A review on transporters in salt tolerant mangroves

Key message

The role of transporters in imparting salt tolerance to mangroves is not yet understood. Identification of the role of transporters in halophytes is promising, as far as the development of genetically engineered salt tolerant crops is concerned.

Abstract

Mangroves are models for stress tolerance and they provide a reservoir for some of the novel genes and proteins, involved in salt tolerance. Biochemical or physiological mechanisms contribute to salt tolerance depending on variations in the environment. A great deal of research on salinity tolerance of plants, probes into water relations, photosynthesis, and accumulation of various in-organic ions and organic metabolites. The ability of the plant to react to high salinity depends on the genes that are expressed during stress. The mechanism of salinity tolerance becomes complicated when the responses of plants varies with salinity and environmental conditions. During the onset and development of salt stress within a plant, major processes such as photosynthesis, protein synthesis and lipid metabolisms are affected. The present review attempts to dissect out the role of transporters in salt tolerance of mangroves.     

Antioxidative response mechanisms in halophytes: Their role in stress defence

Normal growth and development of plants is greatly dependent on the capacity to overcome environmental stresses. Environmental stress conditions like high salinity, drought, high incident light and low or high temperature cause major crop losses worldwide. A common denominator in all these adverse conditions is the production of reactive oxygen species (ROS) within different cellular compartments of the plant cell. Plants have developed robust mechanisms including enzymatic or nonenzymatic scavenging pathways to counter the deleterious effects of ROS production. There are a number of general reviews on oxidative stress in plants and few on the role of ROS scavengers during stress conditions. Here we review the regulation of antioxidant enzymes during salt stress in halophytes, especially mangroves. We conclude that (i) antioxidant enzymes protect halophytes from deleterious ROS production during salt stress, and (ii) genetic information from mangroves and other halophytes would be helpful in defining the roles of individual isoforms. This information would be critical in using the appropriate genes for oxidative stress defence for genetic engineering of enhanced stress tolerance in crop systems.     

Principles and strategies in breeding for higher salt tolerance

Summary Salinity is an environmental component that usually reduces yield. Recent advances in the understanding of salt effects on plants have not revealed a reliable physiological or biochemical marker that can be used to rapidly screen for salt tolerance. The necessity of measuring salt tolerance based upon growth in saline relative to non-saline environments makes salt tolerance measurements and selection for tolerance difficult. Additionally, high variability in soil salinity and environmental interactions makes it questionable whether breeding should be conducted for tolerance or for high yield. Genetic techniques can be used to identify the components of variation attributable to genotype and environment, and the extent of genetic variation in saline and nonsaline environments can be used to estimate the potential for improving salt tolerance. Absolute salt tolerance can be improved best by increasing both absolute yield and relative salt tolerance.     

Regulation of water balance in mangroves

Background Mangroves are a group of highly salt-tolerant woody plants. The high water use efficiency of mangroves under saline conditions suggests that regulation of water transport is a crucial component of their salinity tolerance.Scope This review focuses on the processes that contribute to the ability of mangroves to maintain water uptake and limit water loss to the soil and the atmosphere under saline conditions, from micro to macro scales. These processes include: (1) efficient filtering of the incoming water to exclude salt; (2) maintenance of internal osmotic potentials lower than that of the rhizosphere; (3) water-saving properties; and (4) efficient exploitation of less-saline water sources when these become available.Conclusions Mangroves are inherently plastic and can change their structure at the root, leaf and stand levels in response to salinity in order to exclude salt from the xylem stream, maintain leaf hydraulic conductance, avoid cavitation and regulate water loss (e.g. suberization of roots and alterations of leaf size, succulence and angle, hydraulic anatomy and biomass partitioning). However, much is still unknown about the regulation of water uptake in mangroves, such as how they sense and respond to heterogeneity in root zone salinity, the extent to which they utilize non-stomatally derived CO₂ as a water-saving measure and whether they can exploit atmospheric water sources.     

The role of mitochondrial respiration in salinity tolerance

NaCl is the most abundant salt in salinity-affected land. The ability of plants to sift the water table, limit NaCl uptake, compartmentalise Na?/Cl? ions and prevent negative ionic and osmotic effects on cell function, are the foundations of salinity tolerance mechanisms. In this review, we show that although the quantitative response of respiratory rate to changes in salt concentration is complex, the properties of respiratory processes are crucial for tolerance during ion exclusion and tissue tolerance. We consider whole-plant gas exchange and carbon balance analysis alongside the salt responses of mitochondrial properties and genetic studies manipulating respiratory processes. We showcase the importance of efficient ATP generation, dampened reactive oxygen species and mitochondrial osmolytes for salinity tolerance in plants.     

ATPase 与植物抗盐性

 本文综述了高等植物细胞ATPase在盐胁迫下的活性变化及其调控机制。V型H+_ATPase与细胞离子区隔化和植物抗盐性密切相关。盐胁迫提高抗盐植物液泡膜H+_ATPase活性, 主要是通过增加V型H+_ATPase主要功能亚基的基因表达以及蛋白质合成。盐胁迫通常降低质膜H+-ATPase活性, 很可能是由于酶蛋白质合成受阻, 质膜H+-ATPase活性的变化与盐胁迫的强度和时间长短有关。此外, 本 文还对ABA和Ca2+-CaM等胁迫信号物质对ATPase活性的调控及其与植物抗盐性的关系进行了总结。研究ATPase对盐胁迫的响应和调控机制, 有助于阐明植物的盐生境适应机制, 也有利于植物的抗盐育种工作。     

ATPase与植物抗盐性

本文综述了高等植物细胞ATPase在盐胁迫下的活性变化及其调控机制。V型H+_ATPase与细胞离子区隔化和植物抗盐性密切相关。盐胁迫提高抗盐植物液泡膜H+_ATPase活性,主要是通过增加V型H+_ATPase主要功能亚基的基因表达以及蛋白质合成。盐胁迫通常降低质膜H+-ATPase活性,很可能是由于酶蛋白质合成受阻,质膜H+-ATPase活性的变化与盐胁迫的强度和时间长短有关。此外,本文还对ABA和Ca2+-CaM等胁迫信号物质对ATPase活性的调控及其与植物抗盐性的关系进行了总结。研究ATPase对盐胁迫的响应和调控机制,有助于阐明植物的盐生境适应机制,也有利于植物的抗盐育种工作。     

Plant Growth-Promoting Rhizobacteria-Mediated Adaptive Responses of Plants Under Salinity Stress

In this recent era, several approaches have been developed to alleviate the adverse effects of salinity stress in different plants. However, some of them are not eco-friendly. In this context, evolving sustainable approaches which enhance the productivity of saline soil without harming the environment are necessary. Many recent studies showed that plant growth-promoting rhizobacteria (PGPR) are known to confer salinity tolerance to plants. Salt-stressed plants inoculated with PGPR enhance the growth and productivity of crops by reducing oxidative damage, maintaining ionic homeostasis, enhancing antioxidant machinery, and regulating gene expressions. The PGPR also regulates the photosynthetic attributes such as net photosynthetic rate, chlorophyll, and carotenoid contents and enhances the salinity tolerance to plants. Moreover, PGPR has a great role in the enhancement of phytohormones and secondary metabolites synthesis in plants under salt stress. This review summarizes the current reports of the application of PGPR in plants under salt stress and discusses the PGPR-mediated mechanisms in plants of salt tolerance. This review also discusses the potential role of PGPR in cross-talk with phytohormones and secondary metabolites to alleviate salt stress and highlights the research gaps where further research is needed.

     

植物同源多倍体耐盐性研究进展

多倍化是高等植物进化最重要的动力之一,多倍体植物由于基因组组成以及基因表达方面的变化,通常会表现出不同的生理现象,多倍体的抗性优于其同源二倍体祖先。土壤盐碱化和次生盐渍化是影响农作物生产的重要因素,严重制约着我国农业的可持续发展。同源多倍体植物耐盐能力较强,是作物遗传改良的重要种质资源,了解其耐盐机理对培育耐盐品种具有重要意义。本文从与盐胁迫相关的耐盐性进化、生理生化水平、细胞结构和分子层面等多角度总结了植物同源多倍体盐胁迫研究进展,并以作者所在研究团队培育出的多倍体西瓜为例讨论了多倍体抗逆性研究存在的问题及未来的发展方向,以期为多倍体抗逆优势机理研究提供参考。     

Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field

Drought and salinity are two major limiting factors in crop productivity. One way to reduce crop loss caused by drought and salinity is to increase the solute concentration in the vacuoles of plant cells. The accumulation of sodium ions inside the vacuoles provides a 2-fold advantage: (i) reducing the toxic levels of sodium in cytosol; and (ii) increasing the vacuolar osmotic potential with the concomitant generation of a more negative water potential that favors water uptake by the cell and better tissue water retention under high soil salinity. The success of this approach was demonstrated in several plants, where the overexpression of the Arabidopsis gene AtNHX1 that encodes a vacuolar sodium/proton antiporter resulted in higher plant salt tolerance. Overexpression of AtNHX1 increases sodium uptake in vacuoles, which leads to increased vacuolar solute concentration and therefore higher salt tolerance in transgenic plants. In an effort to engineer cotton for higher drought and salt tolerance, we created transgenic cotton plants expressing AtNHX1. These AtNHX1-expressing cotton plants generated more biomass and produced more fibers when grown in the presence of 200 mM NaCl in greenhouse conditions. The increased fiber yield was probably due to better photosynthetic performance and higher nitrogen assimilation rates observed in the AtNHX1-expressing cotton plants as compared with wild-type cotton plants under saline conditions. Furthermore, the field-grown AtNHX1-expressing cotton plants produced more fibers with better quality, indicating that AtNHX1 can indeed be used for improving salt stress tolerance in cotton.     

Mangroves: obligate or facultative halophytes? A review

Salinity plays significant roles in regulating the growth and distribution of mangroves, and the salt tolerance mechanisms of mangroves have been the focus of research for several decades. There are contradictory views regarding the relationship between mangroves and salt: (1) Mangroves are facultative halophytes, i.e. freshwater is a physiological requirement and salt water is an ecological requirement for mangroves because they are capable of growing in freshwater. The former prevents excess respiratory losses while the latter prevents invasion and competition from non-halophytes. (2) Mangroves are obligate halophytes, i.e. salt is necessary for their growth. Mangroves cannot survive in freshwater permanently and salt water is a physiological requirement. Up to now, mangroves are usually considered as facultative halophytes. In this review, we provided five lines of evidence to evaluate these two contradictory views: (1) the results of laboratory culture experiments and field investigations; (2) the viviparous nature of mangroves; (3) the salt accumulation of mangroves under freshwater or low salinity; (4) the effect of salinity on the photosynthetic rate and in vitro enzyme activities, and (5) the effects of salinity fluctuation on mangrove growth and physiology. Contrary to widely accepted view, our evaluations of the aforementioned evidence suggest that mangroves are obligate halophytes. Mangroves can grow in freshwater for a limited time by drawing upon the nutrients and salt reserves in their hypocotyls while prolonged culture in freshwater is fatal to them. Mangroves have the ability to absorb Na⁺ and Cl⁻ rapidly and preferentially under low-salinity conditions. Not all of the enzymes in mangroves are sensitive to salt. In fact, the activities of some enzymes are even stimulated by low or moderate salinity. Plants grown under constant salinity in a laboratory setting are unlikely to behave in the same way as those in their natural habitat with fluctuating salinity. Thus, studies on the effects of freshwater or low salinity and salinity fluctuation on mangroves, as well as the physiological mechanisms that allow maintenance of function under fluctuating salinity conditions should be strengthened in future research.     

Salinity Adaptation and the Contribution of Parental Environmental Effects in Medicago truncatula

High soil salinity negatively influences plant growth and yield. Some taxa have evolved mechanisms for avoiding or tolerating elevated soil salinity, which can be modulated by the environment experienced by parents or offspring. We tested the contribution of the parental and offspring environments on salinity adaptation and their potential underlying mechanisms. In a two-generation greenhouse experiment, we factorially manipulated salinity concentrations for genotypes of Medicago truncatula that were originally collected from natural populations that differed in soil salinity. To compare population level adaptation to soil salinity and to test the potential mechanisms involved we measured two aspects of plant performance, reproduction and vegetative biomass, and phenological and physiological traits associated with salinity avoidance and tolerance. Saline-origin populations had greater biomass and reproduction under saline conditions than non-saline populations, consistent with local adaptation to saline soils. Additionally, parental environmental exposure to salt increased this difference in performance. In terms of environmental effects on mechanisms of salinity adaptation, parental exposure to salt spurred phenological differences that facilitated salt avoidance, while offspring exposure to salt resulted in traits associated with greater salt tolerance. Non-saline origin populations expressed traits associated with greater growth in the absence of salt while, for saline adapted populations, the ability to maintain greater performance in saline environments was also associated with lower growth potential in the absence of salt. Plastic responses induced by parental and offspring environments in phenology, leaf traits, and gas exchange contribute to salinity adaptation in M. truncatula. The ability of plants to tolerate environmental stress, such as high soil salinity, is likely modulated by a combination of parental effects and within-generation phenotypic plasticity, which are likely to vary in populations from contrasting environments.     

Variation from plant tissue cultures: biotechnological application to improving salinity tolerance

Breeding for salt tolerance in crop plants is envisaged as one way to combat a worldwide problem of increasing soil salinity in agricultural land. Tissue culture techniques may prove valuable as a means of achieving this goal. In this review, reports of the selection and characterization of plant cell cultures tolerant to excess salt are assessed, in the context of variability from tissue culture and the significance of cellular physiological adaptation to salinity. The examples of plant regeneration from salt grown cell cultures are also outlined, with emphasis on correlation to the effect of salt on cell cultures, genetic variability for salt tolerance in vitro, and the value of regenerates in the development of salt tolerant plants.     

Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone

There is large area of saline abandoned and low-yielding land distributed in coastal zone in the world. Soil salinity which inhibits plant growth and decreases crop yield is a serious and chronic problem for agricultural production. Improving plant salt tolerance is a feasible way to solve this problem. Plant physiological and biochemical responses under salinity stress become a hot issue at present, because it can provide insights into how plants may be modified to become more tolerant. It is generally known that the negative effects of soil salinity on plants are ascribed to ion toxicity, oxidative stress and osmotic stress, and great progress has been made in the study on molecular and physiological mechanisms of plant salinity tolerance in recent years. However, the present knowledge is not easily applied in the agronomy research under field environment. In this review, we simplified the physiological adaptive mechanisms in plants grown in saline soil and put forward a practical procedure for discerning physiological status and responses. In our opinion, this procedure consists of two steps. First, negative effects of salt stress are evaluated by the changes in biomass, crop yield and photosynthesis. Second, the underlying reasons are analyzed from osmotic regulation, antioxidant response and ion homeostasis. Photosynthesis is a good indicator of the harmful effects of saline soil on plants because of its close relation with crop yield and high sensitivity to environmental stress. Particularly, chlorophyll a fluorescence transient has been accepted as a reliable, sensitive and convenient tool in photosynthesis research in recent years, and it can facilitate and enrich photosynthetic research under field environment.     

Additive effects of Na+ and Cl- ions on barley growth under salinity stress

Soil salinity affects large areas of the world's cultivated land, causing significant reductions in crop yield. Despite the fact that most plants accumulate both sodium (Na(+)) and chloride (Cl(-)) ions in high concentrations in their shoot tissues when grown in saline soils, most research on salt tolerance in annual plants has focused on the toxic effects of Na(+) accumulation. It has previously been suggested that Cl(-) toxicity may also be an important cause of growth reduction in barley plants. Here, the extent to which specific ion toxicities of Na(+) and Cl(-) reduce the growth of barley grown in saline soils is shown under varying salinity treatments using four barley genotypes differing in their salt tolerance in solution and soil-based systems. High Na(+), Cl(-), and NaCl separately reduced the growth of barley, however, the reductions in growth and photosynthesis were greatest under NaCl stress and were mainly additive of the effects of Na(+) and Cl(-) stress. The results demonstrated that Na(+) and Cl(-) exclusion among barley genotypes are independent mechanisms and different genotypes expressed different combinations of the two mechanisms. High concentrations of Na(+) reduced K(+) and Ca(2+) uptake and reduced photosynthesis mainly by reducing stomatal conductance. By comparison, high Cl(-) concentration reduced photosynthetic capacity due to non-stomatal effects: there was chlorophyll degradation, and a reduction in the actual quantum yield of PSII electron transport which was associated with both photochemical quenching and the efficiency of excitation energy capture. The results also showed that there are fundamental differences in salinity responses between soil and solution culture, and that the importance of the different mechanisms of salt damage varies according to the system under which the plants were grown.     

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.     

Halophytes as a source of genes for abiotic stress tolerance

Agricultural productivity is majorly impacted due to various abiotic stresses, particularly salinity and drought. Halophytes serve as an excellent resource for identifying and developing new crop systems, as these grow very luxuriously in very high saline soils. Understanding salinity stress tolerance mechanisms in such plants is an important step towards generating crop varieties that can cope with environmental stresses. Use of modern tools of ‘omics’ analyses and small RNA sequencing has helped to gain insights into the complex plant stress responses. Salinity tolerance being a multigenic trait requires a combination of strategies and techniques to successfully develop improved crops varieties. Many transgenic crops are being developed through genetic transformation. Besides marker-assisted breeding/QTL approaches are also being used to improve abiotic stress tolerance. In this review, we focus on the recent developments in the utilization of halophytes as a source of genes for genetic improvement in abiotic stress tolerance of crops.     

一年生盐生植物耐盐机制研究进展

盐生植物是一类能够在盐土上完成生活史的天然植物, 在与盐土协同演化过程中形成了一系列适应盐生环境的特殊生存策略。其中一年生盐生植物因其生活史短、方便培养和观察、易于基因转化和后代繁殖, 已成为耐盐机制研究的主要对象。一年生盐生植物面临多变的生境胁迫, 具有更大的生存风险, 所以具有不同于多年生盐生植物的更稳妥的适应机制, 主要体现在种子的高盐休眠、复水速萌、形态和萌发的多态性、存在持久种子库及调节资源分配等方面。种子萌发后的生长、发育和繁殖等生活史的各阶段都要经受严峻的盐生胁迫环境。通常所说的耐盐机理是指成株对盐分的调控, 按照植物种类不同而分为稀盐、泌盐和拒盐3种耐盐形式。该文在对国内外相关文献进行分析归纳的基础上, 首先介绍了一年生盐生植物的常见类型, 然后分别从种子特征、形态结构、生理生化和生态习性等方面综述了一年生盐生植物的耐盐机制。     

Developing salt tolerant plants in a new century: a molecular biology approach

Soil salinity is a major abiotic stress in plant agriculture strongly, influencing plant productivity world-wide. Classical breeding for salt tolerance in crop plants has been attempted to improve field performance without success. Therefore, an alternative strategy is to generate salt tolerant plants through genetic engineering. Several species and experimental approaches have been used in order to identify those genes that are important for salt tolerance. Due to high level of salt tolerance, halophytes are good candidates to identify salt tolerance genes. However, other species such as yeast and glycophytes have also been employed. Three approaches are commonly used to identify genes important for salt tolerance. The first approach is to identify genes involved in processes known to be critical for salt tolerance (osmolyte synthesis, ion homeostasis, etc.). The second approach is to identify genes whose expression is regulated by salt stress. This is relatively simply and applicable to any plant species. Genetic amenability of some species allows the third approach, which consists in the identification of salt tolerance determinants based on functionality. At the moment, there is a large number of reports in the literature claiming that plants with increased salt tolerance have been obtained. The main problem is that different plant species, stage of development, organs, promoters and salt conditions used it is difficult to compare the degree of salt tolerance conferred by different genes. In this review, we discuss progress made towards understanding the molecular elements involved in salt stress responses that have been used in transgenic approaches to improve salt tolerance.