 mmol/dm3 NaCl
0.0 mmol/dm3 NaCl
1000 mmol/dm3 NaCl
Balnokin et
Balnokin et
Balnokin et
Balnokin et
Seawater
Seawater
Seawater
Seawater
Seawater
Seawater
Seawater
Ruprez (2002)
Ruprez (2002)
Ruprez (2002)
Ruprez (2002)
Zubia et al. (2003)
Zubia et al. (2003)
Ruprez (2002)
NA
NA
NA
NA
NA
NA
NA
NA
Ruby et al. (2000)

zcan (2005)
zcan (2005)
Ruby et al. (2000)
Charles et al. (2005)
Ruby et al. (2000)
Ruby et al. (2000)
Ruby et al. (2000)
al. (2005)
al. (2005)
al. (2005)
al. (2005)
In some instances data had to be converted to mg g 1 from ag g 1 dry wt., bmol m 3, c% dry wt., dmmol g 1 dry wt., emmol Kg 1 dry wt., fmg 100 g 1 dry wt., and gppm. Soil salinity had to be
converted to psu from mmol Kg 1i, and salinity was highly variable with soil depth h. Data include ion concentrations (Na+ and K+), mean molar ratios (Na+ K+), type of tissue used during analysis
(Tissue type), salinity or salt conditions (psu, unless otherwise noted), and reference. Mean and standard errors (SE) are also provided for each grouping for general comparative purposes.
Salicornia europaea
Salicornia europaea
Salicornia europaea
Salicornia europaea
Mean 1 SE
Marine Algae
Chondrus crispus
Fucus vesiculosus
Laminaria digitata
Porphyra tenera
Sargassum mangarevense
Turbinaria ornate
Undaria pinnatifida
Mean 1 SE
Terrestrial (higher plants)
Caccinia cordifolia
Capparis ovata
Capparis ovata
Ficus religiosa
Manihot esculenta
Moringa oleifera
Psidium guajava
Tamarindus indica
Mean 1 SE
199
200
et al., 2004). Unfortunately, halophytes apparently lack

adapted metabolic mechanisms that are insensitive to
high Na+ levels (Hasegawa et al., 2000). Consequently,
plants in high saline environments must undergo osmotic
adjustment involving, in part, the localization of toxic
ions (typically Na+ and Cl) into vacuoles and away from
important metabolic processes located within the cytoplasm (Niu et al., 1995; Yeo, 1998).
Unlike Na+ which can adversely affect both catabolism and metabolism, K+ is essential for maintaining
osmotic balance, and supporting biological reactions as
co-factors for numerous vital enzymes. Therefore, the
uptake and assimilation of K+ is imperative for overall
plant health and growth. In both Halophila stipulacea
and Posidonia oceanica, for example, cyclic elevations
in cellular K+ levels corresponded with peak growing
periods (Malea, 1994; Malea et al., 1994). However, Na+
competes with K+ for intracellular influx, such that many
K+ transport systems tend to also have high affinities for
Na+ and thus function as Na+/K+ symporters (Niu et al.,
1995; Amtmann and Sanders, 1999; Blumwald et al.,
2000; Carpaneto et al., 2004). Therefore relatively high
environmental Na+ levels can influence K+ influx
efficiencies in marine plants.
When considering the composition of Na+ and K+ in
seawater (19.3 and 0.4 mg ml 1 at 35 psu, respectively;
Riley and Chester, 1989), it is clear that mechanisms
must be in place to minimize cytosolic Na+ accumulation
while permitting necessary K+ uptake. Even with the
disparity between Na + and K + concentrations in
seawater, seagrasses are able to accumulate comparatively high levels of K+ within their tissues (ca. 17.6 mg g 1
dry wt; Table 2; Albert and Popp, 1977; Van Diggelen
et al., 1987). These K+ levels are more than twice the
amount observed in terrestrial plants (ca. 7.6 mg g 1 dry
wt), comparable to halophytes and coastal wetland
species (mean levels were ca. 18.7 mg g 1 dry wt), but
substantially lower than marine algae (ca. 70.7 mg g 1
dry wt). Among the salt-tolerant plants (i.e., seagrasses,
marine algae, upland halophytes, and coastal wetland
plants) seagrasses have the lowest Na+ concentrations
(ca. 29 mg g 1 dry wt, compared to 40 and 46 mg g 1
dry wt for marine algae and terrestrial halophytes,
respectively; Table 2). These differences may reflect
some general variations in physiological processes
involved in salt tolerance. For example, while marine
algae accumulate relatively high Na+ concentrations,
they also concentrate remarkably high K+ levels;
resulting in a Na+:K+ molar ratio of 1.25 (Fig. 3). This
suggests that K+ functions as a major osmolyte in algae.
In contrast, terrestrial halophytes, which also accumulate
high Na+ levels, have proportionally lower K+ levels as
indicated by a mean Na+:K+ molar ratio of 18.7 (albeit

highly variable in this group, with only 7 of 11 plants
mentioned were greater than the algal mean). This higher
Na+:K+ ratio may indicate a greater dependence on
organic osmolytes in maintaining osmotic equilibrium.
Seagrasses, like marine algae, have comparably low Na+:
K+ molar ratios (ca. 2.7 0.58), however both Na+ and
K+ concentrations in seagrasses are considerably lower
than algae (Albert and Popp, 1977; Van Diggelen et al.,
1987).
It is likely, selective ion flux and ion portioning
between cytoplasm and vacuole play an important role in
establishing and maintaining different ion concentrations
and ratios in marine plants. However, the degree at which
each mechanism is employed by plants is not well
understood, and a more comprehensive study considering
the relative importance of each of these components in
ion maintenance would provide valuable insight into the
eco-physiology of these plants.
4. Ion transport and membrane potentials
The maintenance of a negative membrane potential
(typically between 120 to 200 mV) is important in
plant cells; however during hypersaline conditions the
influx of Na+ can alter the H+ electrochemical gradient.
As mentioned previously, for plants in high saline
environments it is believed that Na+ can cross the plasma
membrane using the same transport systems developed
for K+ (Niu et al., 1995; Amtmann and Sanders, 1999;
Blumwald et al., 2000; Fig. 4). There are a number of
channels involved in K+ transport, including voltageinsensitive, monovalent, cation-permeable channels
(VIC), inward-rectifying K+ channels (KIR), and outward-rectifying K+ channels (KOR; Amtmann and
Sanders, 1999; White, 1999; Blumwald et al., 2000;
Carpaneto et al., 2004). While, it is possible that many
halophytes have not developed K+ specific transport
systems that exclude the movement of Na+ (perhaps due
to the role of Na+ as a vacuolar osmolyte; Garrill et al.,
1994; Hasegawa et al., 2000), sheath protoplasts from the
seagrass Posidonia oceanica contain both KOR and KIR
that are highly selective for K+ and impermeable to other
monovalent cations (including Na+, Li+, and Cs+;
Carpaneto et al., 2004). This outward movement of K+
from sheath cells in P. oceanica is thought to be a
possible mechanism for K+ accretion in xylem vessels,
analogous to SKOR in Arabidopsis roots (Carpaneto
et al., 2004).
Nevertheless seagrasses could maintain ion homeostasis through the use of transmembrane transport
proteins including H + translocating ATPases and
Fig. 3. Tissue Na+ and K+ levels observed in seagrasses (black circles),

marine algae (black inverted triangles), and terrestrial vascular plants
(open triangles). Note marine algae tend to accumulate higher K+
levels relative to seagrasses, and seagrasses accumulate higher Na+
levels than terrestrial plants. Data represent multiple species within
each plant group (see Table 2 for represented species).
pyrophosphatases, Ca 2+ -ATPases, secondary active

transporters, and channels (Niu et al., 1995; Sze et al.,
1999; Blumwald et al., 2000; Binzel and Ratajczak,
201
2002; Fig. 4). While undoubtedly Na+ participates in an

inwardly-directed driving force in seagrasses, inward and
outward ion channels specific for K+ were observed in P.
oceanica, and these channels appeared to be impermeable to Na+ and other monovalent cations (Carpaneto
+ +
et al., 2004). Furthermore, a relative permeability PK
/PNa
ratio of 303 was observed in Zostera marina (with
external K+ levels between 0.05 and 0.5 mM and Na+ of
0.5 mM; Fernndez et al., 1999). This high selectivity,
strongly favoring K+ influx over Na+, likely allows Z.
marina to grow in elevated Na+ environments while
maintaining remarkably negative membrane resting
potentials (156 10 mV; Fernndez et al., 1999). In
contrast to the highly selective channels described above,
an outward K+ channel in Z. muelleri was only five-times
more permeable to K+ than Na+ (Garrill et al., 1994),
which is similar to permeabilities observed in many
glycophytes.
Even with highly selective K+ channels that minimize
the passage of other ions, Na+ accumulation does occur
within seagrasses (Garrill et al., 1994), so other
mechanisms must be employed to remove unwanted
Na+ from the cytosol. The efflux of cytosolic Na+ (either
Fig. 4. Ion transport processes used in plants to achieve osmotic homeostasis. The primary ions (Ca2+, Cl, H+, K+, and Na+) involved in osmotic
adjustment are presented along with transport proteins (antiporters [A], channels [C], and symporters [S]), sub-cellular pH levels (cytoplasmic and
vacuolar), and membrane electrochemical potentials typical for the plasmalema and tonoplast. Note ion levels in the cytoplasm must be carefully
controlled to prevent metabolic disruptions (adapted from Hasegawa et al., 2000 and Taiz and Zeiger 2006).
202
outside the cell or into a vacuole) may be accomplished

through electroneutral Na+/H+ antiporters that depend on
energy from H+-ATPases along the plasmalemma or
tonoplast (Padam and Schuldiner, 1994; Hasegawa et al.,
2000; Garciadeblas et al., 2001). However, because of
thermodynamic restrictions, Na+/H+ antiporters cannot
effectively transport Na+ outside the cell when the pH of
the external medium is relatively high (like those of
seawater; Kiegle and Bisson, 1996; Garciadeblas et al.,
2001). While alternative transport systems have been
described in other organisms, such as Na+-ATPase in
marine algae, these pumps have not been observed in
higher plants, including seagrasses (Niu et al., 1995;
Blumwald et al., 2000; Garciadeblas et al., 2001).
Secondary active ion transport across the plasma
membrane and tonoplast are driven by electrochemical
gradients produced by H+ pumps (Zhien et al., 1997;
Lttge and Ratajczak, 1997; Palmgren and Harper,
1999). This secondary transport will further assist in the
removal of harmful ions from the cytosol and either into
the vacuole or out of the cell. Halophytes under
thermodynamic steady-state conditions maintain between
102- to 103- fold lower concentrations of Na+ and Cl in
the cytosol in comparison to the apoplast or the vacuole
(Hasegawa et al., 2000). The development and maintenance of H+ electrochemical gradients are achieved
through H + -ATPases in the plasma membrane and
H + -ATPases and H+-pyrophosphatases in the tonoplast
(Hasegawa et al., 2000). While H+-pyrophosphatases are
important in the transport of H+ into the vacuole, its role
in salt tolerance is unclear. It is believed that the primary
physiological responsibilities of H+-pyrophosphatase are
to maintain cytosolic pH and to regulate pyrophosphate
turnover (Zhien et al., 1997; Hasegawa et al., 2000).
In seagrasses (e.g., R. maritima, T. testudinum, and
Z. marina), the plasma membrane structure of mature
epidermal cells is morphologically and physiologically
unique (Jagels, 1973; Jagels, 1983; Jagels and Barnabas,
1989; Arai et al., 1991; Pak et al., 1995; Fukuhara et al.,
1996). These cells typically have invaginated plasma
membranes with high ATPase activity. The invaginations
may increase the cellular capacity for solute influx and
efflux by increasing the surface area of the plasma
membrane (Gunning, 1977; Jagels, 1983; Wimmers and
Turgeon, 1991). This, coupled with a high number of
mitochondria located around the periphery of the cell,
could provide the energy necessary for active ion flux
(Fukuhara et al., 1996; Fernndez et al., 1999). As
mentioned previously, plasma membrane H+-ATPases
are responsible for generating electrochemical proton
gradients that facilitate the transport of ions and nutrients
through specific channels and carriers. The high degree
of membrane invagination observed in seagrasses would

increase the membrane's surface area and the number of
H+-ATPases, carriers, and channels (Fukuhara et al.,
1996). In Z. marina, there is also evidence that Na+/H+
antiporters may play an important role in Na+ efflux, and
may serve as an overflow valve during high Na+
accumulations within the cell (Fernndez et al., 1999).
While some seagrasses appear to minimize the influx
of ions into cells, ion sequestering within vacuoles is still
essential in maintaining osmotic equilibrium. In support
of Na+ accumulation in vacuoles of seagrasses, Carpaneto et al. (1997) were able to characterize ion channels
in the tonoplast of P. oceanica. In these plants, ATPases
mediate the translocation of H+ and K+/Na+, and were
found to increase in number during salt stress (Braun
et al., 1986; Watad et al., 1991). It is also possible that
ATPases with a greater affinity for K+ may be actively
involved in ion influx, while a second type of ATPase
transporter, with lower K+/Na+ selectivity, is pumping
ions in the other direction (Mahajan and Tuteja, 2005).
The change in membrane potential (less negative)
associated with Na+ uptake will establish an electrochemical gradient that facilitates the influx of Cl
(Hasegawa et al., 2000). In terrestrial halophytes, it is
believed that anion channels are involved in the passive
influx of Cl (Hedrich, 1994; Czempinski et al., 1999).
Once a steady-state is reestablished, and passive flow of
Cl is minimized, further influx of Cl could be achieved
through H+ translocation involving a ClH+ symporter
(Poole, 1988). Like Na+, Cl- is often sequestered in
vacuoles of halophytes to assist in osmotic adjustment.
The tonoplast Cl transport system is likely a channel or a
carrier that couples Cl transport with an H+ gradient
(Hasegawa et al., 2000). A positive tonoplast potential
(+50 mV) could facilitate a tenfold increase in Cl
levels relative to the cytosol.
Clearly seagrasses can employ a number of mechanisms to maintain suitable ion levels. Through a
combination of selective ion channels and secondary
active transport, plants can minimize harmful ion
accumulation in the cytoplasm, and when in concert
with H+ pumps, could maintain favorable membrane
potentials. Nevertheless, only a few studies actually
consider ion channels in seagrasses, and it is likely that
further studies will demonstrate unique biochemical
adaptations in these plants in comparison to the more
widely studied terrestrial halophytes and glycophytes.
5. Osmotic acclimation and adjustment
Sodium is the most common ion in Z. marina tissue
(250 to 400 mmol dm 3), with higher concentrations
found in leaves and roots relative to shoots (Ye and Zhao,

2003). In contrast, K+ levels in Z. marina (75 to 200 mmol
dm 3) were highest in leaves and lowest in roots (Ye and
Zhao, 2003). However, when considering increases in
osmolyte concentrations due to salinity challenges, it is
important to note where within the cell these ionic and
organic osmolytes are accumulating. As mentioned, it is
generally held that the osmotic potential in vacuoles is
principally controlled by ions, whereas the osmotic
potential in the cytoplasm is controlled by both K+ and
organic osmolytes (Davison and Reed, 1985; Kirst,
1989). Some studies suggest that further compartmentalization of osmolytes can occur in organelles within the
cytoplasm thus allowing for the accumulation of multiple
solute compounds (Gimmler and Lotter, 1982; Setter and
Greenway, 1983). X-ray microanalysis on Z. marina
mesophyll cells revealed 4.5 fold greater concentrations
of Na+ in the vacuole relative to the cytoplasm (Ye and
Zhao, 2003). In contrast, the same cells had a 3.5 fold
higher concentration of K+ in the cytoplasm relative to the
vacuolar fluid (Ye and Zhao, 2003).
It is expected that any substantial change in cellular
turgor pressure in a plant will ultimately induce osmotic
adjustments. These adjustments involve changes in
cellular concentrations of osmotically-active solutes
until a new steady state is achieved. In comparison to
the initial change in pressure, osmotic adjustment is
considerably slower with some macrophytes requiring
days before turgor pressure is fully restored (Kirst, 1989).
This long acclimation period may provide limited benefit
to estuarine species that are subjected to sizeable salinity
variations over shorter intervals. Slow osmotic response
can be attributed to the metabolic nature of osmotic
adjustment involving energy to drive the transport of ions
and the synthesis of organic osmotica. Nevertheless,
seagrasses have demonstrated remarkably quick osmotic
adjustments to small and moderate salinity changes
(Berns, 2003; Murphy et al., 2003). This fairly rapid
adjustment is likely associated with importance of
inorganic osmotica in maintaining osmotic equilibrium.
Studies by Ye and Zhao (2003) suggest that inorganic
ions can contribute between 65 and 70% of the total leaf
water potential in Z. marina, and that Na+ and K+ were
the two most important ions accounting for 33 and 20%
of the water potential, respectively. However the relative
dependence of inorganic versus organic osmotica is
likely tissue specific. For example, in Z. marina, highly
vacuolated mesophyll cells may relay heavily on
inorganic ions (Na+ and K+) for osmotic adjustment,
whereas epidermal cells with proportionally smaller
vacuoles may relay more on organic molecules and K+
(Ye and Zhao, 2003).
203
The principal ions involved in osmotic adjustment are

K+, Na+, and Cl. Not surprisingly, in comparison to
terrestrial plants, seagrasses contain markedly greater
concentrations of K+ and Na+ (Table 2). The ion composition in seagrass cells, especially Na+ and Cl, is quite
different from seawater. For example, cellular K+ concentrations are notably higher than Cl- (75 and 200 mmol
mL 1 in leaf tissue of Z. marina for Cl- and K+, respectively; Ye and Zhao, 2003). This ion imbalance can be
attributed to differences in selective ion uptake accomplished by altering the activities of ion transporters (see
previous section on ion transport and membrane
potentials). This process can be quite costly, for example
marine algae expend between an estimated 10 and 30%
of the total respiratory energy for the maintenance of
ionic balance (Raven, 1985; Ritchie, 1988). While Na+
levels in seagrasses (between 1 and 65 mg g 1 dry wt)
are only slightly lower than those observed in marine
algae (between 15 and 70.6 mg g 1 dry wt), K+ levels in
seagrasses (between 3 and 25 mg g 1 dry wt) are
considerably lower than algae (between 32 and 115 mg
g 1 dry wt; Table 2; Fig. 3). Differences in ion concentrations may, again, reflect the proportional volume of
vacuolar sap within the cell. In most macrophytes the
vacuole is critical in osmotic maintenance as it represents
the greatest portion of the cell volume. Therefore,
dissimilarities in ion levels between seagrasses and
marine algae may reflect differences in cytoplasm-tovacuole ratios. The relationship between vacuole size and
salt tolerance among different seagrass species is poorly
understood and could benefit from further investigation.
For both halophytes and glycophytes, osmotic
adjustment requires coordination between changing ion
concentrations and altering organic osmolyte levels
(Hasegawa et al., 2000). The initial hyperosmotic
response for most plants is to increase ion levels within
the cells until osmotic equilibrium is achieved. Once
steady state is reached, these plants will slowly replace
the metabolically disruptive ions with compatible solutes
(Kirst, 1989; Murphy et al., 2003). In R. maritima,
changes in ion content occur rapidly under hyperosmotic
conditions, however any further osmotic adjustment,
likely associated with the production of compatible
solutes such as proline, required an additional two days
(Berns, 2003; Murphy et al., 2003). Similarly, studies
with Poisodonia australis revealed rapid changes (within
hours) in osmolality with rising salinities, albeit the
osmotic adjustment was considerably slower or absent at
physiologically extreme salinities (Tyerman et al., 1984).
It is likely that seagrasses growing within their optimal
salinity range can achieve equilibrium fairly rapidly.
However plants exposed to waters outside their typical
204
salinity distribution, but within their tolerance range, may

require additional time (days to weeks) to acclimate
(Tyerman et al., 1984; Berns, 2003).
In response to salinity change, many plants will
accumulate or breakdown low-molecular-weight organic
solutes to achieve long-term osmotic adjustment. Prominent organic osmolytes in seagrasses include organic
acids, soluble carbohydrates, and free amino acids
(Touchette and Burkholder, 2000b; Touchette and
Burkholder, 2002; Ye and Zhao, 2003). In Z. marina
and R. maritima, for example, sucrose and proline appear
to be the principle organic osmotica (Murphy et al., 2003;
Ye and Zhao, 2003). In the brackish charophyte, Lamprothamnium succinctum, sucrose levels in the cytoplasm
increased linearly with increased salinity (Okazaki et al.,
1987). However, there are many organic compounds in
plants with osmolyte functions including simple sugars
(fructose and sucrose), sugar alcohols (glycerol, mannitol, and sorbitol), complex sugars (fructans, raffinose, and
trehalose), and charged organic metabolites (ectoine,
glycine betaine, and proline; Fig. 5). Different organic
osmolytes have been found to co-occur as plants undergo
osmotic adjustment, and these compounds may represent
as much as 75% of the change in tissue osmolality
(Brown and Hellebust, 1978).
While the production of organic osmolytes can require
substantial energy expenditures, the expense is offset by
their secondary role as compatible solutes. High
concentrations of ions (N 100 mM) inhibit the activity
of enzymes (Davison and Reed, 1985; Richter and Kirst,
1987), whereas high concentrations of compatible solutes
not only minimally inhibit enzyme activity but also help
stabilize macromolecules (Yancey et al., 1982; Kirst,
1989). The hydrophilic nature of most compatible solutes
Fig. 5. Common organic osmolytes involved in osmotic adjustment and/or osmotic protection in plants. These compounds have been observed to
accumulate in seagrasses and other halophytes during osmotic stress (adapted from Hasegawa et al., 2000).
205
allows them to replace water at the surface of proteins and

membranes and thus serve as osmoprotectants and lowmolecular-weight chaperones (Hasegawa et al., 2000).
Osmoprotectant properties of compatible solutes include
reduced inhibitory effects of ions on enzymes, increased
thermal stability of enzymes, and limited dissociation of
enzyme complexes (including the oxygen-evolving
complex of photosystem II; Brown, 1990; Galinski,
1993; Solomon et al., 1994; Papageorgiou and Murata,
1995). Relatively small increases in glycine betaine
protect thylakoids and plasma membranes against
temperature destabilization (Jolivet et al., 1982; Zhao
et al., 1992). Nevertheless, the protective properties of
organic osmolytes may vary considerably. For example,
proline and glycerol are highly effective compatible
solutes, whereas sucrose is more limited (Kirst, 1989).
6. Cell wall elasticity ( )
In response to sudden changes in environmental
salinity, cells may undergo rapid alterations in turgor
pressure (increase or decrease) due to substantial water
fluxes in the direction of the osmotic gradient. The rate of
water movement into or out of plant cells depends greatly
on the hydraulic conductivity of the cell membrane as
well as the elastic properties of the cell wall. Cell wall
elasticity, or bulk elastic modulus (), considers the
change in pressure (for turgid cells) following a change in
cell volume. The ability of a plant cell to change its
volume is determined by its overall water capacity, which
is dependent on wall elasticity, intracellular osmotic
pressure, and cell size (or volume; Tyerman, 1982). The
value of can be helpful in understanding plant cell
responses to changing water potentials. Two primary
methods have been developed to determine elastic
properties. The pressure-probe technique (commonly
used on algae) measures the instantaneous change in
turgor pressure following a change in cell volume, and is
referred to as the instantaneous (i). The other
technique measures stationary (s) by evaluating
water potential changes at different cell volumes using
either a Scholander pressure chamber or linear displacement transducers (Fig. 6). The latter procedure requires
water potential to reach steady-state (stationary) prior to
measurement. Because the techniques to determine are
quite different, some caution should be used when
making comparisons between s and i, as s is often
considerably lower than i (Tyerman, 1982).
The elasticity of cell walls varies greatly among plant
species (from 0.06 MPa in Halicystis parvula to 70 MPa
in Chara corrallina), or within the same species at
different developmental stages or dissimilar environmen-
Fig. 6. Pressure-volume isotherm (upper panel) and Hfler diagram

(lower panel) illustrating change in water potential ( ) with change
in cell volume for Halodule wrightii. The elevated vertical slope
(on the right side of the figure) on the pressure-volume isotherm
represents the change in cell volume during turgid conditions and thus
can be used to estimate the elasticity of cell walls (s; see text for
further description). The lower slope (on the left side of the figure)
represents flaccid conditions where the cells have become plasmalyzed. The Hfler diagram illustrates decreased turgor pressure (P;
gray circles) as cell volume is reduced. Furthermore, as water is lost
from the tissues, the osmotic potential (s; open circles) and water
potential (; black circles) are expected to decline due to the
increased confinement of solutes with in the cells. To generate this
data, leaf tissues were exposed to air for drying which is atypical for
most seagrasses with underdeveloped xylem tissue. Therefore this
figure is used only for illustrative purposes and values produced using
this technique (e.g. s at full saturation, s at turgor loss point, and
symplastic water fraction) may not be as accurate as those generated
for terrestrial species.
tal conditions (Dainty et al., 1974; Graves and Gutknecht,

1976; Tyerman, 1982; Touchette, 2006; Touchette et al.,
2007). Plants with relatively low (i.e. flexible cell
walls) are more tolerant to short-term fluctuations in
salinity, as cell walls can expand or contract until they
achieve osmotic equilibrium with their environment
206
(Fig. 7). Lower is particularly useful during hyperosmotic conditions by decreasing the likelihood of
plasmolysis during water efflux. In estuarine macroalgae,
osmotic adjustment is often achieved by changing cell
volume and osmolyte concentrations (Kirst, 1989). These
algae have thin cell walls that can expand or shrink as
necessary, thus allowing them to tolerate sudden changes
in salinity typical of estuarine systems. In shoal-grass,
H. wrightii, flexible cell walls may also contribute to
cellular water changes in response to salinity stress. That
is, cell volume (as indicated by a rapid change in plant
mass) can increase or decrease by as much as 20% when
salinity is abruptly changed by 15 psu (plants acclimated
to 25 psu and introduced to 10 or 40 psu; Fig. 8). Furthermore, pressure-volume analysis on H. wrightii collected from a euryhaline estuary also revealed a relatively
low s at 0.3 MPa (Touchette, unpublished data).
In contrast, plants with higher (more rigid cell
walls) must respond quickly to changes in salinity as
even small fluctuations in cell volume will result in
substantial changes in turgor pressure. During hypoosmotic stress, a higher will have minimal water influx
Fig. 8. Change in mass of Halodule wrightii with change in

environmental salinity. To construct this figure leaves from plants
(n = 5) acclimated to 25 psu (6 weeks in greenhouse microcosms) were
place in different salinities (from 10 to 40 psu) for 12 h in the dark at
4 C (to minimize energy dependent osmotic adjustments). The change
in mass represents the increase or decrease in water following a change
in salinity. Data is presented as mean 1 SE (adapted from Salisbury
and Ross 1992).
Fig. 7. Initial cell-water relations (prior to osmotic adjustment) to changing environmental osmotic conditions (hyperosmotic [upper two panels] and
hypoosmotic [lower two panels]) as influenced by cell wall rigidity (elastic modulus; ). Lower cells (left two panels) have greater wall flexibilities
that can maintain positive turgor pressure (within limits) during changing osmotic environments. Higher cells (right two panels) have rigid cell
walls that may cause plasmolysis during hyperosmotic environments, but maintain solute concentrations during hypoosmotic conditions.
with limited cell expansion. Plants occupying more stable

saline environments (such as open coastal areas) would
be expected to have thicker cell walls with relatively high
values (Kirst, 1989). In seagrasses, maximum i
values for Halophila ovalis, Posidonia australis, and
Zostera capricorni were 22, 51, and 17 MPa, respectively
(Tyerman, 1982). These values are among the highest
observed in vascular plants and indicate that these species
have relatively inflexible cell walls. These high values are
particularly surprising in H. ovalis, as this plant has a
wide salinity tolerance between 5 and 45 psu (Tyerman,
1982; Ralph, 1998). Clearly mechanisms beyond are
involved in osmotic adjustments in these plants, and
more studies are needed in determining the role of in
achieving short-term osmotic equilibrium in seagrasses.
7. Salinity influences on photosynthesis and
respiration
Photosynthesis and respiration are often inhibited in
aquatic plants exposed to extreme hypo- or hyperosmotic
conditions, with the degree of inhibition largely dependent upon the acclimation period allowed for the plant. In
marine algae, for example, complete recovery of photosynthesis can be achieved within minutes (most microalgae) to hours (most macroalgae; Gessner and Schramm,
1971; Kirst, 1989). The slower recovery by macrophytes
is attributed to their lower cytoplasmic-to-vacuolar ratios,
preventing them from quickly responding metabolically
to changes in osmotic potential (Kirst, 1989). While
increased salt stress can cause declines in chlorophyll
content (Baek et al., 2005; Karimi et al., 2005), other
inhibitory processes are also involved including inhibition of electron flow, decreased photosystem function,
diminished rubisco abundance and activity, and changes
in chloroplast ultrastructure, (Kirst, 1989; Ziska et al.,
1990; Stoynova-Bakalova and Toncheva-Panova, 2004).
Studies on salinity-induced photosynthetic depressions in macroalgae suggest inhibition of both photosystem I and II following an increase in permeability of ions
(principally Na+ and Cl) across the thylakoid membrane
(Gilmour et al., 1982; Gilmour et al., 1985; Xia et al.,
2004). Satoh et al. (1983) observed inhibition of at least
three sites within the photosynthetic apparatus of a red
alga (Porphyra perforate) following exposure to hypersaline conditions, including: (i) the loss of photoactivated
electron flow on the reducing side of photosystem I,
(ii) the inhibition of electron flow on the water side of
photosystem II, and (iii) the disruption of resonance
energy transfer between pigment complexes within each
photosystem. However, Yang et al. (2006) noted that
while inhibition of photosynthesis was observed in
207
photosystem II (as indicated by a decline in maximal

photochemical efficiency; Fv/Fm) in soybeans (Glycine
maxcultivar Melrose), only nominal photosystem II
inhibitions were detected in a salt-resistant relative
(Glycine cyrtoloba ACC547).
Salinity stress can alter photosynthetic capacities in
seagrasses (Biebl and McRoy, 1971; Kerr and Strother,
1985; Dawes et al., 1989; Ralph, 1998; Murphy et al.,
2003; Torquemada et al., 2005). In Halophila johnsonii,
for example, photosynthetic efficiencies at subsaturation
light () and maximum photosynthetic rate (Pmax) are
highest at 40 psu (study range was 0 to 60 psu) and
lowest at 0 psu (Torquemada et al., 2005). However, in
Zostera muelleri, photosynthetic rates during 2 h of
hypersalinity (up to 140 psu) were fairly similar to
controls (full strength seawater; Kerr and Strother, 1985).
Ralph (1998) reported greater stress in H. ovalis during
hyperosmotic exposure in comparison to hypoosmotic
conditions. During hyperosmotic conditions, H. ovalis
was able to maintain typical Fv/Fm and quantum yield
() over the first 5 h, however as the stress duration
continued these photosynthetic parameters declined
markedly. It was suggested that the decline in photochemical efficiency could be attributed to ion imbalances
(with Na+ and Cl influx and K+ deficiencies), and
membrane destabilization (Ralph, 1998). Similarly,
declines in minimum fluorescence (Fo) was also observed after 48 h of exposure to hypersaline conditions,
indicating possible damage to PSII reaction centers
(Franklin et al., 1992; Ralph, 1998).
Diminished photosynthesis in seagrasses under hyposaline conditions have also been observed in H. ovalis
and Z. muelleri (Kerr and Strother, 1985; Ralph, 1998).
This decline in photosynthetic activity at lower salinities
may be attributed to a decline in cellular ion content,
including necessary ions involved as photosynthetic
cofactors (Simon et al., 1999). In Z. muelleri, photosynthesis began to decline at 25 psu (after a two hr
incubation), and no O2 liberation was observed at 0 psu
(Kerr and Strother, 1985). In H. ovalis, a decline in
maximum fluorescence (Fm), which is linked to inhibition of photosynthesis, was reported after 24 to 48 h of
exposure to freshwater (Ralph, 1998). Furthermore a
hyposaline-induced (9 to 18 psu) decrease in was also
observed in H. ovalis, indicating a disruption of
photosystem II (Ralph, 1998). It is possible that cyclic
electron flow around photosystem I during salinity stress
may assist in the dissipation of excess excitation energy
when coupled with high-energy state nonphotochemical
quenching (qE; Yang et al., 2006).
The elimination of electron flow between and within
photosystems may be an important mechanism for
208
avoiding photodamage caused by the accumulation of

free radicals (Satoh et al., 1983; Kirst, 1989). That is,
salinity-induced inhibitions of photosynthesis may result
in the accumulation of excess energy that can ultimately
damage the photosynthetic apparatus (Demmig-Adams
et al., 1996; Yang et al., 2006). This energy, if not safely
dissipated, can lead to the production of reactive oxygen
species (ROS; e.g., O2, OH, H2O2) that can diminish
photosynthesis by oxidizing membranes, photosynthetic
pigments, and important metabolic enzymes (Yang et al.,
2006). Not surprisingly, many higher plants can enhance
their ability to scavenge ROS during salinity stress by
increasing antioxidants (e.g., xanthophylls) and the
activities of antioxidant enzymes (e.g., catalase, peroxidase, and superoxide dismutase; Ghorbanli et al., 2004;
Rahnama and Ebrahimzadeh, 2005; Lu et al., 2006). For
example, dissipation of excess light energy during salt
stress in Ulva fasciata Delile may involve superoxide
dismutase and catalase (Lu et al., 2006). In some
halophytes, including Thalassia testudinum, the quenching of surplus energy by non-radiative mechanisms
(i.e., non-fluorescence) could also occur through the
accumulation of xanthophylls (Mohanty and Yamamoto,
1995; Qiu et al., 2003; Thorhaug et al., 2006).
Respiratory responses toward changing salinities are
not as consistent as photosynthetic responses (Biebl and
McRoy, 1971; Kerr and Strother, 1985; Dawes et al.,
1989; Ralph, 1998; Berns, 2003; Kahn and Durako,
2006). In Z. marina, only extreme hypersaline conditions
(i.e., 93 psu) resulted in significant increases in cellular
respiration, however respiration in distilled water was
well below normal (ca. 0.25, compared to the more
typical 1.5 relative units O2 h 1 g 1 dry wt; Biebl and
McRoy, 1971). In Z. muelleri no significant changes in
respiration were observed during a 2 h incubation that
included extreme salinities (range 0 to 140 psu; Kerr and
Strother, 1985), and in H. johnsonii, both hypersaline
(50 psu) and hyposaline (5 and 15 psu) conditions
resulted in markedly lower respiration rates relative to
salinities more comparable to full-strength seawater (30
to 35 psu; Dawes et al., 1987; Torquemada et al., 2005).
8. Salinity and carbon metabolism
While hypo- and hypersaline conditions can often
depress carbon fixation in seagrasses, modifications in
carbohydrate catabolism and metabolism would be
necessary to allow for the accumulation or degradation
of organic solutes. A number of organic compounds can
be produced in response to saline stress, with most of
them having similar osmotic potentials (between 2.5 to
2.8 MPa M 1; Kirst, 1989). Nevertheless, the synthesis
of these organic solutes differs greatly in energy costs,

and carbon and nitrogen requirements (Kirst, 1989), and
the stabilizing properties of these compounds towards
macromolecules and ribosomes varies considerably
(Yancey et al., 1982; Brady et al., 1984). In Z. marina,
the primary organic osmotica include dissolved sugars
(mostly sucrose) and free amino acids (primarily proline;
Ye and Zhao, 2003). While the cellular concentration of
sugars and free amino acids appear to be small in
comparison to inorganic osmotica, the localization of
these organic compounds within the relatively confined
cytoplasmic space (ca. 10% of the total cell volume)
maybe enough to achieve osmotic equilibrium (Ye and
Zhao, 2003).
The compositions of organic solutes in seagrasses
have strong seasonal tendencies (Dawes and Lawrence,
1980; Brock, 1981; Lazar and Dawes, 1991; Touchette
and Burkholder, 2002). For example soluble carbohydrates often accumulate just prior to seasonal plant dieback (Lazar and Dawes, 1991). Nevertheless, variations
in amino acids and carbohydrates can be observed over
much smaller scales (Brock, 1981; Touchette and
Burkholder, 2002; Murphy et al., 2003). In R. maritima,
for example, noticeable changes in proline content
occurred within 2 days of osmotic stress including
declines in proline content for plants exposed to hyposaline conditions (Murphy et al., 2003). Brock (1981)
estimated that proline concentrations in the cytosol of
Ruppia spp. could account for as much as 50% of
the cytoplasmic osmotic potential. Proline content in
Z. marina was also elevated at higher salinities (Van
Diggelen et al., 1987). While increased production of
proline could promote internal nitrogen deficiencies
(Cavalieri and Huang, 1981; Cavalieri, 1983), the amount
of proline accumulated in Z. marina accounted for less
than 3.0% of the total plant nitrogen and likely did not
impose any internal nitrogen deficiencies (Van Diggelen
et al., 1987).
In R. maritima, total soluble carbohydrate content
appeared to decrease with increasing salinities. This
decline in carbohydrates could be associated with
conversions of these compounds towards more soluble
forms of organic compounds that would better facilitate
osmotic adjustment (Murphy et al., 2003). In Z. marina,
no significant differences in sucrose content were
observed in above- or belowground tissues in plants
exposed to three different salinities (30, 35, and 40 psu)
over two weeks (Table 3). However there were significant
decreases in sucrose-P synthase (SPS) activities in leaf
tissues in the higher salinity treatments (Table 3). SPS is
an important enzyme involved in the control of sucrose
synthesis with higher activities enhancing sucrose
209
Table 3
Salinity and light responses on above-and belowground sucrose levels (Suc; mg g 1 FW), sucrose-P synthase activity in aboveground tissue (SPS; mg
g 1 FW min 1), and sucrose synthase activity in belowground tissues (SS; mg g 1 FW min 1) of Zostera marina
Treatment
Aboveground tissue
Light30 psu
35 psu
40 psu
Dark30 psu
35 psu
40 psu
Belowground tissue
Light30 psu
35 psu
40 psu
Dark30 psu
35 psu
40 psu
Suc. (day-1)
Suc. (day-7)
Suc. (day-14)
SS or SPS (day-1)
SS or SPS (day-7)
SS or SPS (day-14)
40.0 13.8
46.7 1.1
38.5 4.2
46.5 7.6
62.1 13.0
32.6 0.9
82.7 11.3
61.4 18.0
50.1 1.5
0.77 0.21S
0.52 0.08S
0.18 0.10S
0.81 0.19S
0.35 0.03S
0.29 0.05S
1.48 0.31SL
0.54 0.12S
0.21 0.15S
50.9 21.9
32.3 9.6
30.2 4.8
27.4 4.9
36.2 7.4
43.7 12.3
38.8 8.3
44.9 13.6
60.7 15.6
0.71 0.35S
0.42 0.20S
0.28 0.20S
0.79 0.28S
0.44 0.07S
0.27 0.12S
0.43 0.25
0.37 0.23
0.10 0.08
268 81.1
313 47.5
281 82.3
238 29.4
273 131
206 44.8
279 104
252 40.2
196 32.2
1.11 0.21
0.99 0.63
0.54 0.15
0.57 0.18
1.39 1.10
0.70 0.49
0.96 0.41
1.21 0.26
0.86 0.11
272 12.4
233 25.3
200 20.9
112 13.7L
132 16.5
186 15.8
133 10.4L
139 15.1L
160 2.7L
0.79 0.20
0.63 0.08
1.00 0.51
0.58 0.21
0.66 0.11
0.86 0.29
0.59 0.21
0.34 0.20L
0.61 0.39
Aquaria experiments were conducted on Z. marina over a two-week time course with three salinity levels (30, 35, and 40 psu). Plants were either
exposed to light (250 14 E m 2 s 1; 12L:12D cycle) or complete darkness during the 14 day period. Data are presented as means 1 SE. Significant
differences (GLM, ANOVA; n = 3) are indicated by L (light effects) and/or S (salinity effects).
production (Huber and Huber, 1996). This decrease in

SPS activity was observed in as little as 24-hours of
hypersaline conditions, and continued over the next twoweeks. It is possible, as with R. maritima, that sucrose
production is being suppressed to allow for the accumulation of other, more effective, compatible solutes (e.g.,
proline). Unlike SPS activities which decreased with
increased salinities, sucrose synthase (SS; key enzyme
involved in the degradation of sucrose) activities in
belowground tissues of Z. marina did not respond to any
salinity change (Table 3). Nevertheless in mesocosm
experiments, SS activities in belowground tissues of Z.
marina were positively correlated with salinity, but only
when nitrate was pulsed into the water column (Touchette,
1999). This nitrogen-salinity response with SS activities
in belowground tissues may reflect the importance of
carbon skeletons for the synthesis and accumulation of
proline (and other nitrogen containing osmotica such as
glycine betaine or ectoine) during elevated salinities
(Touchette, 1999).
9. Salinity and plant nutrition
In plants, NO3 uptake across the plasma membrane is
believed to be driven by electrochemical gradients
(Ullrich, 1992; Garca-Snchez et al., 2000; Rubio
et al., 2005). Evidence for this includes concurrent
NO3 and H+ fluxes (Mistrik and Ullrich, 1996), NO3
induced depolarization of membranes (McClure et al.,

1990; Glass et al., 1992), and pH dependent NO3 influx
(Meharg and Blatt, 1995). The plasma membrane
potential (Em) of Z. marina is approximately 160 mV
in full-strength seawater, which is likely maintained by
H+-pumps (Fukuhara et al., 1996; Fernndez et al.,
1999). This highly negative Em can adversely affect the
uptake of essential anions in marine macrophytes
(Garca-Snchez et al., 2000; Rubio et al., 2005). As
mentioned, for many plants, anion uptake is coupled with
H+ influx (Ullrich, 1992; Garca-Snchez et al., 2000).
However for plants residing in seawater, the inwardlydirected electrochemical potential difference created by
Na+ could allow for anionic coupling (Rees et al., 1980;
Garca-Snchez et al., 2000).
Z. marina has a high-affinity Na+-dependent NO3
transport system (Garca-Snchez et al., 2000). This
allows the seagrass to take advantage of the inwardly
driving force for Na + (generated by high saline
environments), stoichiometry yielding as much as one
NO3 for every two Na+ ions (Garca-Snchez et al.,
2000). The key enzyme involved in NO3 reduction/
assimilation, nitrate reductase (NR), also has elevated
activities at higher salinities in Z. marina (salinity range
29 to 37 psu; Touchette and Bukholder, 2001). Nitrate
reductase is up-regulated during periods of increased
NO3 concentrations. It possible that higher salinities
could enhance the uptake of NO3 through a Na+-
210
dependent NO3 transport system resulting in greater

cellular NO3 levels. These Na+-driven higher NO3 levels
could promote increased NR activities within the leaf.
Nevertheless, it is important to note that these studies
were made within the salinity tolerance for this plant, and
how NO3 transport and reduction would change during
extreme hypo-and hypersaline conditions is unknown.
As with NO3, inorganic phosphate (Pi; as H2PO4 and
HPO4 2) uptake may also involve a Na+-dependent
transport system in seagrasses. While most vascular
plants rely on H+ to create an electrochemical potential
across the plasma membrane and thus facilitate H+/Pi cotransport (Schachtman et al., 1998; Rausch and Bucher,
2002), seagrasses (and perhaps upland halophytes and
marine algae) can, again, take advantage of the inwardly
directed electrochemical potential difference for Na+
generated by their presence in seawater (Rubio et al.,
2005). The stoichiometry values for Na+-dependent
phosphate transport in Z. marina are one H2PO4 for
every two Na+ and one HPO4 2 for every three Na+
(Rubio et al., 2005), whereas the strict reliance on H+
gradients are thermodynamically insufficient (HPO4 2) or
infeasible (H2PO4; Rubio et al., 2005).
Enzymes involved in scavenging and recycling of
cellular and extracellular P, acid- and alkaline phosphomonoesterases, have higher activities in Z. marina during
periods of elevated salinities (Touchette and Burkholder,
2007). Phosphomonoesterases (PAs; often referred to as
phosphatases) are important in a number of cellular
processes including: (i) material transport across membranes, (ii) synthesis of P-containing compounds,
(iii) formation of cell walls and cell wall lignification,
and (iv) the synthesis of carbohydrates (Georgieva, 1980;
Basra et al., 1989; Thaker et al., 1996; Touchette and
Burkholder, 2007). Because of the importance of Pi in
carbohydrate synthesis and mobilization, elevated PA
activities have been observed in plants when carbon
metabolism was enhanced (e.g., fruit development, seed
germination, cell wall thickening, and starch mobilization
to glucose and fructose; Chitarra and Lajolo, 1981; Basra
et al., 1989; Thaker et al., 1996; Touchette and
Burkholder, 2007). It is possible that the increased PA
activity observed in Z. marina at higher salinities is
indicative of enhanced carbohydrate mobilization and
metabolism directed towards the production of more
effective organic osmotica (Touchette and Burkholder,
2007).
10. Future research directions
Adaptations by seagrasses to tolerate and even flourish
in high-saline habitats have undoubtedly altered many
physiological processes in these plants. In comparison to

the wealth of information concerning terrestrial (especially agriculturally important) plants, little is known about
salt tolerance in seagrasses. This is unfortunate as many
fundamental aspects of salt tolerance in seagrasses remain unresolved (Touchette and Burkholder, 2000b).
While it is possible that seagrasses in estuarine environments are more tolerant to rapid salinity changes than
those in near-shore coastal areas, this premise is largely
based on studies involving algae and not submersed
vascular plants (Kirst, 1989). Further studies comparing
salinity responses in strictly estuarine species with those
of more coastal species would provide a better understanding on how environmental salinity influences
species distributions. This would also provide valuable
information for seagrass restoration projects, especially in
areas where seagrass die-off is directly linked to altered
water systems (creating hyper- or hyposaline conditions)
caused by human activities. It would also be helpful to
understand how tolerant individual plants are to osmotic
challenges. For example, could a plant that was
acclimated over a long-period of time to a narrow salinity
range survive a salt challenge as well as a plant that has
been living in a more dynamic saline environment?
The role of ionic and organic osmolytes and their
distributions in seagrasses is not well understood. It would
appear that K+ and Na+ are important in maintaining
osmotic equilibrium; however seagrasses seem to accumulate fewer ions than marine algae. This discrepancy in
ion levels in seagrass tissues could be influenced by
differences in cytoplasm-to-vacuole ratios, greater reliance on organic solutes, and/or the presence of highly
selective ion channels and transporters. Unfortunately the
relationship between vacuole size and salt tolerance is
poorly understood in these plants. Comparative studies on
the importance of vacuole size in salt tolerance could help
our understanding of seagrass-salinity interactions.
Only a small number of experiments have been conducted to address the accumulation and control of ionic
and organic osmotica in seagrasses, including more recent
studies on Na+ and K+ transport systems. Consequently,
our understanding of how these plants maintain proper ion
levels is still incomplete. Are different transporters
activated or inactivated to achieve osmotic homeostasis
as environmental salinity changes? Some recent evidence
suggests that multiple ATPase transporters maybe
involved in K+ and Na+ flux in higher plants (Mahajan
and Tuteja, 2005), however such studies are lacking in
seagrasses. Clearly proline and sucrose are important
organic osmolytes in seagrasses, however limited studies
have been conducted to address the protective properties
of other organic compounds.
Finally, the flexibility of cell walls can strongly influence how these plants respond to sudden changes in
salinity. Unfortunately studies on cell wall elasticities are
limited to a few species. Many plants can modify in
response to changing osmotic stress (e.g., Dainty et al.,
1974; Graves and Gutknecht, 1976; Touchette, 2006),
however only a few studies have been conducted on these
ecologically valuable marine angiosperms. The importance of in short-term osmotic adjustment in these
plants needs to be examined further.
Acknowledgements
Support for this synthesis of salinity-seagrasses
interactions, and research that strengthened these connections, was provided by Elon University Center for
Environmental Studies, Elon College of Arts and
Sciences, UNC Water Resources Research Institute, US
Geological Survey, North Carolina State University
Center for Applied Aquatic Ecology (CAAE), and
North Carolina Sate University Department of Plant
Biology. I am grateful to J. MacFall (Elon University) and
J.M. Burkholder (CAAE) for providing laboratory space
and equipment necessary to conduct research presented
here. A. Hamilton and E. Allen (N.C. State University),
and G. Turner (Elon University) provided research assistance for new data introduced in this paper. [SS]
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Journal of Experimental Marine Biology and Ecology 350 (2007) 194 215

Seagrass-salinity interactions: Physiological mechanisms

Tel.: +1 336 278 6185; fax: +1 336 278 6258.

between 30 and 40 psu, although a few species have

Salinity preference (psu)

Salinities tested (psu)

Dawes et al. (1987)

Walker and McComb (1990)

different ions will remain constant during dehydration but

3. Ion flux and ion balance

Malea and Haritonidis (1995)

0.0 mmol/dm3 NaCl

Ruby et al. (2000)

et al., 2004). Unfortunately, halophytes apparently lack

indicated by a mean Na+:K+ molar ratio of 18.7 (albeit

Fig. 3. Tissue Na+ and K+ levels observed in seagrasses (black circles),

pyrophosphatases, Ca 2+ -ATPases, secondary active

2002; Fig. 4). While undoubtedly Na+ participates in an

outside the cell or into a vacuole) may be accomplished

of membrane invagination observed in seagrasses would

found in leaves and roots relative to shoots (Ye and Zhao,

The principal ions involved in osmotic adjustment are

salinity distribution, but within their tolerance range, may

allows them to replace water at the surface of proteins and

Fig. 6. Pressure-volume isotherm (upper panel) and Hfler diagram

tal conditions (Dainty et al., 1974; Graves and Gutknecht,

Fig. 8. Change in mass of Halodule wrightii with change in

with limited cell expansion. Plants occupying more stable

photosystem II (as indicated by a decline in maximal

avoiding photodamage caused by the accumulation of

of these organic solutes differs greatly in energy costs,

production (Huber and Huber, 1996). This decrease in

induced depolarization of membranes (McClure et al.,

dependent NO3 transport system resulting in greater

physiological processes in these plants. In comparison to

Biebl, R., McRoy, C.P., 1971. Plasmatic resistance of respiration and

Dawes, C.J., Lobban, C.S., Tomasko, D.A., 1989. A comparison of the

(Gramineae), and environmental factors affecting its growth and

Murphy, L.R., Kinsey, S.T., Durako, M.J., 2003. Physiological effects of

Rubio, L., Linares-Rueda, A., Garca-Snchez, M.J., Fernndez,

Touchette, B.W., Burkholder, J.M., 2000a. Review of nitrogen and

Zieman, J.C., 1975. Seasonal variation of turtle grass, Thalassia

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