Halophyte Improvement for a Salinized World

It is more important to improve the salt tolerance of crops in a salinized world with the situations of increasing populations, declining crop yields, and a decrease in agricultural lands. Attempts to produce salt-tolerant crops have involved the manipulation of existing crops through conventional breeding, genetic engineering and marker-assisted selection (MAS). However, these have, so far, not produced lines growing on highly saline water. Hence, the domestication of wild halophytes as crops appears to be a feasible way to develop agriculture in highly saline environments. In this review, at first, the assessment criteria of salt tolerance for halophytes are discussed. The traditional criteria for the classification of salinity in crops are less applicable to strong halophytes with cubic growth curves at higher salinities. Thus, realistic assessment criteria for halophytes should be evaluated at low and high salinity levels. Moreover, absolute growth rather than relative growth in fields during a crop's life cycle should be considered. Secondly, the use of metabolomics to understand the mechanisms by which halophytes respond to salt tolerance is highlighted as is the potential for metabolomics-assisted breeding of this group of plants. Metabolomics provides a better understanding of the changes in cellular metabolism induced by salt stress. Identification of metabolic quantitative trait loci (QTL) associated with salt tolerance might provide a new method to aid the selection of halophyte improvement. Thirdly, the identification of germplasm-regression-combined (GRC) marker-trait association and its potential to identifying markers associated with salt tolerance is outlined. Results of MAS/linkage map-QTL have been modest because of the absence of QTLs with tight linkage, the non-availability of mapping populations and the substantial time needed to develop such populations. To overcome these limitations, identification by GRC-based marker-trait association has been successfully applied to many plant traits, including salt tolerance. Finally, we provide a prospect on the challenges and opportunities for halophyte improvement, especially in the integration of metabolomics- and GRC-marker-assisted selection towards new or unstudied halophyte breeding, for which no other genetic information, such as linkage maps and QTL, are available.     

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.     

How Can Stomata Contribute to Salt Tolerance?

Although some of the physiological mechanisms which contributeto salt tolerance in plants are known, there are still somemajor gaps in understanding and it remains impossible to providea satisfactory integrated picture for the plant as a whole.The operation of stomata in halophytes has received little attentioneven though all of the salt present in the shoot (apart fromthat taken in during submergence) is thought to be carried inthe transpiration stream. In non-halophytes, stomatal functionis damaged by sodium ions, and disruption of the normal regulationof transpiration should be seen as a possible contributor totheir inability to survive in salt-laden soils. The developmentof salt-tolerant cultivars of crops may require attention tothe need for appropriate adaptations to the ionic relationsof stomatal guard cells. Despite the small amount of evidenceavailable, it is possible to identify two alternative adaptationsthat occur in the stomata of halophytes: (1) the guard cellscan utilize Na⁺instead of K⁺to achieve their normal regulationof turgor; (2) the guard cells continue to use K⁺and are ableto limit their intake of Na⁺. The second adaptation is worthyof further exploration because it may provide a means for ‘topdown’ control of transpiration and, therefore, of theamount of salt delivered to the shoot. This mechanism may bevery important in some of the glandless halophytes, and it couldbe of particular interest as a potential contributor to thedevelopment of salt tolerance in crops. Salt tolerance; stomata; transpiration; halophytes; ionic regulation; sodium ions     

Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model

Background As important components in saline agriculture, halophytes can help to provide food for a growing world population. In addition to being potential crops in their own right, halophytes are also potential sources of salt-resistance genes that might help plant breeders and molecular biologists increase the salt tolerance of conventional crop plants. One especially promising halophyte is Suaeda salsa, a euhalophytic herb that occurs both on inland saline soils and in the intertidal zone. The species produces dimorphic seeds: black seeds are sensitive to salinity and remain dormant in light under high salt concentrations, while brown seeds can germinate under high salinity (e.g. 600 mm NaCl) regardless of light. Consequently, the species is useful for studying the mechanisms by which dimorphic seeds are adapted to saline environments. S. salsa has succulent leaves and is highly salt tolerant (e.g. its optimal NaCl concentration for growth is 200 mm). A series of S. salsa genes related to salt tolerance have been cloned and their functions tested: these include SsNHX1, SsHKT1, SsAPX, SsCAT1, SsP5CS and SsBADH. The species is economically important because its fresh branches have high value as a vegetable, and its seed oil is edible and rich in unsaturated fatty acids. Because it can remove salts and heavy metals from saline soils, S. salsa can also be used in the restoration of salinized or contaminated saline land.Scope Because of its economic and ecological value in saline agriculture, S. salsa is one of the most important halophytes in China. In this review, the value of S. salsa as a source of food, medicine and forage is discussed. Its uses in the restoration of salinized or contaminated land and as a source of salt-resistance genes are also considered.     

Increasing salinity tolerance of grain crops: Is it worthwhile?

The productivity of wheat and barley was compared in soils of different salt concentrations with a limited water supply. Productivity was assessed as total dry weight or dry weight per unit of water used (water use efficiency, WUE). Barley achieved the highest productivity because it used more of the available water and it had a greater WUE for above-ground dry weight. However, when WUE for total organic weight of roots and shoots was determined, or WUE was corrected for grain production, wheat and barley had the same productivity. In two experiments in drying soils with different salt concentrations but the same amount of soil water, wheat and barley had a higher dry weight than salt-tolerant grasses and they were more productive than C₄ halophytes and non-halophytes when adjusted for water use. In one experiment, sown at a low plant density, barley and wheat used less water than some halophytes and they completed their life cycle leaving some water behind in the soil. Their higher WUE did not compensate for their lower water use. However, when all species were sown at a high density, wheat and barley were either as productive or more productive than the most salt-tolerant species, including a C₄ halophyte, as they used all the available water and had the highest WUE. A sunflower cultivar was similary more productive than a salt-tolerant relative. The contribution that salt-tolerant relatives of wheat, barley and sunflower can make to genetically improving the productivity of these species in dry saline soils is questioned.     

Physiological and molecular mechanisms of plant salt tolerance

Salt tolerance is an important economic trait for crops growing in both irrigated fields and marginal lands. The plant kingdom contains plant species that possess highly distinctive capacities for salt tolerance as a result of evolutionary adaptation to their environments. Yet, the cellular mechanisms contributing to salt tolerance seem to be conserved to some extent in plants although some highly salt-tolerant plants have unique structures that can actively excrete salts. In this review, we begin by summarizing the research in Arabidopsis with a focus on the findings of three membrane transporters that are important for salt tolerance: SOS1, AtHKT1, and AtNHX1. We then review the recent studies in salt tolerance in crops and halophytes. Molecular and physiological mechanisms of salt tolerance in plants revealed by the studies in the model plant, crops, and halophytes are emphasized. Utilization of the Na⁺ transporters to improve salt tolerance in plants is also summarized. Perspectives are provided at the end of this review.     

Leaf gas exchange and solute accumulation in the halophyte Salvadora persica grown at moderate salinity

The domestication of halophytes has been proposed as a strategy to expand cultivation onto unfavorable land. However, halophytes mainly have been considered for their performance in extremely saline environments, and only a few species have been characterized in terms of their tolerance and physiological responses to moderately high levels of salinity. Salvadora persica is an evergreen perennial halophyte capable of growing under extreme conditions, from very dry environments to highly saline soils. It possesses high potential economic value as a source of oil and medicinal compounds. To quantify its response to salinity, S. persica seedlings were exposed to 200 mM NaCl for 3 weeks, and growth, leaf gas exchange and solute accumulation were measured. The presence of NaCl induced a 100% increase in fresh weight and a 30% increase in dry weight, relative to non-salinized controls. Increases in fresh weight and dry weight were not associated with higher rates of net CO(2) assimilation, however. Analysis of ion accumulation revealed that S. persica leaves accumulated Na(+) as a primary osmoticum. The concentration of Na(+) in leaves of salinized plants was approximately 40-fold greater than that measured in non-salinized controls, and this was associated with significant reductions in leaf K(+) and Ca(2+) concentrations. In addition, a significant accumulation of proline, probably associated with osmotic adjustment and protection of membrane stability, occurred in roots of salinized plants.     

Salt-tolerant crops: origins,development, and prospects of the concept

Summary The genetic approach to the problems posed by salt-affected soils and water,i.e., breeding crops resistant to salinity stress, is traced to two principal origins: the European ecological interest in halophytes, and the exigencies of growing crops in the arid and semi-arid lands of the American West. The point is made that breeding for resistance to salinity stress cannot be divorced from breeding for various other desirable traits of mineral plant nutrition and metabolism. A survey is conducted of the existing body of information on breeding for desiderata of mineral nutrition in general and salt tolerance in particular. The prospects of breeding crops for salt tolerance are discussed, with emphasis on a) its relation to breeding for resistance to other mineral stresses; b) field trials; c) collaboration between plant physiologists and geneticist-breeders; and d) extensive exploration of germplasm.     

Halophytes--an emerging trend in phytoremediation

Halophytic plants are of special interest because these plants are naturally present in environments characterized by an excess of toxic ions, mainly sodium and chloride. Several studies have revealed that these plants may also tolerate other stresses including heavy metals based on the findings that tolerance to salt and to heavy metals may, at least partly, rely on common physiological mechanisms. In addition, it has been shown that salt-tolerant plants may also be able to accumulate metals. Therefore, halophytes have been suggested to be naturally better adapted to cope with environmental stresses, including heavy metals compared to salt-sensitive crop plants commonly chosen for phytoextraction purposes. Thus, potentially halophytes are ideal candidates for phytoextraction orphytostabilization of heavy metal polluted soils and moreover of heavy metal polluted soils affected by salinity. Some halophytes use excretion processes in order to remove the excess of salt ions from their sensitive tissues and in some cases these glandular structures are not always specific to Na+ and Cl- and other toxic elements such as cadmium, zinc, lead, or copper are accumulated and excreted by salt glands or trichomes on the surface of the leaves--a novel phytoremediation process called "phytoexcretion". Finally, the use of halophytes has also been proposed for soil desalination through salt accumulation in the plant tissue or dissolution of soil calcite in the rhizosphere to provide Ca2+ that can be exchanged with Na+ at cation exchange sites.     

Agricultural production of halophytes irrigated with seawater

Summary Growing agricultural crops with direct seawater irrigation has progressed within the past few years from the conceptual to the experimental phase. This has been accomplished by selecting halophytes with inherently high salinity tolerance for use as crop plants rather than by increasing the ability of traditional crop plants to tolerate seawater. Some of the halophytes being investigated for use as crops in seawater irrigation scenarios have high nutritional value as forage or fodder crops. Most of them also have high digestibility. The limiting factor in such use is their high salt content, but this limitation can be moderated. However, since seeds of halophytes do not accumulate salt any more than do those of glycophytes, the greatest promise for seawater-irrigated halophytes probably will be as seed crops. The seeds of many halophytes have high protein and oil contents and compare favorably with traditional oilseed crops. Sustained high yields of seed and biomass already have been obtained from some halophytes irrigated with seawater, and within the next few years seawater agriculture should proceed from the experimental to the operational phase.     

Salt Tolerance and Crop Potential of Halophytes

Although they represent only 2% of terrestrial plant species, halophytes are present in about half the higher plant families and represent a wide diversity of plant forms. Despite their polyphyletic origins, halophytes appear to have evolved the same basic method of osmotic adjustment: accumulation of inorganic salts, mainly NaCl, in the vacuole and accumulation of organic solutes in the cytoplasm. Differences between halophyte and gly-cophyte ion transport systems are becoming apparent. The pathways by which Na⁺ and Cl^? enters halophyte cells are not well understood but may involve ion channels and pinocytosis, in addition to Na⁺ and Cl^? transporters. Na⁺ uptake into vacuoles requires Na⁺/H⁺ antiporters in the tonoplast and H⁺ ATPases and perhaps PP_i ases to provide the proton motive force. Tonoplast antiporters are constitutive in halophytes, whereas they must be activated by NaCl in salt-tolerant glycophytes, and they may be absent from salt-sensitive glycophytes. Halophyte vacuoles may have a modified lipid composition to prevent leakage of Na⁺ back to the cytoplasm. Becuase of their diversity, halophytes have been regarded as a rich source of potential new crops. Halophytes have been tested as vegetable, forage, and oilseed crops in agronomic field trials. The most productive species yield 10 to 20 ton/ha of biomass on seawater irrigation, equivalent to conventional crops. The oilseed halophyte, Sali-cornia bigelovii, yields 2?t/ha of seed containing 28% oil and 31% protein, similar to soybean yield and seed quality. Halophytes grown on seawater require a leaching fraction to control soil salts, but at lower salinities they outperform conventional crops in yield and water use efficiency. Halophyte forage and seed products can replace conventional ingredients in animal feeding systems, with some restrictions on their use due to high salt content and antinutritional compounds present in some species. Halophytes have applications in recycling saline agricultural wastewater and reclaiming salt-affected soil in arid-zone irrigation districts.     

Distribution of VA mycorrhiza on halophytes on inland salt playas

The value of mycorrhizal association for higher plants has been well established. However, the impact of high salinity on the mycorrhizal relationship has not been investigated to any great extent. Inland salt playas represent an opportunity to test the impact of salinity because it is possible to obtain a gradient by following a transect from the centre of the salt playa to the higher outer zones. In a salt playa near Goshen, Utah, the sodium concentration ranged from 27,150 ppm in the centre to 25 ppm in the outer zone. In the playas with sodium concentrations of 20,000 ppm, no mycorrhiza were detected on the halophytes and no spores of mycorrhizal fungi were found in the soil. One percent of the roots of salt grass in soils containing 8,450 ppm of sodium were mycorrhizal. In soils containing 622 ppm of 45 percent of the roots of a salt-tolerant grass (hybrid ofAgropyron repens × Agropyron spicatum) were mycorrhizal. Halophytes such asSalicornia pacifica var.utahensis which are among the most salt tolerant halophytes of the inland salt playas rarely had mycorrhizal roots. The mycorrhizal associations appear to be very limited in inland salt playas with sodium content.     

Transcriptome Analysis of the Heritable Salt Tolerance of Prairie Cordgrass (<Emphasis Type="Italic">Spartina pectinata Link</Emphasis>)

The salt-tolerant capability of the candidate bioenergy crop prairie cordgrass greatly surpasses that of previously characterized prairie grass species and most other plants. To understand the mechanism of inherited salt tolerance, we compared phenotypic and genetic qualities in half-sib families of prairie cordgrass after salt treatment. Each family was treated with a 400 mM NaCl solution or a water control and then measured for various health phenotypes. Phenotypes associated with salt tolerance were shown to be moderately heritable between parent and offspring. RNA-seq analysis revealed differential regulation in unique pathways including metabolism, signaling, photosynthesis, and the circadian rhythm. The studies herein suggest that alternative regulation of the photosynthetic pathway could confer increased salt resistance in halophytes and can be monitored phenotypically or genetically in breeding programs. The improvement of salt-tolerant traits in prairie cordgrass would increase its potential to be grown as a bioenergy crop on lands that are not suitable for the growth of food crops.     

Symbiosis between the root-nodule bacterium Sinorhizobium meliloti and alfalfa (Medicago sativa) under salinization conditions

Two hundred forty-three isolates of alfalfa root-nodule bacteria (Sinorhizobium meliloti) were obtained from nodules and soils sampled in the northern Aral region, experiencing secondary salinization. Isolates obtained from nodules (N isolates) were significantly more salt-tolerant than those from soils (T isolates) when grown in a liquid medium with 3.5% NaCl. It was found that wild species of alfalfa, melilot, and trigonella preferably formed symbioses with salt-tolerant root-nodule bacteria in both salinized and nonsalinized soils. Only two alfalfa species, Medicago falcata and M. trautvetteri, formed efficient symbioses in soils contrasting in salinity. The formation of efficient symbiosis with alfalfa in the presence of 0.6% NaCl was studied in 36 isolates (N and T) differing in salt tolerance and symbiotic efficiency. Fifteen isolates formed efficient symbioses in the presence of salt. The increase in the dry weight of the plants was 25–68% higher than in the control group. The efficiency of symbiotic interaction under salinization conditions depended on the symbiotic efficiency of the isolates under standard conditions but did not correlate with the source of root-nodule bacteria (soil or nodule) or their salt tolerance. The results indicate that the strains of root-nodule bacteria forming efficient symbioses under salinization conditions can be found.     

Improving Salinity Tolerance in Cereals

Cereals are grown in almost every region of the world and are exposed to a variety of environmental stresses that severely affect their growth and grain yield. Of various abiotic stresses, salinity is one of the more significant threats to cereal crops. To ensure food security, there is a need to adopt strategies to overcome this specific threat. Undoubtedly, plant scientists have been exploiting a variety of approaches to achieve enhanced crop productivity on salt affected soils. Of the various biotic approaches, conventional breeding, marker-assisted selection and genetic engineering to develop salt-tolerant lines/cultivars of cereals all seem plausible. Some success stories have been reported for improvement in salt tolerance of wheat and rice, but are scarce for other cereals. A number of barriers to the development of salt-tolerant cultivars/lines have been identified and include a lack of knowledge about the genetics of crops, their physiological and biochemical behavior, wide variation in environmental conditions, and the complex polygenic nature of the salt tolerance character. This review focuses on how improvements have been made in salt tolerance in cereals through different biotic means, such as conventional breeding, marker assisted selection and genetic engineering.     

Halophytes can salinize soil when competing with glycophytes,intensifying effects of sea level rise in coastal communities

Sea level rise (SLR) and land-use change are working together to change coastal communities around the world. Along Florida’s coast, SLR and large-scale drying are increasing groundwater salinity, resulting in halophytic (salt-tolerant) species colonizing glycophytic (salt-intolerant) communities. We hypothesized that halophytes can contribute to increased soil salinity as they move into glycophyte communities, making soils more saline than SLR or drying alone. We tested our hypothesis with a replacement-series greenhouse experiment with halophyte/glycophyte ratios of 0:4, 1:3, 2:2, 3:1, 4:0, mimicking halophyte movement into glycophyte communities. We subjected replicates to 0, 26, and 38‰ salinity for one, one, and three months, respectively, taking soil salinity and stomatal conductance measurements at the end of each treatment period. Our results showed that soil salinity increased as halophyte/glycophyte ratio increased. Either osmotic or ionic stress caused decreases in glycophyte biomass, resulting in less per-plant transpiration as compared to halophytes. At 38‰ groundwater, soil salinity increased as halophyte density increased, making conditions more conducive to further halophyte establishment. This study suggests that coastal plant community turnover may occur faster than would be predicted from SLR and anthropogenic disturbance alone.     

The Effects of Soil Salinity and Meloidogyne javanica on Tomato

A non-sodic, non-saline sandy loam soil was salinized to anion-cation ratios similar to those naturally occurring in Iraq and California. The interactions of saline soils (conductivities 4, 8, 12 and 16 mmhos/cm) with a moderately salt-tolerant plant (Lycopersicon esculentum ''Marimond'') and a plant parasitic nematode (Meloidogyne javanica) were investigated. Plant parasitic nematodes were shown to be an important modifying influence within the plant environment, either accentuating or ameliorating salinity stress effects.     

Growing floricultural crops with brackish water

In the current review we focus on the opportunity to use brackish water in the cultivation of floricultural plants, plants for which, due to their high economic value, growers have traditionally used good quality water for irrigation. Now, even for these crops the use of alternative water sources for irrigating nursery plants is needed because of the limited supplies of fresh water in many countries; understanding how saline water can be used will also enhance sustainable development in floriculture. While salt stress usually reduces plant growth, any such reduction might not be negative for ornamentals, where shoot vigour is sometime undesirable, although on flower crops salt stress can delay flowering or decrease flower quality characteristics. However, a decrease in growth rate is not enough to characterize the salt tolerance of ornamental plants, but traits like tip and marginal leaf burn, as consequence of sodium and chlorine accumulation, have to be considered for their effects on aesthetical value. With this in mind, some halophytes should be considered for floriculture because of their ability to cope with saline environments; their potential to tolerate salt is an important factor in reducing production costs. Consequently, the identification of ornamental halophytes is important for producing a commercially acceptable crop when irrigated with brackish waters. Many aspects of a plant's reaction to salt are genetically determined, so selection of suitable genotypes or breeding for salt tolerance in ornamentals are interesting options. Developing salt-tolerant floricultural crops, together with typical management practices that avoid excessive salinity stress in the root media, will provide the grower with economically and environmentally sound wastewater reuse options.     

基于CSCD的盐生植物研究文献计量评价

以中国科学引文数据库（CSCD,477篇）为主线,以维普、万方和CNKI数据库（3329篇）为基础数据,采用文献计量分析的方法,对盐生植物研究文献进行统计分析,分别从文献的年代、机构、作者、来源期刊、学科类别、高被引论文和文献的关键词这7个方面,对盐生植物研究文献的分布规律和研究现状进行总体回顾与评价。全面概括、总结和分析该研究领域研究热点、区域、内容、技术和方法,优秀人才、领先机构和主要团队,揭示中国盐生植物研究的进展情况。结果表明：1956年有盐生植物论文发表,2007年文献总量340篇为最高记录;在CSCD,1991年有盐生植物论文发表,至2011年62篇为最高,均呈逐年上升趋势。中国在盐生植物研究方面已经形成了引领该研究方向的4个主要科研团队,分别是山东师范大学、中国科学院新疆生态与地理研究所、中国农业大学和南京大学。盐生植物的研究呈现明显的地域相关性,热点地区包括新疆、山东、北京、南京、东北、内蒙古、宁夏、兰州等地。盐生植物研究热点是：耐盐性（耐盐机制）、盐胁迫、盐碱地、基因克隆、土壤盐分、植物生长、开发利用、渗透调节、生理指标、种子萌发、脯氨酸、基因工程（基因表达）和植物群落等。     

新疆乌尔禾地区盐渍土壤耐盐细菌多样性与群落结构研究

研究新疆北部乌尔禾地区盐渍土壤中微生物群落结构及多样性,以期发现新的高盐环境耐盐性微生物资源菌株。采用传统分离培养法获得可培养耐盐菌株并对菌株形态学、16S rRNA基因测序、耐盐特性进行研究,同时结合高通量测序技术分析新疆乌尔禾地区盐渍土壤耐盐细菌的多样性与群落结构。共分离得到耐盐细菌11株,分属6个属,均为中度耐盐菌,以芽胞杆菌属(Bacillus)为优势菌。对盐渍土壤微生物16S rRNA(V3～V4)基因测序,共获得细菌序列290 952条,分属24个门410个属,变形菌门(Proteobacteria, 60.31%)、厚壁菌门(Firmicutes, 21.52%)、拟杆菌门(Bacteroidetes, 6.9%)和放线菌门(Actinobacteria, 6%)相对丰度较高。优势属为克吕沃尔菌属(Kluyvera,21%)、Hafnia-Obesumbacterium(19.6%)和假单胞菌属(Pseudomonas,7.5%)。结果表明,新疆乌尔禾地区盐渍土壤耐盐细菌优势菌群以芽胞杆菌属(Bacillus)居多,细菌群落结构较复杂,潜在可利用微生物资源较为丰富,对高盐极端环境耐盐微生物新资源有进一步研究的意义。