Introduction

High soil salinity is a worldwide problem. Increased salt concentration in the soil affects crop productivity, changes the microbial community, and consequently negatively impacts on agricultural economy (FAO 2016). Over 2% of the total and nearly 20% of agricultural irrigated lands suffer from high salinity (FAO 2016). It is expected that soil salinization further increases due to global climate changes and as consequences of wrong irrigation techniques (Munns and Tester 2008a, b). Expansion of salinity on arable areas might reduce agricultural lands up to 30% by 2050 (FAO 2016). Huge economic losses of over 10 billion USD occur annually due to the soil salinization (Qadir et al. 2014).

High soil salinity can inhibit and impair plant development and productivity because of the decrease of water potential of plant cell and ion cytotoxicity, mainly sodium (Na+) and chloride (Cl−), causing metabolic dysfunction, alteration of membrane integrity and function as well as the nutritional disorders due to the excess of Na+ and Cl− in soil (Tester and Davenport 2003). Additionally, salinity is very often accompanied by oxidative stress due to generation of reactive oxygen species (ROS) (Tsugane et al. 1999).

During evolution many plant species developed unique ways to resist and to survive in harsh saline environments. Moreover, lower plants, fungi and animals reveal outstanding capabilities to adapt to the saline conditions due to the development of specific mechanisms of salt tolerance. Unravelling these salt tolerance mechanisms and identification of key salt tolerance genes can be used for the further biotechnological improvement of our major agricultural crops.

In order to improve salt tolerance of crops a broad spectrum of methods and approaches has been introduced such as high throughput phenotypic screening methods, molecular genetics, genetic engineering, different types of “omics” (genomics, transcriptomics, proteomics, microbiomics, ionomics, etc.). However, it is still challenging to transfer the identified desirable trait into cultivated crop plants. Both the exploration of gene sources and an introduction of novel genes from other types of living organisms is one of the important and essential ways to uphold the enormous challenges for the design and creation of modern crop cultivars. Molecular biology and genetics can supply the tools for the gene identification and isolation. The genes of interest have to be transferred either through conventional introgression methods or through advanced genetic engineering methods including genome editing techniques.

In this review the halophytic plants, wild crop relatives, as well as some types of eukaryotes are discussed as the resources for the salt stress tolerance genes. The most important and promising candidate genes from this network and also their possible application and delivery in molecular breeding and genetic engineering are presented here.

Types of salt tolerance

Plant salinity tolerance is governed by action of many physiological and molecular mechanisms. Usually these mechanisms are classified into three major categories: osmotic tolerance, ionic tolerance, tissue tolerance (Roy et al. 2014).

According to the growth performance in saline environments, plants can characterised as salt-tolerant (halophytes) and salt-sensitive (glycophytes) (Fig. 1). Halophytes are capable to tolerate high Na+ and Cl− concentrations in their shoots in comparison with the glycophytic plants. The salt tolerance of halophytes and other plants is mediated by two major mechanisms—salt exclusion or inclusion. According to these mechanisms plants can be grouped into two types—includers and excluders. The representatives of the first group are capable to accumulate high NaCl concentrations in their tissues equal or higher as then water salinity level. In turn, glycophytic plants are mostly regarded as salt excluders due to their capacity to prevent accumulation of salts in photosynthetic tissues. In contrast to glycophytes, the majority of halophytes belongs to includers and are able to transport Na+ actively from root to shoot (Flowers et al. 1977; Läuchli 1984). Numerous data suggests that the majority of halophytic monocot species are strong exluders (Colmer et al. 1995; Garthwaite et al. 2005). Interestingly, the cultivated common barley (Hordeum vulgare) belongs to halophytic includer type. It is believed that the includers employ progressive mechanisms of intracellular NaCl compartmentation and effectively regulate cytoplasmic homeostasis and synthesis of compatible solutes. The majority of the plant species belong to salt excluders employing the mechanisms of salt avoidance and revealing wide range of adaptations aimed to minimize the cytosolic salt concentrations or physiological exclusion by root membranes.

Fig. 1
figure 1

Comparative diagram and overview of major plant salt tolerance mechanisms in glycophytic and halophytic plants. In comparison with glycophytes, halophytic plants exhibit efficient salt excretion systems (salt glands or hydathodes) and absorption capacity for K+ over Na+. Halophytes are capable to accumulate toxic ions in older leaves and restrict ion uptake to the roots or ion migration from the roots to the shoots. The salt tolerance of halophytic is often accompanied by succulence and improved capacity to maintain increased water content

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Halophytes

Halophytes are capable to grow and reproduce themselves on salt concentration equal to 200 mM NaCl or even higher (Flowers and Colmer 2008, 2015). Only 500 species, comprising 0.14% of the world’s floristic diversity, are able to live in saline areas (Flowers et al. 2010). Thus every individual halophytic plant species evolved their own adaptation mechanism to survive in saline conditions. The mechanisms of salt tolerance in halophytic plants emerged via the consequent accumulation of beneficial mutations leading to physiological and adaptive changes required to survive in harsh environments of high salinity (Rozema and Flowers 2005; Bromham and Bennett 2014). In turn, halophytic plants can be subdivided into two different groups—obligate halophytes (require salt for their growth) and facultative halophytes (can grow without salt) (Braun-Blanquet 1932; Polunin 1960). Halophytes play an important role as a valuable resource for livestock and are good candidates for the phytoremediation of degraded lands (Flowers et al. 2010). It seems that the domestication of new crops from halophytic species would be also a good solution to solve many problems associated with the intense agriculture and promote agricultural diversity. For example, the halophytic crop Quinoa (Chenopodium quinoa) whose cultivation is expanding globally, because of high resistance to multiple abiotic stresses and good nutritional value (Zou et al. 2017). Moreover, grain of Quinoa has high nutritious value due to its exceptional protein quality and wide range of minerals and vitamins. The Quinoa grain proteins are enriched in amino acids like lysine and methionine that are deficient in many cereals (Bhargava et al. 2006). This plant species is also considered as a future crop for food security improvement and model halophytic plant to study the molecular mechanisms of salt bladder function to generate novel salt tolerant crops (Zou et al. 2017). The domestication and production of new crop varieties will support diversity of the sustainable provision of food in the nearest future. Besides this, halophytic plants are a good option to study the adaptation strategies to high salinity as well as an important genetic pool for improvement of tolerance to saline environments and other abiotic stresses (Mishra and Tanna 2017) (Fig. 1). Moreover, the salt-tolerant genes from halophytes could be potential key players of salt tolerance in glycophytic plants including crops (Himabindu et al. 2016). Successful gene transfer from halophytes for salt tolerance improvement has been shown for many plant species (Mishra and Tanna 2017). Therefore, the introduction of halophytic genes via genetic engineering or conventional breeding aimed to develop modern salt-tolerant crop varieties is an important approach for plant scientists and breeders (Munns and Tester 2008a, b; Bose et al. 2015).

Halophytes are capable to tolerate high Na+ and Cl− concentrations in their shoots in comparison with glycophytic plants. The mechanisms of salt tolerance of halophytes rely on the adjustment of cellular water potential, enhancement of the exclusion and sequestration of excess salt, and control of uptake and compartmentalization of ions (Mishra and Tanna 2017). Moreover, many halophytic plant species developed specialized organs such as salt glands and bladders for additional salt accumulation and removal. Halophytes are capable to maintain a high K+ to Na+ selectivity, produce a wide range of organic solutes, detoxify ROS, and use water efficiently. All these mechanisms are important contributions to efficiency of salt tolerance of halophytes (Shabala and Mackay 2011; Ozgur et al. 2013; Shabala et al. 2014; Shabala and Pottosin 2014). Accordingly, there is no single salinity tolerance mechanism of halophytes. Instead, they employ a range of adaptation mechanisms such as osmotic tolerance, ion exclusion or inclusion, tissue tolerance, and ROS detoxification (Shabala and Pottosin 2014).

It is worth to mention that some genes from halophytes are of exquisite interest because they might be more efficient than their glycophytic homologs regarding salinity stress (Himabindu et al. 2016; Mishra and Tanna 2017) (Table 1). Thus, big attention is now given to the evaluation of the molecular mechanisms of halophyte adaptation to saline environments. For instance, the halophytic plant Thellungiella parvula is a dicotyledonous species closely related to A. thaliana. The study of its salinity tolerance and the comparison with the model species A. thaliana has revealed some differences in the adaptation mechanisms and ion transport in saline conditions (Orsini et al. 2010). It was shown that TsHKT1;2 from the related halophyte T. salsuginea acts as a potassium transporter even under salinity stress in comparison with A. thaliana AtHKT1. It is noteworthy that the TsHKT1;2 includes a conserved Asp (D) residue in the 2nd pore-loop domain. Most other HKT1 sequences, including AtHKT1, contain an Asn (N) in this position. According to this data the complementation of A. thaliana athkt1-1 mutants by TsHKT1;2 under control of the native AtHKT1 promoter resulted in improved salt tolerance. On the other hand, the substitution of Asp (D207) by Asn significantly reduced the resistance to salinity (Ali et al. 2017). Thus, during the evolution process, T. salsuginea acquired the Asp (D207) substitution that substantially changed the cation selectivity of the HKT1-type transporter and significantly increased the salt tolerance of the plant (Ali et al. 2017). Another study demonstrated that transgenic A. thaliana lines expressing PutAKT1 from the halophytic relative Puccinellia tenuiflora exhibit lower Na+ and elevated K+ contents in plant tissues under salinity stress or normal growing conditions (Ardie et al. 2010). Further study of the physiological role of PutAKT1suggested that PtAKT1 is a key factor regulating selective uptake capacity for K+ over Na+ in P. tenuiflora under saline conditions (Wang et al. 2015a, b). In addition, a recent study reported that SsHKT1;1 from the halophytic plant Suaeda salsa mainly functions as K+ transporter in heterologous expression systems and in S. salsa. The main role of this HKT transporter is the maintenance of K+ nutrition and cytosolic cation homeostasis under high salinity (Shao et al. 2014). Thus, this HKT1 may contribute to halophytism by the enhancement of K+ transport (Ali et al. 2017). It is noteworthy that S. salsa is considered to be a promising model to understand the mechanisms of salt tolerance and to develop saline agriculture (Song and Wang 2015). A number of salt tolerance-related genes including SsNHX1, SsHKT1, SsAPX, SsCAT1, SsP5CS and SsBADH from S. salsa have been cloned and analysed (Song and Wang 2015) (Table 1). The genes related to the biosynthesis of osmolytes play an important role in tolerance mechanisms of halophytes (Table 1). For example, SsP5CS and SsBADH are involved in biosynthesis of proline and betaine, respectively, in S. salsa.

Table 1 Examples of gene transfer associated with salinity tolerance from halophytes
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The study of differences in sequences and structures between the homologs from halophytic and glycophytic relatives has a high potential to reveal novel adaptation mechanisms and physiological strategies to tolerate high salinity. For instance, NHX1 from the halophyte Aeluropus littoralis comprises ten putative hydrophobic regions, which differ from the nine transmembrane domains of OsNHX1 and AtNHX1 (Zhang et al. 2008). The expression of AlNHX1 in transgenic soybean leads to a reduced accumulation of Na+ in shoots and enhanced K+ levels in both roots and shoots, suggesting a role of AlNHX1 in K+ homeostasis instead of vacuolar Na+ sequestration (Liu et al. 2014) (Table 1). Another study showed that transgenic rice expressing Puccinellia tenuiflora NHX exhibited higher K+ content in shoots under NaCl treatment (Kobayashi et al. 2012). It was shown that expression of SeNHX1 from Salicornia europaea leads to improvement of both salt tolerance and disease resistance in tobacco (Chen et al. 2015).

The lack of whole-genome sequence data presents difficulties in considering these unique plant species for understanding their response to salt stress on molecular basis. Only few studies comparing salt response between the glycophytes and the halophytes at transcript and protein levels involve A. thaliana and Thellungiella halophila (Taji et al. 2004; Gong et al. 2005; Amtmann 2009; Pang et al. 2010), common wheat (Triticum aestivum) and Thinopyrum ponticum (Wang et al. 2008; Peng et al. 2009) as well as rice and its wild relative Porteresia coarctata (Sengupta and Majumder 2009). These studies suggest that salt-tolerant species have higher constitutive levels of stress- and anabolism-related proteins, the former including ROS scavenging enzymes, salt ion transporters, or V-ATPases. In contrast, salt-sensitive species demonstrate a relatively higher abundance of catabolism-related proteins.

There are relations between activities of antioxidant enzymes, stress-induced proteins and mechanisms of salt tolerance. Genes encoding ascorbate peroxidase (APX) or superoxide dismutase (SOD) from halophytic plants could be potential targets for gene transfer to crops. For example, it was demonstrated that SbpAPX from Salicornia brachiata plays an important role in the protection against oxidative stress. Unlike wild type plants, transgenic SbpAPX-expressing peanut lines were capable to grow and reproduce under salt stress conditions (Table 1) (Singh et al. 2014). Another study demonstrates the role of SbMT-2 metallothionein from S. brachiata in abiotic stress tolerance and ROS scavenging in transgenic tobacco (Chaturvedi et al. 2014). There are some other successful applications of halophytic genes encoding antioxidant enzymes for salt tolerance improvement (Table 1). Stress-related proteins such as LEA may also contribute to abiotic stress tolerance. It was demonstrated that the expression level of TsLEA1 gene in seedlings of halophytic plant T. salsuginea increased upon salt treatment. Expression of TsLEA1 in yeast and Arabidopsis resulted in an improvement of salinity tolerance of both organisms. Thus LEA proteins may play an important role in stress responses (Table 1) (Zhang et al. 2012).

Recently, high-throughput transcript sequencing techniques were used as a powerful approach for the study of the molecular basis of salinity stress regulation in halophytes. Transcript profiling for several halophytic species, such as Sporobolus virginicus (Yamamoto et al. 2015), Porteresia coarctata (Garg et al. 2014), Salicornia europaea (Ma et al. 2013), Mesembryanthemum crystallinum (Tsukagoshi et al. 2015), Suaeda fruticose (Diray-Arce et al. 2015), Zostera marina (Kong et al. 2014), Halogeton glomeratus (Wang et al. 2015a, b), Kosteletzkya virginica (Tang et al. 2015), Suaeda maritime (Gharat et al. 2016), Cakile maritima (Megdiche et al. 2008) and Salicornia brachiata (Singh et al. 2016; Udawat et al. 2016, 2017) was reported.

Since the majority of agricultural crops are monocots, this type of halophytic species is discussed here. Interestingly, monocotyledonous halophytes contain lower Na+ concentrations and exhibit higher selectivity for K+ uptake as compared to dicotyledonous halophytes (Flowers and Colmer 2008, 2015). Among monocots, there are plenty of plant species including Bromus danthoniae, Hordeum glaucum, H. marinum and others showing exceptional salinity tolerance, suggested for the detailed research aimed to the development of salinity stress-tolerant crops for sustainable agriculture.

Wild crop relatives and their potential use

The development of new salt-tolerant crops is an essential part of biotechnological plant improvement. The domestication of crops resulted the truncation of genetic variation present in the population of wild crop relatives. Closely related species of cereals are valuable genetic resources for modern agriculture and plant biotechnology, and the progenitors and other wild crop relatives provide a solid platform to promote new gene discoveries and mechanisms of physiological adaptations. The introduction of genes from wild relatives into crop cultivars is of primary importance for global food security (Hajjar and Hodgkin 2007). The study of the salinity tolerance in wild crop relatives could significantly facilitate the improvement of common agricultural plants. Many successful breeding efforts involving wild relatives for the significant improvement of drought and salinity tolerance in crops have been conducted.

Wheat, barley and rice are the major cereal crops in the world. Usually domesticated crop cultivars and varieties lack the genetic resources for the development and production of new salt-tolerant genotypes. Among the Triticeae tribe exist around 38 species, belonging to Triticum, Aegilops, Hordeum, Elytrigia, Elymus, Leymus and Thinopyrum genera as potential sources of salinity tolerance (Colmer et al. 2006). One of the easiest possibilities is to create amphidiploid hybrids as new crops being implicated in the saline areas. However, many of these amphidiploid hybrids did not perform well argonomically and exhibited low yield potential. For instance, it was shown that Hordeum chilense/Triticum turgidum ssp. durum and T. turgidum ssp. durum/Thinopyrum bessarabicum amphidiploids did not show good productivity (Martin and Chapman 1977; King et al. 1997). The accumulation of high Na+ concentrations in plant tissues significantly inhibits leaf function in cereal crops. In order to overcome this problem, the enhancement of shoot Na+ exclusion capacity of cereal crops may be very useful for salt tolerance improvement (Munns and Tester 2008a, b, Horie et al. 2009) (Table 2).

Table 2 Examples of gene transfer or crosses associated with salinity tolerance from wild crop relatives
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Wheat

The modern wheat species used for bread production and feed have a hexaploid (Triticum aestivum L.) or tetraploid (Triticum turgidum) genome. The tetraploid T. turgidum is a natural hybrid between a T. urartu with genome A (Khlestkina and Salina 2001) and an unknown diploid caring genome B. Aegilops is the closest relative of Triticum genus. It is believed that the Aegilops genus is most probably the B genome donor species (Kerby and Kuspira 1987). From the 22 wild Aegilops species, A. cylindrica has the biggest potential for salt tolerance improvement (Arzani and Ashraf 2016). The hexaploid genome of T. aestivum comprises genomes of the diploid species A. tauschii (DD) and the tetraploid species T. turgidum (AABB) (Colmer et al. 2006). The estimation of salt tolerance capacity of A. tauschii revealed lower Na+ accumulation and higher K+/Na+ ratios in their leaves in comparison with durum wheat (Gorham 1990). According to experimental data A. cylindrica demonstrates its halophytic capacity to secrete salt on leaves under high salinity (400 mM NaCl) (Arabbeigi et al. 2014). It was shown that the enhanced K+/Na+ discrimination in A. tauschii is associated with chromosome 4D (Shah et al. 1987). The plant species containing the D genome (Ae. tauschii, T. ventricosum, and T. crissum) displayed high salt tolerance capacity (Xu et al. 1993).

The “primitive” wild wheat species, T. turgidum spp. diccocum and T. monocotum, might have desirable traits and genes for the improvement of the salinity tolerance (James et al. 2006; Shavrukov et al. 2010; Munns et al. 2012; Table 2). Among wheat progenitors, wild relatives and halophytic species of Triticeae, variation in mechanisms of Na+ ‘exclusion’ and K+/Na+ discrimination is observed (Gorham 1994; Garthwaite et al. 2005). The mechanisms of salt tolerance among wheat species comprises the ability to maintain low Na+ and high K+ concentrations in leaves (Maas and Grieve 1990; Dvorak et al. 1994; Munns and James 2003; Poustini and Siosemardeh 2004). However, relatively small variation in Cl− accumulation in leaves among cultivated wheat species was observed (Gorham 1990; Husain et al. 2004; Colmer et al. 2005a). The crossing of Nax2, a gene locus in the wheat relative Triticum monococcum into a commercial durum wheat (T. turgidum ssp. durum var. Tamaroi) significantly reduced Na+ contents in leaves (James et al. 2011). Further studies revealed that a gene in the Nax2 locus is TmHKT1;5-A encoding Na+-selective transporter in the plasma membrane of root cells around the xylem vessels, which, therefore, is ideally localized to withdraw Na+ from the xylem and reduce transport of Na+ to leaves (Munns et al. 2006). The transfer of the Kna1 locus from D genome of hexaploid wheat into tetraploid T. turgidum significantly enhanced K+/Na+ ratios (Dvorak et al. 1994; Byrt et al. 2007). Interestingly, under salinity stress (150 mM NaCl) T. aestivum excludes nearly 99% of the Na+ from the transpiration stream. In contrast with bread wheat, T. turgidum has lower Na+ exclusion capacity (95–94%) (Munns 2005). Another study of wheat demonstrates that during salinity stress the key enzymes of the TCA cycle are physiochemically inhibited by salt. In order to compensate this enzyme inhibition wheat increases the GABA shunt activity. An increase of GABA shunt activity provides an alternative carbon source for mitochondria (Che-Othman et al. 2019).

Among halophytic plants of the Triticeae tribe, tall wheatgrass species, Elytrigia elongata, Thinopyrum bessarabicum, Thinopyrum ponticum and Thinopyrum junceum, have to be mentioned. These wild species of wheatgrass are considered as valuable genetic sources for the improvement of salt tolerance in wheat (Colmer et al. 2005a). It was demonstrated that amphiploid T. aestivum–E. elongata exhibits an enhanced capacity of Na+ and Cl− exclusion and elevated levels of K+ in leaves (Schachtman et al. 1989; Omielan et al. 1991). Moreover, some studies indicate a fivefold lower Na+ concentration, better maintenance of K+ concentrations, and enhanced levels of glycinebetaine, in the youngest leaf blades of the T. aestivum–E. elongata amphiploid in conditions of salinity stress (200 mM NaCl) in comparison with parent T. aestivum (Colmer et al. 1995). A salinity tolerance trait originating from T. bessarabicum (King et al. 1997) has been introgressed into durum wheat (Colmer et al. 2006). The capability to survive on 750 mM NaCl was shown for several accessions of T. ponticum (McGuire and Dvorak 1981). The mechanisms of salt tolerance of many halophytic wheatgrass species are associated with their capacity to restrict the Na+ and/or Cl− accumulation in shoots (Shannon 1978; Weimberg and Shannon 1988), and elevated levels of glycine-betaine accumulation in leaves (Weimberg and Shannon 1988). The transfer of T. ponticum chromosomes into bread wheat resulted in growth improvement of two introgression lines on 250 mM NaCl in comparison with bread wheat (Xia et al. 2003; Chen et al. 2004) (Table 2).

There are no clear data available regarding the salt tolerance of T. junceum. However, in sap from mature leaves after 4 months of growth on 200 mM NaCl, concentration for Na+ was 146 mM, that of Cl− was 248 mM, and the K+/Na+ ratio was only 1.0 (Gorham 1994) Thus, more data have to be obtained to evaluate this species as genetic source for salt tolerance.

Barley

Hordeum vulgare is considered as salt-tolerant crop in comparison with wheat and other cultivated species of Triticeae. Cultivated barley is able to grow on 150 mM NaCl, but in these conditions the loss of biomass is nearly 55–58% (Greenway 1962). Recently it was demonstrated that, in contrast with rice, barley plants are capable to quickly increase their xylem Na+ concentration and subsequent Na+ delivery to the shoot. However, barley plants were able to reduce this process later and keep most accumulated Na+ in the root. Thus, cultivated barley was able to maintain non-toxic shoot Na+ levels. Differences in control of xylem Na+ loading between rice and barley may explain their different capacities to tolerate salinity (Ishikawa and Shabala 2019). The salt tolerance may vary among the different Hordeum vulgare cultivars. For example, recent study suggest that salt-tolerant barley cultivars rely on the ability to counter Na+-induced oxidative stress by increasing antioxidant enzyme levels, on possible intensification of vacuolar Na+ sequestration, and on the prevention of cellular K+ leakage (Elsawy et al. 2018).

The genetic resources of wild Hordeum species for salt tolerance traits are largely unexplored. The ecogeographical study of Hordeum spp. demonstrates that more than a half of the barley species are capable to grow and develop on saline habitats, for example, H. patagonicum (von Bothmer et al. 1995) and H. brevisubulatum (Li et al. 2012). Previously, it was suggested that wild barley—H. vulgare ssp. spontaneum may serve as a source of the salinity tolerance (Nevo et al. 1993). Nonetheless, other studies demonstrated just limited enhancement of salinity tolerance in H. vulgare ssp. spontaneum (Forster et al. 1994; Ellis et al. 2000). Perhaps, the wild barley H. vulgare ssp. spontaneum has to be considered as a drought- and heat-tolerant, rather than a salt-tolerant species.

Among Hordeum species, H. marinum (sea barley grass or sea side barley) is considered to be one of the major genetic sources for salinity tolerance. H. marinum is a halophytic wild relative of the cultivated barley. This typical species of salt marshes and coastal areas is known to inhabit saline areas owing to its considerable tolerance to waterlogging and salinity (Garthwaite et al. 2005). The sea side barley is capable to control concentrations of Na+ and Cl− in leaves, even after exposure to 450 mM NaCl in the root-zone. Moreover, the analysis of plant water content and osmotic potential under high salinity revealed a relatively higher water saturation deficiency in H. marinum in comparison with H. vulgare. In contrast, H. vulgare had a lower osmotic potential, corresponding to high levels of proline and dehydrins (Maršálová et al. 2016). Analysis of salt-treated H. marinum plants displays enhanced levels of proteins involved in energy metabolism (glycolysis, ATP metabolism, photosynthesis) (Maršálová et al. 2016). These data indicate the high fitness capability of H. marinum in saline environments. Recently, a H. marinum–bread wheat amphiploid was created (Colmer et al. 2005b) (Table 2) demonstrating intermediate salt and waterlogging tolerance as compared to its parents (Colmer et al. 2005b). Another wild relative of barley, H. brevisubulatum, also needs elaborated research, since some reports indicating successful utilization of genes involved in salinity tolerance of this species aimed to improve salt tolerance in other plant species (Lu et al. 2005; Li et al. 2012) (Table 2). It is noteworthy that the salinity tolerance originating from another halophytic barley species, H. chilense, has been introgressed into durum wheat (Forster et al. 1990). Thus, wild Hordeum species may serve as a good source for the genetic salt tolerance improvement of our crops. Moreover, these halophytic barley species deserve more intense and detailed attention to reveal their adaptation mechanisms to harsh saline environments.

Rice

Rice (Oryza sativa L.) is supposed to be one of the most salt-sensitive crop species. The majority of the relatively salt-tolerant rice varieties originated from coastal areas and belong to the Indica group (Negrão et al. 2011). The O. sativa cv. Japonica cultivar Moroberekan originated from Guinea. Due to the specific environment of this country, with mangrove forests nearby cultivated areas, it has been used as a donor of salinity tolerance for other rice cultivars (Kim et al. 2009).

Recently, a large-scale genetic study was conducted to isolate a salt-tolerant introgression line, Dongxiang/Ningjing 15 (DJ 15), from a population of the salt tolerant wild rice Oryza rufipogon (Quan et al. 2018; Table 2). Using QTL mapping analysis, 9 QTLs for salt tolerance at the seedling stage located on chr. 1, 3, 4, 5, 6, 8, and 10 were found. Moreover, a sequence variation analysis within the QTL regions revealed that SKC1, HKT8, HKT1;5, and HAK6 transporters together with various transcription factors were candidate genes for the salt tolerance trait (Quan et al. 2018).

Among wild rice species Oryza glaberrima has to be mentioned. This plant is the second cultivated species of the Oryza genus and potentially grows in mangrove and brackish marshes (Linares 2002). However, the O. glaberrima salt tolerance is controversial and seems to be lower than that of O. sativa (Awala et al. 2010; Gregorio et al. 2002). Of the rice wild relatives only Porteresia coarctata has been extensively studied for its potential as genetic source of salt tolerance for rice (Flowers et al. 1990). This plant species is abundant near coastal areas and mangrove forests, where soils are subjected to salinity twice a day by sea tides or saline rivers (Bal and Dutt 1986).

Porteresia is an important genetic source of salt-tolerant genes/traits for the development of novel tolerant rice varieties (Latha et al. 2004). The use of P. coarctata for rice breeding programs is limited by the difficulties to obtain viable embryos (Gregorio et al. 2002) (Table 2). Nevetherless, several studies have shown that the application of some genes from Porteresia can improve the salinity tolerance of cultivated rice. These genes are involved in the inositol metabolic pathway (Majee et al. 2004; Sengupta et al. 2008; Morozova et al. 2009). Transcriptome analysis of P. coarctata under the salinity stress revealed upregulation of genes encoding stress-responsive transcription factors from different families including MYB, bHLH, AP2-EREBP, WRKY, bZIP and NAC (Garg et al. 2014). It has to be emphasised that Porteresia transcripts showed low similarity to the rice orthologs. The similarity levels of P. coarctata genes to rice were lower than those of other sequenced wild rice species (Sakai et al. 2011; Chen et al. 2013; Garg et al. 2014). Moreover, the analysis of ion content and physiological status of Porteresia plants have shown accumulation of less sodium and more potassium in leaves and roots in comparison to the Pokkali and IR64 rice varieties (Sengupta and Majumder 2009). Further studies of genes involved in metabolic pathways of salt stress in wild rice species may be a promising approach to improve salinity tolerance in cultivated rice.

Other crops

There are few economically important crops salt-tolerant wild relatives were described. Several halophytic wild relatives exhibit desirable characteristics that can be introgressed into the crop plants through conventional breeding. It was shown, that salt tolerance of sunflower could be substantially enhanced by the introduction of genes originated from their wild relative Heliantus paradoxus (Lexer et al. 2003; Kane et al. 2013). The other crop species are tomato (Lycopersicum cheesmanii and L. pimpinellifolium; Asins et al. 1993), and Beta vulgaris ssp. vulgaris (B. vulgaris ssp. Maritime; Rozema et al. 1993). It was demonstrated, that L. pimpinellifolium exhibit high productivity under saline condition as much as 15 dS/m. It is one of the closest related species to L. eseulentum and could be considered as potential donor of salt tolerance traits for tomato (Asins et al. 1993). The comparative analysis of growth capacities between the coastal halophyte Beta vulgaris ssp. Maritima (seabeet) (L.) Arcang and the fodder beet (Beta vulgaris ssp. Vulgaris L. cv. Majoral) under salinity has shown that relative growth rate of sea beet decreased by 20% and of fodder beet by 30% with salinity increasing to 400 mol m−3 NaCI (Rozema et al. 1993). Perhaps, it would be an option to look for salinity tolerance traits in Beta vulgaris ssp. Maritima. However, the further detailed study of this wild crop relatives have to be conducted. Moreover, the crosses of cultivated plant varieties with their halophytic relatives will provide possibility to raise salt tolerance in the amphiploids.

Lower plants, yeasts and animals

One strategy to engineer salt-tolerant plants is to keep cytosolic Na+ concentrations below toxic levels. To achieve this goal, genetic manipulations with native or heterologous ion transporters involved in Na+ extrusion and sequestration may be performed (Shi et al. 2002; Munns et al. 2012). Many attempts to generate salt-resistant high-yielding crops by the manipulation of plant membrane ion transporters genes have been unsuccessful (Roy et al. 2014).

Lower plants, including algae, have ion transporters, channels, and pumps potentially unknown in land plants. Fungi and animals could be a good source of useful transporters absent in plant kingdom as well. For example, expression of a yeast Na+/H+ antiporter (SOD2) resulted in increased salt tolerance in transgenic rice plants (Zhao et al. 2006a, b).

Animal cells have a completely different approach to handle Na+ than plants, since they are much more tolerant to saline conditions because of the capability to extrude Na+ by an efficient Na+/K+-ATPase (Pedersen and Palmgren 2017). The Na+/K+-ATPase system is exceptionally efficient, since the export of three Na+ ions and import of two K+ by this enzyme requires only one ATP (Pedersen and Palmgren 2017). The result of the Na+/K+-ATPase activity is developing of chemical Na+ and K+ gradients and subsequent creation of difference in electrical charge across the plasma membrane. The created electrochemical gradient could be used by many transport processes (Pedersen and Palmgren 2017). For animal growth the Na+ extrusion is an essential part of metabolism (Fig. 2). In contrast to this, canonical plant Na+/H+-antiporters indirectly consume one ATP molecule per one exported Na+. Thus, this type of Na+ export is considered to be costlier in terms of energy (Pedersen and Palmgren 2017) (Table 3). Some lower plants could also have Na+/K+-ATPases. For example, Chlamydomonas reinhardtii has a Na+/K+-ATPase, A8HX15 (Pedersen and Palmgren 2017). However, this type of gene does not exist in fungi and mosses (Pedersen and Palmgren 2017).

Fig. 2
figure 2

The perspective targets from animals, yeast and lower plants to increase salt tolerance in plants. Overexpression of exogenous genes encoding Na+-ATPases (ScENA1, PpENA1), Na+/K+-ATPases (A8HX15, HsATA1, HsATA2, HsATA3), vacuolar cation/Ca2+ exchangers (CrCAX1, Vnx1p) may favour to an increased salt tolerance

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Table 3 Examples of gene transfer resulted improvement of plant salinity tolerance from lower plants or fungi
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Furthermore, Na+-ATPases, similar to those in fungi, have been identified in mosses (Pardo et al. 2006). It was shown that moss ENA Na+-ATPases work together with the SOS1-like Na+/H+−-antiporters. Although in fungi, ENA Na+-ATPases play the major role in Na+ export (Prista et al. 1997). It was reported that some green algae have genes encoding homologues of animal Na+/K+-ATPases (Pedersen et al. 2012). Therefore, one of the differences between the lower plants (green algae and mosses) and vascular plants is absence of genes that encode Na+/K+-ATPases or Na+-ATPases. It is postulated that Na+/K+-ATPases or Na+-ATPases may give an advantage under salt stress for green algae and mosses (Pedersen and Palmgren 2017). Perhaps, these ATPases were lost during evolution of flowering plants (Pedersen and Palmgren 2017). It is very likely that the first land plants which colonised land originated from freshwater (Kenrick and Crane 1997). Some experimental studies reveal a positive correlation between salt tolerance and ENA1 expression in the moss Physcomitrella patens (Pedersen and Palmgren 2017). Thus, it is possible that plants transformed with animal, moss, or algal type of Na+/K+-ATPase or Na+_ATPase could have a significantly improved salt tolerance. For example, the expression of ENA1 from P. patens in rice leads to greater biomass production under salinity stress (Jacobs et al. 2011). Consequently, it is obvious that the strategy to produce transgenic plants heterologously expressing these types of genes for salinity tolerance improvement needs to be considered (Fig. 2).

It seems that the yeast protein Vnx1p, belonging to the CAX Type II subfamily, is capable to mediate transport of Na+ and K+ into the vacuole (Cagnac et al. 2007). Higher plants do not have those type II cation/proton exchangers. In contrast to higher plants, mammals and fungi (yeasts) have CAX proteins exhibiting Na+/Ca2+ and Na+/H+ exchange activities (Manohar et al. 2011). Moreover, another member of CAX proteins, CrCAX1 from C. reinhardtii, has Ca2+/H+ and Na+/H+ exchange activities (Pittman et al. 2009) (Table 3). A role of CrCAX1 in providing tolerance to cation stress, including Na+, based on heterologous expression experiments in yeast and Arabidopsis (Pittman et al. 2009), has suggested. The identification of CrCAX1 as a Na+ transporter may help to understand the osmotic stress regulation by this unicellular organism (Fig. 2).

It would be a good opportunity to test if the application of these type of CAX proteins with Na+/Ca2+ and Na+/H+ exchange activities can improve salinity tolerance of higher plants. Alternatively, the use of synthetic biology approaches to generate novel CAX transporters with the desired transport and selectivity properties will be a promising option as well.

Salt tolerance genes

There are several possibilities to use genetic sources to improve salt tolerance. In order to succeed in salt tolerance improvement, the careful selection of candidate genes for gene transfer or manipulation have to be conducted. Moreover, detailed functional analysis of gene products and determination of place of these genes in the molecular network of salinity tolerance is required. Among the prospective genes for genetic engineering and molecular breeding the several functional groups have to be highlighted.

First group comprises the genes encoding ion transporters. These group is most prominent and well-studied. The ion transporters are involved in many mechanisms of salinity tolerance including osmotic adjustment; accumulation of toxic ions into intracellular compartments; ion retranslocation to the non-active metabolically tissues; toxic ions removal from cells and plant tissues; limitation of Na+ and Cl− uptake; maintenance of low Na+/K+ (Cl−/NO3−) ratio in cytosol (Isayenkov 2012; Isayenkov and Maathuis 2019). The wide range of genes were identified and characterised for salt tolerance improvement, among these genes the SOS (Salt-Overly-Sensitive) genes, the Na + transporter genes NHX1 and HKT1, genes encoding K+ transporters and channels (HAK, SKOR, AKT, KAT, TPK), family of Ca2+/cation exchangers, H+:monovalent cation exchanger family (CHX) (Maathuis and Amtmann 1999; Schachtman 2000; Hasegawa et al. 2000; Flowers and Colmer 2008; Ashraf and Akram 2009; Shabala and Cuin 2007; Pardo et al. 2006; Fuchs et al. 2005; Obata et al. 2007; Shabala and Mackay 2011; Wang et al. 2012; Isayenkov 2012). Moreover, the genes encoding the tonoplast and plasma membrane proton-pumps are crucial for generating the electric potential and proton gradients (Ashraf and Akram 2009). Beside this, it should be noted big potential of genes encoding anion, in particular Cl−, transport (Li et al. 2017). According to the experimental data the major gate of Na+ entry belong to NCCC channels. Therefore, knock out or limitation of some NCCC genes expression could be beneficial for salinity tolerance (Tester and Davenport 2003; Horie and Schroeder 2004; Demidchik and Maathuis 2007).

Second gene group is related to osmolyte biosynthesis proteins. However, the application of this type genes may solve the problems of osmotic adjustment, but not ion toxicity. Therefore application of genes involved in biosynthesis of betaine, proline, myo-inositol, sugars or other types of osmolyte would beneficial for plant tolerance (Rhodes et al. 2002; Flowers and Colmer 2008; Kalinina et al. 2012). However, the experimental data suggest that from the point of energy use, cellular osmotic adjustment is more efficient by application of ions than organic solutes (Greenway and Munns 1980; Flowers et al. 2010).

Third group of genes is involved in antioxidant machinery. In the battle with ROS, plants recruit an efficient antioxidant system comprising enzymatic antioxidants including superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), peroxidase (POX), redox regulatory enzymes such as monodehydroascorbate reductase (MDAR), glutathione reductase (GR), glutathione peroxidase (GPX), glutathione S- transferases (GST) (Gao et al. 2008; Isayenkov 2012; Negrão et al. 2011). Therefore, gene transfer or modulation of gene expression for plant protection against ROSs deserves our attention.

Forth group of genes is encoding stress-induced proteins such as LEA. The LEA proteins is involved in protection of molecules under the water deficiency. These group of proteins is providing a water-like rich environment to their target enzymes (Negrão et al. 2011). Among the different LEA proteins, the group 2 of LEAs (dehydrins) is very important for plant tolerance improvement to various stresses (Hanin et al. 2011). Therefore, application of genes encoding these type proteins deserve to be considered.

Last functional group belong to the genes is encoding transcription factors known to be involved in salinity stress response. This group comprise MYB, bHLH, AP2-EREBP, WRKY, bZIP and NAC families. Many transcription factors were successfully tested in various glycophytic crops including tobacco, maize, rice, wheat, potato, tomato, cabbage (Joshi et al. 2015).

Conclusion

From the more than 300,000 plant species in the world, less than 200 are commercially important. It remains still challenging to create and commercialize crops with the increased tolerance to salinity or any other abiotic stress and also laboratory growth and experiment setup are far different from field conditions. However, to create successful salt-tolerant crop the large-scale and long-term field trials under the monitored conditions have to be conducted. Besides field trials there are the plethora of challenges still waiting to be solved. However, different halophytic plant species, lower plants and fungi use different mechanisms to respond on salt stress, since a single species as a model for study salt tolerance is not enough. Therefore, the detailed studies of the molecular mechanisms of salt stress regulation for the wide range of halophytic species from plant, animal and fungi kingdoms might significantly improve our understanding of the salinity tolerance nature. The identification and characterization of the novel specific genes involved in the regulation of the plant salinity tolerance from different plants and other organism will significantly improve quality of the engineered salt tolerant crops. High-throughput phenotyping, expression profiling, genome sequencing of both economically important crops and their relatives, as well as halophytic plants are required to achieve desirable goals in salt tolerance engineering. An alternative approach is the synthetic biology tools for the modification of the existing membrane transport proteins or other key proteins of salt tolerance. Engineering of the completely novel proteins, with the desired properties, for the regulation of salt crop tolerance will be a good option. It has to be mentioned that the several traits in crops crucial for their domestication are results of mutations, which can be easily reproduced by genome-editing techniques, offering the potential for the enhanced domestication of the new crops. Thus, the engineering of salt tolerance mechanisms via the genome editing will progress in the upcoming years, and, in the meanwhile, the domestication of new crops might increase agricultural diversity and provide an alternative solution to solve various problems of modern agriculture.