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, Volume 24, Issue 2, pp 199–217 | Cite as

Salt tolerance mechanisms in mangroves: a review

  • Asish Kumar Parida
  • Bhavanath Jha
Review

Abstract

Mangroves are woody plants which form the dominant vegetation in tidal, saline wetlands along tropical and subtropical coasts. The current knowledge concerning the most striking feature of mangroves i.e., their unique ability to tolerate high salinity is summarized in the present review. In this review, we shall discuss recent studies that have focused on morphological, anatomical, physiological, biochemical, molecular and genetic attributes associated with the response to salinity, some of which presumably function to mediate salt tolerance in the mangroves. Here we shall also review the major advances recently made at both the genetic and the genomic levels in mangroves. Salinity tolerance in mangroves depends on a range of adaptations, including ion compartmentation, osmoregulation, selective transport and uptake of ions, maintenance of a balance between the supply of ions to the shoot, and capacity to accommodate the salt influx. The tolerance of mangroves to a high saline environment is also tightly linked to the regulation of gene expression. By integrating the information from mangroves and performing comparisons among species of mangroves and non-mangroves, we could give a general picture of salt tolerance mechanisms of mangroves, thus providing a new avenue for development of salt tolerance in crop plants through effective breeding strategies and genetic engineering techniques.

Keywords

Antioxidant Compatible solutes Mangrove Na+/H+ antiporter Salt tolerance Salt secretor Salt exclusion Propagules Viviparous 

Introduction

True mangroves and mangrove associates

Mangroves are constituent plants of tropical intertidal forest community. They include woody trees and shrubs, which flourish in the zone between land and sea along the tropical coastline of the globe. They fall into two groups according to their habitats in nature: true mangroves and mangrove associates. True mangroves occur only in mangrove habitat and their existence is rare elsewhere such as Rhizophora, Kandelia, Ceriops, Bruguiera, Avicennia, Xylocarpus, Aegiceras, Sonneratia, Laguncularia, Lumnitzera, Nypha etc. Mangrove associates are non-exclusive mangrove species occurring in the landward margin of mangal and often non-mangal habitats such as rainforest, salt marsh or lowland freshwater swamps (e.g. Excoecaria, Camptostemon, Pemphis, Osbornia, Pelliciera, Aegialitis, Acrostichum, Scyphiphora, Heritiera etc.). Heritiera fomes is a true mangrove with tolerance to high-saline conditions (Santisuk 1983; Naskar and Mandal 1999), but the status of H. littoralis as mangrove is controversial. The species H. littoralis has been described by most of the authors as fresh water loving back mangal or mangrove associate (Kartawinata et al. 1979; Mukherjee et al. 2003), whereas a few authors have described it as true mangrove (Das et al. 1994; Tam et al. 1997; Parani et al. 1998). Mangroves are taxonomically diverse. True mangroves include about 54 species in 20 genera belonging to 16 families (Hogarth 1999). Mangroves grow in the intertidal zone between land and sea. They are frequently inundated by tide leading to waterlogging and fluctuation in salinity (Naidoo et al. 2002; Sengupta and Chaudhuri 2002; Paliyavuth et al. 2004; Jagtap and Nagle 2007). Like other marine organisms, they are exposed to the air and thus to the risk of desiccation and overheating; on the other hand they face waterlogging and salinity (Naidoo et al. 2002; Sengupta and Chaudhuri 2002; Paliyavuth et al. 2004; Jagtap and Nagle 2007). Under high temperature conditions in tropics the above problems become worse. Firstly, at low tide, overheating and desiccation is greater, and secondly, through evapotranspiration, any water that remains may become even more highly saline than that of the open sea. At high tide, the warmth of water lowers the oxygen in water (Hogarth 1999). High salinity makes it more difficult for mangroves to extract water from the soil, even though the soils on which mangroves grow are usually waterlogged. Consequently, many mangrove species have morphological characteristics and high water-use efficiencies characteristic of terrestrial xerophytes (Clough et al. 1982; Ball 1988a; Clough and Sim 1989).

Economic and ecological importance of mangroves

The mangrove forests have enormous economic potentiality and utilitarian value at the ecosystem as well as at the component levels (Robertson and Alongi 1992; UNEP-WCMC 2006). Mangroves have been playing a significant role in the economy of tropical societies for thousands of years, providing a wide variety of goods and services including wood production, support for commercial and subsistence fisheries, salt production and shoreline protection and coastal erosion control (Hamilton and Murphy 1988; Krauss et al. 2008). Mangrove trees are good sources of firewood for local communities; their wood makes a superior kind of charcoal and is a source of tannins, resins, medicines, etc. (Hamilton and Murphy 1988; Baconguis and Mauricio 1991). Many of the animals found within the mangal are harvested for food: fish, crabs and prawns in particular. Therefore, mangrove trees are very important for conserving and maintaining mangrove ecosystems. Mangrove ecosystems constitute a refuge, feeding ground and nursery for species of cyanobacteria, red algae, manglicolous fungi, invertebrates, fish and shrimp (Martosubroto and Naamin 1977; Sheridan 1991; Turner 1992; Sasekumar et al. 1992; Hyde and Lee 1995; De Graaf and Xuan 1999). Reptiles, including crocodiles, alligators, lizards, snakes and sea turtles also live in many mangroves. Mangroves provide important nesting sites for land birds, shorebirds and waterfowl, and they are home to a number of threatened species including spoonbills, large snowy egrets, scarlet ibis, fish hawks, royal terns, West Indian whistling-ducks, and Storm’s Storks (Staus 1998). A variety of mammals make their homes in the mangal by association with the mangroves. Some of the noteworthy species present include dolphins, crab-eating monkeys, proboscis monkeys, fishing cats, mangrove monkeys and otters in India (Gopal and Krishnamurthy 1993), flying fox in northern Australia (Loughland 1998) and capuchin in Brazil (Fernandes 1991).

Exploitation of mangroves

Finally, mangroves are currently threatened by many different human activities. Exploitation is often taken beyond the level of natural replacement. Inland irrigation schemes divert river water from coastal regions and mangroves suffer from the resulting increase in salinity. Pollution takes its toll. Deliberate clearance for the development of aqua-culture takes place without consideration of what may be lost. Mangroves are likely to be one of the first ecosystems to be affected by global changes because of their location at the interface between land and sea. It has been predicted that as sea level rises, accompanying the rapid climate changes (Pernetta 1993; Field 1995; Ellison and Farnsworth 1997; Das et al. 2002; Kim et al. 2005; Jagtap and Nagle 2007; Gilman et al. 2008), mangroves tend to retreat landwards. And, of course, any significant rise in sea level resulting from global warming will mean encroachment on the relatively narrow zone within which mangroves flourish (Pernetta 1993; Das et al. 2002; Kim et al. 2005; Jagtap and Nagle 2007; Gilman et al. 2008). Destruction of mangrove habitats means a loss of the mangrove resource: as mangroves decline, so too do timber and charcoal production and fisheries, and the livelihood of the people who depend on them. This seems almost too obvious to need pointing out. The productivity and diversity of mangroves as well as their considerable social and economic values therefore make them of great interest to biologists and ecologists to understand their significance.

Mangroves and salt tolerance

Salt tolerance is the ability of plants to grow and complete their life cycle on a substrate that contains high concentrations of soluble salt. Plants that can survive on high concentrations of salt in the rhizosphere and grow well are called halophytes. Depending on their salt-tolerating capacity, halophytes are either obligate, and characterized by low morphological and taxonomical diversity with relative growth rates increasing up to 50% seawater or facultative and found in less saline habitats along the border between saline and non-saline upland and characterized by broader physiological diversity which enables them to cope with saline and non saline conditions. Mangroves are facultative halophytes tolerant to both high and fluctuating salinity. Some authors have also categorized mangroves under obligate halophytes (Downton 1982; Clough 1984). Several mangrove tree species reach an optimum growth at salinities of 5–25% of standard seawater (Downton 1982; Clough 1984; Ball 1988a; Burchett et al. 1989; Ball and Pidsley 1995). However, the range of salinity in which the plant is able to survive varies according to the species (Ball 1988a); in several species growth may be affected by either absence of or excess of NaCl in the substrate (Downton 1982; Clough 1984; Burchett et al. 1989; Pezeshki et al. 1990; Ball and Pidsley 1995). Because mangroves successfully live in high salinity environments it is advantageous to use them to study the mechanisms by which plants respond and adapt to these environments. Mangrove research has advanced considerably in the last few years, and the time seems right for an attempt to present our current understanding of the mechanisms of salt tolerance in mangroves. Although voluminous works are available on salt tolerance mechanism taking the model plant Arabidopsis thaliana (Apse et al. 1999; Nanjo et al. 1999; Quesada et al. 2000; Shi et al. 2000; Liu et al. 2000; Zhu 2000; Elphick et al. 2001), facultative model halophyte Mesembryanthemum crystallinum (Ratajczak et al. 1994; Low et al. 1996; Su et al. 2001; Golldack and Deitz 2001; Agarie et al. 2007), the information on morphological, anatomical, physiological, biochemical and molecular basis of salt tolerance mechanisms in mangroves which are facultative halophytes and potential stress adaptor (Downton 1982; Clough 1984) will throw new light and give a new dimension to salt stress research. Understanding the mechanisms of salt tolerance in mangroves and identification of salt tolerant genes from mangroves will lead to effective means to breed or genetically engineer salt tolerant crops.

Mechanisms of salt tolerance in mangroves

The ecological success of the mangroves under harsh conditions is explained by several morphological, anatomical, physiological, biochemical and molecular features. Mangroves develop a plethora of mechanisms to cope with salt stress that are discussed under following headings.

Morphological and anatomical features

Mangroves grow in a soil that is more or less waterlogged and in water whose salinity fluctuates and may be as high as that of the open sea (Naidoo et al. 1997). Mangrove trees adapt to survive such uncompromising surroundings with several morphological features such as salt-excreting leaves, and viviparous water dispersed propagules. In response to salinity where water economy is stringent, leaves tend to be smaller and thicker in mangroves (Ball 1988a). A small leaf design enhances cooling as small leaves lose more heat by convection than do large ones. There are interspecific differences in salt tolerance among the mangroves (Ball and Pidsley 1995). Ball and Pidsley (1995) examined the effects of soil salinity on the growth of two closely related species, Sonneratia alba and S. lanceolata in relation to their differential distributions along naturally seasonal salinity gradients. They showed that there were interspecific differences in salt tolerance which were founded on the inherent growth characteristics of the two species. In fact, these species showed a neat trade-off between growth and salt tolerance with S. lanceolata growing in salinities of up to 50% that of seawater while S. alba can grow in 100% seawater. Both the species, however, showed optimal growth in culture at 5% seawater. Nevertheless, at optimal salinity the growth of more salt tolerant species S. alba, measured as biomass, height and leaf area, is less than half that of the less salt tolerant species S. lanceolata, indicating that S. lanceolata will be the successful competitor even at a salinity that is optimal for both the species. On the other hand, S. lanceolata could not grow or compete in high salinities. In this species pair, a species can apparently opt for salt tolerance, or for rapid growth and competitive ability under low salinity conditions, not both (Ball and Pidsley 1995). The root-to-shoot ratio becomes relatively high and increases with increasing concentration of salinity in Avicennia and Aegiceras (Ball 1988b; Saintilan 1997). In addition, vivipary is also a characteristic that might have some role to tolerate high salinity in mangroves (Zheng et al. 1999). Vivipary is the condition found in some species of mangroves in which the sexually produced embryo of the seed continues its development without dormancy into a seedling, while still attached to the mother plant (Elmqvist and Cox 1996). Vivipary is known in the four genera of mangroves such as Bruguiera, Kandelia, Rhizophora and Ceriops of Rhizophoraceae (Tomlinson 1986). The seedling develops without dormancy largely by elongation of the hypocotyl to produce a cigar-shaped seedling known as propagule, which remains conspicuously pendulous on the mother tree for several months (Tomlinson and Cox 2000). The viviparous condition is so strongly associated with mangroves that it is suggested to have adaptive significance in the intertidal environment (Tomlinson 1986). It was assumed that vivipary in mangroves may be an adaptive characteristic permitting avoidance of high salinity at germination (Henkel 1979). Some evidence has proved that developing viviparous propagules (i.e. hypocotyls) in Rhizophoraceae retain lower salt concentrations than in other organs of mother trees especially the leaves, but it increases gradually during the process of propagule maturation (Wang et al. 2002). This lowered salt concentration in developing propagules, whatever its origin, is interpreted as a mechanism to “protect” the embryo from the deleterious effects of high salt concentrations until maturity (Hogarth 1999). Nevertheless, a few authors have argued that the adaptation of developing propagules (hypocotyls) to salt originates when it is still attached to the mother tree by continuously absorbing salt from the mother tree (Lin 1988). After following the element concentrations on a dry weight basis, Zheng et al. (1999) concluded that the development of propagules was not a salt accumulation process, but a desalinating process, because salt concentration on a dry weight basis declined with propagule development. If it were truly a desalinating process, how can the propagule keep the osmotic balance and by what means can the propagule cope with the salt stress and osmotic stress after the propagule settles down in the hyposaline environment? Little research has dealt with the changes after a propagule leaves the mother plant (Tomlinson and Cox 2000). Wang et al. (2002) reported that no direct correlation was found between salt tolerance and vivipary. All features mentioned above reveal higher competence of salt tolerance of mangroves in terms of morphology.

Mangroves develop diverse mechanisms associated with anatomic characteristics in order to tolerate high salinity. Mangrove species usually have salt resistant-associated anatomic structures. Many species of mangrove possess salt glands in their leaves. All species in genus Aegiceras, Avicennia, Acanthus and Aegialitis have typical salt gland structures, and species in Laguncularia and Conocarpus have analogous structure to salt glands (Tomlinson 1986). In L. racemosa and C. erectus “tiny bumps” or “pimples” like structures are found on the petioles of the leaves that somewhat resemble salt glands (Tomlinson 1986). However, the salt secretory ability of these structures has not been precisely demonstrated. Biebl and Kinzel (1965) describe three morphologically different structures in the leaves of L. racemosa, the smallest of which sit in deep, irregular epidermal depressions and extrude chains of salt crystals. However, Kemis (1984) raised specimens of Conocarpus and observed them to secrete clear, sweet-tasting nectar. His observations and electron microscope studies led him to conclude that the “pimples” are, in fact, “extra floral nectarines (EFN)”. Kemis (1984) reported that these extra-floral nectaries (EFN) may serve an adaptive role and used mutualistically to attract ants to defend the tree from herbivorous pests. Kemis and Lersten (1984) follow up the study of Conocarpus with a similar electron microscope study of Laguncularia and conclude that, the pimples lack a salt excretory function, but the morphology is so different that there is “no evidence of an opening”. No evidence of an opening indicates that these pimples secrete neither salt nor nectar. They suggest a theory regarding the differences in the L. racemosa and C. erectus petiolar “pimples.” They suggest that the apparently non-functional nature of the pimples on Laguncularia is a consequence of a reversion from functionality to vestigiality. It is suspected that the mythical salt glands in Conocarpus are really the sugar glands become vestigial remnant in Laguncularia. Saenger (2002) pointed out that in L. racemosa, the formation of these salt glands analogous structures or pimples is found only in the presence of salt implying a secretory function (2002). Saenger (2002) reported that these salt glands analogous structures may be interpreted as hydathodes, salt glands or nectaries. Leaves of Aegiceras and Avicennia have deposits of salt crystals as a result of salt leak from the salt glands. The lower leaf surface of Avicennia is densely covered with hairs, which raise the secreted droplets of salt water away from the leaf surface, preventing the osmotic withdrawal of water from the leaf tissues (Osborne and Berjak 1997). In species of Rhizophora, Sonneretia, Avicennia and Xylocarpus, salt is also deposited in the bark of stem and roots (Scholander 1968). Another typical characteristic of mangrove is the induction of leaf succulence by thickening of leaves with increasing water content (Suarez and Sobrado 2000). For example, Laguncularia racemosa can increase leaf thickness and water content when stressed with high salinity (Sobrado 2005), by which absorbed salt was diluted and salt-induced damage was reduced to some extent. Under the condition of high salinity, there is increase of leaf thickness from the youngest to the oldest leaves along shoot in L. racemosa (Werner and Stelzer 1990). Salt-induced succulence can lower the resistance to CO2 uptake and this increases the photosynthetic rate by increasing the internal leaf surface for gas exchange. The waxed epidermis in the leaves is also a protective trait in some mangroves, which contributes to low transpiration of mangrove species relative to that of other plants without this trait (Werner and Stelzer 1990). Several species deposit salt in senescent leaves, which are then shed (Zheng et al. 1999). This helps in removing salt from the metabolic tissues. There is also change in leaf anatomy i.e. development of kranz anatomy and dimorphism of chloroplast, reduction in number of stomata per leaf area and wide opening of stomata which is a typical feature of succulence (Werner and Stelzer 1990; Parida et al. 2004a).

In Rhizophora mangle salt-induced increase in succulence is predominantly based on the considerable expansion of the hyalinous hypodermal cells below the upper epidermis (Werner and Stelzer 1990). The high Na+ and Cl concentrations in hypodermal and endodermal vacuoles of Rhizophora are the result of cellular metabolism. These vacuoles represent storage pools, supplied and/or unloaded by membrane activity. Apparently, the outer hypodermis and the endodermis represent ion regulating steps or two sheaths of the ultrafilter, respectively. The hypodermal cells layers of Rhizophora form a tight ring of cells with relatively long radial cell walls. Their vacuoles represent more than 40% of the total root volume and they contain relatively high Na+ and Cl concentrations. The vacuoles of these cells act as salt traps, protecting the subsequent cell layers (Werner and Stelzer 1990). The processes of root elongation and suberization of cell walls are two possible other ways to avoid an invasion of these cells by salt. Root elongation maintains the capacity for accumulating ions by providing new cells (Stelzer et al. 1988); suberization seals the ion-invaded cells and blocks the apoplasmic pathway (Peterson 1988; Taura et al. 1988).

The mangrove species have several morphological and anatomical features which are quite similar to high water-use efficiency characteristics of terrestrial xerophytes (Clough et al. 1982; Ball 1988a; Clough and Sim 1989). These characteristics enable the mangroves to grow in a “physiologically” dry (or) saline environment without apparent adverse effects of severe water stress. The water conserving function of mangroves is very much similar to xerophytes (Ball 1988a). Most of the mangrove genera have thick-walled epidermis with waxy cuticle and sunken stomata. The waxy cuticles are covered by a tomentum of various shaped hairs, like tricellular peltale hairs in Avicennia sp., stellate hairs in Hibiscus tiliaceous and stellate scales in Heritiera sp. (Miller et al. 1975). This tomentum-like outgrowth reduced water loss via the stomata and the salt gland. Sunken stomata beneath the epidermis are prominent in Avicennia sp., Bruguiera spp., Ceriops spp., Lumnitzera spp. and Rhizophora spp. (Miller et al. 1975). Sclerenchymatous cells are distributed throughout the mangrove leaves including the epidermis (Sidhu 1975). The presence of large-celled water-storing hypodermis with strongly developed palisade mesophylls with small intercellular spaces in the mangrove leaves indicate their xerophytic characters (Sidhu 1975). The isobilateral leaves of Aegialitis rotundifolia have no hypodermal tissue and spongy mesophyll; on the other hand the isobilateral leaves of Ceriops tagal have enlarged spongy mesophyll cells both in upper and lower hypodermis (Saenger 1982). The isobilateral leaves of Sonneratia caseolaris and Lumnitzera racemosa also have enlarged water-storing hypodermal cells. The dorsiventral leaves of Acanthus ilicifolius, B. gymnorrhiza, Excoecaria agallocha and xylocarpus spp. have several layers of hypodermal cells (Saenger 1982). Rhizophora spp. also have marked differentiation of hypodermis with small tannin cells and large colorless water-storing cells. The leaves of most of the mangroves are succulent due to the well-developed large-celled water storing hypodermis and strongly developed palisade mesophyll tissues with small intercellular spaces (Saenger 1982). Several layered hypodermal aqueous tissues are present in most of the mangroves, e.g., Avicennia sp., Hibiscus spp., Acrostichum spp. and single-layered hypodermal cells have also been reported in Bruguiera spp., Ceriops spp., Cynometra spp., Accanthus spp. and Excoecaria spp. (Saenger 1982). Large undifferentiated mesophyll cells have formed a central aqueous tissue in Sonneratia sp. and Lumnitzera sp. (Saenger 1982). In Aviccenia spp., Bruguiera spp. and Ceriops spp., the ends of the vascular bundles are surrounded by irregular groups of tracheids (Saenger 1982). The walls of the tracheids bear spiral reticulated or pitted thickenings and the water storage function has been attributed to them (Saenger 1982). The stone cells and sclereides have been reported from Avicennia spp., Rhizophora spp., Sonneratia spp., Bruguiera spp., and Xylocarpus spp. (Saenger 1982). These cells give toughness and rigidity to leaves. The mucilaginous cells have been reported from Sonneratia spp. and Rhizophora spp. and these mucilaginous cells may be involved in reducing damages from wilting by conserving water (Ball 1988a). The water use efficiency of glycophytes is comparatively less than that of mangroves.

Physiological and biochemical mechanisms

Some of the most salt-tolerant mangrove species grow in an environment where tidal influence is minimized but evaporation of water from the soil surface is high. In these areas the concentration of salt in the soil rises to such an extent that it becomes hypersaline (more salty than seawater, Lovelock and Feller 2003). Seawater contain 35 g/l of salt (3.5%), 483 mM Na+ and 558 mM Cl) with an osmotic potential of −2.5 MPa (Scholander 1968). Mangroves, therefore, have to maintain continuous water uptake, and regulate ion uptake and compartmentation against a strong external salt gradient (Ball 1996). To maintain water uptake, mangroves not only have to restrict water loss by means of conservative morphological and physiological adaptations such as thickening of leaves giving rise to greater retention times for leaf nitrogen and conservative water use efficiency (Ball 1996; Lovelock and Feller 2003) but also they need to maintain sufficiently low water potentials. Agricultural crops under well-saturated conditions generally have water potentials of approximately −1.0 MPa. However, as the osmotic potential of seawater is approximately −2.5 MPa (Sperry et al. 1988), mangrove leaf water potentials have to range between −2.5 and −6.0 MPa (Scholander et al. 1966; Aziz and Khan 2001a; Sobrado and Ewe 2006). Salinity stress causes low stomatal conductance, which decreases the rate of CO2 accumulation and uptake, rate of transpiration and increase in xylem tension (Ball and Farquhar 1984; Aziz and Khan 2001a; Parida et al. 2004a). The low transpiration rates and slow water uptake are common features for all mangroves (Scholander et al. 1966). However, increase in transpiration in response to increase in salinity has also been reported in B. gymnorrhiza (Takemura et al. 2000) and in both Avicennia alba and Rhizophora apiculata (Becker et al. 1997). This is suggested to be the aim at increasing internal salt concentration and eventually balance the increased external salt concentration. As water salinity increases, some species of mangroves simply become increasingly conservative in their water use, thus achieving greater tolerance (Ball and Passioura 1995). Because mangrove roots exclude salts when they extract water from soil, soil salts could become very concentrated, creating strong osmotic gradients (Passioura et al. 1992). Zimmermann et al. (1994) reported that the xylem vessels of the roots and stems of mangrove (Rhizophora mangle) contain high molecular weight viscous, mucilage made up of acid polysaccharides (mucopolysaccharides). These mucopolysaccharides in the xylem sap are apparently involved in water transport in the xylem conduit of R. mangle (Zimmermann et al. 1994). Accumulation of mucilage in xylem vessels is an important strategy of mangrove trees to save water on its tortuous pathway to the uppermost crown (Zimmermann et al. 1994, 2002). The viscous, polymeric substances in the xylem sap limit flow rate and decrease transpiration (Zimmermann et al. 1994, 2002). This, combined with high water-use efficiency, slows the rate of water uptake and prevents salts from accumulating in the soil surrounding the roots. This helps the mangroves conserve water and regulate internal salt concentrations (Ball and Passioura 1995; Ball 1996).

Mangroves experience hypersaline conditions as a result of evaporation (which raises the salinity level) and fluctuation of salinity caused by tide (Lovelock and Feller 2003). High salinity and salinity variation pose a problem for mangroves (Lovelock and Feller 2003). To cope with this uncompromising situation, a number of physiological and biochemical mechanisms are adopted by mangroves, namely, salt excretion (Hanagata et al. 1999), salt accumulation (Popp 1984a, b; Kura-Hotta et al. 2001; Mimura et al. 2003), salt secretion (Sobrado and Greaves 2000), accumulation of compatible solutes (Ashihara et al. 1997) and induction of antioxidative enzymes (Takemura et al. 2000; Parida et al. 2004b) which are discussed under the following headings.

Salt secretion, salt exclusion and salt accumulation

Depending on their salt eliminating mechanism mangroves and their associates have been classified into three groups: (1) salt excluders, (2) salt secretors and (3) salt accumulators (Table 1). The salt-excluding mangrove species (e.g. Rhizophora spp., Ceriops spp., Bruguiera spp., Lumnitzera spp., Excoecaria spp.) eliminate excess salt by an ultrafiltration mechanism occurring at the root cell membranes of cortical cells (Scholander 1968; Zheng et al. 1999; Takemura et al. 2000; Aziz and Khan 2001a; Khan and Aziz 2001; Wang et al. 2002). Though the exact mechanism of ultrafiltration is not well characterized, it is understood that the process is a physical one. Negative hydrostatic pressure developed in plants by transpiration is enough to overcome negative osmotic pressure in the environment of the roots. Water is therefore drawn in, unwanted ions and other substances are excluded. Rhizophora mangle is not provided with salt glands, but it keeps the xylem sap essentially free of NaCl by ultrafiltration at the membranes of root cells (Scholander et al. 1966; Scholander 1968). The concentration of xylem sap is about one-tenth than that of seawater (Lawton et al. 1981). Furthermore, in B. gymnorrhiza, hypocotyls function as an additional filter to retain salt from the shoot (Lawton et al. 1981).They maintain ionic balance through K+/Na+ exchange at the xylem parenchyma cells in the basal part of the plants and vacuolar K+/Na+ exchange in transpiring leaves and circulation of exchanged ions within the plants. The ultrafiltration process and K+/Na+ exchange contribute to keeping the xylem sap concentration of salt-treated plants low with mean rates of net ion transport into the shoot being even lower due to recirculation of exchanged ions (Mallery and Teas 1984; Werner and Stelzer 1990).
Table 1

Mechanism of salt adaptation and their known distribution in some mangrove species

Species

Exclude

Secrete

Accumulate

References

Acanthus

 

+

 

Hogarth (1999); Ye et al. (2005); Nguyen et al. (2007)

Aegialitis

+

+

 

Naidoo and von Willert (1995); Hogarth (1999)

Aegiceras

+

+

 

Naidoo and von Willert (1995); Mishra and Das (2003); Ye et al. (2005)

Avicennia

+

+

+

Sobrado (2002); Ye et al. (2005); Suarez and Medina (2006); Griffiths et al. (2008)

Bruguiera

+

 

+

Takemura et al. (2000); Kura-Hotta et al. (2001); Li et al. (2008); Miyama and Tada (2008)

Ceriops

+

  

Hogarth (1999); Zheng et al. (1999); Aziz and Khan (2001b)

Excoecaria

+

  

Tomlinson (1986); Hogarth (1999)

Laguncularia

 

+

 

Hogarth (1999); Sobrado (2004)

Osbornia

+

 

+

Tomlinson (1986); Hogarth (1999)

Rhizophora

+

 

+

Clough (1984); Werner and Stelzer (1990); Hogarth (1999)

Sonneratia

+

+

+

Tomlinson (1986); Hogarth (1999); Yasumoto et al. 1999

Xylocarpus

  

+

Hogarth (1999); Paliyavuth et al. (2004)

Salt secretors regulate internal salt levels by secreting excess salt through foliar glands and are represented by Acanthus spp., Avicennia marina, Av. officinalis, Av. alba, Aegiceras corniculatum and Aegialitis spp. (Meher-Homji 1988; Selvam 2003). Salt stimulation to secretion was a common feature in salt-secreting mangrove species (Ball 1988a; Drennan et al. 1992; Sobrado 2002). Salt secretion occurs through glands and it is facilitated by efficient leaf turnover for salt shedding (Aziz and Khan 2001b). Dschida et al. (1992) identified an energy-dependent process in salt excretion, achieved by plasma membrane H+-ATPase in Avicennia germinans. The salt tolerance of three salt-secreting mangrove species, i.e. Acanthus ilicifolius, Aegiceras corniculatum and A. marina was compared by Ye et al. (2005). They reported that all of the three species exhibited increases in salt secretion with increases in salinity. The capacity to secrete salts at any given salinity was different between species, following an order of A. marina > A. corniculatum > A. ilicifolius, similar to the case of seedling growth. The salt tolerance of the three salt-secreting mangrove species was in the descending order of A. marina > A. corniculatum > A. ilicifolius. This indicated that salt secretion from leaves was related to salt tolerance (Ye et al. 2005). There are species, which can employ more than one mechanism to protect against adverse effects of salinity (Table 1). Aegiceras and Avicennia, which are provided with salt glands also, exclude 90–97% salt through the process of ultrafiltration (Ball 1988b). Salt-secreting ability is absent in glycophytes.

Salt accumulators accumulate high concentration of salts in their cells and tissues and avoid salt damage by efficient sequestering of ions to the vacuoles in the leaf, translocation outside the leaf, possible cuticular transpiration and efficient leaf turnover to salt shedding (Tomlinson 1986; Aziz and Khan 2001b). Species of Lumnitzera and Excoecaria accumulate salts in leaf vacuoles and become succulent. Salt concentrations in the sap may also be reduced by transferring the salts into senescent leaves or by storing them in the bark or roots (Tomascik et al. 1997; Perry et al. 2008). Regulation of K+ uptake and/or prevention of Na+ entry, efflux of Na+ from the cell, and utilization of Na+ for osmotic adjustment are strategies commonly used by plants to maintain desirable K+/Na+ ratios in the cytosol. Osmotic homeostasis is established either by Na+ compartmentation into the vacuole or by biosynthesis and accumulation of compatible solutes. A high K+/Na+ ratio in the cytosol is essential for normal cellular function of plants. Na+ competes with K uptake through Na+–K+ co-transporters, and may also block the K+-specific transporters of root cells under salinity (Zhu 2003). This results in toxic levels of sodium as well as insufficient K+ concentration for enzymatic reactions and osmotic adjustment. Under salinity, sodium gains entry into root cell cytosol through cation channels or transporters (selective and nonselective) or into the root xylem stream via an apoplastic pathway depending on the plant species (Chinnusamy et al. 2005). Silica deposition and polymerization of silicates in the endodermis and rhizodermis block Na+ influx through the apoplastic pathway in the root (Yeo et al. 1999). Restriction of sodium influx either into the root cells or into the xylem stream is one way of maintaining the optimum cytosolic K+/Na+ ratio of plants under high salinity. In saline conditions, cellular potassium level can be maintained by activity or expression of potassium-specific transporters. In Mesembryanthemum crystallinum L., high affinity K+ transporter-K+ uptake genes are up-regulated under NaCl stress (Su et al. 2002). Sodium efflux from root cells prevents accumulation of toxic levels of Na+ in the cytosol and transport of Na+ to the shoot. Molecular genetic analysis in Arabidopsis have led to the identification of a plasma membrane Na+/H+ antiporter, SOS1 (Salt Overly Sensitive 1), which plays a crucial role in sodium extrusion from root epidermal cells under salinity (Chinnusamy et al. 2005). Sodium efflux by SOS1 is also vital for salt tolerance of meristem cells such as growing root-tips and shoot apex as these cells do not have large vacuoles for sodium compartmentation (Shi et al. 2002). The expression of SOS1 is ubiquitous, but stronger in epidermal cells surrounding the root-tip, as well as parenchyma cells bordering the xylem. Thus, SOS1 functions as a Na+/H+ antiporter on the plasma membrane and plays a crucial role in sodium efflux from root cells and the long distance Na+ transport from root to shoot (Shi et al. 2002). Sodium efflux through SOS1 under salinity is regulated by SOS3–SOS2 kinase complex (Chinnusamy et al. 2005).

Vacuolar sequestration of Na+ is an important and cost-effective strategy for osmotic adjustment that also reduces the Na+ concentration in the cytosol. Na+ sequestration into the vacuole depends on expression and activity of Na+/H+ antiporters as well as V-type H+- ATPase and H+- PPase. These phosphatases generate the necessary proton gradient required for activity of Na+/H+ antiporters. Salt accumulation in mangroves occurs with the sequestration of Na+ and Cl into the vacuoles of the hypodermal storage tissue of the leaves (Werner and Stelzer 1990; Aziz and Khan 2001a; Kura-Hotta et al. 2001; Mimura et al. 2003). Cram et al. (2002) reported two subsequent phases of salt accumulation in leaves of Bruguiera cylindrica, Avicennia rumphiana and A. marina. The first phase is the rapid increase in leaf salt concentration, as it grows from bud to maturity followed by a slower but continuous change in salt content via changes in ion concentration and/or in increased leaf thickness. Increased accumulation of Na+ is generally coupled with reduced Ca++ and Mg++ uptake (Greenway and Munns 1980; Delphine et al. 1998) and sometimes with decline in carbon assimilation (Parida et al. 2004a). It was reported that Na+ and Cl ion levels increase in root and shoot tissues of Kandelia candel and B. gymnorrhiza with increasing NaCl stress but, B. gymnorrhiza shows a rapid Na+ accumulation upon the initiation of salt stress and leaves contain 90% more Na+ and 40% more Cl than K. candel (Li et al. 2008). The X-ray microanalysis of leaf mesophyll cells shows evidence of distinct vacuolar compartmentation of Na+ in K. candel but Cl in B. gymnorrhiza seedlings subjected to 100 mM NaCl. Moreover, Na+ within cell wall, cytoplasm, vacuole and chloroplast remains 23–72% lower in stressed B. gymnorrhiza as compared to K. candel. It was concluded that B. gymnorrhiza exhibit effective salt exclusion from chloroplasts although increasing salt stress causes a rapid and higher build up of Na+ and Cl in the leaves (Li et al. 2008). Net photosynthetic rate (P N) declines with increasing salinity in both the species, and the most marked reduction occurred after exposure of mangrove seedlings to a severe salinity, 400 mM NaCl. However, the inhibitory effects of severe stress varied with species: P N decreased by 80% in K. candel whereas in B. gymnorrhiza the decline was 60%. The lesser reduction in photosynthesis in B. gymnorrhiza could be a consequence of salt exclusion from mesophyll chloroplasts (Li et al. 2008). Compartmentalizing NaCl into the vacuole is likely to depend on Na+/H+ antiporter systems (Garbarino and DuPont 1988; Tanaka et al. 2000; Fu et al. 2005), H+-coupled Cl antiport (Schumaker and Sze 1987) or ion channels (Pantoja et al. 1989; Maathuis and Prins 1990). Ion compartmentation in the vacuole would limit excessive salt accumulation in the symplast, thus protecting salt-sensitive enzymes in the cytoplasm and chloroplasts. Hence, the ability to maintain lower Na+ and Cl in the symplast may be an underlying determinant of the tolerance of mangroves (Li et al. 2008).

Accumulation of compatible solutes and osmolytes

One of the important biochemical mechanisms by which mangroves counter the high osmolarity of salt is accumulation of compatible solutes (Takemura et al. 2000; Parida et al. 2004c). To accommodate the ionic balance in the vacuoles, cytoplasm accumulates low-molecular-mass compounds termed compatible solutes because they do not interfere with normal biochemical reactions; rather they replace water in biochemical reaction (Hasegawa et al. 2000; Ashihara et al. 2003). With accumulation proportional to the change of external osmolarity within species-specific limits, protection of structures and osmotic balance supporting continued water influx (or reduced efflux) are accepted functions of compatible solutes (Parida et al. 2005). Hibino et al. (2001) reported that three mangroves, B. gymnorrhiza, K. candel, and R. stylosa, accumulate exclusively pinitol as compatible solute. Mannitol is the compatible solute for intact plants of Sonneratia alba under salinity (Yasumoto et al. 1999). Although, pinitol and mannitol are the most common compatible solutes of a number of mangrove species, proline (in Xylocarpus species), methylated quaternary ammonium compounds (in Avicennia eucalyptifolia, A. marina, Acanthus ilicifolius, Heritiera littoralis and Hibiscus tiliaceus), and carbohydrates (in Acanthus ilicifolius, Heritiera littoralis and Hibiscus tiliaceus) are found to be dominant osmoregulating compounds (Popp et al. 1985). Glycinebetaine, the most common compatible solute, which offers protection to photosynthetic machinery, is found in some mangroves like A. marina (Ashihara et al. 1997; Hibino et al. 2001). Although glycinebetaine accumulates as compatible solute in mangroves and many species of non-mangrove halophytes such as Suaeda maritima, Atriplex nummularia and Salicornia europoea but is absent from many crop species (e.g. rice) and the model species in plant transformation, tobacco (Flowers and Colmer 2008). There has therefore been considerable work on engineering the production of glycinebetaine in crop species that do not produce it naturally. Compatible solutes of Rhizophora stylosa and B. gymnorrhiza are O-methylmucoinositol (Ashihara et al. 2003). Mannitol is a compatible solute in Sonneratia alba and Lumnitzera racemosa (Ashihara et al. 2003). Many mangrove species e.g. Sonneratia alba, A. marina also accumulate inorganic ions and use them as osmolytes to maintain osmotic and water potential (Yasumoto et al. 1999; Suarez and Medina 2006). Salt tolerance of B. gymnorrhiza might be attributed to their ability to accumulate high concentrations of Na+ and Cl (Miyama and Tada 2008). The uptake of additional Na+ and Cl by this mangrove is used as osmolytes and to maintain K+ homeostasis under salt stress (Miyama and Tada 2008). A summary of specific compatible solutes in mangrove species is given in Table 2. The increased synthesis of compatible solutes is achieved by modulating genes encoding enzymes of the osmolyte biosynthetic pathway. For instance, upregulation of pyrroline-5-carboxylate synthetase (P5CS) gene that is involved in proline biosynthesis leads proline accumulation during salt stress in A. marina (Mehta et al. 2005). A significant upregulation of AcP5CS gene was also observed in A. corniculatum during salinity stress. The upregulation of Betaine-aldehyde dehydrogenase (BADH) gene that is involved in glycinebetaine synthesis results in the accumulation of glycinebetaine in A. marina under salt stress (Hibino et al. 2001). Waditee et al. (2002) reported that under high salinity conditions, the betaine/proline transporters (AmT1, -2, and -3) also involved in the accumulation of betaine by increasing the mRNA levels as well as post-translational activation in A. marina.
Table 2

Compatible solutes in mangroves and mangrove associates

Compatible solutes

Mangrove species

References

Pinitol

Kandelia candel, Rhizophora stylosa, Bruguiera gymnorrhiza, Avicennia marina

Hibino et al. (2001)

Ceriops tagal

Popp et al. (1985)

Mannitol

Kandelia candel, Rhizophora stylosa, Bruguiera gymnorrhiza

Hibino et al. (2001)

Sonneratia alba

Yasumoto et al. (1999); Ashihara et al. (2003)

Lumnitzera racemosa

Ashihara et al. (2003)

Proline

Kandelia candel, Rhizophora stylosa, Bruguiera gymnorrhiza

Hibino et al. (2001)

Bruguiera parviflora

Parida et al. (2002)

Aegiceras corniculatum

Fu et al. (2005)

Bruguiera sexangula, Avicennia alba, Xylocarpus granatum

Datta and Ghosh (2003)

Acanthus ilicifolius, Hibiscus tiliaceus

Datta and Ghosh (2003)

Avicennia marina

Datta and Ghosh (2003); Hibino et al. (2001)

Ceriops roxburghiana

Rajesh et al. (1999)

Ceriops tagal

Aziz and Khan (2001b)

Glycinebetaine

Avicennia marina

Hibino et al. (2001); Ashihara et al. (1997); Popp et al. (1985)

Ceriops roxburghiana

Rajesh et al. (1999)

Hibiscus tiliaceus

Popp et al. (1985)

O-methylmucoinositol

Rhizophora stylosa, Bruguiera gymnorrhiza

Ashihara et al. (2003)

Starch/polysaccharide

Aegiceras corniculatum

Parida et al. (2004c)

Aspartic acid

Aegiceras corniculatum, Acanthus ilicifolius

Datta and Ghosh (2003)

Sterol

Ceriops roxburghiana

Suarez and Medina (2006)

Induction of antioxidative enzymes

Mangroves inhabiting the intertidal zones suffer from diverse stresses such as high salinity, hypoxia, ultraviolet radiation, nutrition deficiency and so on. These primary stresses may lead to secondary oxidative stress, resulting in accumulation of reactive oxygen species (ROS) such as superoxide (O 2 .− ), hydrogen peroxide (H2O2), hydroxyl radical and singlet oxygen (1O2) (Parida et al. 2004b). These cytotoxic reactive oxygen species can seriously disrupt normal metabolism through oxidative damage to lipids, protein and nucleic acids (Parida et al. 2004b). Mangroves with high levels of antioxidants, either constitutive or induced, have been reported to have greater resistance to this oxidative damage (Cheeseman et al. 1997; Takemura et al. 2000; Parida et al. 2004b; Jithesh et al. 2006). The activities of the antioxidative enzymes such as catalase (CAT), ascorbate peroxidase (APX), guaiacol peroxidase (POD), glutathione reductase (GR), and superoxide dismutase increase under high salinity and a correlation of these enzyme levels and salt tolerance exists in mangroves (Parida et al. 2004b; Takemura et al. 2000). There are several reports of upregulation of antioxidative enzymes and their corresponding genes in mangroves under salinity. In B. gymnorrhiza, the activities of the antioxidant enzymes, superoxide dismutase (SOD) and catalase, show an immediate increase after the plants are transferred from water to high salinity (Takemura et al. 2000). In B. parviflora, salt treatment preferentially enhances the content of H2O2 as well as the activity of ascorbate peroxidase (APX), guaiacol peroxidase (GPX), glutathione reductase (GR), and superoxide dismutase (SOD), whereas it induces the decrease of catalase (CAT) activity (Parida et al. 2004b). It has also been reported that in the salt-secreting mangrove Aegiceras corniculatum, there is a linear increase of salt secretion of leaf with increase in period of salt treatment and a concomitant decrease in antioxidative enzymes such as catalase, ascorbate peroxidase and guaiacol peroxidase (Mishra and Das 2003).

Molecular mechanism of salt tolerance in mangroves

The mechanism of salt tolerance of mangroves can be partially explained by morphological, anatomical, physiological and biochemical studies. However, these are insufficient to clarify the salt tolerance mechanism. Recently, some progress has been achieved in understanding the mechanism of salt tolerance in mangroves at a molecular level. Several salt stress-associated genes from mangroves have been evaluated for their contribution to salt tolerance in laboratory studies (Table 3). Table 4 also lists some relevant studies in mangroves at the genomic levels. These results indicated that the tolerance of mangroves to a high-saline environment is indeed tightly linked to the regulation of gene expression. Some molecular biological studies of mangroves are discussed below in order to illustrate this point.
Table 3

Salt inducible genes reported in mangroves

Mangrove species

Genes

Characteristic feature(s)

References

Aegiceras corniculatum

P5CS

Delta 1-pyrroline-5-carboxylate synthetase, a key enzyme of proline synthesis pathway Accumulation of transcript of this gene under high salinity tended to accompany recruitment of proline in Aegiceras corniculatum

Fu et al. (2005)

PIP1

PIP1 aquaporin—This gene was upregulated by salt stress

Fu et al. (2005)

PIP2

PIP2 aquaporin—This gene was upregulated by salt stress

Fu et al. (2005)

NHA

Na+/H+ antiporter—This gene was upregulated by salt stress

Fu et al. (2005)

BADH

Betaine-2-aldehyde dehydrogenase—High salinity induced increase of transcript level and such an increase was accompanied by accumulation of betaine. Although activity of this enzyme decreased with an increase in salinity, the extent of decrease is less than its homologue in E. coli and spinach

Hibino et al. (2001)

Avicennia marina

Sod1

Cytosolic Cu/Zn superoxide dismutase—Overexpression of this gene in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance

Prashanth et al. (2008)

Sod1

Cu/Zn superoxide dismutase—High salinity did not lead to transcriptional change but osmotic stress decreased transcript level of this gene. Under oxidative stress, its transcription was transiently upregulated

Jithesh et al. (2006)

Cat1

Catalase—It was upregulated by saline or oxidative stress but downregulated by osmotic stress

Jithesh et al. (2006)

Fer1

Ferritin 1—It was transcriptionally Upregulated by saline or oxidative stress but didn’t change under osmotic stress

Jithesh et al. (2006)

AmT1; AmT2

Betaine/Proline transporter—Transgenic E. coli with such genes could accumulate

Waditee et al. (2002)

AmT3 [partial]

Betaine under salt stress; In Avicennia marina, salt stress induced transcription of such genes in root and leaf

 

Bruguiera gymnorrhiza

OEE1

OEE1 is one component of PS II and high salinity induced accumulation of its transcript and protein

Sugihara et al. (2000)

DLDH

Dihydrolipoamide dehydrogenase—Upregulated when treated with 500 mM NaCl for 1 day

Banzai et al. (2002)

LAS

Lipoic acid synthase—Being upregulated when treated with 500 mM NaCl for 1 day

Banzai et al. (2002)

Unnamed gene

Fructose-6-phosphate, 2-kinase/fructose-2, 6-bisphophatase—Transcription of this gene increased after 6 h of salt stress. It was supposed to act in osmotic regulation process by controlling the content of Fru-2, 6-P2

Banzai et al. (2002, 2003)

Cytosolic

Cytosolic Cu/Zn superoxide dismutase—High salinity, mannitol and ABA induced accumulation

Takemura et al. (2002)

Cu/Zn SOD

Of its transcripts in leaves; Transcript was induced by high salinity in young and mature leaves rather than in old leaves

 

Cytosolic CAT (partial)

Catalase——No significant change occurred in the expression of this gene during the treatment with NaCl, mannitol and ABA, but CEPA (2-chloroethylphosphonic acid) can increase its transcript level

Takemura et al. (2002)

Bruguiera sexangula

CCTα

CCTα α subunit of CCT complex——Transgenic E. coli with one domain of this subunit displayed enhanced tolerance to high salinity

Yamada et al. (2002a)

Mangrin

Partially homologous to gene encoding Allene Oxide Cyclase (AOC)——It was upregulated by high salinity and its overexpression enhanced salt tolerance of transgenic yeast and tobacco cell

Yamada et al. (2002b)

Kandelia candel

SIGKC1; SIGKC2

Cytosolic low molecular mass heat shock protein (sHSPs)—sHSPs act as molecular chaperones to prevent thermal aggregation of proteins by binding non-native intermediates

Huang et al. (2003)

SIGKC3

ADP-ribosylation factor (ARF)—a ubiquitous, highly conserved 21 kDa GTP-binding protein; The ARF proteins are thought to function as regulators of membrane traffic

Huang et al. (2003)

SIGKC4; SIGKC5

Unknown function

Huang et al. (2003)

The names of various genes have been by and large reproduced here as per the original publications of the authors

Table 4

Genomic studies in mangroves

Mangrove species

Description

References

Aegiceras corniculatum

A leaf SSH library was constructed. By sequencing the whole SSH library 577 ESTs were found that are up-regulated by high salinity. Fourteen catagories were assigned for this EST collection and those categories of “protein synthesis”, “defense”, “transport”, “ion homeostasis”, “protein destination” and “signal transduction” were remarkable

Fu et al. (2005)

Avicennia marina

A leaf cDNA library was constructed from 500 mM NaCl-treated seedlings. Random sequencing generated 1602 ESTs which were grouped into 13 categories; Among these, 7% were homologous with stress-responsive genes

Mehta et al. (2005)

Bruguiera gymnorrhiza

Large-scale sequencing of ESTs collected from high salinity or hormone treated leaves and roots. Assembly of 14,842 high quality sequences generated 6,943 unique genes and 62.5% of such EST collection matched known proteins in Blast searching. Totally 129 statistically-confident genes were grouped into 4 clusters depending on their EST frequency and each group has specific pattern of transcript profiling under high salinity

Miyama et al. (2006)

Salt-responsive transcript profilings of 7,029 unique genes in leaf and root tissues were monitored using microarray technique. Clustering generated at least six categories of transcript accumulating under saline condition; Some genes displayed similar salt-responsive patterns to those in other plants, indicating shared mechanisms in Bruguiera gymnorrhiza and other glycophytes. Distinct expression patterns of other genes suggested existence of specific mechanisms in this species

Miyama and Hanagata (2007)

Differentially expressed candidates genes were identified through differentially display technique from leaves stressed with 500 mM NaCl for 0 h, 6 h, 3 days, and 28 days. Totally 89 clones were identified as differentially expressed candidates; nine out of these candidates were verified by Northern Blot and classed into three groups depending on their salt-induced patterns of transcript accumulation

Banzai et al. (2002)

Bruguiera cylindrica

126 salt tolerant cDNAs were identified and isolated from the root using suppression subtractive hybridization (SSH) and bacterial functional screening. Sequencing of 51 subtracted cDNA clones that were differentially expressed in the root of B. cylindrica exposed to 342 mM NaCl revealed 10 tentative unique genes (TUGs) with putative functions in protein synthesis, storage and destination, metabolism, intracellular trafficking and other functions; and nine unknown proteins. The 75 cDNA sequences of B. cylindrica that conferred salinity tolerance to Escherichia coli consisted of 29 TUGs with putative functions in transportation, metabolism and other functions; and 33 with unknown functions. Both approaches yielded 42 unique sequences that have not been reported elsewhere to be stress related

Wong et al. (2007)

Acanthus ebracteatus

A leaf cDNA library was constructed from seawater-growing seedlings. Random sequencing generated 521 readable sequences and 67% of them matched function-known genes by homolog searching; among which, 18% were predicted to function in stress response, 23.9% in metabolism, 7.3% in regulation of transcription and 2.7% in others

Nguyen et al. (2006)

Sesuvium portulacastrum

In an attempt to isolate and identify the target genes relevant to salt tolerance in the mangrove associate (Sesuvium portulacastrum L.), a subtracted cDNA library was constructed via suppressive subtractive hybridization (SSH). Screening of this subtracted cDNA library revealed five clones involved in salt-tolerance pathways. Among the clones isolated, P66, P175, and P233 are novel because no significant similarity was obtained upon alignment with the GenBank database. Clone P89 demonstrated high homology with NADPH of Arabidopsis thaliana, whereas clone P152 was highly homologous with the gene encoding late embryogenesis abundant (LEA) protein of A. thaliana

Zeng et al. (2006)

A molecular biological study of salt tolerance was first reported in a mangrove B. gymnorrhiza by Sugihara et al. (2000) and they suggested that an oxygen evolving enhancer protein 1 (OEE1) has an important role in the salt tolerance of this mangrove. They reported that when young plants of B. gymnorrhiza are transferred from freshwater to a medium with a seawater salt level (500 mM NaCl), the intensity of a 33 kDa protein with pI 5.2 increases in the leaf extract as observed in 2-D gel electrophoresis. The N-terminal amino acids sequence of this protein has a significant homology with the mature region of the oxygen evolving enhancer protein 1 (OEE1) precursor. The deduced amino acid sequence consists of 322 amino acids and is 87% identical to that of Nicotiana tobacum. The expression of OEE1 was analyzed together with other OEE subunits (OEE2 and OEE3) and D1 protein of photosystem II. The transcript levels of all the three OEEs were enhanced by NaCl treatment, but the significant increase of D1 protein was not observed in B. gymnorrhiza. Sugihara et al. (2000) suggested that not only the OEE1 but also the OEE2 and OEE3 play an important role in the maintenance of PSII activity under NaCl stress conditions. In particular, OEE1 is essential for oxygen evolving activity and PSII stability. The expression of OEE1 is also considered to be the rate-limiting step in the assembly of the PSII subunit (Mizobuchi and Yamamoto 1989). Therefore, it is considered that the recovery or turnover of OEE1 is one of the mechanisms to maintain the capacity of PSII under NaCl stress.

Currently there are also ongoing genomic studies of B. gymonorrhiza. The first B. gymonorrhiza expressed sequence tag (EST) library, which collected 14,842 ESTs from leaves and roots after high salinity or hormone treatments were established by Miyama et al. (2006). Clustering and assembling of these sequences resulted in 6,943 unique genes. The EST collection of B. gymonorrhiza includes genes that share significant similarities with salt stress inducible genes. These genes can be categorized into five major categories such as (1) osmolyte biosynthesis, (2) reactive oxygen scavenger, (3) chaperones, (4) transporters and (5) signaling components. The unique gene collections obtained from the assembly of those ESTs were later used in microarray experiments to monitor transcript profiling in leaves and roots of salt-stressed B. gymonorrhiza (Miyama and Hanagata 2007). Totally, 228 genes displayed transcript levels fivefold higher than in controls, while 61 genes were downregulated to one-fifth of control levels. Among these remarkably differentially expressed genes, only 32.5% upregulated and 3.3% downregulated genes were co-regulated in upper and lower leaves, as well as in roots (Miyama and Hanagata 2007). The rest showed tissue-specific expression patterns (Miyama and Hanagata 2007). Differing from EST analysis, differentially expressed genes in microarray analysis fell into six categories of gene expression patterns (Miyama and Hanagata 2007).

The transcriptional response of B. gymnorrhiza to high salinity (500 mM NaCl) and hyperosmotic stress (1 M sorbitol) was investigated by microarray analysis (Miyama and Tada 2008). Statistical analysis of microarray revealed that 865 of 11,997 genes showed significant differential expression under salt and osmotic stress. Comparison of gene ontology (GO) categories of differentially expressed genes under the stress conditions revealed that the adaptation of B. gymnorrhiza to salt stress was accompanied by the upregulation of genes categorized for cell communication, signal transduction, lipid metabolic process, photosynthesis, multicellular organismal development and transport, and by downregulation of genes categorized for catabolic process. Hierarchical clustering of the 865 genes showed that expression profiles under salt stress were distinctly different from those under osmotic stress. B. gymnorrhiza maintains its leaf water potential and recovered from its photosynthesis rate that declined temporarily under salt stress, but not under osmotic stress. These results demonstrated a fundamental difference between the responses to salt and osmotic stress (Miyama and Tada 2008). The salt-responding genes that showed no sequence similarity to the public database entries were also detected in B. gymnorrhiza (Miyama and Tada 2008). Therefore, it is possible that these unknown salt-responding genes may contribute to the salt adaptation of B. gymnorrhiza in a unique and specific manner.

The differential display method was applied to transcripts extracted from leaves of B. gymnorrhiza treated with 500 mM NaCl for 0, 6 h, 3 and 28 days to identify genes that are differentially expressed in response to salt stress (Banzai et al. 2002). The expression of 12 transcripts, whose corresponding cDNA fragments differentially appeared on differential display, was then analyzed by Northern hybridization. Nine of them were affirmed to be upregulated or induced by salt treatment. The nine transcripts were divided into three groups based on their expression patterns. RNA transcripts to BG7, BG50, BG51, BG55 and BG67, whose levels were temporarily raised at 6 h, were assigned to Group I. Transcripts to BG60 and BG70, whose levels increased at 6 h, and remained at a high level for at least 28 days were assigned to Group II. Transcripts to BG56 and BG64 were assigned to Group III as their levels increased at 3 days, but then decreased (Banzai et al. 2002). By screening a cDNA library, five full-length cDNAs were cloned and putative protein products were identified for three of them by homology with known protein. The RNA transcript bg51 encodes a protein with homology to fructose-6-phosphate, 2-kinase/fructose-2,6-bisphophatase (F6P, 2-K/F26BPase), the bifunctional enzyme catalyzing both synthesis and degradation of fructose-2,6-bisphosphate (Fru-2,6-P2) which is an important regulator in the carbohydrate metabolism. The protein encoded by bg55 has homology with a protein of A. thaliana whose function is unknown. Transcripts bg56 and bg64 are encoded by proteins having very significant homology with dihydrolipoamide dehydrogenase (DLDH) and lipoic acid synthase (LAS), respectively. The results suggest that these RNA transcripts and their respective encoding proteins have some role in salt tolerance in B. gymnorrhiza (Banzai et al. 2002). The protein encoded by bg70, Group II transcript, is a novel protein with no homology with any proteins registered in the databases so far (Banzai et al. 2002). Further analysis of such Group II genes will reveal how B. gymnorrhiza adapts to high salinity.

In order to identify key genes in the regulation of salt tolerance in the mangrove plant B. gymnorrhiza, cDNA expression libraries were constructed from salt-treated roots and leaves using the host organism Agrobacterium tumefaciens (Ezawa and Tada 2009). Functional screening of the Agrobacterium libraries identified 44 putative salt tolerance genes in B. gymnorrhiza. A cDNA clone which is homologous to an unknown cDNA from the mangrove plant K. candel and the cyc02 gene from Catharanthus roseus conferred the highest level of salt tolerance to A. tumefaciens, which indicates that it plays a major role in the regulation of salt tolerance in mangrove plants. Several of the genes that were identified have not previously been implicated in plant salt tolerance (Ezawa and Tada 2009). Transgenic Arabidopsis plants expressing Bg70 and cyc02 homolog exhibited increased tolerance to NaCl. These results demonstrate that Agrobacterium functional screening is an effective supplemental method to pre-screen genes involved in salt tolerance (Ezawa and Tada 2009).

Screening for salinity tolerant genes was done in the root of the mangrove plant Bruguiera cylindrica by using suppression subtractive hybridization (SSH) and bacterial functional screening (Wong et al. 2007). One hundred twenty-six salinity tolerant cDNAs were identified and isolated from the root of B. cylindrica by both approaches (Wong et al. 2007). Sequencing of 51 subtracted cDNA clones that were differentially expressed in the root of B. cylindrica exposed to 342 mM NaCl revealed 10 tentative unique genes (TUGs) with putative functions in protein synthesis, storage and destination, metabolism, intracellular trafficking and other functions; and 9 unknown proteins. Bacterial functional screening revealed that the 75 cDNA sequences of B. cylindrica that conferred salinity tolerance to Escherichia coli consisted of 29 TUGs with putative functions in transportation, metabolism and other functions; and 33 with unknown functions. Both approaches yielded 42 unique sequences that have not been reported elsewhere to be stress related might have some role in salt tolerance in B. cylindrical (Wong et al. 2007). These unique genes may be valuable gene candidates for further analyses to unravel the mystery of salinity tolerance in mangrove plants.

In order to reveal the molecular mechanism of salt tolerance in mangroves gene expression pattern was identified in Kandelia candel (Huang et al. 2003). Ten cDNAs of genes were isolated and identified from K. candel by representational difference analysis of cDNA (cDNA RDA) under different NaCI concentrations (Huang et al. 2003). Of five genes expressed preferentially under salt condition, two were unknown; three were two kinds of cytosolic low-molecular mass heat-shock proteins (sHSPs) and ADP-ribosylation factor (ARF), respectively. The upregulation of sHSPs and ARF has some role in osmotic equilibrium by which the K. candel plant can resist salt damage. The expressions of other five genes were repressed under NaCI stress, two encoded cyclophilins; three were tonoplast intrinsic protein, early light-induced protein and 60S ribosomal protein, respectively.

Betaine-aldehyde dehydrogenase (BADH) gene that is involved in glycinebetaine synthesis in A. marina was first identified and cloned by Hibino et al. (2001). BADH was upregulated under salt stress, and this tendency was consistent with the accumulation of glycinebetaine in A. marina. Three other genes that encode A. marina betaine and/or proline transporters 1 (AmT1), 2 (AmT2) and 3 (AmT3), respectively, were also isolated by Waditee et al. (2002). The mRNA levels of the three transporters were measured, and it was observed that the levels of mRNAs for AmT1, AmT2 and AmT3, were constitutively low and almost the same in both leaf and root when A. marina was grown without salt stress. Upon the salt stress (400 mM NaCl), the levels of mRNAs in all three transporters, AmT1, -2 and -3, increased in both leaf and root. However, the increases in leaf were more pronounced than those in root for all three transporters. Salt stress induced the highest level of mRNA for AmT1 followed by AmT2 and AmT3, respectively. The accumulation levels of mRNA for AmT1, -2 and -3 increased with increasing concentration of NaCl, especially in leaves (Waditee et al. 2002). Since betaine synthesis occurs in chloroplasts upon the salt stress, it is reasonable that the synthesis of betaine transporters is also induced upon the salt stress because the synthesized betaine must be transported to the other plant organs where betaine synthesis activity is low (Takabe et al. 1997). Therefore, under high-salinity conditions, the betaine/proline transporters (AmT1, -2 and -3) appear to be involved in the accumulation of betaine by increasing the mRNA levels as well as post-translational activation in betaine-accumulating A. marina (Waditee et al. 2002).

In order to characterize the genes that contribute to combating salinity stress, the cDNA library of A. marina genes was constructed by Mehta et al. (2005). Random EST sequencing of 1,841 clones produced 1,602 quality reads. These clones were classified into functional categories, and BLAST comparisons revealed that 113 clones were homologous to genes earlier implicated in stress responses. Of the ESTs analyzed, 30% showed homology to previously uncharacterized genes in the public plant databases. Of this 30%, 52 clones were selected for reverse Northern analysis: 26 were shown to be upregulated and 5 shown to be downregulated under NaCl stress (Mehta et al. 2005). Expression patterns for the ‘unknown’ genes provide a starting point for the isolation of salt tolerance candidate genes, and further functional analysis will elucidate their role in salt tolerance. ESTs showing homology to stress-tolerant genes reported in literature represent the sixth most abundant category. Dehydrins (34 clones/12 genes) predominate in this class and include late-embryogenesis-related proteins and desiccation or drought-induced proteins. Other stress-induced genes present in this category include heat shock proteins, thioredoxin, osmotin and genes for osmolyte production such as BADH and pyrroline-5-carboxylate synthase. The analyzed EST pool contained transcripts coding for enzymes involved in the oxidative stress response such as catalase, superoxide dismutase, peroxidases, glutathione S-transferase and epoxide hydrolase. In addition, genes reported to be induced by heavy metal stress, such as metallothioneins, aluminum-induced protein(s), truncated copper-binding protein CUTA and divalent cation-tolerant gene, and those induced by anaerobic stress, such as alcohol dehydrogenases and submergence-induced genes, were also found in the ESTs sequenced. Transcripts coding for proteins involved in membrane transport and processing play an integral role in the response to water deficit such as that imposed by salt stress and include aquaporins, proline/glycine betaine transporter and Na+/H+ antiporter. In addition, protein factors involved in the regulation of signal transduction events, such as receptors, protein and lipid kinases, calmodulins and protein phosphatases, which may have a role in stress signaling pathways, have been categorized separately. Genes for a variety of transcription factors that contain typical DNA binding motifs, such as MYB, bZIP, ERF/AP2, have been demonstrated to be stress-inducible (Zhu 2002). Transcription factors containing similar domains are present in the A. marina ESTs and may have a role in regulating the response to salt stress (Mehta et al. 2005). At the genomic level, a large number of ESTs have been collected from NaCl stressed seedlings of A. marina through techniques of differential display or random sequencing of cDNA library clones (Mehta et al. 2005). Some genes in such EST collections, e.g., those coding for dehydrin and polypeptide hormone phytosulphokine, were continuously upregulated after 48 h of salt-stress (Mehta et al. 2005). Their transcript abundance returned to the normal level if salt stress was prolonged to 12–24 weeks, indicating adaptation of A. marina after long-term stress (Mehta et al. 2005).

Jithesh et al. (2006) studied the expression of antioxidant genes such as Cu–Zn SOD (Sod1), catalase (Cat1) and ferritin (Fer1) in response to salt, iron, hydrogen peroxide, mannitol and light stress by mRNA expression analysis in A. marina. In response to NaCl stress Cat1, Fer1 showed short-term induction while Sod1 transcript was found to be unaltered. Sod1, Cat1 and Fer1 mRNA levels were induced by iron, light stress and by direct H2O2 stress treatment, thus confirming their role in oxidative stress response.

Transcripts that showed enhanced expression during salt stress was cloned in the leaves of a salt-tolerant mangrove species, Aegiceras corniculatum using suppressive subtractive hybridization (SSH, Fu et al. 2005). cDNAs of freshwater germinated and irrigated seedling were used as driver and cDNAs of 6 h salt-stress seedling were used as tester. By sequencing the whole SSH library, 577 ESTs were found. Among which, 30 had no significant homology to any previously identified genes and 527 of the remaining 547 ESTs represent singletons. Real-time quantitative RT-PCR analysis of four transcripts’ expression pattern showed that all of their transcripts were up-regulated during 24 h after salt shock. Their sequences showed high homology to the delta-1-pyrroline-5-carboxylate synthetase, Na+/H+ antiporter and plasma membrane intrinsic proteins, respectively.

Another salt secreting mangrove species Acanthus ebracteatus has also been of concern recently. A. ebracteatus was chosen as a source for the generation of ESTs to isolate genes involved in salt tolerance of this mangrove plant (Nguyen et al. 2006). In this study, they isolated and sequenced 864 randomly selected cDNA clones from the primary cDNA library of A. ebracteatus. Sequence analyses demonstrated that 349 of these ESTs showed significant homology to functional proteins, of which 18% are particularly interesting as they correspond to genes involved in stress response. Some of these clones, including putative mannitol dehydrogenase, plastidic aldolase, secretory peroxidase, ascorbate peroxidase, and vacuolar H+-ATPase, may be related to osmotic homeostasis, ionic homeostasis, and detoxification (Nguyen et al. 2006). Hundred seven salinity tolerance candidate genes have been identified and isolated from the mangrove plant, A. ebracteatus by using bacterial functional assay (Nguyen et al. 2007). Sequence analysis of these putative salinity tolerant cDNA candidates revealed that 65% of them have not been reported to be stress related and may have great potential for the elucidation of unique salinity tolerant mechanisms in mangrove. Among the genes identified were also genes that had previously been linked to stress response including salinity tolerance (Nguyen et al. 2007). Even though many of these mangrove genes or gene products were reported in stress tolerance of higher plants, the mangrove proteins may display unique properties and function. For example, the mangrove allene oxide cyclise (AOC) homolog or “mangrin” (Yamada et al. 2002b), containing an usual sequence of 70 amino acids that is essential to salt tolerant phenotype, is not found in Lycopersicon and Arabidopsis AOC homologs. The successful identification and isolation of salt-tolerant candidates from A. ebracteatus provide a basis for further function elucidation, in addition to providing useful information for plant breeding and genetic engineering of crop plants with greater salinity tolerance that allow agriculture on saline soil.

Conclusion and future prospects

Salinity is a major abiotic stress that greatly affects plant growth and crop production globally. Sodium ions in saline soil are toxic to plants because of their adverse effects on potassium nutrition, cytosolic enzyme activities, photosynthesis, and metabolism. Mangroves tolerate high salinity by rejecting potentially harmful salts. Some species of mangroves actively excrete those salts leaking into the plant by means of specialized salt glands in their leaves and some species excrete salt by ultra filtration at the root cell membranes of cortical cells. Salt accumulators avoid the toxic effects of salt by compartmentation of Na+ and Cl ions into the vacuoles by Na+/H+ antiporter system. Accumulation of compatible solutes and induction of antioxidative enzymes are other mechanisms of salt tolerance in mangroves. Mangroves also provide a reservoir for some of the best known, and at times, novel genes and proteins, involved in tolerance to salinity stress, that are likely at work in other plants. The salt tolerance genes listed in this review most likely represent only the tip of the iceberg, and continuous efforts to isolate and identify novel useful genes and promoters from mangroves are necessary; DNA microarray technology in particular is likely to become a powerful tool for this purpose. Eventually, the largest challenge will be to combine these genes and promoters in a systematic and logical way in order to maximize plant salinity tolerance. When realized, genetic engineering of crop and industrial plant for salinity tolerance using genes isolated from mangroves will be a vitally important tool in the quest to alleviate the earth’s future problems concerning food, energy, and the environment.

Notes

Acknowledgments

The financial support received from Council of Scientific and Industrial Research (CSIR), India (project no. NWP-020) is gratefully acknowledged.

References

  1. Agarie S, Shimoda T, Shimizu Y, Baumann K, Sunagawa H, Kondo A, Ueno O, Nakahara T, Nose A, Cushman JC (2007) Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum. J Exp Bot 58:1957–1967PubMedGoogle Scholar
  2. Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedGoogle Scholar
  3. Ashihara H, Adachi K, Otawa M, Yasumoto E, Fukushima Y, Kato M, Sano H, Sasamoto H, Baba S (1997) Compatible solutes and inorganic ions in the mangrove plant Avicennia marina and their effects on the activities of enzymes. Z Naturforsh 52c:433–440Google Scholar
  4. Ashihara H, Wakahara S, Suzuki M, Kato A, Sasamoto H, Baba S (2003) Comparison of adenosine metabolism in leaves of several mangrove plants and a poplar species. Plant Physiol Biochem 41:133–139Google Scholar
  5. Aziz I, Khan MA (2001a) Effect of seawater on the growth, ion content and water potential of Rhizophora mucronata Lam. J Plant Res 114:369–373Google Scholar
  6. Aziz I, Khan MA (2001b) Experimental assessment of salinity tolerance of Ceriops tagal seedlings and saplings from the Indus delta, Pakistan. Aquat Bot 70:259–268Google Scholar
  7. Baconguis SR, Mauricio RA (1991) Forage and livestock production in the mangrove forest. Canopy 16:9–10Google Scholar
  8. Ball MC (1988a) Ecophysiology of mangroves. Trees Struct Funct 2:129–142Google Scholar
  9. Ball MC (1988b) Salinity tolerance in the mangrove Aegiceras corniculatum and Avicennia marina. I. Water use in relation to growth, carbon partitioning, and salt balance. Aust J Plant Physiol 15:447–464Google Scholar
  10. Ball MC (1996) Comparative ecophysiology of mangrove forest and tropical lowland moist forest. In: Mulkey SS, Chazdon RL, Smith AO (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 461–469Google Scholar
  11. Ball MC, Farquhar MC (1984) Photosynthetic and stomatal responses of two mangrove species, Aegiceras corniculatum and Avicennia marina, to long term salinity and humidity conditions. Plant Physiol 74:7–11PubMedGoogle Scholar
  12. Ball MC, Passioura JB (1995) Carbon gain in relation to water use: photosynthesis in mangroves. In: Schulze ED, Caldwell NM (eds) Ecophysiology of photosynthesis. Springer, Berlin, Heidelberg, New York, pp 247–257Google Scholar
  13. Ball MC, Pidsley SM (1995) Growth responses to salinity in relation to distribution of two mangrove species, Sonneratia alba and S. lanceolata, in northern Australia. Funct Ecol 9:77–85Google Scholar
  14. Banzai T, Hershkovits G, Katcoff DJ, Hanagata N, Dubinsky Z, Karube I (2002) Identification and characterization of mRNA transcripts differentially expressed in response to high salinity by means of differential display in the mangrove, Bruguiera gymnorrhiza. Plant Sci 162:499–505Google Scholar
  15. Banzai T, Hanagata N, Dubinsky Z, Karube I (2003) Fructose-2, 6-bisphosphate contents were increased in response to salt, water and osmotic stress in leaves of Bruguiera gymnorrhiza by differential changes in the activity of the bifunctional enzyme 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphate 2-phosphatase. Plant Mol Biol 53:51–59PubMedGoogle Scholar
  16. Becker P, Asmat A, Mohamad J, Moksin M, Tyree MT (1997) Sap flow rates of mangrove trees are not usually low. Trees Struct Funct 11:432–443Google Scholar
  17. Biebl R, Kinzel H (1965) Blattbau und Salzhaushalt von Laguncularia racemosa (L) Gaertn. f. und anderer Mangrovenbäume auf Puerto Rico. Ost Bot Zeit 112:56–93Google Scholar
  18. Burchett MD, Clarke CJ, Field CD, Pulkownik A (1989) Growth and respiration in two mangrove species at a range of salinities. Physiol Plant 75:299–303Google Scholar
  19. Cheeseman JM, Herendeen LB, Cheeseman AT, Clough BF (1997) Photosynthesis and photoprotection in mangroves under field conditions. Plant Cell Environ 20:579–588Google Scholar
  20. Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448CrossRefGoogle Scholar
  21. Clough BF (1984) Growth and salt balance of the mangroves. Avicennia marina (Forsk.) Vierh. and Rhizophora stylosa Griff. in relation to salinity. Aust J Plant Physiol 11:419–430Google Scholar
  22. Clough BF, Sim RG (1989) Changes in gas exchange characteristics and water use efficiency of mangroves in response to salinity and vapor pressure deficit. Oecologia 79:38–44Google Scholar
  23. Clough BF, Andrew TJ, Cowan IR (1982) Physiological processes in mangroves. In: Clough BF (ed) Mangrove ecosystems in Australia: structure, function and management. Australian National Press, Canberra, pp 193–210Google Scholar
  24. Cram JW, Torr PG, Ross DA (2002) Salt allocation during leaf development and leaf fall in mangroves. Trees Struct Funct 16:112–119Google Scholar
  25. Das AB, Basak UC, Das P (1994) Karyotype diversity in three species of Heritiera, a common mangrove tree on the Orissa coast. Cytobios 80:71–78Google Scholar
  26. Das AB, Parida AK, Basak UC, Das P (2002) Studies on pigments, proteins and photosynthetic rates in some mangroves and mangrove associates from Bhitarkanika. Orissa Mar Biol 141:415–422Google Scholar
  27. Datta PN, Ghosh M (2003) Estimation of osmotic potential and free amino acids in some mangroves of the Sundarbans, India. Acta Bot Croast 62:37–45Google Scholar
  28. De Graaf GJ, Xuan TT (1999) Extensive shrimp farming, mangrove clearance and marine fisheries in the southern provinces of Vietnam. Mangroves Salt Marshes 2:159–166Google Scholar
  29. Delphine S, Alvino A, Zacchini M, Loreto F (1998) Consequence of salt stress on conductance to CO2 diffusion, Rubisco characteristics of spinach leaves. Aust J Plant Physiol 25:395–402Google Scholar
  30. Downton WJS (1982) Growth and osmotic relations of the mangrove, Avicennia marina, as influenced by salinity. Aust J Plant Physiol 9:519–528Google Scholar
  31. Drennan PM, Berjak P, Pammenter NW (1992) Ion gradients and adenosine triphosphatase localization in the salt glands of Avicennia marina (Forssk.) Vierh. S Afr J Bot 58:486–490Google Scholar
  32. Dschida DJ, Platt-Aloia KA, Thomson WW (1992) Epidermal peels of Avicennia germinans (L.) Stearn: a useful system to study the function of salt gland. Ann Bot 70:501–509Google Scholar
  33. Ellison AM, Farnsworth EJ (1997) Simulated sea-level change alters anatomy, physiology, growth, and reproduction of red mangrove (Rhizophora mangle L.). Oecologia 112:435–446Google Scholar
  34. Elmqvist T, Cox PA (1996) The evolution of vivipary in flowering plants. Oikos 77:3–9Google Scholar
  35. Elphick CH, Sanders D, Maathuis FJM (2001) Critical role of divalent cations and Na+ efflux in Arabidopsis thaliana salt tolerance. Plant Cell Environ 24:733–740Google Scholar
  36. Ezawa S, Tada Y (2009) Identification of salt tolerance genes from the mangrove plant Bruguiera gymnorrhiza using Agrobacterium functional screening. Plant Sci 176:272–278Google Scholar
  37. Fernandes MEB (1991) Tool use and predation of oysters (Crassostrea rhizophorae) by the tufted capuchin, Cebus apella apella, in brackish-water mangrove swamp. Primates 32:529–531Google Scholar
  38. Field CD (1995) Impact of expected climate change on mangroves. Hydrobiologia 295:75–81Google Scholar
  39. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedGoogle Scholar
  40. Fu XH, Huang YL, Deng SL, Zhou RC, Yang GL, Ni XW, Li WJ, Shi SH (2005) Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Plant Sci 169:147–154Google Scholar
  41. Garbarino J, DuPont FM (1988) NaCl induces a Na+/H+ antiport in tonoplast vesicles from barley roots. Plant Physiol 86:231–236PubMedGoogle Scholar
  42. Gilman EL, Ellison J, Duke NC, Field C (2008) Threats to mangroves from climate change and adaptation options. Aquat Bot 89:237–250Google Scholar
  43. Golldack D, Deitz KJ (2001) Salt induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol 125:1643–1654PubMedGoogle Scholar
  44. Gopal B, Krishnamurthy K (1993) Wetlands of South Asia. In: Whigham DF, Dy Kyjova D, Hejny S (eds) Wetlands of the world. Kluwer, Netherlands, pp 345–414Google Scholar
  45. Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190Google Scholar
  46. Griffiths ME, Rotjan RD, Ellmore GS (2008) Differential salt deposition and excretion on leaves of Avicennia germinans mangroves. Caribb J Sci 44:267–271Google Scholar
  47. Hamilton LS, Murphy DH (1988) Use and management of nipa palm (Nypa fruticans, Arecaeae): a review. Econ Bot 42:206–213Google Scholar
  48. Hanagata N, Takemura T, Karube I, Dubinsky Z (1999) Salt water relationships in mangrove. Isr J Plant Sci 47:63–76Google Scholar
  49. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedGoogle Scholar
  50. Henkel PA (1979) The concept of vivipary in the plant world (in Russian). Zh Obshch Biol 40:60–66Google Scholar
  51. Hibino T, Meng YL, Kawamitsu Y, Uehara N, Matsuda N, Tanaka Y, Ishikawa H, Baba S, Takabe T, Wada K, Ishii T, Takabe T (2001) Molecular cloning and functional characterization of two kinds of betaine-aldehyde dehydrogenase in betaine-accumulating mangrove Avicennia marina (Forsk.) Vierh. Plant Mol Biol 45:353–363PubMedGoogle Scholar
  52. Hogarth PJ (1999) The biology of mangroves. Oxford University Press, New YorkGoogle Scholar
  53. Huang W, Fang XD, Li GY, Lin QF, Zhao WM (2003) Cloning and expression analysis of salt responsive gene from Kandelia candel. Biol Plant 47:501–507Google Scholar
  54. Hyde KD, Lee SY (1995) Ecology of mangrove fungi and their role in nutrient cycling: what gaps occur in our knowledge? Hydrobiologia 295:107–118Google Scholar
  55. Jagtap TG, Nagle VL (2007) Response and adaptability of mangrove habitats from the Indian subcontinent to changing climate. Ambio 36:328–334PubMedGoogle Scholar
  56. Jithesh MN, Prashanth SR, Sivaprakash KR, Parida A (2006) Monitoring expression profiles of antioxidant genes to salinity, iron, oxidative, light and hyperosmotic stresses in the highly salt tolerant grey mangrove, Avicennia marina (Forsk.) Vierh. by mRNA analysis. Plant Cell Rep 25:865–876PubMedGoogle Scholar
  57. Kartawinata K, Adisomarto S, Soemodihardjo S, Tantra IGM (1979) Status Pengetahuan Hutan Bakau di Indonesia. In: Soemodihardjo S, Nontji A, Djamali A (eds) Proceedings of seminar ecosystem Hutan mangrove, LIPI, Indonesia, pp 21–39Google Scholar
  58. Kemis JR (1984) Petiolar glands in Combretaceae: new observations and an anatomical description of the extra-floral nectar of buttonwood (Conocarpus erectus). Am J Bot 71:34Google Scholar
  59. Kemis JR, Lersten NR (1984) Petiolar glands in Combretaceae: review of past ambiguities and an anatomical description of the sunken gland of white mangrove (Laguncularia racemosa). Am J Bot 71:34–35Google Scholar
  60. Khan MA, Aziz I (2001) Salinity tolerance in some mangrove species from Pakistan. Wetl Ecol Manag 9:219–223Google Scholar
  61. Kim JH, Dupont L, Behling H, Versteegh GJM (2005) Impacts of rapid sea-level rise on mangrove deposit erosion: application of taraxerol and Rhizophora records. J Quat Sci 20:221–225Google Scholar
  62. Krauss KW, Lovelock CE, McKee KL, Lopez-Hoffman L, Ewe SML, Sousa WP (2008) Environmental drivers in mangrove establishment and early development: a review. Aquat Bot 89:105–127Google Scholar
  63. Kura-Hotta M, Mimura M, Tsujimura T, Washitani-Nemoto S, Mimura T (2001) High salt-treatment-induced Na+ extrusion and low salt-treatment-induced Na+ accumulation in suspension-cultured cells of the mangrove plant, Bruguiera sexangula. Plant Cell Environ 24:1105–1112Google Scholar
  64. Lawton JR, Todd A, Naidoo DK (1981) Preliminary investigations into the structure of the roots of the mangroves Avicennia marina and Bruguiera gymnorrhiza in relation to ion uptake. New Phytol 88:713–722Google Scholar
  65. Li NY, Chen SL, Zhou XY, Li CY, Shao J, Wang RG, Fritz E, Huettermann A, Polle A (2008) Effect of NaCl on photosynthesis, salt accumulation and ion compartmentation in two mangrove species, Kandelia candel and Bruguiera gymnorrhiza. Aquat Bot 88:303–310Google Scholar
  66. Lin P (1988) Mangrove vegetation. China Ocean Press, BeijingGoogle Scholar
  67. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734PubMedGoogle Scholar
  68. Loughland RA (1998) Mangal roost selection by the flying-fox Pteropus alecto (Megachiroptera: Pteropodidae). Mar Freshw Res 49:351–352Google Scholar
  69. Lovelock CE, Feller IC (2003) Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest. Oecologia 134:455–462PubMedGoogle Scholar
  70. Low R, Rockel B, Kirsch M, Ratajczak R, Hortensteiner S, Martinoia E, Luttge U, Rausch T (1996) Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol 110:259–265PubMedGoogle Scholar
  71. Maathuis FJM, Prins HBA (1990) Patch clamp studies on root cell vacuoles of a salt-tolerant and a salt-sensitive Plantago species. Plant Physiol 92:23–28PubMedGoogle Scholar
  72. Mallery CH, Teas HJ (1984) The mineral ion relations of mangroves. I. Root cell compartments in a salt excluder and salt secreter species at low salinities. Plant Cell Physiol 25:1123–1131Google Scholar
  73. Martosubroto P, Naamin N (1977) Relationship between tidal forests (mangroves) and commercial shrimp production in Indonesia. Mar Res Indones 18:81–86Google Scholar
  74. Meher-Homji VM (1988) The Pichavaram mangroves. Blackbuck 4:1–12Google Scholar
  75. Mehta PA, Sivaprakash K, Parani M, Venkataraman G, Parida AK (2005) Generation and analysis of expressed sequence tags from the salt-tolerant mangrove species Avicennia marina (Forsk) Vierh. Theor Appl Genet 110:416–424PubMedGoogle Scholar
  76. Miller PC, Hom J, Poole DK (1975) Water relations of three mangrove species in South Florida. Ecol Plant 10:355–367Google Scholar
  77. Mimura T, Kura-Hotta M, Tsujimura T, Ohnishi M, Miura M, Okazaki Y, Mimura M, Maeshima M, Washitani-Nemoto S (2003) Rapid increase of vacuolar volume in response to salt stress. Planta 216:397–402PubMedGoogle Scholar
  78. Mishra S, Das AB (2003) Effect of NaCl on leaf salt secretion and antioxidative enzyme level in roots of a mangrove, Aegiceras corniculatum. Indian J Exp Biol 41:160–166PubMedGoogle Scholar
  79. Miyama M, Hanagata N (2007) Microarray analysis of 7029 gene expression patterns in Burma mangrove under high-salinity stress. Plant Sci 172:948–957Google Scholar
  80. Miyama M, Tada Y (2008) Transcriptional and physiological study of the response of Burma mangrove (Bruguiera gymnorrhiza) to salt and osmotic stress. Plant Mol Biol 68:119–129PubMedGoogle Scholar
  81. Miyama M, Shimizu H, Sugiyama M, Hanagata N (2006) Sequencing and analysis of 14,842 expressed sequence tags of Burma mangrove, Bruguiera gymnorrhiza. Plant Sci 171:234–241Google Scholar
  82. Mizobuchi A, Yamamoto Y (1989) Assembly of photosystem II polypeptides and expression of oxygen evolution activity in the chloroplasts of Euglena gracilis Z. during the dark–light transition. Biochim Biophys Acta 977:26–32Google Scholar
  83. Mukherjee AK, Acharya LK, Mattagajasingh I, Panda PC, Mohapatra T, Das P (2003) Molecular characterization of three Heritiera species using AFLP markers. Biol Plant 47:445–448Google Scholar
  84. Naidoo G, von Willert DJ (1995) Diurnal gas exchange characteristics and water use efficiency of three salt secreting mangroves at low and high salinities. Hydrobiologia 295:13–22Google Scholar
  85. Naidoo G, Rogalla H, von Willert DJ (1997) Gas exchange responses of a mangrove species, Avicennia marina, to waterlogged and drained conditions. Hydrobiologia 352:39–47Google Scholar
  86. Naidoo G, Tuffers AV, von Willert DJ (2002) Changes in gas exchange and chlorophyll fluorescence characteristics of two mangroves and a mangrove associate in response to salinity in the natural environment. Trees Struct Funct 16:140–146Google Scholar
  87. Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210PubMedGoogle Scholar
  88. Naskar KR, Mandal RN (1999) Ecology and biodiversity of Indian mangroves, vol I & II. Daya Publishers, New Delhi, IndiaGoogle Scholar
  89. Nguyen PD, Ho CL, Harikrishna JA, Wong MCVL, Rahim RA (2006) Generation and analysis of expressed sequence tags from the mangrove plant, Acanthus ebracteatus Vahl. Tree Genet Genomes 2:196–201Google Scholar
  90. Nguyen PD, Ho CL, Harikrishna JA, Wong MCVL, Rahim RA (2007) Functional screening for salinity tolerant genes from Acanthus ebracteatus Vahl using Escherichia coli as a host. Trees Struct Funct 21:515–520Google Scholar
  91. Osborne DJ, Berjak P (1997) The making of mangroves: the remarkable pioneering role played by the seed of Avicennia marina. Endeavour 21:143–147Google Scholar
  92. Paliyavuth C, Clough B, Patanaponpaiboon P (2004) Salt uptake and shoot water relations in mangroves. Aquat Bot 78:349–360Google Scholar
  93. Pantoja O, Dainty J, Blumwald E (1989) Ion channels in vacuoles from halophytes and glycophytes. FEBS Lett 255:92–96Google Scholar
  94. Parani M, Lakshmi M, Senthilkumar P, Ram N, Parida A (1998) Molecular phylogeny of mangroves. V. Analysis of genome relationships in mangrove species using RAPD and RFLP markers. Theor Appl Genet 97:617–625Google Scholar
  95. Parida A, Das AB, Das P (2002) NaCl stress causes changes in photosynthetic pigments, proteins and other metabolic components in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. J Plant Biol 45:28–36Google Scholar
  96. Parida AK, Das AB, Mittra B (2004a) Effects of salt on growth, ion accumulation photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees Struct Funct 18:167–174Google Scholar
  97. Parida AK, Das AB, Mohanty P (2004b) Defense potentials to NaCl in a mangrove, Bruguiera parviflora: differential changes of isoforms of some antioxidative enzymes. J Plant Physiol 161:531–542PubMedGoogle Scholar
  98. Parida AK, Das AB, Sanada Y, Mohanty P (2004c) Effects of salinity on biochemical components of the mangrove, Aegiceras corniculatum. Aquat Bot 80:77–87Google Scholar
  99. Parida AK, Mittra B, Das AB, Das TK, Mohanty P (2005) High salinity reduces the content of a highly abundant 23-kDa protein of the mangrove Bruguiera parviflora. Planta 221:135–140PubMedGoogle Scholar
  100. Passioura JB, Ball MC, Knight JH (1992) Mangroves may salinize the soil and in so doing limit their transpiration rate. Funct Ecol 6:476–481Google Scholar
  101. Pernetta JC (1993) Potential impact of climate change and sea level rise. In: Mangrove forests, climate change and sea level rise, IUCN, Gland, Switzerland, pp 22–32Google Scholar
  102. Perry CT, Berkeley A, Smithers SG (2008) Microfacies characteristics of a tropical, mangrove-fringed shoreline, Cleveland Bay, Queensland, Australia: sedimentary and taphonomic controls on mangrove facies development. J Sediment Res 78:77–97Google Scholar
  103. Peterson CA (1988) Exodermal casparian bands: there significance for ion uptake by roots. Physiol Plant 72:204–208Google Scholar
  104. Pezeshki SR, De Laune RD, Patrick WH Jr (1990) Differential response of selected mangroves to soil flooding and salinity: gas exchange and biomass partitioning. Can J For Res 20:869–874Google Scholar
  105. Popp M (1984a) Chemical composition of Australian mangroves I. Inorganic ions and organic acids. Z Pflangenphysiol 113:395–409Google Scholar
  106. Popp M (1984b) Chemical composition of Australian mangroves II. Inorganic ions and organic acids. Z Pflangenphysiol 113:411–421Google Scholar
  107. Popp M, Larther F, Weigel P (1985) Osmotic adaptation in Australian mangroves. Vegetatio 61:247–253Google Scholar
  108. Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia mayina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res 17:281–291PubMedGoogle Scholar
  109. Quesada V, Ponce MR, Micol JL (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154:421–436PubMedGoogle Scholar
  110. Rajesh A, Arumugam R, Venkatesalu V (1999) Responses of Ceriops roxburghiana to NaCl stress. Biol Plant 42:143–148Google Scholar
  111. Ratajczak R, Richter J, Luttge U (1994) Adaptation of the tonoplast V-type H1-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age. Plant Cell Environ 17:1101–1112Google Scholar
  112. Robertson AI, Alongi DM (1992) Tropical mangrove ecosystems. American Geophysical Union, Washington, DCGoogle Scholar
  113. Saenger P (1982) Morphological, anatomical and reproductive adaptations of Australian mangroves. In: Clough BF (ed), Mangrove ecosystems in Australia: structure, function and management. Australian Institute of Marine Science, Townsville, in association with Australian National University Press, Canberra, pp 153–191Google Scholar
  114. Saenger P (2002) Mangrove ecology, silvaculture and conservation. Kluwer, Dordrecht, the NetherlandsGoogle Scholar
  115. Saintilan N (1997) Above-and below-ground biomasses of two species of mangrove on the Hawkesbury river estuary, New South Wales. Mar Freshw Res 48:147–152Google Scholar
  116. Santisuk T (1983) Taxonomy of the terrestrial trees and shrubs in the mangrove formation in Thailand. In: The First UNDP/UNESCO Regional Training Course on Introduction to mangrove ecosystem. National Research Council, BangkokGoogle Scholar
  117. Sasekumar A, Chong VC, Leh MU, Cruz RD (1992) Mangroves as a habitat for fish and prawns. Hydrobiologia 247:195–207Google Scholar
  118. Scholander PF (1968) How mangroves desalinate seawater. Physiol Plant 21:251–261Google Scholar
  119. Scholander PF, Bradstreet ED, Hammel HT, Hemmingsen EA (1966) Sap concentrations in halophytes and other plants. Plant Physiol 41:529–532PubMedGoogle Scholar
  120. Schumaker KS, Sze H (1987) Decrease of pH gradients in tonoplast vesicles by NO3 and Cl: evidence for H+-coupled anion transport. Plant Physiol 83:490–496PubMedGoogle Scholar
  121. Selvam V (2003) Environmental classification of mangrove wetlands of India. Curr Sci 84:757–765Google Scholar
  122. Sengupta A, Chaudhuri S (2002) Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174PubMedGoogle Scholar
  123. Sheridan RP (1991) Epicaulous, nitrogen-fixing microepiphytes in a tropical mangal community, Guadeloupe, French West Indies. Biotropica 23:530–541Google Scholar
  124. Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901PubMedGoogle Scholar
  125. Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477PubMedGoogle Scholar
  126. Sidhu SS (1975) Structure of epidermis and stomatal apparatus of some mangrove species. In: Walsh GE, Snedaker SC, Teas HJ (eds) Proceedings of the international symposium on biology and management of mangroves, vol I. Institute of Food and Agricultural Science, University of Florida, Gainesville, pp 394–401Google Scholar
  127. Sobrado MA (2002) Effect of drought on leaf gland secretion of the mangrove Avicennia Germinans L. Trees Struct Funct 16:1–4Google Scholar
  128. Sobrado MA (2004) Influence of external salinity on the osmolality of xylem sap. leaf tissue and leaf gland secretion of the mangrove Laguncularia racemosa (L.) Gaertn. Trees Struct Funct 18:422–427Google Scholar
  129. Sobrado MA (2005) Leaf characteristics and gas exchange of the mangrove Laguncularia racemosa as affected by salinity. Photosynthetica 43:217–221Google Scholar
  130. Sobrado MA, Ewe SML (2006) Linking hypersalinity to leaf physiology in Avicennia germinans and Laguncularia racemosa coexisting in a scrub mangrove forest at the Indian River Lagoon Florida. Trees 20:679–687Google Scholar
  131. Sobrado MA, Greaves ED (2000) Leaf secretion composition of the mangrove species Avicennia germinans (L.) in relation to salinity: a case study by using total-reflection X-ray fluorescence analysis. Plant Sci 159:1–5PubMedGoogle Scholar
  132. Sperry JS, Tyree MT, Donnelly JR (1988) Vulnerability of xylem to embolism in a mangrove vs. an inland species of Rhizophoraceae. Physiol Plant 74:276–283Google Scholar
  133. Staus NL (1998) Habitat use and home range of West Indian whistling-ducks. J Wildl Manage 62:171–178Google Scholar
  134. Stelzer R, Kuo J, Koyro HW (1988) Substitution of Na+ by K+ in tissues and root vacuoles of barley (Hordeum vulgare L. cv.Aramir). J Plant Physiol 132:671–677Google Scholar
  135. Su H, Golldack D, Katsuhara M, Zhao C, Bohnert HJ (2001) Expression and stress-dependent induction of potassium channel transcripts in the common ice plant. Plant Physiol 125:604–641PubMedGoogle Scholar
  136. Su H, Golldack D, Zhao C, Bohnert HJ (2002) The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant. Plant Physiol 129:1482–1493PubMedGoogle Scholar
  137. Suarez N, Medina E (2006) Influence of salinity on Na+ and K+ accumulation, and gas exchange in Avicennia germinans. Photosynthetica 44:268–274Google Scholar
  138. Suarez N, Sobrado MA (2000) Adjustments in leaf water relations of mangrove Avicennia germinans (L.) seedlings grown in salinity gradient. Tree Physiol 20:277–282PubMedGoogle Scholar
  139. Sugihara K, Hanagata N, Dubinsky Z, Baba S, Karube J (2000) Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza. Plant Cell Physiol 41:1279–1285PubMedGoogle Scholar
  140. Takabe T, Nakamura T, Nomura M, Hayashi Y, Ishitani M, Muramoto Y, Tanaka A, Takabe T (1997) Glycinebetaine and the genetic engineering of salinity tolerance in plants. In: Satoh K, Murata N (eds) Stress responses of photosynthetic organisms. Elsevier Science, Amsterdem, pp 115–132Google Scholar
  141. Takemura T, Hanagata N, Sugihara K, Baba S, Karube I, Dubinsky Z (2000) Physiological and biochemical responses to salt stress in the mangrove, Bruguiera gymnorrhiza. Aquat Bot 68:15–28Google Scholar
  142. Takemura T, Hanagata N, Dubinsky Z, Karube I (2002) Molecular characterization and response to salt stress of mRNAs encoding cytosolic Cu/Zn superoxide dismutase and catalase from Bruguiera gymnorrhiza. Trees Struct Funct 16:94–99Google Scholar
  143. Tam NFY, Wong YS, Lu CY, Berry R (1997) Mapping and characterization of mangrove plant communities in Hong Kong. Hydrobiologia 352:25–37Google Scholar
  144. Tanaka Y, Fukuda A, Nakamura A, Yamada A, Saito T, Ozeki Y, Mimura T (2000) Molecular cloning and characterization of mangrove Na+/H+ antiporter cDNA. Plant Cell Physiol 41(Suppl):27Google Scholar
  145. Taura T, Jwaikawa Y, Furumoto M, Katou K (1988) A model for radical radial water transport across plant roots. Protoplasma 144:170–179Google Scholar
  146. Tomascik T, Mah AJ, Nontji A, Moosa MK (1997) The ecology of the Indonesian seas, Part II. Eric Oey, SingaporeGoogle Scholar
  147. Tomlinson PB (1986) The botany of mangroves. Cambridge University Press, CambridgeGoogle Scholar
  148. Tomlinson PB, Cox PA (2000) Systematic and functional anatomy of seedlings in mangrove Rhizophoraceae: vivipary explained? Bot J Linn Soc 134:215–231Google Scholar
  149. Turner RE (1992) Coastal wetlands and penaeid shrimp habitat. In: Stroud RE (ed) Stemming the tide of coastal fish habitat loss. Marine Recreational Fisheries Publication, vol 14. National Coalition for Marine Conservation, Savannah, GA, USA, pp 97–104Google Scholar
  150. UNEP-WCMC (2006) In the front line: shoreline protection and other ecosystem services from mangroves and coral reefs. UNEP-WCMC, Cambridge, UK, p 33Google Scholar
  151. Waditee R, Hibino T, Tanaka Y, Nakamura T, Incharoensakdi A, Hayakawa S, Suzuki S, Futsuhara Y, Kawamitsu Y, Takabe T (2002) Functional characterization of betaine/proline transporters in betaine-accumulating mangrove. J Biol Chem 277:18373–18382PubMedGoogle Scholar
  152. Wang WQ, Ke L, Tam NFY, Wong YS (2002) Changes in the main osmotica during the development of Kandelia candel hypocotyls and after mature hypocotyls were transplanted in solutions with different salinities. Mar Biol 141:1029–1034Google Scholar
  153. Werner A, Stelzer R (1990) Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl. Plant Cell Environ 13:243–255Google Scholar
  154. Wong YY, Ho CL, Nguyen PD, Teo SS, Harikrishna JA, Rahim RA, Wong MCVL (2007) Isolation of salinity tolerant genes from the mangrove plant, Bruguiera cylindrica by using suppression subtractive hybridization (SSH) and bacterial functional screening. Aquat Bot 86:117–122Google Scholar
  155. Yamada A, Saitoh T, Mimura T, Ozeki Y (2002a) Expression of mangrove allene oxide cyclase enhances salt tolerance in Escherichia coli, yeast, and tobacco cells. Plant Cell Physiol 43:903–910PubMedGoogle Scholar
  156. Yamada A, Sekiguchi M, Mimura T, Ozeki Y (2002b) The role of plant CCT alpha in salt- and osmotic-stress tolerance. Plant Cell Physiol 43:1043–1048PubMedGoogle Scholar
  157. Yasumoto E, Adachi K, Kato M, Sasamoto H, Baba S, Ashihara H (1999) Uptake of inorganic ions and compatible solutes in cultured mangrove cells during salt stress. In Vitro Cell Dev Biol Plant 35:82–85Google Scholar
  158. Ye Y, Tam NFY, Lu CY, Wong YS (2005) Effects of salinity on germination, seedling growth and physiology of three salt-secreting mangrove species. Aquat Bot 83:193–205Google Scholar
  159. Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ (1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant Cell Environ 22:559–565Google Scholar
  160. Zeng HC, Deng LH, Zhang CF (2006) Cloning of salt tolerance-related cDNAs from the Mangrove plant Sesuvium portulacastrum L. J Integr Plant Biol 48:952–957Google Scholar
  161. Zheng WJ, Wang WQ, Lin P (1999) Dynamics of elemental contents during the development of hypocotyls and leaves of certain mangrove species. J Exp Mar Biol Ecol 233:247–257Google Scholar
  162. Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124:941–948PubMedGoogle Scholar
  163. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedGoogle Scholar
  164. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445PubMedGoogle Scholar
  165. Zimmermann U, Zhu JJ, Meinzer FC, Goldstein G, Schneider H, Zimmermann G, Benkert R, Thuermer F, Melcher P, Webb D, Haase A (1994) High molecular weight organic compounds in the xylem sap of mangroves: implications for long-distance water transport. Bot Acta 107:218–229Google Scholar
  166. Zimmermann U, Wagner HJ, Heidecker M, Mimietz S, Schneider H, Szimtenings M, Haase A, Mitlohner R, Kruck W, Hoffmann R, Konig W (2002) Implications of mucilage on pressure bomb measurements and water lifting in trees rooting in high-salinity water. Trees 16:100–111Google Scholar

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© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Discipline of Marine Biotechnology and Ecology, Central Salt and Marine Chemicals Research InstituteCouncil of Scientific and Industrial Research (CSIR)BhavnagarIndia

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