Flooding tolerance in halophytes
Author for correspondence:
Timothy D. Colmer
Tel: +61 8 6488 1993
Fax: +61 8 6488 1108
Flooding is a common environmental variable with salinity. Submerged organs can suffer from O2 deprivation and the resulting energy deficits can compromise ion transport processes essential for salinity tolerance. Tolerance of soil waterlogging in halophytes, as in glycophytes, is often associated with the production of adventitious roots containing aerenchyma, and the resultant internal O2 supply. For some species, shallow rooting in aerobic upper soil layers appears to be the key to survival on frequently flooded soils, although little is known of the anoxia tolerance in halophytes. Halophytic species that inhabit waterlogged substrates are able to regulate their shoot ion concentrations in spite of the hypoxic (or anoxic) medium in which they are rooted, this being in stark contrast with most other plants which suffer when salinity and waterlogging occur in combination. Very few studies have addressed the consequences of submergence of the shoots by saline water; these have, however, demonstrated tolerance of temporary submergence in some halophytes.
Terrestrial halophytes can be defined as ‘plants that complete their 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 & Colmer, 2008). Many of the habitats occupied by terrestrial halophytes are not only saline, but also are prone to flooding (e.g. coastal mangroves and coastal and inland salt marshes), whereas others (e.g. salt deserts) rarely flood. Previous reviews of terrestrial halophytes (listed in Flowers & Colmer, 2008) have hardly touched upon the effects of combined salinity and flooding (with one exception; Ungar, 1991) although the adverse interactive effects of these stresses combined are now regarded as crucial in determining the failure of crops in many saline soils, and need also to be considered in the design of revegetation programmes for salt-affected lands (Barrett-Lennard, 2003).
Flooding typically causes soils to become anaerobic (Ponnamperuma, 1984). Soil hypoxia, and subsequent anoxia, result from biological consumption of O2 without effective replacement, because the flux of O2 into soils is c. 320 000 times less when soil pores are filled with water than when they are gas-filled (Armstrong & Drew, 2002). In addition to O2 deficiency in flooded soils, other compounds and ions that influence plant growth can accumulate, such as CO2, ethylene, Mn2+, Fe2+, S2− and carboxylic acids (Ponnamperuma, 1984; McKee & McKevlin, 1993; Greenway et al., 2006). Furthermore, when completely submerged (e.g. during deep floods or in the case of small seedlings), access of the shoot to O2 (and CO2) can also be diminished. If underwater photosynthesis is restricted by low CO2 and/or low light, less O2 is available to diffuse, where possible, through the plant body. Despite these challenges of flooding, together with those of salinity (Flowers & Colmer, 2008), some halophytes thrive in flooded saline soils, as evidenced by the high productivity of salt marshes; for example, the net primary productivity in Spartina marshes can exceed 40 t dry matter ha−1 yr−1 (Long & Woolhouse, 1979).
Plant responses to flooding events will be determined by the timing, duration, and depth of the floods (cf. Setter & Waters, 2003) and plant genotype (e.g. Voesenek et al., 2006). For coastal marshes, tides will flood some areas daily and others less frequently (e.g. monthly or seasonally), with the depths and durations of floods dependent on height relative to mean sea level (Armstrong et al., 1985; Silvestri et al., 2005). Many coastal marshes can also be prone to storm surges, and these events might increase as sea levels rise (Reed, 2002). For inland marshes (e.g. salt lakes), flooding events occur during periods of high precipitation, and can be prolonged (Egan & Ungar, 2000; Pedersen et al., 2006), depending on prevailing weather conditions and the surrounding catchment that influences water run-off onto, and possible flows from, these low-lying areas. The timing of flooding events can influence plant responses; important factors are growth stage (e.g. Sporobolus virginicus, Breen et al., 1977) and season (e.g. winter versus summer floods; warmer temperatures increase O2 demand) (van Eck et al., 2005). For transient waterlogging, the adverse effects on plants can occur during the event (Barrett-Lennard, 2003) as well as after the water recedes, especially if the remaining roots are superficial and the upper soil dries (e.g. Mediterranean-type environments with wet winters and dry summers).
The degree of flooding can determine species distributions within coastal salt marshes (Mahall & Park, 1976; Snow & Vince, 1984; Armstrong et al., 1985; Davy et al., 1990) and inland marshes (Ungar et al., 1979): examples in coastal marshes are Salicornia spp. (Mahall & Park, 1976) and mangrove communities (Ball, 1988). Further discussion of halophyte zonation is beyond the scope of the present short review (instead see Ungar, 1991); rather, the focus will be on physiological adaptations of halophytes to soil flooding and inundation, and possible interactive effects of flooding when combined with salinity. Adverse waterlogging × salinity interactions have been documented for annual crops, and in some woody perennials (Barrett-Lennard, 2003; see section ‘Interaction between waterlogging and salinity: is there evidence for adverse effects on ion regulation in halophytes?’), but the physiology of halophytes exposed to combined salinity and flooding has rarely been studied. In this short review we discuss tolerance of halophytes to soil waterlogging, possible adverse interactions between soil waterlogging and salt tolerance, and then submergence tolerance.
Tolerance of soil waterlogging
Mechanisms of flooding tolerance in plants include the capacity to develop a large adventitious root system (Jackson & Drew, 1984), aerenchyma formation and associated traits for effective internal aeration (Armstrong, 1979; Colmer, 2003) and anoxia tolerance in tissues (Gibbs & Greenway, 2003). This section will summarize knowledge of these adaptations to flooding in halophytes.
Production of adventitious roots is regarded as an important morphological trait contributing to waterlogging tolerance (Jackson & Drew, 1984). In many wetland species, adventitious roots dominate root biomass (e.g. the glycophytic Rumex spp.; Laan et al., 1989) and such roots also form in wetland halophytes (e.g. S. virginicus, Naidoo & Mundree, 1993; Halosarcia pergranulata, Pedersen et al., 2006). The influence of salinity on development of adventitious roots during flooding has, however, rarely been studied. Production of ‘aboveground’ (i.e. aquatic) roots was not influenced by salinity (highest treatment was 400 mM NaCl) in the perennial grass S. virginicus (Naidoo & Mundree, 1993), whereas saline floodwater reduced adventitious root formation in the salt-tolerant semi-xerophyte tree Eucalyptus camaldulenis (42 dS m−1; van der Moezel et al., 1988) and the halophytic tree Melaleuca ericifolia (49–60 dS m−1; Salter et al., 2007). In Casurina obesa, adventitious roots were produced in saline (42 dS m−1) floodwater, but these roots deteriorated in health compared with those of plants flooded with nonsaline water (van der Moezel et al., 1988). Further information is needed on whether salinity has specific effects on adventitious rooting, beyond those that would be expected as a result of overall reductions in growth at high external NaCl concentrations.
Aerenchyma and internal O2 movement
Aerenchyma consists of large interconnected gas channels that greatly enhance O2 movement into submerged portions of plants (Armstrong, 1979). The most comprehensive study of the capacity to develop root aerenchyma (quantified as gas volume per unit root volume, i.e. porosity) was a survey of 91 species (nonwetland, ‘intermediate’, and wetland plants) grown in nonsaline waterlogged conditions in pots (Justin & Armstrong, 1987); 19 of the species studied are listed as halophytes by Aronson (1989). Before we consider these data on root porosity for halophytes, the difficulty in distinguishing the ‘arbitrary boundary’ between halophytes and nonhalophytes (discussed in Flowers & Colmer, 2008) should be noted, and considered for Phragmites australis. Aronson (1989) included P. australis as a halophyte; however, P. australis occurs predominately in fresh waters, but also in brackish marshes. Phragmites australis‘types’ with relatively high salt tolerance have been described (e.g. Lissner & Schierup, 1997; Vasquez et al., 2006; Takahashi et al., 2007) and although P. australis occurs in some saline marshes, in some cases the plants have been shown to be accessing interstitial water of salinity considerably lower than that of the surface water (e.g. Lissner & Schierup, 1997; Adams & Bate, 1999), so that some authors have referred to P. australis as a ‘pseudo-halophyte’ (Adams & Bate, 1999). The majority of studies of internal aeration in P. australis have, with two exceptions (discussed later in this section), been conducted in fresh water.
Root porosity in the two ‘nonwetland’ halophytes (Festuca rubra and Cochlearia danica) was ~2 to 4%, in the four ‘intermediate’ halophytes (Halimione portulacoides, Suaeda maritima, Juncus bufonius and Lepidium latifolium) it was ~2 to 23%, in 13 of the ‘wetland’ halophytes (e.g. Cochlearia anglica, Salicornia europaea, Puccinellia maritima and Spartina anglica) it was ~3 to 33%, and in P. australis it was 52% (Justin & Armstrong, 1987). Although roots of some wetland halophytes developed high porosity (e.g. S. anglica, 33%; P. australis, 52%) the values (except for that of P. australis) were generally less than those in roots of several glycophytic wetland species in the study (e.g. Juncus inflexus, 53%) (Justin & Armstrong, 1987). Some halophytes can develop high root porosity (e.g. 48% in Spartina patens; Burdick & Mendelssohn, 1990) almost as high as in roots of glycophytic wetland species (cf. 53% in J. inflexus; Justin & Armstrong, 1987). Thus, we conclude that the range of root porosity in halophytes is similar to that in glycophytes and the limited data available indicate that, as in glycophytes, the capacity to develop high root porosity tends to be greatest in species originating from flood-prone habitats.
The study by Justin & Armstrong (1987) was conducted under nonsaline conditions. The question of whether salinity influences aerenchyma formation has been addressed on few occasions. Sporobolus virginicus grown in N2-bubbled solution contained 32% aerenchyma in rhizomes when in fresh water and 28% when in coastal water (~410 mM Na+) (Donovan & Gallagher, 1985). Naidoo & Mundree (1993) reported that salinity reduced the air spaces in the culm of S. virginicus; the area of aerenchyma decreased from 30–32% to ~22% when salinity was increased from 0 or 100 mM to 200 or 400 mM NaCl. By way of contrast, in Spartina alterniflora and S. patens, increasing salinity from 25 to 325 mM NaCl did not affect root porosity measured as root specific gravity (Naidoo et al., 1992). The lack of influence of salinity on root porosity in S. patens is consistent with the high porosity (48%) of roots collected from plants growing in a salt marsh (Burdick & Mendelssohn, 1987).
In addition to high porosity, other features also enhance the capacity for longitudinal O2 diffusion in roots (e.g. root diameter, numbers of laterals, relative stele volume, and a barrier to radial O2 loss (ROL)) (Armstrong, 1979; Colmer, 2003). A barrier to ROL in cell layers exterior to the aerenchyma is present in the basal zones of roots of numerous wetland species; the barrier restricts O2 losses to the rhizosphere, and thus enhances longitudinal diffusion towards the root tip (Armstrong, 1979; Colmer, 2003). For example, roots of waterlogging-tolerant species in the genus Hordeum, including the halophyte Hordeum marinum, form a barrier to ROL when grown in an O2-deficient stagnant medium (Garthwaite et al., 2003). In roots of H. marinum the barrier is formed by putative suberin deposits in cell walls in the hypodermal layer (Garthwaite et al., 2008); suberin deposits have also been implicated in barrier formation in roots of P. australis (Soukup et al., 2007). Whether salinity influences the formation of a barrier to ROL in roots of wetland halophytes that possess this feature, and whether having a barrier to ROL influences the regulation of ion ‘exclusion’ by roots in saline substrates, are both unknown.
Diffusion is the mechanism by which O2 moves along aerenchyma in roots (Beckett et al., 1988). In rhizomes of some wetland species, through-flows (i.e. pressure-driven mass flows of gas) occur, but even in these species O2 still diffuses into, and along, roots subtending rhizomes (Colmer, 2003). Through-flows along rhizomes (and petioles or culms) enable plants to grow deeper into waters and/or anoxic sediments (Vretare-Strand, 2002) than would be possible if O2 moved only via diffusion through the entire plant body. Such through-flows increase the O2 available to rhizomes at depth, and higher O2 at root–rhizome junctions enhances internal O2 supply to roots (through-flow mechanisms, as studied in water lilies and common reed, are reviewed in Colmer, 2003). Through-flows have been documented in several wetland species, including the halophyte S. alterniflora (Hwang & Morris, 1991).
The influence, if any, of salinity on through-flows has not been studied for halophytes; but through-flows have been evaluated for P. australis at brackish and low-salinity sites in Europe (Rolletschek et al., 1999; Rolletschek & Hartzendorf, 2000). At brackish sites, growth of P. australis was inhibited so that plants had smaller sheath areas and thinner culms than those in low-salinity sites; these changes reduced the ventilation capacity of the plants at the brackish sites. Resistances to flows in rhizomes (and/or exit culms) were also higher, further reducing ventilation in plants at the brackish sites compared with the low-salinity sites. Through-flows in halophytes might therefore also be influenced by salinity at sites where the salt concentration impedes shoot growth.
Shallow rooting in aerobic upper soil layers, in addition to some internal O2 movement, presumably contributes to the means by which some marsh halophytes (e.g. the annual species of Salicornia) with low root porosity (namely 3–6%) can tolerate flooding in salt marshes (Mahall & Park, 1976; Pearson & Havill, 1988a). In addition, tolerance of high sulphide concentrations might also contribute to the persistence of Salicornia spp. in marsh soils (Ingold & Havill, 1984). Superficial rooting presumably also contributes to survival of other salt marsh species with low root porosity (e.g. ~3% in the annual leaf-succulent Suaeda maritima, Justin & Armstrong, 1987), whereas for others (e.g. perennial Sarcocornia perennis) growth is restricted to nonreducing, well-drained sandy sediments in tidal marshes (Davy et al., 2006). Small, locally raised areas of sediments can also support ‘patches’ of S. perennis within some marshes (Davy et al., 2006). We have not been able to locate data on anoxia tolerance per se in salt marsh species with low root porosity, although ADH activity has been measured (e.g. Salicornia spp.; Pearson & Havill, 1988b). Anoxia tolerance might be important during short periods of tidal submergence, so it remains to be resolved whether this aspect of waterlogging tolerance differs between these marsh species with low root porosity and those with higher root porosity. Aspects of anoxia tolerance in roots of halophytes are discussed in the next section.
Even in species with large volumes of aerenchyma in rhizomes and roots, O2 deficiency can still occur in some parts of the roots in flooded soils (e.g. S. patens; Burdick & Mendelssohn, 1990). Deeper parts of root systems, and even some tissues within individual roots (e.g. apices and stele), may suffer suboptimal O2, while other parts remain aerobic (Armstrong, 1979; Armstrong et al., 2000). Tissue anoxia results in the cessation of oxidative phosphorylation, and thus a severe energy deficit. Anaerobic carbohydrate catabolism, together with other essential traits (e.g. regulation of ATP-consuming processes), enables survival during anoxia; the period of survival depending on the supply of carbohydrates, the species, and the tissue or organ (Gibbs & Greenway, 2003; Greenway & Gibbs, 2003). Fermentative metabolism provides at least some ATP during anoxia, albeit only 3 to 35% of the rate of energy production in aerobic cells (Gibbs & Greenway, 2003). The anoxia-tolerant coleoptiles of rice (Oryza sativa) (Huang et al., 2005; Lasanthi-Kudahettige et al., 2007) and anoxia-sensitive Arabidopsis (Klok et al., 2002; Gonzali et al., 2005), both glycophytes with sequenced genomes, have been used in comprehensive gene expression and proteomic studies. It is beyond the scope of the present short review to consider the findings of these studies in glycophytes; the point made here is that such studies are lacking for wetland halophytes as suitable genetic resources are not presently available.
Biochemical studies related to anoxia tolerance in wetland halophytes are largely restricted to assessments of alcohol dehydrogenase (ADH) activities in roots; even ethanol production data per se appear to be lacking. Several studies demonstrate large increases in ADH activity in roots of S. patens when in waterlogged (or O2-deficient) conditions (e.g. 6-fold in the first weeks after flooding, Burdick & Mendelssohn, 1990; 17-fold, Naidoo et al., 1992). Interestingly, although the increase in ADH activity was 17-fold at 25 mM NaCl, it was only 4-fold at 325 mM NaCl, a reduction attributed by Naidoo et al. (1992) to ‘unhealthy looking roots’ in the high-salinity treatment. By contrast, ADH activities in roots of S. alterniflora were much lower than in those of S. foliosa, and were not affected by increasing salinity from 25 to 325 mM NaCl (Naidoo et al., 1992). Nevertheless, induction of ADH in roots of S. patens by waterlogging in controlled pot experiments is consistent with 3- to 15.8-fold higher activities of this enzyme in roots of this species sampled from a marsh, compared with a dune, environment (Burdick & Mendelssohn, 1987). Thus, at least ADH in roots of halophytes appears to respond similarly to that in roots of some freshwater marsh species (e.g. Smith et al., 1986). We expect that other aspects of anoxic metabolism in halophytes will probably reflect those in glycophytes, although further studies, particularly to measure rates of ethanol production in anoxia and of pyruvate decarboxylase activity (the rate-limiting enzyme in conversion of pyruvate to ethanol, Gibbs & Greenway, 2003), should also be assessed for a range of halophytic species. In addition, the hypothesis of Rivoal & Hanson (1993) that alternative end-products to ethanol, especially lactate, might benefit whole-plant C balance for some halophytes with anoxic roots should also be further explored. We refer the reader to Gibbs & Greenway (2003) for further consideration of lactate production, as well as other end-products (e.g. alanine), during fermentative metabolism in plants. Anoxia tolerance and metabolism in halophytes should be assessed at a range of external NaCl concentrations.
Interaction between waterlogging and salinity: is there evidence for adverse effects on ion regulation in halophytes?
Few data are available for plant responses to combined waterlogging and salinity, and most of these studies have been conducted on species used in agriculture (mainly glycophytes; reviewed by Barrett-Lennard, 2003). Barrett-Lennard (2003) listed annual crops and woody perennials for which waterlogging × salinity interactions had been studied. In some of the glycophytic annual crops (e.g. Zea mays and Phaseolus vulgaris), waterlogging in saline conditions increased shoot Na+ concentrations above those in plants in drained (or aerated) saline root-zones by as much as 6-fold. In other species, increases in shoot Na+ concentrations ranged from 1.5- to 5.4-fold; the exception was Hordeum vulgare, which only showed a 10% rise in shoot Na+ concentration when waterlogging was combined with salinity (70 mM NaCl). The magnitude of the increase in shoot Cl− was similar to that of Na+ in some species (e.g. Lycopersicon esulentum and O. sativa), whereas it was less than for Na+ in others (e.g. Helianthus annuus and P. vulgaris). The higher Na+ and Cl− concentrations in shoots of plants exposed to combined waterlogging and salinity, as compared with salinity alone, had adverse effects on plant growth and survival (Barrett-Lennard, 2003). Poorly adapted species can suffer severe adverse effects from combined waterlogging and salinity.
Barrett-Lennard (2003) presented a persuasive analysis that suggested that the elevated shoot Na+ (and Cl−) concentrations occurred as a result of increased delivery of these ions to the shoots, presumably as a result of the low energy status of roots impairing ion transport processes that regulate net uptake. Root O2 deficiency would restrict respiration, so that membrane H+-ATPase activities and thus H+ gradients would be diminished, in turn reducing the capacity for ion transport across membranes, so that uptake of K+ and ‘exclusion’ of Na+ would both be inhibited (cf. Barrett-Lennard, 2003). For roots in hypoxic solution, the stele is likely to be the first tissue to suffer anoxia, a condition that can disrupt xylem loading (Gibbs et al., 1998) and presumably also retrieval of unwanted ions (i.e. Na+) from the transpiration stream. Low energy availability would also be expected to diminish Na+ efflux, one process that contributes to determining net Na+ uptake by roots. Thus, an energy deficit would compromise regulation of ion transport by the roots to the shoots. In longer term anoxia, membranes might deteriorate more generally (Gibbs & Greenway, 2003), and if this occurred, regulation of ion uptake would be further compromised. Thus, species with large volumes of root aerenchyma, which enables internal O2 transport to support respiration, would be expected to be better able to tolerate the combined effects of waterlogging and salinity than those with little aerenchyma (Barrett-Lennard, 2003).
Data were presented by Barrett-Lennard (2003) for only two genera with halophytic species: Atriplex (Atriplex amnicola, a shrub used for fodder) and Casuarina species (trees used in revegetation). Barrett-Lennard (2003) did not include data from Cooper (1982) for several salt marsh species in his analysis as the waterlogged saline treatment was established by addition of nonsaline water to a drained saline soil, so that salinity in the waterlogged saline treatment was unknown but would have been substantially lower than in the drained saline treatment (E. G. Barrett-Lennard, pers. comm.). A few Eucalyptus species regarded as being salt-tolerant were also in the list of Barrett-Lennard (2003); for these and the Casuarina species, waterlogging in saline conditions again increased shoot Na+ concentrations above those in plants in drained (or aerated) saline root zones, by 1.6- to 9.5-fold. In A. amnicola, however, shoot Na+ (and Cl−) only increased by 10% during the first 7 d of root-zone hypoxia (N2-flushed nutrient solution containing 400 mM NaCl), although by 14 d shoot Na+ and Cl− concentrations had increased, respectively, by 1.6- and 2.1-fold above the concentrations in plants in saline aerated nutrient solution (Galloway & Davidson, 1993). Barrett-Lennard (2003) suggested that, in A. amnicola, greatly reduced transpiration during combined waterlogging and salinity (Galloway & Davidson, 1993) might enable this species to restrict, at least initially, the flux of ions into the shoots.
Additional data to those analysed by Barrett-Lennard (2003) are available for growth and tissue ion concentrations in halophytes exposed to combined waterlogging and salinity (Table 1). When waterlogging was imposed in addition to salinity, shoot growth was inhibited in several species; for example in Casuarina glauca, dry mass was 74% of that under drained saline conditions. By contrast, in several species growth declines were only moderate, and in a few (e.g. Puccinellia maritima and S. alterniflora) growth was even stimulated. In stark contrast to the data presented for glycophytes by Barrett-Lennard (2003), for the 14 halophytes in Table 1 shoot Na+ concentrations only increased significantly (1.4- to 5.0-fold) in five species. In the other nine species, waterlogging only caused slight increases in shoot Na+ concentration, did not influence it, or even reduced it (namely 71% to 111% of values in shoots of plants in drained or aerated saline treatments). Those species tolerant of combined waterlogging and salinity, not surprisingly, typically inhabit flooded saline soils.
Table 1. The influence of waterlogging on shoot ion (Na+, K+ and Cl−) concentrations1 in halophytes, under saline conditions2
|Glaux maritima||Sand culture, 300 mM NaCl, D or WL to soil surface, ~2 months at 15°C (data also available for 150 mM NaCl and for +50 mm WL) ||Growth shoot FM||~1||1140||1.07||361||1.24||NA||NA||Rozema et al. (1978)|
|Juncus gerardii||Compost:sand mixture (1 : 1), D or WL to soil surface, 50% seawater (i.e. 240 mM Na+), 6 wk at 20°C, RH 80% (data also available for +50 mm WL). ||Growth: shoot DM||0.84||688||1.05||771||0.79||NA||NA||Rozema & Blom (1977)|
|Agrostis stolonifera||As above||As above||1.14||278||1.4||480||0.85||NA||NA||Rozema & Blom (1977)|
|Salicornia dolichostachya3||Nutrient solution, aerated or N2-flushed, 150 mM NaCl, 8 wk at 22 : 18°C d:n, RH 80% (Experiment 1)||Growth: whole plant RGR||0.81||6870||0.9||720||0.61||NA||NA||Schat et al. (1987)|
|Salicornia ramosissima||As above||As above||0.85||7740||0.91||760||0.58||NA||NA||Schat et al. (1987)|
|Spartina alterniflora||Marsh sediment with artificial seawater, waterlogged to +150 mm undisturbed or with aeration of the sediment, 3 months (data available for 15, 30 and 45 ppt salinity; 30 ppt plus mineral N treatment presented here)||Growth: above-ground DM||3.3||883||1.05||330||1.12||NA||NA||Linthurst & Seneca (1981)|
|Juncus kraussii||River sand: potting mix (3 : 1), D or WL to +50 mm, nutrient solution and 70% seawater, 10 wk at 25°C (other dilutions of seawater, below 70% also used)||Growth: total DM||~1||*~430 mM||1.12||*~180 mM||1.05||*~900 mM||1.22||Naidoo & Kift (2006)|
|Ions: shoots (culms), on tissue water basis|
|Atriplex amnicola||Solution culture, aerated or N2-flushed, 400 mM NaCl, 14 d with 19 : 8°C d:n||Growth: shoot EtOH-insoluble DM||0.98||9840||1.59||820||0.87||7000||2.08||Galloway & Davidson (1993)|
|Ions: leaves, on EtOH-insoluble DM basis|
|Casuarina glauca||Sand culture, D or WL to +10 mm, salinity used 10:2:1 Na:Mg:Ca, reached 5600 mS m−1 in the final 2 wk of a 12 wk treatment, 27 : 12°C d:n||Growth: shoot DM||0.74||152||3.89||315||0.95||271||2.67||van der Moezel et al. (1989)|
|Ions: shoot (values are means of 6–9 accessions)|
|Casuarina obesa||As above||As above||0.79||122||5.04||248||0.90||214||3.43||van der Moezel et al. (1989)|
|Casuarina obesa||Sand culture, D or WL, 400 mM NaCl, 22 d at 25 : 20°C d:n (lower salinity levels also used) ||No growth data (but gas exchange data)||NA||*~130 mM||2.31||*~190 mM||0.79||*~160 mM||1.75||Carter et al. (2006)|
|Ions: cladodes, on tissue water basis|
|Melaleuca cuticularis||As above||No growth data (but gas exchange data)||NA||*~280 mM||1.11||*~145 mM||0.97||*~200 mM||1.35||Carter et al. (2006)|
|Ions: leaves on tissue water basis|
|Avicennia marina||Mangrove sediment, D or WL to +50 mm, 33% sea water, 60 d at 25°C ||No growth data||NA||722||1.07||340||0.89||NA||NA||Naidoo (1985)|
|Rhizophora mucronata||As above||As above||NA||318||0.95||33||1.62||NA||NA||Naidoo (1985)|
|Bruguiera gymnorrhiza||As above||As above||NA||239||1.35||102||1.1||NA||NA||Naidoo (1985)|
|1 Tissue ion data in µmol g−1 dry mass, except where indicated by * as being mM on a tissue water basis.|
|2 Data in Cooper (1982) for several salt marsh species were not considered, as the waterlogged saline treatment was established by addition of nonsaline water to a drained saline soil. Thus, salinity in the waterlogged saline treatment was unknown but would have been substantially lower than in the drained saline treatment (E. G. Barrett-Lennard, pers. comm.).|
|3Salicornia dolichostachya was also studied by Rozema et al. (1987). After 9–12 wk at 250 mM NaCl, WL/D for shoot DM was 1.39, for shoot Na+ 0.78, and for shoot K+ ~1. Values are not included in the table as the units for shoot Na+ and K+ were uncertain.|
|D, drained; WL, waterlogged. Experiments that used nutrient solution with low O2 treatment and aerated controls are also included in the table (see column ‘Growth conditions’).|
|d, day; DM, dry mass; EtOH, ethanol; FM, fresh mass; n, night; NA, not available; ppt, parts per thousand; RGR, relative growth rate; RH, relative humidity.|
Tolerance to combined waterlogging and salinity is not simply related to root porosity, as species differing widely in this parameter (e.g. 3–6% in Salicornia spp. vs 50% in S. alterniflora; section ‘Aerenchyma and internal O2 movement’) did not suffer adverse effects on shoot ion concentrations from combined waterlogging with salinity (Table 1). Moreover, although species with salt glands should be able to remove any extra Na+ (and Cl−) delivered to shoots when in combined salinity and waterlogging (cf. Barrett-Lennard, 2003), maintenance of shoot Na+ concentrations by the various species in Table 1 was not simply related to the presence or absence of salt glands. Interestingly, some wetland halophytes might be sensitive to soil drying (drought and concentrating of ions in soil), rather than to soil waterlogging (e.g. S. alterniflora; Brown et al., 2006).
Tolerance of complete submergence (inundation)
When shoots become completely submerged (e.g. during deep floods or in the case of small seedlings) direct access to atmospheric O2 (and CO2) is prevented. Instead, the O2 potentially available to plants is that in the water column or that produced internally via photosynthesis (e.g. the halophyte H. pergranulata; Pedersen et al., 2006). The O2 supply to roots will depend upon the concentration in the shoots, as well as physical resistances and consumption rates along the diffusion pathway (Armstrong, 1979). Shoot O2 concentration is highest during light periods, as a result of underwater photosynthesis; thus, submerged plants experience diurnal changes in tissue O2 (Sand-Jensen et al., 2005; Pedersen et al., 2006). During dark periods, roots can become anoxic and fermentative metabolism is engaged (e.g. in the glycophyte rice; Waters et al., 1989). In many wetland species, shoot extension is promoted during submergence, so that leaves reach flowing water containing O2 or adequate light for photosynthesis, or shoots can even emerge above the floodwaters to establish contact with air (Voesenek et al., 2006). The adaptive value of such an elongation response, however, depends on the depth and duration of flooding in the habitat (studied for numerous glycophytes; Voesenek et al., 2004).
Tolerance of complete submergence by halophytes has rarely been studied. Notable exceptions are growth experiments using (artificial) tidal submergence which showed greater tolerance of submergence in a coastal, compared with an inland, species of Salicornia (Langlois & Ungar, 1976); and those assessing submergence tolerance, as influenced by NaCl concentrations, in S. perennis (Adams & Bate, 1994) and in S. maritima (Adams & Bate, 1995). Stem elongation when submerged was much slower in the marsh species S. perennis, which would naturally experience short periods of tidal submergence (Adams & Bate, 1994), as compared with some glycophytic wetland species that experience more prolonged floods (c.f. Voesenek et al., 2004). For both S. perennis and S. maritima studied by Adams & Bate (1994, 1995), no severe interaction of increasing salinity × submergence was evident. By contrast, when submerged at low salinity, S. perennis suffered injury, an effect attributed to swelling of succulent shoot tissues as a result of high osmotic gradients for water entry into these tissues (Adams & Bate, 1994).
The influence of submergence on shoot ion relations in halophytes requires further study. Transpiration would cease with complete submergence so that delivery of ions from the roots would presumably decline; however, for shoots in direct contact with floodwaters, ions might be taken up directly into the tissues, particularly those ions at high concentrations (i.e. Na+ and Cl−). However, ions (and other solutes) might also be ‘leached’ from the shoots to the floodwaters. Loss of 32P has been reported for submerged leaves of S. alterniflora (Reimold, 1972), a phenomenon considered by the author to be ‘leaching’ from the tissues, as described for solute losses from wet leaves of many species, although leaching of P is generally low (Tukey, 1970). Reimold (1972) did not discuss whether 32P loss from S. alterniflora leaves might also occur via salt glands. Although glands can secrete a range of ions (e.g. S. anglica; Rozema et al., 1991), phosphate was not secreted by glands of Leptochloa fusca (Gorham, 1987; Klagges et al., 1993), supporting the view that phosphate (and other solutes) might be lost from submerged leaves via ‘leaching’ rather than secretion. These processes should be evaluated for a range of halophytes with and without salt glands.
In addition to the growth experiments on salinity × submergence interactions under laboratory conditions described above, submergence responses in situ have been evaluated for the halophytes S. alterniflora (brackish tidal river marsh; Gleason & Zieman, 1981) and H. pergranulata (saline inland lake with 31 g salts l−1; Pedersen et al., 2006). For S. alterniflora, tidal inundation during darkness resulted in depletion of O2 in the shoot base from ~10 kPa to below detection, whereas in the light O2 only declined to ~5 kPa. Underwater photosynthesis during light periods presumably contributed to tissue O2 status during tidal inundation (Gleason & Zieman, 1981). The marked differences in tissue O2 concentrations during light/dark periods when submerged were confirmed for the shoot and roots of the halophytic stem-succulent H. pergranulata, both in situ during a diurnal cycle in a salt lake and in plants in sediment transplants under artificial conditions (Pedersen et al., 2006). The consequence (if any) of anoxia in at least some tissues during dark periods, for salt tolerance in halophytes, requires further elucidation.
Flooding is a common environmental variable in many habitats occupied by halophytes. Tolerance of soil waterlogging in halophytes, as in glycophytes, is often associated with the production of adventitious roots containing aerenchyma, so that internal O2 movement largely prevents tissue anoxia. For some species with low root porosity, however, shallow rooting in aerobic upper soil layers appears to be the key to survival on frequently flooded soils, although little is known of the anoxia tolerance in halophytes. Halophytic species that typically inhabit waterlogged substrates are able to regulate their shoot ion concentrations in spite of the hypoxic (or anoxic) medium in which they are rooted, this being in stark contrast with most other plants which suffer when salinity and waterlogging occur in combination (Barrett-Lennard, 2003). Tolerance to combined waterlogging and salinity is not simply related to the amount of root porosity. Future research on waterlogging and submergence tolerances in halophytes, as also suggested for salinity tolerance (Flowers & Colmer, 2008), should, at least initially, be focused on selected ‘model’ species representative of various mechanisms that might be involved in tolerance of flooding (see above) and salinity (see Flowers & Colmer, 2008).
We thank Ed Barrett-Lennard for comments on a draft of this review. The University of Western Australia provides 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 the potential use and the ecophysiology of halophytes.