Soil salinization is becoming a serious problem worldwide [1
]. Among 230 million hectares of farmland currently in use globally, 20% are affected by salt and this number increases every year as a result of illogical crop irrigation practices, excessive fertilization, and excessive plowing as well as natural causes such as salt intrusion into coastal zones resulting from the sea-level rise [3
]. At present, due to the poor salt tolerance of the crops plants, it is impossible to plant crops on the saline-alkali land. The challenge of feeding about 10 billion people by the next century is forcing agricultural production into salinized wasteland so that it appears likely to be achieved only through a major breakthrough in breeding crops for salinity tolerance [7
]. Therefore, understanding the salt-tolerant mechanism of plants especially halophytes, which can survive and complete their life cycles in harsh, saline environments, will be a key step in improving crop salt tolerance for adaptation to saline habitats [7
Halophytes are generally recognized as plants that can survive high concentrations of electrolytes in their environments [9
]. Ecologically, halophytes have been defined as “the native flora of saline soils” [10
]. In this context, saline soils are those containing solutions with an osmotic pressure (П) of at least 3.3 bar, which is equivalent to 70 mM monovalent salts [calculated from [11
]. Recently, halophytes refer to the plants that are adapted to saline soil environments and are able to survive and reproduce at salt concentrations of 200 mM or greater [13
]. On the basis of the physiological basis of salt tolerance as well as the accumulation and transport of ions, the German botanist Breckle [16
] classified halophytes into three major categories. (A) Recretohalophytes can secrete salt from the plant body to the outside through salt glands (as in Limonium bicolor
) or into salt bladders for temporary storage and then the salt will scatter from salt bladders when it encounters strong winds or other external stimuli (as in Chenopodium quinoa
). Salt entering the plant body is secreted by salt glands or salt bladders, which reduces the salt content of plant life tissue and guarantees its normal growth and development in saline soil environments [17
]. (B) Euhalophytes such as Suaeda salsa
and Mesembryanthemum crystallinum
, which are divided into two categories known as leaf succulent euhalophytes and stem succulent euhalophytes accumulate salt in the vacuoles of succulent green tissues of leaves or stems, respectively [14
]. Euhalophytes compartmentalize excessive salt ions, which enter the plant cells into the vacuole. On the one hand, this reduces the water potential of the plant and helps it to absorb water from the saline soil and, on the other hand, this reduces the ions content in cytoplasm and avoids damage to enzymes and biological substances in the cytoplasm [14
]. (C) Salt-exclusion halophytes, which are also called salt excluders such as reed plant (Phragmites communis
L.), accumulate much more salt in the vacuoles of parenchyma tissues and parenchyma of roots and xylem than in the shoot [27
Up to now, many review papers have been published dealing with a salt tolerance mechanism of euhalophytes and recretohalophytes [13
], and a halophyte database has been established to help exploit the characteristics of halophytes [30
]. However, few papers focus on the salt tolerant mechanism of salt excluders.
Salt-exclusion halophytes achieve salt tolerance through salt exclusion [31
] by either excluding most of the Na+
into the soil solution or by accumulating salt ions in the roots and root–stem junctions [32
]. Therefore, shoots of these plants can maintain low concentrations of salt and are free from salt damage. A unique feature of salt exclusion in halophytes is that the Na+
concentrations are significantly lower in shoots than in roots [27
]. Under NaCl treatment, the Na+
content is significantly increased in both shoots and roots of reed plants, but it is much higher in roots than in shoots [27
Most salt-exclusion halophytes only transport 2% of the salt absorbed by the roots to the shoots and the remaining salt is excluded into the soil solution [33
]. At present, the key locations for salt exclusion in salt-exclusion halophytes are reported to be the pericycle and xylem parenchyma cells, the root cortex (especially the casparian strip), and the phloem cells [34
]. Salt-exclusion halophytes survive in saline habitats by controlling the uptake of Na+
and the distribution of Na+
Most monocotyledon crops have the same salt tolerance mechanism as salt-exclusion halophytes even though monocotyledon crops have a significantly lower salt tolerance than salt-exclusion halophytes. Therefore, understanding the molecular mechanisms of salt tolerance in salt-exclusion plants is very important for improving the salt tolerance of monocotyledon crops such as maize (Zea mays), wheat (Triticum spp.), rice (Oryza sativa), and sorghum. In this review, we summarize the current knowledge about the molecular regulation of salt tolerance in salt-exclusion halophytes and some gramineous plants.
4. Using Improved Salt Tolerance to Improve Crops
The majority of reports to date related to plant breeding have focused on maintaining or increasing annual yields [81
]. However, if new crop cultivates with characteristics of both high-yield and salt-tolerant are bred, they can be used to improve saline-alkali land while improving food production. Therefore, breeding focused on improving the yields of crops under salt stress is becoming increasingly important. Conventional plant breeding has long been used to generate stress-tolerant crop varieties. However, this process is time consuming and labor intensive, relies on the existence of well-characterized germplasms, and can result in the introduction of undesirable traits along with those selected for [82
]. Therefore, advanced breeding strategies such as marker-assisted selection and genetic engineering seem to be more attractive. It is particularly important to explore the mechanism of salt tolerance in crops, to reveal important pathways in response to salt resistance in crops, and to find key genes related to salt tolerance in crops.
Encouragingly, salt exclusion is found in some form in most crops especially among the salt-exclusion halophytes, which encompass a group that includes most monocotyledon (e.g., grain) species. The key pathways and genes involved in the salt-exclusion processes of different groups of plants are also beginning to be understood, as described above. In addition, the function and mechanism of some key genes related to salt tolerance have also been revealed. This information can be used in combination with QTL, Genome-wide association analyses (GWAS), and genetic engineering techniques to provide guidance for the molecular breeding of crop salt tolerance. After key pathways and genes involved in the salt-exclusion processes are understood, the applications of new technologyies such as CRISPER, RNAi, and overexpression are very important for improving salinity stress tolerance. The overexpression of SOS1
can reconstruct Na+
homeostasis of cytoplasm and withdraw more ions, which ensures low ion concentration in the transpiration stream under salt stress [84
]. The PKS5 (SOS2-Like Protein Kinase 5) kinase activity can be completely removed or reduced by CRISPR, which is an RNAi technique that can increase the PM H+
-ATPase activity since PKS5 negatively regulates the PM H+
Based on the related knowledge, we think that the main aim of future crop breeding are controlling the uptake of Na+ and distributing Na+ (entering the plant body) to specific parts that are not sensitive to salt. The main directions of breeding are discussed below.
4.1. Exploiting the Key Genes Responsible for Forming Apoplastic Barrier (Especially the Casparian Strip)
The apoplastic barrier (especially the casparian strip) plays a critical role in controlling Na+
uptake and transport to the shoots. The changes of the expression level of genes related to biosynthesis of components of apoplastic barriers were more forehanded and significant. Our recent research results showed that suberin-forming key genes (SbKCS11
) of root apoplast barriers in salt exclusion of sweet sorghum plays an important role. It has developed a strategy to resist salinity by accumulating Na+
in the roots to limit the excess accumulation of Na+
in leaves under salt stress, which plays an important role in the sorghum root rejection of Na+
]. These factors are responsible for increasing the salt tolerance of sweet sorghum.
4.2. Increasing the Activities of the SOS Pathway and the H+-ATPase
One of the important functions of the SOS pathway activated by salt stress is to reconstruct Na+/K+ homeostasis of cytoplasm and exclude excess Na+ from root cells under salt stress. Another important function is to maintain the Na+ stability in the pericycle where Na+ can be transported to the shoot with the transpiration stream. The increased SOS1 and PM H+-ATPase activity can withdraw more ions, which will ensure low ion concentration in the transpiration stream. Therefore, the increasing activities of the SOS pathway and the H+-ATPase can maintain low Na+ concentration in cytoplasmic streams and in the transpiration stream.
4.3. Increasing the Activities of HKT-Like Transporters
HKT-like transporters are involved in improving plant salt tolerance by increasing the efflux of Na+ in the cytoplasm, withdrawing Na+ from the xylem sap, reducing Na+ transport to shoots, and distributing Na+ to specific parts (These parts are not sensitive to salt such as root, root–stem junctions, leaf sheath, and old leaf). These transporters are responsible for Na+ recirculation in the phloem.
Soil salinity is a severe problem for agriculture worldwide. Exploring the mechanism, pathways, and key genes related to salt tolerance in crops is meaningful for salt-tolerant crops breeding and improvement of saline land. As most monocotyledonous crops are salt-excluders, understanding the mechanisms of salt exclusion at the molecular level is critical for improving the salt tolerance of monocotyledonous crops such as maize, wheat, rice, and sorghum. In the present review, we summarize recent research into salt-exclusion mechanisms and the genes that underlie them. However, even though knowledge on the molecular mechanisms of plant salinity tolerance is dramatically expanding, there remain many uncertainties. Further dissection of the complex regulatory networks of plant salt exclusion tolerance and, in particular, the key genes controlling the apoplastic barrier of plant roots will provide a molecular basis for improving the salt tolerance of crop plants.