• chloride;
  • compatible solutes;
  • halophyte;
  • ion transport;
  • osmotic adjustment;
  • potassium;
  • salt and stress tolerance;
  • sodium


  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information


  • Summary 945

  • I.
    Introduction 946
  • II.
    Growth and osmotic adjustment 946
  • III.
    Uptake and transport of monovalent ions 950
  • IV.
    Conclusions and perspectives 956
  • Acknowledgements 957

  • References 959

I. Introduction

  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information

Halophytes are remarkable plants that tolerate salt concentrations that kill 99% of other species. However, although halophytes have been recognized for hundreds of years, their definition remains equivocal. We base our definition on an ability ‘to complete the life cycle in a salt concentration of at least 200 mm NaCl under conditions similar to those that might be encountered in the natural environment’ (Flowers et al., 1986). Adopting a definition based on completion of the life cycle should allow separation of what might be called ‘natural halophytes’ from plants that tolerate salt but do not normally live in saline conditions (see Breckle (2002) for a further discussion of the classification of halophytes).

Other classifications of halophytes have been suggested that are based on the characteristics of naturally saline habitats (Waisel, 1972; Le Houérou, 1993) or the chemical composition of the shoots (‘physiotypes’; Albert & Kinzel, 1973; Albert et al., 2000) or the ability to secrete ions (recreto-halophytes, Breckle, 1986, 2002). However, although saline habitats do differ in many regards (e.g. soil water content) and differences do exist amongst species in the balance of Na+ and K+ in shoot tissues (Wang et al. 2002; see Section III.2, ‘Uptake and accumulation of K+ and its selectivity over Na+’), we have not, at this stage, embraced the suggested subdivisions of halophytes, as the underlying mechanisms remain unclear (salt glands excepted).

The general physiology of halophytes has been reviewed occasionally (Flowers et al., 1977, 1986; Flowers, 1985) and since then other reviews have examined their ecophysiology (Ball, 1988; Rozema, 1991; Ungar, 1991; Le Houérou, 1993; Breckle, 2002), photosynthesis (Lovelock & Ball, 2002), response to oxidative stress (Jithesh et al., 2006) and flooding tolerance (Colmer & Flowers, 2008) as well as the physiology of seagrasses (Touchette, 2007). The potential of halophytes as donors of tolerance for cereals (Colmer et al., 2005, 2006) and as crops in their own right has also been reviewed (Glenn et al., 1999; Colmer et al., 2005), as have the effects of salinity on plants in general (Hasegawa et al., 2000; Zhu, 2001; Munns, 2002, 2005; Chinnusamy & Zhu, 2003; Sairam & Tyagi, 2004; Bartels & Sunkar, 2005; Chinnusamy et al., 2005; Munns & Tester, 2008). In the following pages, we discuss (Section II, ‘Growth and osmotic adjustment’) the basic physiology of salinity tolerance in halophytes – growth, osmotic adjustment, ion compartmentation and compatible solutes; limitations of space have precluded a review of transpiration in halophytes and of salt glands. We continue with what is known of the uptake and transport of monovalent ions (Section III, ‘Uptake and transport of monovalent ions’), the crux of being salt-tolerant, and conclude (Section IV.2, ‘Use of model species to enhance future research’) with the suggestion that research should be concentrated on a limited number of species, representative of the main taxonomic groups of halophytes, to provide ‘models’ to develop detailed understanding of the molecular and physiological bases of salinity tolerance in halophytes.

II. Growth and osmotic adjustment

  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information

1. Growth

Although our definition of a halophyte involves growth and survival under saline conditions, the effect of salinity on growth varies amongst halophytes (Fig. 1). Many, but not all, dicotyledonous halophytes show optimal growth in concentrations of 50–250 mm NaCl (Flowers et al., 1986), while monocotyledonous halophytes generally grow optimally in the absence of salt or, if growth is stimulated, this is by a low (50 mm or less) concentration of NaCl (Glenn, 1987; Glenn et al., 1999). Changes in the amount of water per unit dry mass can make a large contribution to changes in the fresh biomass of halophytes grown at different salinities and massive ion accumulation can also occur, particularly in succulent dicotyledonous species, where ‘ash’ content can represent almost half the shoot dry mass. Organic dry mass is stimulated by growth in saline conditions in at least some dicotyledonous halophytes (Yeo & Flowers, 1980; Glenn & O’Leary, 1984), although the stimulation is less dramatic than is seen for fresh or dry mass. The observation that dry mass of dicotyledonous halophytes increases at moderate salinity calls into question the appropriateness of a ‘control’ being growth in the absence of salinity; suboptimal salt solutions might formally be described as deficient (Yeo & Flowers, 1980).


Figure 1. Effect of increasing salinity on the growth (relative to that in the absence of, or very low, NaCl) on shoot dry mass of a range of halophytes. The length of exposure to salt is given in parentheses. Solid lines, dicotyledonous species; broken lines, monocotyledonous species. Diamonds, Suaeda maritima (35 d; Yeo & Flowers, 1980); squares, Thellungiella halophila (14 d; M’Rah et al., 2007); triangles, Disphyme australe (60 d; Neales & Sharkey, 1981); stars, Puccinellia peisonis (42 d; Stelzer & Läuchli, 1977); circles, Distichlis spicata (21 d; Parrondo et al., 1978).

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Relative growth rates for dicotyledonous halophytes in 200–360 mm NaCl range, on a dry mass basis, between 6 and 160 mg g−1 d−1, and, for monocotyledonous halophytes, between 15 and 26 mg g−1 d−1 (Rozema & van Diggelen, 1991; Wickens & Cheeseman, 1991; Nerd & Pasternak, 1992; Ayala & O’Leary, 1995; Khan et al., 1999; Harrouni et al., 2003; Debez et al., 2006); in terms of ash-free dry mass, relative growth rates of 10 species of dicotyledonous halophytes lay between 31 and 70 mg g−1 d−1 (Glenn & O’Leary, 1984). Growth rates of the dicotyledonous halophytes can match those of glycophytes with annual dry matter production obtained from field experiments on saline soils of between 0.08 and 18 t ha−1 yr−1 (O’Leary et al., 1985): these higher-end rates are, as discussed by Glenn et al. (1999), comparable with the biomass production of conventional forage crops. Even if perhaps a third to half of the dry mass is inorganic matter (i.e. ash), the data indicate that dicotyledonous halophytes are able to grow at similar rates to glycophytes even though they use energy in the accumulation and compartmentalization of the ions required for osmotic adjustment (Yeo, 1983). Unlike the situation of xerophytes, which survive drought with very low growth rates, making them unsuitable as crops, halophytes can grow rapidly in saline conditions.

Why growth should decline at supra-optimal salinities is not known, although there are a number of possibilities. As examples, reduced C fixation could be responsible, as could changes in biomass allocation between leaf, stem and root, which would alter the balance of photosynthesis and respiration (Ball, 1988; Lovelock & Ball, 2002). Another possibility is a change in growth as a result of a fall in turgor (Clipson et al., 1985; Rozema, 1991; Balnokin et al., 2005), consequent upon high concentrations of ions in the apoplast (Harvey et al., 1981; James et al., 2006), or a change in cell wall elasticity (Tomos & Wyn Jones, 1982; Touchette, 2006). Other possibilities relate to osmotic adjustment: perhaps an inability to accumulate and/or distribute sufficient nutrients or synthesize sufficient organic solutes, the futile cycling of ions (Britto & Kronzucker, 2006) or the energetic demands of ion compartmentation per se (Yeo, 1983).

The energetic demands of processes essential to salt tolerance in halophytes might be substantial (Yeo, 1983); energy would be consumed in ion transport to regulate net uptake and cellular compartmentation of Na+ and Cl, as well as in the synthesis of compatible solutes. The extent of these demands, however, remains unknown; and if the tonoplast membranes in halophytes are particularly efficient at preventing Na+ and Cl leakage (Leach et al., 1990), then the costs of ion compartmentation would not be excessive (Yeo, 1981, 1983). For leaves of halophytes exposed to increasing salinity, rates of respiration have been reported: not to change (e.g. Spartina alterniflora, dry mass basis, Hwang & Morris, 1994; Salicornia bigelovii, area basis, Ayala & O’Leary, 1995; Avicennia germinans, area basis, Lopez-Hoffman et al., 2007); to increase (e.g. two mangrove species, dry mass basis, Burchett et al., 1989); and even to decrease (e.g. Plantago coronopus, area basis, Koyro, 2006). Early work on this topic with Suaeda maritima showed respiration was highest in leaves of plants grown without NaCl; rates on a dry mass basis in leaves from plants at 340 or 680 mm NaCl were, respectively, 45 and 53% of that in nonsaline plants (Flowers, 1972). It is tempting to speculate that without a ‘normal’ Na+ supply, futile cycling of K+ (Britto & Kronzucker, 2006; but at the tonoplast), resulting from a poor capacity of S. maritima to retain K+ in vacuoles (Yeo, 1981), might contribute to the high respiration in the succulent leaves of this species when in nonsaline conditions; when external Na+ is low, succulent halophytes, such as S. maritima, accumulate high K+ (Yeo & Flowers, 1980). Further work is needed to understand better the energy requirements associated with salt tolerance, in both leaves and roots, of halophytes. Care should be taken with the basis upon which respiration is expressed, particularly in succulent leaves. Increased succulence could decrease rates on a fresh mass basis, increased ‘ash’ could decrease rates on a dry mass basis, and rates expressed on a projected surface area basis do not take into account increased thickness in succulent leaves, so it would seem useful to express rates on a total protein basis in the tissues/organs studied.

2. Osmotic adjustment, ion compartmentation and compatible solutes

All halophytes must meet the challenge of osmotic adjustment to a low external water potential. However, species differ in succulence (water content per unit area of leaf; Flowers et al., 1986) and in the solutes accumulated (Flowers & Yeo, 1988). For example, among 32 species of the Chenopodiaceae analysed by Albert et al. (2000), Na+ and Cl contributed 67% of the solute concentration (molar in shoot water), whilst in the Poaceae the same ions averaged only 32% of the solutes in 17 species; sugars were just 1% in the Chenopodiaceae, but 19% in the Poaceae (we have utilized a classical nomenclature, in line with that used by Aronson, 1989, but recognize there is debate (APG, 2003) over the classification of this family). Not only does the proportion of organic to inorganic solutes vary, but so do the anions accumulated (Hütterer & Albert, 1993) and the ratio of ions utilized by different groups. For example, the Aizoaceae and Chenopodiaceae have more than 10-fold higher Na+/K+ ratios than the Poaceae, Cyperaceae and Juncaceae (Flowers et al., 1986).

Since monovalent ions are judged toxic at the concentrations required for osmotic adjustment, it is generally assumed that Na+ and Cl are compartmentalized, predominantly in vacuoles, so that concentrations in the cytoplasm are maintained within tolerable limits (Wyn Jones & Gorham, 2002). Experimental evidence for compartmentalization of Na+ into vacuoles is, however, limited. The data summarized in Table 1 indicate concentrations of Na+ in the cytoplasm of c. 180 mm (the range is between 150 and 220 mm for plants growing in 40–500 mm Na+). The activity would be less than this (c. 110–150 mm in an aqueous solution of NaCl), but how much less is unknown, because the cytosol is not a simple aqueous solution. The cytoplasmic concentration of Cl in S. maritima has been estimated to be 86 mm, about half that for Na+ (Flowers & Yeo, 1988). There are, however, no data obtained by direct measurement using ion-specific microelectrodes in the cells of halophytes, as far as we are aware.

Table 1.  Compartmentation of Na+ and K+ in the cells of the shoot tips or leaves of some halophytes
GenusFamilyNa+ cyt (mm)Na+ vac/Na+ cytNa+/K+ vacNa+/K+ chlNa+/K+ cytExternal Na+ (mm)
Range (n)Range (n)Range (n)Range (n)Range (n)Range
Suaeda maritimaa and Suaeda salsabChenopodiaceae150–218 (5)1.2–7.1 (4)3.6–27 (4)4–5 (2)1–2.1 (3)50–400
Atriplex spongiosacChenopodiaceaenana6.7–8 (2)na0.44–0.53 (2)50–400
Puccinellia peisonisdPoaceaenana0.42na0.0240
Spartina townsendiiePoaceaenana0.83na0.1540
Zostera marinafZosteraceaena4.71.8na0.1SW

Toxicity has been judged from the in vitro effects of ions on enzyme activity, where high concentrations of K+ may be as detrimental as those of Na+ (Heimer, 1973; Greenway & Sims, 1974; Flowers & Dalmond, 1992). The relative importance of the activity per se as opposed to the ratio of Na+/K+ or the ratio of (Na+ K+)/organic solutes that may modulate the effects of the ions (Pollard & Wyn Jones, 1979) is unknown. Where they can be calculated, Na+/K+ ratios are between 2.5 and 21 times higher in the vacuole than in the cytoplasm (Table 1 summarizes representative data from five species) and this difference between cytoplasm and vacuoles is found in the Poaceae as well as the Chenopodiaceae. Interestingly, Na+/K+ ratios in the vacuoles of the grasses are very much lower than in the Chenopodiaceae (see also Section III.2).

Ion transport across the tonoplast, into vacuoles, is energized by a proton motive force (PMF) generated by the vacuolar H+-ATPase (V-ATPase) and a H+-pyrophosphatase (V-PPiase) (Bartels & Sunkar, 2005; Gaxiola et al., 2007). Tonoplast ATPase activity in Mesembryanthemum crystallinum increased with the addition of NaCl (Ratajczak et al., 1994), as did the expression of the E-subunit in leaves (but not roots) of mature plants on exposure to salinity (Golldack & Dietz, 2001). Na+/H+ exchange in vesicles prepared from leaves was constitutively high and increased with salinization of the plant (Barkla et al., 2002): these changes in M. crystallinum have been interpreted as indicating that accumulation of Na+ in vacuoles is suppressed in root cells and activated in the cells of the leaves as an acclimation to increasing salinity. In Salicornia bigelovii, the activity of both the PM- and V-ATPases increased on addition of NaCl to the growth medium (Ayala et al., 1996), as did activity of the V-PPiase (Parks et al., 2002). In Suaeda salsa, salinity increased the activity of the V-ATPase in tonoplast vesicles, rather than the V-PPiase (Wang et al., 2001), and this was associated with an increase in activity of the Na+/H+ antiporter (Qiu et al., 2007). Growth of Thellungiella halophila in NaCl increased the Na+/H+ exchange of vesicles prepared from the tonoplast, but not from the plasma membrane (Vera-Estrella et al., 2005). Although the evidence is limited, Na+/H+ exchange appears to increase on salinization, as does the activity of one or more of the PMF-generating enzymes, suggesting that these play a role in the accumulation of Na+. However, efficient ion compartmentation relies not only on transport across the tonoplast, but also on retention of ions within vacuoles, a property previously correlated with a high ratio of phospholipids to protein, highly saturated fatty acid complement, a high proportion of cholesterol and an overall low fluidity of the tonoplast (Leach et al., 1990).

It is generally presumed that halophytes require K+ for the same metabolic functions as in glycophytes, and the few estimates of cytoplasmic concentrations of K+ in growing cells of halophytes suggest these are similar to those of glycophytes (Table 1: Gorham & Wyn Jones, 1983; Flowers et al., 1986). However, there is evidence that the cytoplasmic K+ concentration of mature leaf cells of S. maritima is relatively low (c. 30 mm, see Flowers & Yeo, 1988) and that the metabolism of at least halophytes in the Chenopodiaceae has evolved to adjust to these concentrations. Flowers & Dalmond (1992) found from in vitro studies using polysomes of three dicotyledonous halophytes (Atriplex isatidea, Inula crithmoides and S. maritima) that incorporation of 35S-methionine into protein was stimulated by Na+ (100 mm) in the presence of a suboptimal concentration (25 mm) of K+, an effect that was not found in wheat or pea.

A rider to the cellular compartmental model of salt tolerance at the cellular level is the need for accumulation of metabolically ‘compatible’ (organic) solutes in the cytoplasm to balance the osmotic potential of the Na+ and Cl accumulated in the vacuole (Wyn Jones & Gorham, 2002). A range of molecules such as sugars (e.g. sucrose), sugar alcohols (e.g. sorbitol), amino acids (e.g. proline), methylated proline-related compounds (e.g. methyl-proline), betaines (e.g. glycinebetaine) and methylated sulphonio compounds (e.g. dimethylsulphonioproprionate, DMSP) have been proposed to fulfil this function in halophytes (Hasegawa et al., 2000; Rhodes et al., 2002), albeit with different C and N costs. Some of these compounds (e.g. DMSP in Spartina spp.; methylated proline compounds in Melaleuca spp.) accumulate in just a few halophytes, whereas others (e.g. glycinebetaine) accumulate in numerous species across many genera (Rhodes & Hanson, 1993; Naidu et al., 2000). Gorham et al. (1980) reported amounts of quaternary ammonium compounds, proline, inositol and pinitol in 27 species collected from a salt marsh in North Wales. More recently, the organic solutes in leaves of 51 species from the neighbourhood of a salt lake in Turkey (Tipirdamaz et al., 2006) were analysed. These, and other studies, have confirmed the presence of species-specific solutes; the following generalizations can be drawn:

  • • 
    The quaternary ammonium compound, glycinebetaine, is present in numerous halophytes from a large number of families (Rhodes & Hanson, 1993). In the Plumbaginaceae, however, four other quaternary ammonium compounds (choline-0-sulfate and the betaines of β-alanine, proline, and hydroxyproline) have evolved to supplement or replace glycinebetaine (Hanson et al., 1994). In addition, a few species (e.g. Spartina spp.) accumulate DMSP, a sulphonium-analogue of quaternary ammonium compounds (Rhodes & Hanson, 1993).
  • • 
    Proline is also present in halophytes from a wide range of families; however, Tipirdamaz et al. (2006) noted that ‘species that behaved as glycinebetaine accumulators contained little proline and vice versa’. In Melaleuca spp., several proline analogues and methylated proline compounds are the main organic solutes (Naidu et al., 2000).
  • • 
    The sugar alcohol inositol is present in some but not all halophytes in the Aizoaceae, Apiaceae, Cyperaceae, Iridaceae, Juncaceae, Juncaginaceae, Poaceae, Primulaceae, and Zosteraceae (Gorham et al., 1980, 1981; Ishitani et al., 1996).
  • • 
    Pinitol is present in some but not all halophytes in the Aizoaceae, Chenopodiaceae, Cyperaceae, Plumbaginaceae, and Tamaricaceae (Gorham et al., 1980, 1981; Vernon & Bohnert, 1992; Ishitani et al., 1996; Murakeozy et al., 2003; Arndt et al., 2004).
  • • 
    Sorbitol appears to be confined to the Plantaginaceae (Gorham et al., 1981; Koyro, 2006).
  • • 
    Mannitol is not widely reported in halophytes, but is present in many families of flowering plants, including the mangrove Lagunculana racemosa in the Combretaceae (Stoop et al., 1996; Noiraud et al., 2001).

This diversity in type of organic solute accumulated has been considered to reflect phylogeny (e.g. glycinebetaine, Weretilnyk et al., 1989) and/or functional needs of halophytes in diverse environments (e.g. Rhodes & Hanson, 1993; Colmer et al., 1996; McNeil et al., 1999).

The effects of increasing external NaCl on the concentrations of organic solutes have been assessed for numerous species. Concentrations can increase manyfold; for example, in M. crystallinum, proline increased between 20 to 30 times (Sanada et al., 1995; Ishitani et al., 1996) for a change in salt concentration of 400 mm, while inositol and pinitol increased over 80-fold (Ishitani et al., 1996). In some cases, however, the concentrations of compatible solutes do not increase with increasing external salinity, suggesting the synthesis of these compounds is constitutive in some species (e.g. A. griffithii and S. fruticosa; Khan et al., 1998), while in other species (e.g. Spartina alterniflora) some solute types are constitutive (e.g. DMSP) while others are modulated by salinity (e.g. proline and glycinebetaine; Colmer et al., 1996). It is also possible that some organic solutes might be redistributed between compartments as salinity changes, with no measurable effect on the concentration on a whole-tissue basis. It is important to note that on a whole-tissue basis, the concentration of organic solutes is often well below that necessary to make any significant contribution to the overall solute potential; however, if largely confined to the cytoplasm, an assumption for which there is some evidence (e.g. S. maritima, Hall et al., 1978; Atriplex gmelini, Matoh et al., 1987), the solutes would contribute significantly within that volume (Rhodes et al., 2002).

Little is known of the signalling cascades regulating the synthesis of compatible solutes in plants (Hare et al., 1998; Chinnusamy et al., 2005), although the molecular basis of NaCl-enhanced accumulation of some organic solutes has been studied in a few halophytes. Examples are inositol in M. crystallinum (Vernon et al., 1993), proline in T. halophila (Kant et al., 2006) and glycinebetaine in several halophytes. The accumulation of proline by T. halophila (Inan et al., 2004) is consistent with the finding that the expression of genes encoding for the first enzyme of the biosynthetic pathway of proline, the Δ1-pyrroline-5-carboxylate synthetase (P5CS), increased in shoots and roots with increasing NaCl, while the gene encoding proline dehydrogenase (PDH, the first step of the breakdown of proline) was not detectable in the shoot and decreased in the root with increasing external NaCl (Kant et al., 2006). In T. halophila, the expression of the gene for ornithine aminotransferase, responsible for an alternative route to the biosynthesis of proline, was unresponsive to change in the external NaCl concentration (Kant et al., 2006).

Glycinebetaine is synthesized from choline in two steps (Rhodes & Hanson, 1993): the two enzymes are choline monooxygenase (CMO) and betaine aldehyde dehydrogenase (BADH). Salt-responsive enhancer regions have been identified for a BADH gene cloned from Atriplex centralasiatica, but the exact regulatory pathway remains to be elucidated (Yin et al., 2002). BADH mRNA concentrations were also enhanced during salt exposure in three Atriplex species, as were concentrations of CMO mRNA (Shen et al., 2002; Wang & Showalter, 2004; Tabuchi et al., 2005). Although ABA treatment enhanced CMO mRNA in A. hortensis (Shen et al., 2002), this was not the case in A. prostrata (Wang & Showalter, 2004), so that whether ABA signalling is involved in the signal-transduction pathway remains uncertain. Tabuchi et al. (2005) demonstrated that increased CMO mRNA resulted in higher CMO protein amounts in A. nummularia after exposure to 500 mm NaCl, when compared with a ‘control’ at 1 mm NaCl. Enhanced expressions of proteins related to glycinebetaine synthesis were also observed in a proteomic study of Suaeda aegyptiaca (Askari et al., 2006). Most of these molecular studies used ‘controls’ with zero or low external Na+ (i.e. below the growth optimum), so that dose-response studies are required to separate the effects of growth in a deficient medium from those of salinity. Although Moghaieb et al. (2004) also used a zero NaCl treatment, this study of Salicornia europaea and S. maritima included three higher NaCl concentrations, where BADH mRNA increased with higher NaCl treatments.

In the case of transgenics aimed at increasing glycinebetaine synthesis in plants that do not naturally contain this solute (e.g. tobacco, rice; see Supporting Information, Table S1), substrate availability of the precursor (choline) has constrained glycinebetaine synthesis (McNeil et al., 1999), so that glycinebetaine was not present at osmotically significant concentrations (Rathinasabapathi, 2000; Su et al., 2006). As an alternative approach to raising the amounts of compatible solutes, wide-crossing of wheat with halophytic relatives in the Triticeae containing relatively higher glycinebetaine, has lead to amphiploids with increased glycinebetaine in the expanding leaves (Colmer et al., 1995; Islam et al., 2007). These manipulative experiments with whole genome addition of the halophytic relative into a nonhalophyte, as compared with single gene manipulations, support the view that the evolution of organic solute synthesis in halophytes has involved metabolic networks rather than just changes in one or few enzymes.

III. Uptake and transport of monovalent ions

  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information

1. Uptake and accumulation of Na+

Sea water contains, on a molar basis, approx. 50 times more Na+ than K+ (Harvey, 1966). Since, in spite of their physicochemical similarities, it is K+ rather than Na+ that is essential to plant life, this means that plants in saline habitats have acquired mechanisms that allow the selective uptake of K+ in the face of considerable competition from Na+ (Maathuis & Amtmann, 1999). The situation, however, is not simply one of the evolution of a highly selective K+-uptake system, as halophytes also utilize Na+ for osmotic adjustment, albeit to different degrees in different families. Halophytes, therefore, require to be able to select K+ from a mixture dominated by Na+ and yet to accumulate sufficient Na+ for the purposes of osmotic adjustment.

Halophytes support relatively high rates of net Na+ uptake of between c. 1 and 10 nmol Na+ g−1 fresh mass roots s−1 without injury to the plant (c. 8.5–85 nmol Na+ g−1 dry mass roots s−1, depending on the external salt concentration; Table 2). Na+ influx into the halophyte, Spergularia marina, was first measured in the 1980s and showed uptake of 22Na+ into whole plants in a ‘steady state’ salinity was linear over a period of 2 h (Cheeseman et al., 1985; Lazoff & Cheeseman, 1988); Yeo (1974) had previously measured net uptake of 22Na+ over 24 h and, alongside others (Jefferies, 1973; Shepherd & Bowling, 1979; Mills et al., 1985), had estimated influx (Joc) from flux analysis data. Recently, influx has been estimated from short exposure (2 min; the period over which the 22Na+ content of the tissue increased linearly with time and so was argued to represent influx) to a solution containing 22Na+ (Essah et al., 2003; Wang et al., 2006, 2007a). The range of influx of Na+ into halophytes, between 2 and 13 nmol g−1 root fresh mass s−1 at NaCl concentrations of 25–500 mm, is similar to that for net uptake. Na+ influx rates in halophytes, however, are much lower than that recorded for the glycophyte arabidopsis (30 nmol g−1 root fresh mass s−1 at just 50 mm external NaCl), which also has a much higher influx than another glycophyte, durum wheat (1.1 nmol g−1 root fresh mass s−1 in 25 mm NaCl; Table 2).

Table 2.  Na+ fluxes in roots of some halophytes and the glycophytes Arabidopsis thaliana and Triticum turgidum ssp. durum (species are arranged alphabetically by family)
SpeciesNa+ flux (nmol g−1 root fresh mass s−1) and period of measurementNaCl (mm)Reference
<5 min24–48 hd
  • na, not available.

  • a

    Two examples; not a comprehensive list.

  • *

    Calculated from analysis of efflux.

  Arabidopsis thaliana (Brassicaceae)31.3na0.5050Essah et al. (2003)
  Triticum turgidum ssp. durum Tamaroi (Poaceae)1.1na0.3025Davenport et al. (2005)
  Aster tripolium (Asteraceae)nana2.30100Shennan et al. (1987)
  Thellungiella halophila (Brassicaceae)5.2nana100Wang et al. (2006)
  Thellungiella halophila (Brassicaceae)na1.2na100Wang et al. (2006)
  Spergularia marina (Caryophyllaceae)13.1nana25Lazof & Cheeseman (1988)
  Spergularia marina (Caryophyllaceae)11.7nana90Lazof & Cheeseman (1986)
  Atriplex nummularia (Chenopodiaceae)2.7*nana50Mills et al. (1985)
  Suaeda maritima (Chenopodiaceae)nana10.2340Yeo & Flowers (1986)
  Suaeda maritima (Chenopodiaceae)na3.7na100Yeo & Flowers (1986)
  Suaeda maritima (Chenopodiaceae)na7.2na300Yeo & Flowers (1986)
  Suaeda maritima (Chenopodiaceae)na3.3na25Wang et al. (2007a)
  Suaeda maritima (Chenopodiaceae)3.8nana25Wang et al. (2007a)
  Suaeda maritima (Chenopodiaceae)na9.3 150Wang et al. (2007a)
  Suaeda maritima (Chenopodiaceae)12.7nana150Wang et al. (2007a)
  Eleocharis uniglumis (Cyperaceae)2.1*nana74Shepherd & Bowling (1979)
  Triglochin maritimum (Juncaginaceae)3.4*nana500Jefferies (1973)

That there is uncertainty over the mode of entry of Na+ into the roots of halophytes is highlighted by recent studies. Na+ influx into T. halophila from 100 mm NaCl was stimulated by the K+ channel blockers tetraethyl ammonium ions (TEA+) and Cs+ (to 161 and 156%, respectively, of controls in the absence of Cs+ or TEA+), although neither Cs+ nor TEA+ (20 mm) had any effect on shoot Na+ concentrations (per unit dry mass) after 2 d of exposure to NaCl (100 mm) (Volkov & Amtmann, 2006). Patch-clamp studies, in the whole-cell mode, of ion channels in the root cortical cells of T. halophila demonstrated the presence of time-dependent inward (on hyperpolarization of the membrane) and outward (on depolarization) currents as well as instantaneous currents (induced by a voltage pulse) (Volkov & Amtmann, 2006). The net selectivity for all three was greater (by up to an order of magnitude) for K+ than for Na+. The inward-rectifying channels in T. halophila root cells were inhibited by Cs+ and the outward currents by TEA+, channel blockers that had no effect on the instantaneous current. Volkov & Amtmann (2006) concluded that Na+ uptake was mediated by the instantaneous current while K+ influx would occur through the inward-rectifying channels. These data, together with the fact that Na+ influx measured over 15 min in 100 mm NaCl was inhibited by Ca2+ (Wang et al., 2006), have been used to argue that Na+ uptake in T. halophila is mediated by a voltage-independent channel (Demidchik & Maathuis, 2007; see Table 3 for a note on the various transporters implicated in the movement of monovalent cations) as suggested for glycophytes (e.g. arabidopsis, Demidchik & Tester, 2002; wheat, Davenport & Tester, 2000). For S. maritima, there is evidence, however, that neither NSCSs nor LCT (Table 3 lists the abbreviations) is involved in Na+ influx, as neither cAMP nor Ca2+ (blockers of NSCCs) had any significant effect on Na+ uptake (Wang et al., 2007a). There is also evidence that the pathway of Na+ influx changed with increasing salt concentration. In 25 mm NaCl, a salt concentration that supports some 85% of the optimal growth (Yeo & Flowers, 1980), Na+ influx and net uptake were insensitive to Cs+ and TEA+ or competition with K+, while at a NaCl concentration of 150 mm, close to the optimum for growth, K+, Cs+ and TEA+ reduced Na+ influx and net uptake (Wang et al., 2007a). In the halophyte M. crystallinum, myo-inositol, the most common natural form of inositol and precursor of D-onitol and pinitol, is important in its tolerance (Adams et al., 1998) and it has been hypothesized that Na+/myo-inositol symporters have a central role in Na+ uptake (Chauhan et al., 2000). An HKT transporter (McHKT1) has been localized to the plasma membrane of cells of both the leaves and roots, and expression of McHKT1 is up-regulated after a sudden increase in external salinity (400 mm NaCl; Su et al., 2003), as are SOS1 and some HAK transporters (see Su et al., 2003 for a table of changes). In Xenopus oocytes, this HKT1-like protein (McHKT1) transports Na+ and K+ equally (Su et al., 2003). By 6 h after treatment with 400 mm NaCl, the expression of McHKT1 increased almost threefold and was most highly expressed in the plasma membrane of leaves (Su et al., 2003). A model in which the storage of Na+in the root decreased and transport to the shoot was enhanced (including up-regulation of the Na+/myo-inositol symporter) was proposed (Su et al., 2003), with the up-regulation of McHKT1 suggested to contribute to storage of Na+ in the leaves. Taken all together, the evidence from the range of studies discussed earlier indicates that there may be considerable variation in the transporters involved in the uptake of Na+, not just between glycophytes and halophytes, but also between species of halophyte and even at different external salt concentrations.

Table 3.  Some of the monovalent ion transporters in plants involved with Na+, K+ and Cl transport, and thus presumably regulation of ion transport associated with salt tolerance
Protein familyTransporterCommentsSee also
Cation-chloride co-transportersCCCCation-chloride co-transporters; a family of proteins where the movement of Cl is coupled to that of Na+ and/or K+; better characterized in animals than in plantsVery & Sentenac (2003); Colmenero-Flores et al. (2007)
Cation proton antiportersCHXCation/H+ eXchangers, whose function is not well characterized in plants, but may play a role in xylem loading of Na+Very & Sentenac (2003); Gierth & Maser (2007)
 NHXaNa+/H+ eXchangers found in plasmamembrane, tonoplast and other endomembranes. One of two families of cation/proton antiporters. NHX1 is a tonoplast Na+/H+ antiporter: SsNHX1 has been identified in Suaeda salsa 
 SOSaSalt overly sensitive; includes SOS1. ThSOS1 has been identified in Thellungiella halophila 
HKTHKTaHigh-affinity K transporter. Something of a misnomer as there is a family of cation transporters itself divided into two subfamilies, with high- and low-affinity Na+/K+ symporters and Na+-selective transporters. Members of subfamily 1 contain low-affinity Na+ transporters (when expressed in yeasts and Xenopus oocytes) and members of subfamily 2 have only been found in monocotyledonous species (see Munns & Tester, in press for more detail). McHKT has been identified in Mesembryanthemum cystallinumVery & Sentenac (2003); Platten et al. (2006); Gierth & Maser (2007)
K inward rectifiersKir-likeK+ inward rectifiers, active at the tonoplastVery & Sentenac (2003); Lebaudy et al. (2007)
KUP/HAK/KTKUP/HAK/KTK+ uptake permeases/high-affinity K+/K+ transporter. Members of a family of cation symporters; assumed to be responsible for high-affinity K+ uptakeVery & Sentenac (2003); Gierth & Maser (2007)
Low-affinity cation transporterLCT1Low-affinity cation transporter reported in wheat, but with no recent data availableVery & Sentenac (2003)
Nonselective cation channelsNSCCsNonselective cation channels. Responsible for passive fluxes of cationsVery & Sentenac (2003); Demidchik & Maathuis (2007)
 VI-NSCCsVoltage-independent nonselective cation channels 
 VICsVoltage-independent channels 
 CNGCsCyclic nucleotide-gated channels are NSCCs activated by cAMP or cGMP 
 GLRsGlutamate-like receptors are inferred to be glutamate-activated NSCCs; little is known of their role(s) in plants 
Shaker Shaker family of K+ channelsVery & Sentenac (2003); Lebaudy et al. (2007)
 AKTArabidopsis K+ transporter AKT1 is likely responsible for low-affinity K+ uptake 
 GORKGuard cell outwardly rectifying K+ channel 
 KIRCK+ inwardly rectifying channel. Proposed as main pathway for low-affinity K+ uptake (positive charge inward is positive rectification). These are shaker-type channels 
 KORCK+ outwardly rectifying channel. These shaker-type channels are assumed to represent a K+ release pathway 
 SKORStelar K+ outward rectifier, SKOR, is virtually impermeable to Na+ 

The Na+ influx, expressed relative to the net flux (net uptake over hours or days) has been used to estimate the extent of efflux across the root plasma membrane: for T. halophila such an analysis shows that close to 80% of influx is immediately effluxed (Wang et al., 2006), suggesting efflux to be highly significant in determining the net Na+ uptake by the roots. T. halophila growing for a few weeks in 100–200 mm NaCl accumulates between 1.2 and 2.3 mmol Na+ g−1 dry mass of shoot tissue (Inan et al., 2004; Kant et al., 2006; Wang et al., 2006; M’Rah et al., 2007), similar concentrations to those seen in other dicotyledonous halophytes growing in similar external salt concentrations (and are not as low as 30 mm as suggested by Vera-Estrella et al., 2005 for the data of Inan et al., 2004). T. halophila is much more salt-tolerant than arabidopsis, which hardly survives a week or two in 100–200 mm NaCl in natural light intensities (Inan et al., 2004; Volkov et al., 2004; Kant et al., 2006). Na+ influx into the roots of T. halophila equilibrated in 100 mm NaCl was 5.2 nmol Na+ g−1 fresh mass roots s−1, about half that in arabidopsis (conditions that are, however, toxic to arabidopsis). Although arabidopsis is a valuable model plant for many aspects of plant physiology, it is salt-sensitive and so research on this species when exposed to high NaCl provides information on stress rather than tolerance (Zhu, 2001; Volkov et al., 2004).

The efflux of Na+ from the cytoplasm is assumed to be mediated by Na+/H+ exchange, either by SOS1 at the plasma membrane or NHX1 at the tonoplast (Apse & Blumwald, 2007). It has been suggested that SOS1 acts as a sensor for cellular Na+, an increase of which, perhaps acting through changing cytosolic Ca2+, up-regulates ABA concentrations and leads to an increase in reactive oxygen species (see Chinnusamy et al., 2005). SOS1 is particularly expressed in the plasma membrane of root tips and in the vascular tissues, where the Na+/H+ antiporter it encodes is postulated to play a role in the efflux of Na+ to the transpiration stream (Chinnusamy et al., 2005). SOS1 is present in membrane vesicles prepared from T. halophila shoots and roots (using antibody to AtSOS1; Vera-Estrella et al., 2005) and is highly expressed even in the absence of salt (Taji et al., 2004) – expression patterns do differ between roots and shoots (Kant et al., 2006) in a way that is consistent with a role for SOS1 in loading the xylem in roots, although this process is thermodynamically unlikely (Munns & Tester, 2008).

The similarity between the genomes of T. halophila and arabidopsis has allowed the rapid development of methods to evaluate the effects of salinity on gene expression in T. halophila (Taji et al. 2004; Volkov et al., 2004; Wang et al., 2004; Gong et al., 2005; Wong et al., 2006). For genes putatively involved in Na+ transport, these types of study have shown that SOS1 (ThSOS1) levels in the roots and shoots of T. halophila increased in plants grown in 200 mm NaCl for 2 wk, when compared with plants grown in the absence of salt (Vera-Estrella et al., 2005). In the shoots of T. halophila, expression increased with increasing external NaCl concentration, although in the roots, while expression increased on the addition of NaCl, there was no further change from 100 to 500 mm NaCl in the external solution (Kant et al., 2006): there was about sevenfold more ThSOS1 transcript in roots than in shoots. Salt-sensitive mutants of T. halophila, with reduced ability to control Na+ accumulation, have been obtained and demonstrate that sensitivity can be induced by mutations at a single locus (let1) thought to be involved in the control of ion accumulation (Inan et al., 2004).

The accumulation of Na+ into vacuoles, whether of roots or shoots, is presumed to be via a Na+/H+ exchange mediated by NHX (Apse & Blumwald, 2007), but NHX was only detected in the plasma membrane fraction prepared from T. halophila roots (NHX was not detected, using antibody to AtNHX1, in root or shoot tonoplast or shoot plasma membrane fractions; Vera-Estrella et al., 2005). Genes for the Na+/H+ antiporter have been cloned from S. salsa (Ma et al., 2004) and A. gmelini (Hamada et al., 2001) and identified in M. crystallinum (Chauhan et al., 2000). The relative ability of AtNHX1 to transport Na+ or K+ can be altered by deletion of the hydrophilic C-terminus of the protein (Yamaguchi et al., 2003) and binding of calmodulin-like protein (Yamaguchi et al., 2005).

Little is known about the proteins involved in the other stages of the accumulation of Na+ by plants or their regulation. Members of the CHX family of cation exchangers have been shown to play a role in Na+ transport to the xylem in arabidopsis (Hall et al., 2006; Pardo et al., 2006), and the possibility of the involvement of cation-chloride co-transporters has been raised by the recent identification of a gene encoding such a protein in arabidopsis (Colmenero-Flores et al., 2007).

We have summarized these experiments on the uptake of Na+ in some detail, as many have only recently been reported. The results reflect the general uncertainty (Apse & Blumwald, 2007; Demidchik & Maathuis, 2007) in the way in which Na+ enters cells of plants, not just halophytes, and is exported to the xylem. For halophytes, there is an added complication over glycophytes in determining the nature of the transporters involved in the uptake of Na+: these are methodological problems of investigating transporters involved in influx of Na+ at high external concentrations that relate to pleiotropic effects in the cases of gene knockouts, the inability to use yeast mutants at high external NaCl concentration and the fact that heterologous expression systems may not reproduce the kinetic characteristics of transporters (Wang et al., 2007a). The apparent differences in the characteristics of Na+ uptake in different species demonstrate the need for detailed investigation of ion transport in a number of ‘model’ halophytes (Section IV, ‘Conclusions and perspectives’): it is quite possible that different species have evolved to achieve the same ends by different means. The pathway of uptake of Na+ in halophytes remains as enigmatic as in glycophytes.

2. Uptake and accumulation of K+ and its selectivity over Na+

Influx data for K+ for cells in a ‘steady state’ are not obtained as easily as for Na+. The radioactive isotopes of K+ are relatively short-lived and 86Rb+ may be a poor substitute for 42K+, depending on the nature of the transporter involved (Rodriguez-Navarro & Ramos, 1984). As one example, in S. maritima the ratio of uptake of 86Rb+ to 42K+, measured over a 24 h period, decreased linearly from 6.9 at an external concentration of 0.1 mm to 1.4 at 100 mm (Yeo, 1974). We do not know of any estimates of influx (2 min) of K+ for halophytes, although fluxes of K+ and Na+ estimated using isotopes have been obtained over periods of a few hours. For example, Na+ stimulated the uptake of K+ measured under nonsteady-state conditions over 60 min in Triglochin maritima (Jefferies, 1973). In S. maritima, uptake of 42K+ and 22Na+ over 3.5 or 20 h from 1, 10 or 100 mm concentrations were similar (Yeo, 1974). In another dicotyledonous halophyte, S. marina, Na+ and K+ fluxes measured over 2 h from 90 mm concentrations of Cl were again similar (Wickens & Cheeseman, 1991), suggesting that these dicotyledonous halophytes have high rates of transport of monovalent cations in general.

Net uptake of K+ is far easier to determine than influx and there have been many reports of the K+ concentrations in halophytes. As with glycophytes, when halophytes are transferred from a medium with a high K+/Na+ ratio (e.g. a ‘normal’ culture solution) to one with a low K+/Na+ ratio (a salinized culture solution), plant K+ concentrations fall as Na+ concentrations rise (although for Sesuvium portulacastrum there was no change in plant K+ as external NaCl was raised to 900 mm; Venkatesalu et al., 1994). In the absence of salinity, net uptake of K+ in S. maritima, at c. 12 nmol g−1 dry mass roots s−1 (from a 6 mm concentration), is approximately twice the value of 5 nmol g−1 dry mass roots s−1 for maize and barley (estimated from data in Marschner, 1995). In the halophytic grass, Puccinellia tenuiflora, Cs+ (10 mm) inhibited net uptake of K+ (from a 3 mm solution) into roots and transport to the shoots, whereas TEA+ only inhibited net transport to the shoots (Peng et al., 2004). However, marine halophytes accumulate K+ from a relatively high concentration and in the presence of Na+: what is now needed is to evaluate the characteristics of K+ influx from a solution with the composition of sea water. A supplementary approach would be to search for homologues of known K+ transporters – as, for example, the reporting of homologues of AKT (see Table 3 for abbreviations of ion transporters) whose expression changed on salinization in the halophyte M. crystallinum (Golldack & Dietz, 2001). However, the functional characteristics of the transport process still require to be evaluated. As already discussed in Section III.1, in M. crystallinum, expression of an HKT transporter (McHKT1; transports Na+ and K+ equally in Xenopus oocytes) is up-regulated following sudden exposure to high salinity (400 mm NaCl; Su et al., 2003). Moreover, concentrations of free polyamines also increase after upshock in roots and leaves of M. crystallinum (Shevyakova et al., 2006; Kuznetsov et al., 2007) and these could play a role in regulating K+ fluxes (Shabala et al., 2007). In the monocotyledonous halophyte Aneurolepidium chinense, a membrane protein (AcPMP3) which is localized in the root cap, has been proposed to act as a regulator of Na+ and K+ accumulation (Inada et al., 2005), but additional work is required to test whether an analogue of this protein is found in other halophytes. In conclusion, as for Na+, little is known of the proteins involved in the uptake of K+ by halophytes; if the candidates are the same as in glycophytes (Gierth & Maser, 2007), the range of possibilities is large.

Halophytes grown in nonsalinized culture solution accumulate high concentrations of K+ (e.g. S. maritima, Yeo & Flowers, 1980). Such accumulation can occur in succulent halophytes even when a relatively low external Na+ (viz. 10 mm) is provided and growth is near optimal (e.g. the stem succulent Halosarcia pergranulata; Short & Colmer, 1999). However, K+ (as KCl) cannot substitute for Na+ in all halophytes; K+ does not stimulate the growth of S. maritima and can be inhibitory, 340 mm KCl producing only 28% of the dry mass of plants growing in an equivalent concentration of NaCl (Yeo & Flowers, 1980). A similar situation is reported for other members of the Chenopodiaceae, for example, A. nummularia and A. inflata (where growth was inhibited in KCl concentrations of 200 mm and above; Ashby & Beadle, 1957); A. halimus (inhibited by 31 mm KCl; Mozafar et al., 1970); A. nummularia (500 mm; Ramos et al., 2004); A. gmelini (250 mm; Matoh et al., 1986); Halogeton glomeratus (10 mm; Williams, 1960), S. europaea (83 mm; Van Eijk, 1939) and S. salsa (400 mm; Wang et al., 2001). KCl is also more toxic to the growth of the grass Puccinellia paisonis than is NaCl (Stelzer & Läuchli, 1977). Why this should be so is not known, although a number of years ago Yeo (1981) concluded, based on data from flux analysis, that halophytes such as S. maritima were able to retain Na+, but not K+ in vacuoles.

Estimates of the selectivity of the overall uptake for K+ over Na+, net SK:Na, are available for many species, both halophytes and glycophytes. These net selectivities, generally calculated from the ion contents of the shoots relative to those in the external medium, indicate differences between mono- and dicotyledonous halophytes. On average, the net SK:Na by monocotyledonous halophytes is twice that of dicotyledonous halophytes at low salinity, increasing to four times at high salinity (Table 4), reflecting the ratio of Na+ to K+ in the vacuole (cf. Table 1). However, the contribution of ion transport parameters to the net selectivity may be confounded with differences in compartmental volumes: with Na+ and K+ concentrations in the vacuole of 400 and 50 mm, respectively, and with cytoplasmic Na+ and K+ being 177 and 100 mm, respectively, net SK:Na increases by 34% as the relative vacuolar volume decreases from 0.9 to 0.7 (with an external K+/Na+ ratio of 0.03). That monocotyledonous and dicotyledonous halophytes differ in their relative vacuolar volumes is suggested by their differences in succulence: succulence is very much greater in dicotyledonous than in monocotyledonous species (with only the Juncaginaceae among the monocots being succulent; Flowers et al., 1986). There is also evidence of a rapid increase in vacuolar volume and in the concentration of Na+, but not K+, in cells of the mangrove Bruguiera sexangula when exposed to NaCl (150 mm), a potential mechanism to allow the cells to acclimate to a rise in external salt concentration (Mimura et al., 2003). However, there are, as far as we are aware, no stereological analyses of the effects of salinity on monocotyledonous halophytes (cf. Hajibagheri et al., 1984a).

Table 4.  Net K : Na selectivity (SK:Na) for shoots of some halophytes
Genus/orderSelectivity (na) at salinities which were:
  • Net selectivity was calculated as the ratio of K+ : Na+ in the plant divided by K+ : Na+ in the medium. Families where salt-secreting glands were commonly present in the species whose selectivity is included are marked with a ‘§’ (salt bladders present in members of the Aizoaceae and Chenopodiaceae do not secrete salt but act as an additional storage compartment): in the Poaceae, there was no apparent difference in SK:Na between species with and without salt secreting glands. The data were collected for species listed in Aronson (1989; plus some glycophytes), where there are also data for the sequence of the gene that encodes the large subunit of ribulose-1,5-bisphosphate carboxylase (rbcL). The averages for the Dicotyledonae and Monocotyledonae were calculated from the full dataset, which is available in the Supporting Information, Table S2.

  • na, not available.

  • a

    n is the number of species for which the selectivity was calculated.

  • b

    Low, 20–100 mm;

  • c

    medium, 101–201 mm;

  • d

    high, 202 mm NaCl and above.

Aizoaceae7 (4)4 (3)16 (5)
Asteraceae18 (4)16 (4)14 (7)
Avcenniaceae§10 (1)5 (3)10 (9)
Brassicaceae7 (2)9 (1)12 (1)
Chenopodiaceae4 (16)6 (31)9 (39)
Cyperaceae15 (7)nana
Juncaginaceaenana22 (2)
Plantaginaceae6 (2)6 (2)9 (2)
Plumbaginaeae§20 (5)23 (6)21 (6)
Poaceae22 (5)42 (7)60 (11)
Rhizophoraceae13 (1)10 (2)13 (12)
Tamaricaceae§na12 (2)9 (3)
Dicotyledoneae11 (42)12 (67)11 (89)
Monocotyledoneae18 (12)42 (7)48 (20)

There are interesting, but unexplained, differences in selectivity amongst the dicotyledonous halophytes: the Brassicaceae and the Chenopodiaceae have, for example, lower net SK:Na at salt concentrations below c. 200 mm than the Asteraceae; the Plumbaginaceae, characterized by the presence of salt glands, have higher net SK:Na values than the Tamaricaceae, another family where many of the species have salt glands. Wang et al. (2002) reported Na+ and K+ in different parts of a range of plants and, for S. salsa, demonstrated differences in selectivity on the path between root and shoot: selectivity between the base and the top of a stem branch was almost twice that between the shoot and the medium (i.e. the overall net SK:Na). This approach could be used more widely to evaluate differences between net fluxes in components of the transport path. In terms of the understanding of salt tolerance and its evolution, it will be important to determine whether apparent differences in net SK:Na between species reflect variations in the physiological and biochemical bases of salt tolerance.

3. Uptake and accumulation of Cl

There has been surprisingly little emphasis on Cl in investigations of the ion relations of halophytes, perhaps reflecting the ease of measurement of Na+ and K+. Flowers et al. (1986) noted that Cl : (Na++ K+) ratios were generally < 1 in the cells of halophytes, speculating that this might be the result of the greater toxicity of Cl than organic anions to protein synthesis, but this was based on few data. Since then, the situation has changed little. It is clear that halophytes do accumulate significant concentrations of Cl in their shoots, but that (Na++ K+) exceeds Cl by c. 35% in dicotyledonous species and by at least double in grasses (Table 5).

Table 5.  The ratio of Na+ and K+ to Cl in some halophytes
SpeciesNa+/Cl(Na++ K+)/ClExternal NaCl concentration (mm)Reference
Aster tripolium (Asteraceae)1.031.32300Ueda et al. (2003)
Suaeda fruticosa (Chenopodiaceae)1.231.35200Khan et al. (2000)
Plantago coronopus (Plantaginaceae)1.311.37500Koyro (2006)
Armeria maritima (Plumbaginaeae)0.741.19200Kohl (1997)
Reaumuria hirtella (Tamaricaceae)1.651.83448Ramadan (1998)
Sporobolus virginicus (Poaceae)2.263.29300Marcum & Murdoch (1992)
Diplachne fusca (Poaceae)0.982.14200Warwick & Halloran (1991)
Hordeum marinum (Poaceae)0.421.40300Garthwaite et al. (2005)

The uptake of Cl from low external concentrations is thought to be via Cl : 2H+symport, but at the higher concentrations at which halophytes normally grow, influx is likely to be via an anion channel while the Cl concentration remains low in the cytoplasm and if the membrane is depolarized (Tyerman & Skerrett, 1999; White & Broadly, 2001). The concentration of Cl in leaf cytoplasm of S. maritima growing in 340 mm NaCl has been estimated to be c. 90 mm (Flowers & Yeo, 1988); if this concentration difference existed across the root plasma membrane, the Nernst potential would be c. −33 mV. Uptake into the vacuole could be mediated by H+ exchange. Interestingly, a bumetanide-sensitive cation-Cl co-transporter has recently been discovered in arabidopsis (Colmenero-Flores et al., 2007), which warrants further investigation in halophytes; we are not, however, aware of any studies of Cl transporters or Cl channels in terrestrial halophytes.

There has long been a suggestion for a role for vesicular transport of ions in plant cells (Lüttge & Higinbotham, 1979), supported by the localization of ATPase activity (Hall, 1970). Localization of Rb+ (Field et al., 1980) and Cl (Balnokin et al., 2007) in vesicles in the cells of Suaeda species lends some support to suggestions of vesicular transport mechanisms (Glenn et al., 1999), one attraction of which is the separation of ions from enzymes even within the cytosol.

IV. Conclusions and perspectives

  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information

1. Conclusions on the physiology of salinity tolerance in halophytes

Halophytes show a diversity of growth responses to increasing salinity, from a dramatic stimulation to inhibition. To what extent there is also a diversity of mechanisms remains to be resolved. All halophytes display a common need to regulate cellular Na+, Cl and K+ concentrations as they adjust to the external water potential. As with plants in general, the proteins involved in transport of these ions are uncertain. There is a clear difference in the balance of Na+ and K+ used by different halophytes, as exemplified by the high values of net SK:Na in monocotyledonous halophytes and differences in net SK:Na between families of dicotyledonous halophytes. The regulation of the large fluxes of Cl is also largely unstudied. In some species, salt glands aid the maintenance, over time, of relatively constant shoot ion concentrations; in others, growth and ion accumulation are tightly coupled to achieve the same end, some also displaying increased succulence. The Na+ and Cl must largely be compartmentalized into vacuoles, with production of a range of compatible solutes for the cytoplasm. Just how halophytes manage to regulate the constancy of their ion concentrations requires further investigation, as does what must be a co-ordinated network of gene regulation; neither sensors nor signalling cascades are known.

There is clearly still much to learn about halophytes and the diversity of mechanisms that they employ to cope with salinity. A fundamental question to tolerance is how plants discriminate between Na+ and K+, and whether this differs between closely and distantly related species. An ancillary question is the functional roles of efflux to the medium as well as transport to the shoot. There are clearly innumerable other specific questions; examples are the mechanism(s) of Cl transport, the energetics of ion transport and compartmentation, the regulation of ion transport, the cause(s) of growth reduction at high salinity, the influence of O2 supply on transport (Colmer & Flowers, 2008), the importance of transpiration in ion accumulation in the shoot, and the control of stomatal aperture in halophytes, topics not covered in this review. Answering such questions requires not only the use of modern molecular genetic techniques, but also a good understanding of the basic physiology and growth requirements. A consequence of the large number of halophytic species, spread across some 500 genera of flowering plants, is that choosing ‘models’ (see later) is likely to be essential if real progress in understanding the mechanisms of tolerance is to be made. Ideally, such models need to reflect mechanisms of tolerance seen across the spectrum of halophytes, be amenable to experimental treatments and be open to genetic analyses. As tolerance is complex and halophytes are found in a range of environments, we firmly believe that a number of species need be considered. Important questions are: (i) whether all halophytes tolerate salt in, fundamentally, the same way; (ii) whether specific mechanisms can be identified and, if so, whether these are linked taxonomically; and (iii) whether specific mechanisms have evolved to deal with interactions between salinity and other environmental variables (e.g. flooding; Colmer & Flowers, 2008). If so, are these common to different taxonomic groups and how often has salt tolerance evolved?

2. Perspectives for future research on halophytes

Comments on some of the approaches used The future use of comparative physiology, coupled with genomic, proteomic and metabolomic approaches, should yield much new information on salt tolerance. It will be possible to test the view that halophytes have similar ‘salt tolerance genes’ to glycophytes (Zhu, 2000), and so similar regulatory networks to those found in glycophytes, but with different thresholds. Comparisons between T. halophila and arabidopsis (Inan et al., 2004) should enable this, and other specific related hypotheses, to be tested. Current knowledge on responses to NaCl, at the molecular level, of T. halophila and M. crystallinum were described in preceding sections, and use of these species is highlighted below in Section IV.2, ‘Use of model species to enhance future research’. In addition, expressed sequence tags for other halophytic species are beginning to be published (Chen et al., 2007; Wang et al., 2007b), as are cDNA-AFLP (Baisakh et al., 2006) and protein separation and analyses (Askari et al., 2006), as means of evaluating differential expression of genes.

In comparative studies of glycophytes and halophytes it should, however, be recognized that what is considered a ‘normal’ (low) salinity for a glycophyte is not ‘normal’ for a halophyte. For halophytes, salinity is the norm: it need not be stressful. Stressful situations, as indicated by reduced growth rates, occur at low and high salinities. Consequently, care is required in interpreting differences in gene expression between halophytes and glycophytes growing in saline conditions in terms of the multitude of ‘stress-related’ regulatory pathways that have been described (Chen & Zhu, 2004; Sreenivasulu et al., 2007); ‘controls’ with zero NaCl would not typically be apposite for halophytes, and dose-response experiments should cover a range of appropriate external NaCl concentrations.

Many studies have assessed responses to sudden increases in external salinity. Although halophytes can adjust to sudden changes in external salinity over a period of 24–48 h (Clipson & Flowers, 1987; Hasegawa et al., 2000), as in other plants, initial responses to an upshock are presumably to the osmotic component of the imposed NaCl treatment. Changes in turgor can be rapidly transmitted throughout plants, but how this change is sensed is still uncertain (Bartels & Sunkar, 2005; Chinnusamy et al., 2005). It must also be questionable whether pressure sensing would be effective in halophytes if these plants operate at low turgor (Clipson et al., 1985; Balnokin et al., 2005; James et al., 2006). As Na+ and Cl enter the cytosol, these ions are presumably also sensed, but again how this is achieved is not known. Subsequently, a range of signal transduction pathways, perhaps involving SOS1 and Ca2+, as has been identified using glycophytes (Hasegawa et al., 2000; Bartels & Sunkar, 2005), would presumably by involved; these should be further explored in both glycophytes and halophytes. Regulation of adaptive processes involved in tolerance to high, prolonged salinity, although not as easy to ascertain as short-term changes, also require elucidation.

Use of model species to enhance future research  A close relative of arabidopsis, described initially as Thellungiella halophila, has been promulgated as a valuable model halophyte, owing to its genetic proximity to arabidopsis and salt tolerance (Bressan et al., 2001; Zhu, 2001; Inan et al., 2004; Taji et al., 2004; Amtmann et al., 2005). Although the salt tolerance of T. halophila is clearly superior to that of arabidopsis, and the genetic tools available will expedite research on this species, its relevance to other halophytes needs to be determined. Firstly, salt tolerance of T. halophila is substantially lower than in many other halophytes. Although T. halophila survives in 500 mm NaCl (Inan et al., 2004) and it is claimed that its growth is unimpeded in 150 mm NaCl (Gong et al., 2005; although see substantial inhibition in Inan et al., 2004; Fig. 1), others have found signs of chlorosis after 2 wk in salt concentrations above 200 mm (Vera-Estrella et al., 2005). Secondly, T. halophila is in a family (the Brassicaceae) with relatively few halophytic species (c. 19 in five genera), as compared with the two major groups of halophytes, the Chenopodiaceae and the Poaceae; the Chenopodiaceae has over 380 halophytic species and the Poaceae over 140 (Flowers et al., 1986).

Another species, in addition to T. halophila, that is well established as a model in halophyte research is Mesembryanthemum crystallinum (Adams et al., 1998; Bohnert & Cushman, 2000). This species not only tolerates high concentrations of salt and accumulates inositol and its derivatives, but is also able to switch the pathway of photosynthetic carbon assimilation from C3 to CAM; M. crystallinum also has bladder cells that have been investigated with respect to their ability to accumulate ions. Although M. crystallinum has the complication of changing the nature of its photosynthesis, it is in an order, the Caryophyllales, which includes the Chenopodiaceae and Aizoaceae, families with significant numbers of halophytic species. However, it is important to remember that the majority of halophytes do not utilize glands or external bladders to modulate their tissue ion concentrations. Further investigation of the mechanisms of salt tolerance in a genus such as Suaeda therefore seems warranted. Suaeda is representative of a group of very tolerant halophytes with highly succulent leaves and able to accommodate ions without the need for secretion via salt glands.

The clear difference in the use of Na+ and K+ between mono- and dicotyledonous halophytes and the great importance of cereals as crops means that salt tolerance in monocotyledonous halophytes should be further investigated. Here the differences between species with and without salt glands and those tolerant and sensitive to flooding need to be taken into account. Because of the importance of members of the Triticeae as crops, it would seem pertinent that halophytic relatives of wheat and barley (species of Thinopyrum and Hordeum) should be investigated. Other potential monocotyledonous models to be considered are species of Distichlis, Spartina and Puccinellia.

In Table 6 we have summarized the attributes of some halophytes that might be used as models. The use of model species on which to concentrate research does carry a risk. If salt tolerance has evolved on numerous occasions, as seems likely, and if tolerance does not always rely on the same mechanisms, as we have suggested, then understanding the diversity of mechanisms is important. Conceivably, halophytes might use the same range of transporters and regulatory networks seen in other, less tolerant, species but with different set points; less likely is that they may use novel transporters and regulatory networks. Comparisons of mechanisms in different species will be vital for achieving this understanding. However, in the immediate future, it may be efficient to concentrate effort on a few species, with choices based on the criteria outlined earlier as well as other important features such as ploidy (diploids being preferred for genetic aspects) and genome size, as technological developments in sequencing might remove reliance on species with genomes that are already sequenced, or close relatives of these. Finally, other aspects, such as an annual habit to enable ease of experimentation and amenability to genetic transformation and plant regeneration, will also be important considerations in the selection of ‘model’ halophytes for future research.

Table 6.  Representative halophytes offering potential as models for the study of salt tolerance
FamilyApproximate number of halophytic species in the familyaEstimated percentage of C3 speciesbRepresentative generaNumber of papersc published between 1997 and Nov-2007 abstract (title)Notes (C is the amount of DNA in the unreplicated gametic nucleusd)
  • a

    Based on Aronson (1989).

  • b

    Based on the known and predicted pathways of photosynthesis in Aronson (1989): the Aizoaceae are the only one of the listed families with a significant number (9%) of species using CAM.

  • c

    The Web of Science was searched (09 Dec 07) for ‘((salt or salin*) or halophyt*) and genus’ or in the case of Hordeum, ‘((salt or salin*) or halophyt*) and ((Hordeum marin*) or (Hordeum marit*))’for papers published between 1997 and 2007; the number in parentheses is the number of papers where the terms occur in the title alone. Searching for ‘arabidopsis’ as the genus yielded 1813 papers, with 188 in which the terms appeared in the title alone.

  • d

    For comparative purposes, the C-value for Arabidopsis thaliana is 0.16 pg (

Aizoaceae5281Mesembryanthemum212 (34)Succulent dicotyledonous plants. M. crystallinum has inducible CAM and salt bladders. Easily cultivated and an established ‘model’ (Bohnert & Cushman, 2000). The taxonomy of the Aizoaceae is ‘volatile’; many species are succulent xerophytes. C-value of M. crystallinum is 0.43 pg
Avicenniaceae19100Avicennia 204 (18)A. marina is a mangrove with salt glands and, being a tree, a potentially valuable model since there are few halophytic trees (see also Rhizophora, below). Its viviparous habit means seeds cannot be stored, so inconvenient
Brassicaceae19100Thellungiella 42 (21)T. halophila is a close relative of arabidopsis and has the attributes of arabidopsis as a genetic model species; its rosette form makes some physiological experiments difficult. The Brassicaceae does not have many halophytic species
Chenopodiaceae38157Atriplex242 (44)The chenopods are the largest group of halophytes. Succulent dicotyledonous herbs and shrubs. Some species possess salt bladders. Some are waterlogging-tolerant. Annual species of the genus Suaeda (e.g. maritima) are easily grown and manipulated experimentally, but as yet lack ‘genetics’
Salicornia201 (38)
Suaeda165 (44)
Plumbaginaeae60100Limonium62 (12)Dicotyledonous halophytes with salt glands and some unusual compatible solutes, including choline-0-sulphate and the betaines of β-alanine, proline, and hydroxyproline
Poaceae14336Distichlis69 (7)The Poaceae are the major group of monocotyledonous halophytes. Some species possess salt glands. Some are relatives of crops. Some species such as H. marinum (C-value, 5.5 pg) are waterlogging-tolerant and in the Triticeae. Species of Spartina are a valuable contrast to Hordeum, in having salt glands
Leptochloa22 (6)
Puccinellia85 (6)
Thinopyrum31 (4)
Spartina915 (88)
Hordeum marinum14 (4)
Rhizophoraceae31100Rhizophora165 (4)Rhizophora mangle is another mangrove (cf. Avicennia), but without salt glands; limited experimentally, as it is a tree. Viviparous habit means seeds cannot be stored, so inconvenient
Zosteraceae18100Zostera194 (9)A seagrass; the marine halophytes are not subject to the vicissitudes of the atmosphere and so are not representative of terrestrial halophytes. Z. marina has a C-value of 0.32 pg


  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information

We thank Rana Munns, Ed Barrett-Lennard and Suo-Min Wang for their comments on a draft of this review. UWA provides travel support for TJF as ‘Visiting Professor’ in the School of Plant Biology. TDC thanks the Grains Research and Development Corporation (GRDC) and the Future Farms Industries CRC for support to research halophytes in the Triticeae, and ARC-Linkage for research on potential use and the ecophysiology of halophytes.


  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information
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Supporting Information

  1. Top of page
  2. I. Introduction
  3. II. Growth and osmotic adjustment
  4. III. Uptake and transport of monovalent ions
  5. IV. Conclusions and perspectives
  6. Acknowledgements
  7. References
  8. Supporting Information

Table S1 Genes from halophytes used in the transformation of glycophytes

Table S2 K-Na selectivities at different external sodium concentrations in a range of halophytes and some glycophytes and, where known, an indication of the presence or absence of salt glands or bladders

Please note: Blackwell Publishing are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office.

NPH_2531_sm_Table S1.xls22KSupporting info item
NPH_2531_sm_Table S2.xls81KSupporting info item