Economic Uses of Salt-Tolerant Plants.

Climate change is likely to affect the ability of world agricultural systems to provide food, fibre, and fuel for the growing world population, especially since the area of salinised land will increase. However, as few species of plants (less than 1% of all plant species) can tolerate saline soils, we believe it is important to evaluate their potential as crops for salinised soils. We have analysed the economic and potential economic uses of plants that are listed in the database eHALOPH, including the most tolerant species, halophytes. For nine main categories of economic value, we found a total of 1365 uses amongst all species listed in eHALOPH as of July 2022; this number reduced to 918 amongst halophytes. We did not find any obvious differences in rankings between the more tolerant halophytes and the whole group of salt-tolerant plants, where the order of use was medical, followed by forage, traditional medicine, food and drink, fuel, fuelwood, and bioenergy. While many species are potentially important as crops, the effects of salt concentration on their uses are much less well documented. Increasing salt concentration can increase, decrease, or have no effect on the concentration of antioxidants found in different species, but there is little evidence on the effect of salinity on potential yield (the product of concentration and biomass). The effect of salinity on forage quality again varies with species, often being reduced, but the overall consequences for livestock production have rarely been evaluated. Salt-tolerant plants have potential uses in the bioremediation of degraded land (including revegetation, phytoremediation, and extraction of NaCl) as well as sources of biofuels, although any use of saline water for the sustainable irrigation of salt-tolerant crops must be viewed with extreme caution.

Potential use of saline resources for biofuel production using halophytes and marine algae: prospects and pitfalls.

There exists a global challenge of feeding the growing human population of the world and supplying its energy needs without exhausting global resources. This challenge includes the competition for biomass between food and fuel production. The aim of this paper is to review to what extent the biomass of plants growing under hostile conditions and on marginal lands could ease that competition. Biomass from salt-tolerant algae and halophytes has shown potential for bioenergy production on salt-affected soils. Halophytes and algae could provide a bio-based source for lignoceelusic biomass and fatty acids or an alternative for edible biomass currently produced using fresh water and agricultural lands. The present paper provides an overview of the opportunities and challenges in the development of alternative fuels from halophytes and algae. Halophytes grown on marginal and degraded lands using saline water offer an additional material for commercial-scale biofuel production, especially bioethanol. At the same time, suitable strains of microalgae cultured under saline conditions can be a particularly good source of biodiesel, although the efficiency of their mass-scale biomass production is still a concern in relation to environmental protection. This review summaries the pitfalls and precautions for producing biomass in a way that limits environmental hazards and harms for coastal ecosystems. Some new algal and halophytic species with great potential as sources of bioenergy are highlighted.

Salt tolerance in rice: seedling and reproductive stage QTL mapping come of age.

KEY MESSAGE: Reproductive stage salinity tolerance is most critical for rice as it determines the yield under stress. Few studies have been undertaken for this trait as phenotyping was cumbersome, but new methodology outlined in this review seeks to redress this deficiency. Sixty-three meta-QTLs, the most important genomic regions to target for enhancing salinity tolerance, are reported. Although rice has been categorized as a salt-sensitive crop, it is not equally affected throughout its growth, being most sensitive at the seedling and reproductive stages. However, a very poor correlation exists between sensitivity at these two stages, which suggests that the effects of salt are determined by different mechanisms and sets of genes (QTLs) in seedlings and during flowering. Although tolerance at the reproductive stage is arguably the more important, as it translates directly into grain yield, more than 90% of publications on the effects of salinity on rice are limited to the seedling stage. Only a few studies have been conducted on tolerance at the reproductive stage, as phenotyping is cumbersome. In this review, we list the varieties of rice released for salinity tolerance traits, those being commercially cultivated in salt-affected soils and summarize phenotyping methodologies. Since further increases in tolerance are needed to maintain future productivity, we highlight work on phenotyping for salinity tolerance at the reproductive stage. We have constructed an exhaustive list of the 935 reported QTLs for salinity tolerance in rice at the seedling and reproductive stages. We illustrate the chromosome locations of 63 meta-QTLs (with 95% confidence interval) that indicate the most important genomic regions for salt tolerance in rice. Further study of these QTLs should enhance our understanding of salt tolerance in rice and, if targeted, will have the highest probability of success for marker-assisted selections.

ZxNHX1 indirectly participates in controlling K+ homeostasis in the xerophyte Zygophyllum xanthoxylum.

The succulent xerophyte Zygophyllum xanthoxylum (Bunge) Engl. can absorb Na+ from the soil as an osmoticum in order to resist osmotic stress. The tonoplast Na+/H+ antiporter ZxNHX1 is essential for maintaining the salt-accumulation characteristics of Z. xanthoxylum by compartmentalizing Na+ into vacuoles. Previous results revealed that the silencing of ZxNHX1 greatly decreased Na+ accumulation in Z. xanthoxylum under 50 mM NaCl due to the weakened compartmentalisation; in addition, K+ concentration also significantly reduced in ZxNHX1-RNAi lines. Yet, whether the reduction of K+ concentration was directly triggered by the silencing of ZxNHX1 remains unclear. In this study, the growth parameters and expression levels of ZxSOS1, ZxHKT1;1, ZxAKT1 and ZxSKOR were measured in wild-type and ZxNHX1-RNAi lines under control or -0.5 MPa osmotic stress. The results showed that the silencing of ZxNHX1 inhibited the plant growth, decreased Na+ concentration in leaves, reduced the transcript abundance of ZxSOS1 and dramatically increased that of ZxHKT1;1 in roots of Z. xanthoxylum under osmotic stress; whereas tissue K+ concentrations and the expression level of ZxSKOR displayed no significant variations, and the expression of ZxAKT1 were significantly reduced in ZxNHX1-RNAi lines under osmotic stress, compared with the wild type. These results suggest that in Z. xanthoxylum, ZxNHX1 can maintain the normal growth by compartmentalizing Na+ into vacuoles, and regulate the spatial distribution of Na+ indirectly by affecting the expressions of ZxSOS1 and ZxHKT1;1. Moreover, the silencing of ZxNHX1 is not the main reason that led to the reduction of K+ concentration in ZxNHX1-RNAi lines under 50 mM NaCl, and ZxNHX1 might be indirectly involved in regulating K+ homeostasis.

Improving crop salt tolerance using transgenic approaches: An update and physiological analysis.

Salinization of land is likely to increase due to climate change with impact on agricultural production. Since most species used as crops are sensitive to salinity, improvement of salt tolerance is needed to maintain global food production. This review summarises successes and failures of transgenic approaches in improving salt tolerance in crop species. A conceptual model of coordinated physiological mechanisms in roots and shoots required for salt tolerance is presented. Transgenic plants overexpressing genes of key proteins contributing to Na+ 'exclusion' (PM-ATPases with SOS1 antiporter, and HKT1 transporter) and Na+ compartmentation in vacuoles (V-H+ ATPase and V-H+ PPase with NHX antiporter), as well as two proteins potentially involved in alleviating water deficit during salt stress (aquaporins and dehydrins), were evaluated. Of the 51 transformations, with gene(s) involved in Na+ 'exclusion' or Na+ vacuolar compartmentation that contained quantitative data on growth and include a non-saline control, 48 showed improvements in salt tolerance (less impact on plant mass) of transgenic plants, but with only two tested in field conditions. Of these 51 transformations, 26 involved crop species. Tissue ion concentrations were altered, but not always in the same way. Although glasshouse data are promising, field studies are required to assess crop salinity tolerance.

Secretory structures in plants: Lessons from the Plumbaginaceae on their origin, evolution and roles in stress tolerance.

The Plumbaginaceae (non-core Caryophyllales) is a family well known for species adapted to a wide range of arid and saline habitats. Of its salt-tolerant species, at least 45 are in the genus Limonium; two in each of Aegialitis, Limoniastrum and Myriolimon, and one each in Psylliostachys, Armeria, Ceratostigma, Goniolimon and Plumbago. All the halophytic members of the family have salt glands and salt glands are also common in the closely related Tamaricaceae and Frankeniaceae. The halophytic species of the three families can secrete a range of ions (Na+ , K+ , Ca2+ , Mg2+ , Cl- , HCO3- , SO42- ) and other elements (As, Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn). Salt glands are, however, absent in salt-tolerant members of the sister family Polygonaceae. We describe the structure of the salt glands in the three families and consider whether glands might have arisen as a means to avoid the toxicity of Na+ and/or Cl- or to regulate Ca2+ concentrations with the leaves. We conclude that the establishment of lineages with salt glands took place after the split between the Polygonaceae and its sister group the Plumbaginaceae.

Could vesicular transport of Na+ and Cl- be a feature of salt tolerance in halophytes?

Background: Halophytes tolerate external salt concentrations of 200 mm and more, accumulating salt concentrations of 500 mm and more in their shoots; some, recretohalophytes, excrete salt through glands on their leaves. Ions are accumulated in central vacuoles, but the pathway taken by these ions from the outside of the roots to the vacuoles inside the cells is poorly understood. Do the ions cross membranes through ion channels and transporters or move in vesicles, or both? Vesicular transport from the plasma membrane to the vacuole would explain how halophytes avoid the toxicity of high salt concentrations on metabolism. There is also a role for vesicles in the export of ions via salt glands. Scope and Methods: We have collected data on the fluxes of sodium and chloride ions in halophytes, based on the weight of the transporting organs and on the membrane area across which the flux occurs; the latter range from 17 nmol m-2 s-1 to 4.2 µmol m-2 s-1 and values up to 1 µmol m-2 s-1 need to be consistent with whatever transport system is in operation. We have summarized the sizes and rates of turnover of vesicles in plants, where clathrin-independent vesicles are 100 nm or more in diameter and can merge with the plasma membrane at rates of 100 s-1. We gathered evidence for vesicular transport of ions in halophytes and evaluated whether vesicular transport could account for the observable fluxes. Conclusions: There is strong evidence in favour of vesicular transport in plants and circumstantial evidence in favour of the movement of ions in vesicles. Estimated rates of vesicle turnover could account for ion transport at the lower reported fluxes (around 20 nmol m-2 s-1), but the higher fluxes may require vesicles of the order of 1 µm or more in diameter. The very high fluxes reported in some salt glands might be an artefact of the way they were measured.

Metabolic and physiological adjustment of Suaeda maritima to combined salinity and hypoxia.

Background and Aims: Suaeda maritima is a halophyte commonly found on coastal wetlands in the intertidal zone. Due to its habitat S. maritima has evolved tolerance to high salt concentrations and hypoxic conditions in the soil caused by periodic flooding. In the present work, the adaptive mechanisms of S. maritima to salinity combined with hypoxia were investigated on a physiological and metabolic level. Methods: To compare the adaptive mechanisms to deficient, optimal and stressful salt concentrations, S. maritima plants were grown in a hydroponic culture under low, medium and high salt concentrations. Additionally, hypoxic conditions were applied to investigate the impact of hypoxia combined with different salt concentrations. A non-targeted metabolic approach was used to clarify the biochemical pathways underlying the metabolic and physiological adaptation mechanisms of S. maritima . Key Results: Roots exposed to hypoxic conditions showed an increased level of tricarboxylic acid (TCA)-cycle intermediates such as succinate, malate and citrate. During hypoxia, the concentration of free amino acids increased in shoots and roots. Osmoprotectants such as proline and glycine betaine increased in concentrations as the external salinity was increased under hypoxic conditions. Conclusions: The combination of high salinity and hypoxia caused an ionic imbalance and an increase of metabolites associated with osmotic stress and photorespiration, indicating a severe physiological and metabolic response under these conditions. Disturbed proline degradation in the roots induced an enhanced proline accumulation under hypoxia. The enhanced alanine fermentation combined with a partial flux of the TCA cycle might contribute to the tolerance of S. maritima to hypoxic conditions.

eHALOPH a Database of Salt-Tolerant Plants: Helping put Halophytes to Work.

eHALOPH (http://www.sussex.ac.uk/affiliates/halophytes/) is a database of salt-tolerant plants-halophytes. Records of plant species tolerant of salt concentrations of around 80 mM sodium chloride or more have been collected, along with data on plant type, life form, ecotypes, maximum salinity tolerated, the presence or absence of salt glands, photosynthetic pathway, antioxidants, secondary metabolites, compatible solutes, habitat, economic use and whether there are publications on germination, microbial interactions and mycorrhizal status, bioremediation and of molecular data. The database eHALOPH can be used in the analysis of traits associated with tolerance and for informing choice of species that might be used for saline agriculture, bioremediation or ecological restoration and rehabilitation of degraded wetlands or other areas.

Tissue tolerance: an essential but elusive trait for salt-tolerant crops.

For a plant to persist in saline soil, osmotic adjustment of all plant cells is essential. The more salt-tolerant species accumulate Na+ and Cl- to concentrations in leaves and roots that are similar to the external solution, thus allowing energy-efficient osmotic adjustment. Adverse effects of Na+ and Cl- on metabolism must be avoided, resulting in a situation known as 'tissue tolerance'. The strategy of sequestering Na+ and Cl- in vacuoles and keeping concentrations low in the cytoplasm is an important contributor to tissue tolerance. Although there are clear differences between species in the ability to accommodate these ions in their leaves, it remains unknown whether there is genetic variation in this ability within a species. This viewpoint considers the concept of tissue tolerance, and how to measure it. Four conclusions are drawn: (1) osmotic adjustment is inseparable from the trait of tissue tolerance; (2) energy-efficient osmotic adjustment should involve ions and only minimal organic solutes; (3) screening methods should focus on measuring tolerance, not injury; and (4) high-throughput protocols that avoid the need for control plants and multiple Na+ or Cl- measurements should be developed. We present guidelines to identify useful genetic variation in tissue tolerance that can be harnessed for plant breeding of salt tolerance.

Plant salt tolerance: adaptations in halophytes.

BACKGROUND: Most of the water on Earth is seawater, each kilogram of which contains about 35 g of salts, and yet most plants cannot grow in this solution; less than 0·2% of species can develop and reproduce with repeated exposure to seawater. These 'extremophiles' are called halophytes. SCOPE: Improved knowledge of halophytes is of importance to understanding our natural world and to enable the use of some of these fascinating plants in land re-vegetation, as forages for livestock, and to develop salt-tolerant crops. In this Preface to a Special Issue on halophytes and saline adaptations, the evolution of salt tolerance in halophytes, their life-history traits and progress in understanding the molecular, biochemical and physiological mechanisms contributing to salt tolerance are summarized. In particular, cellular processes that underpin the ability of halophytes to tolerate high tissue concentrations of Na+ and Cl−, including regulation of membrane transport, their ability to synthesize compatible solutes and to deal with reactive oxygen species, are highlighted. Interacting stress factors in addition to salinity, such as heavy metals and flooding, are also topics gaining increased attention in the search to understand the biology of halophytes. CONCLUSIONS: Halophytes will play increasingly important roles as models for understanding plant salt tolerance, as genetic resources contributing towards the goal of improvement of salt tolerance in some crops, for re-vegetation of saline lands, and as 'niche crops' in their own right for landscapes with saline soils.

Introduction to the Special Issue: Halophytes in a changing world.

Climate change will bring about rising sea levels and increasing drought, both of which will contribute to increasing salinization in many regions of the world. There will be consequent effects on our crops, which cannot withstand significant salinization. This Special Issue looks at the roles that can be played by halophytes, extremophiles that do tolerate salinities toxic to most plants. In an ecological context, papers deal with the conservation of a rare species, the effects of rising concentrations of CO2 and flooding on coastal vegetation, and the consequences of tree planting in inland plains for salinization. Physiological studies deal with the different effects of chlorides and sulfates on the growth of halophytes, the ability of some parasitic plants to develop succulence when growing on halophytic hosts and the interesting finding that halophytes growing in their natural habitat do not show signs of oxidative stress. Nevertheless, spraying with ascorbic acid can enhance ascorbic acid-dependent antioxidant enzymes and growth in a species of Limonium. Enzymes preventing oxidative stress are expressed constitutively as is the case with the vacuolar H-ATPase, a key enzyme in ion compartmentation. A comparison of salt-excreting and non-excreting grasses showed the former to have higher shoot to root Na(+) ratios than the latter. A particularly tolerant turf grass is described, as is the significance of its ability to secrete ions. A study of 38 species showed the importance of the interaction of a low osmotic potential and cell wall properties in maintaining growth. From an applied point of view, the importance of identifying genotypes and selecting those best suited for the product required, optimizing the conditions necessary for germination and maximizing yield are described. The consequence of selection for agronomic traits on salt tolerance is evaluated, as is the use of halophytes as green manures. Halophytes are remarkable plants: they are rare in relation to the total number of flowering plants and they tolerate salinities that most species cannot. It is clear from the papers published in this Special Issue that research into halophytes has a distinct place in aiding our understanding of salt tolerance in plants, an understanding that is likely to be of importance as climate change and population growth combine to challenge our ability to feed the human population of the world.

Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes.

BACKGROUND: Halophytes are the flora of saline soils. They adjust osmotically to soil salinity by accumulating ions and sequestering the vast majority of these (generally Na(+) and Cl(-)) in vacuoles, while in the cytoplasm organic solutes are accumulated to prevent adverse effects on metabolism. At high salinities, however, growth is inhibited. Possible causes are: toxicity to metabolism of Na(+) and/or Cl(-) in the cytoplasm; insufficient osmotic adjustment resulting in reduced net photosynthesis because of stomatal closure; reduced turgor for expansion growth; adverse cellular water relations if ions build up in the apoplast (cell walls) of leaves; diversion of energy needed to maintain solute homeostasis; sub-optimal levels of K(+) (or other mineral nutrients) required for maintaining enzyme activities; possible damage from reactive oxygen species; or changes in hormonal concentrations. SCOPE: This review discusses the evidence for Na(+) and Cl(-) toxicity and the concept of tissue tolerance in relation to halophytes. CONCLUSIONS: The data reviewed here suggest that halophytes tolerate cytoplasmic Na(+) and Cl(-) concentrations of 100-200 mm, but whether these ions ever reach toxic concentrations that inhibit metabolism in the cytoplasm or cause death is unknown. Measurements of ion concentrations in the cytosol of various cell types for contrasting species and growth conditions are needed. Future work should also focus on the properties of the tonoplast that enable ion accumulation and prevent ion leakage, such as the special properties of ion transporters and of the lipids that determine membrane permeability.

Silicon decreases chloride transport in rice (Oryza sativa L.) in saline conditions.

Silicon can alleviate salt damage to plants, although the mechanism(s) still remains to be elucidated. In this paper, we report the effect of silicon on chloride transport in rice (Oryza sativa L.) seedlings in saline conditions. In the absence of salinity, silicon enhanced the growth of shoots, but not roots in three cultivars (cv. GR4, IR36, and CSR10). Salinity reduced the growth of both shoots and roots in all three genotypes. In saline conditions, addition of silicon to the culture solution again improved the growth of shoots, but not of roots. Under these saline conditions, the concentrations of chloride in the shoot were markedly decreased by adding silicon and the ratio of K(+)/Cl(-) was significantly increased, while the concentration of chloride in the roots was unchanged. The decrease in chloride concentration in the shoot was correlated with the decrease in transpirational bypass flow in rice, as shown by the transport of the apoplastic tracer trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS). Addition of silicon increased the net photosynthetic rate, stomata conductance, and transpiration of salt-stressed plants in cv. IR36, indicating that the reduction of chloride (and sodium) uptake by silicon was not through a reduction in transpiration rate. Silicon addition also increased the instantaneous water use efficiency of salt-stressed plants, while it did not change the relative growth rate of shoots. The results suggest that silicon addition decreased transpirational bypass flow in the roots, and therefore decreased the transport of chloride to the shoot.

High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis.

BACKGROUND AND AIMS: Phenotypic plasticity, the potential of specific traits of a genotype to respond to different environmental conditions, is an important adaptive mechanism for minimizing potentially adverse effects of environmental fluctuations in space and time. Suaeda maritima shows morphologically different forms on high and low areas of the same salt marsh. Our aims were to examine whether these phenotypic differences occurred as a result of plastic responses to the environment. Soil redox state, indicative of oxygen supply, was examined as a factor causing the observed morphological and physiological differences. METHODS: Reciprocal transplantation of seedlings was carried out between high and low marsh sites on a salt marsh and in simulated tidal-flow tanks in a glasshouse. Plants from the same seed source were grown in aerated or hypoxic solution, and roots were assayed for lactate dehydrogenase (LDH) and alcohol dehydrogenase, and changes in their proteome. KEY RESULTS: Transplanted (away) seedlings and those that remained in their home position developed the morphology characteristic of the home or away site. Shoot Na(+), Cl(-) and K(+) concentrations were significantly different in plants in the high and low marsh sites, but with no significant difference between home and away plants at each site. High LDH activity in roots of plants grown in aeration and in hypoxia indicated pre-adaptation to fluctuating root aeration and could be a factor in the phenotypic plasticity and growth of S. maritima over the full tidal range of the salt marsh environment. Twenty-six proteins were upregulated under hypoxic conditions. CONCLUSIONS: Plasticity of morphological traits for growth form at extremes of the soil oxygenation spectrum of the tidal salt marsh did not correlate with the lack of physiological plasticity in the constitutively high LDH found in the roots.

A new screening technique for salinity resistance in rice (Oryza sativa L.) seedlings using bypass flow.

A lack of screening techniques delays progress in research on salinity resistance in rice. In this study, we report our test of the hypothesis that an apoplastic pathway (the so-called bypass flow) causes a difference in salt resistance between rice genotypes and can be used in screening for salinity resistance. Fourteen-day-old seedlings of low- and high-Na(+) -transporting recombinant inbred lines (10 of each) of rice IR55178 were treated with 50 mm NaCl and 0.2 mm trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS), a bypass flow tracer, for short (4 d) and long (90 d) periods of time. The results showed that the average shoot Na(+) concentration and bypass flow for high-Na(+) -transporting lines were 1.4 and 2.4 times higher than those of low-Na(+) -transporting lines, respectively. There was a positive linear correlation between the percentage of bypass flow and Na(+) concentrations in the shoots, suggesting that the difference in Na(+) transport in rice is a consequence of different degrees of bypass flow. Moreover, a high correlation was found between bypass flow and seedling survival after prolonged salt stress: the lower the magnitude of bypass flow, the greater the seedling survival. We conclude that bypass flow could be used as a new screening technique for salt resistance in rice.

The role of lateral roots in bypass flow in rice (Oryza sativa L.).

Although an apoplastic pathway (the so-called bypass flow) is implicated in the uptake of Na(+) by rice growing in saline conditions, the point of entry of this flow into roots remains to be elucidated. We investigated the role of lateral roots in bypass flow using the tracer trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS) and the rice cv. IR36. PTS was identified in the vascular tissue of lateral roots using both epifluorescence microscopy and confocal laser scanning microscopy. Cryo-scanning electron microscopy and epifluorescence microscopy of sections stained with berberine-aniline blue revealed that the exodermis is absent in the lateral roots. We conclude that PTS can move freely through the cortical layers of lateral roots, enter the stele and be transported to the shoot via the transpiration stream.

Studies on sodium bypass flow in lateral rootless mutants lrt1 and lrt2, and crown rootless mutant crl1 of rice (Oryza sativa L.).

An apoplastic pathway, the so-called bypass flow, is important for Na+ uptake in rice (Oryza sativa L.) under saline conditions; however, the precise site of entry is not yet known. We report the results of our test of the hypothesis that bypass flow of Na+ in rice occurs at the site where lateral roots emerge from the main roots. We investigated Na+ uptake and bypass flow in lateral rootless mutants (lrt1, lrt2), a crown rootless mutant (crl1), their wild types (Oochikara, Nipponbare and Taichung 65, respectively) and in seedlings of rice cv. IR36. The results showed that shoot Na+ concentration in lrt1, lrt2 and crl1 was lower (by 20-23%) than that of their wild types. In contrast, the bypass flow quantified using trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid (PTS) was significantly increased in the mutants, from an average of 1.1% in the wild types to 3.2% in the mutants. Similarly, bypass flow in shoots of IR36 where the number of lateral and crown roots had been reduced through physical and hormonal manipulations was dramatically increased (from 5.6 to 12.5%) as compared to the controls. The results suggest that the path of bypass flow in rice is not at the sites of lateral root emergence.