Skip to main content
PMC home page
Frontiers in Plant Science logoLink to Frontiers in Plant Science
. 2017 May 18;8:829. doi: 10.3389/fpls.2017.00829

Halophytes: Potential Resources for Salt Stress Tolerance Genes and Promoters

Avinash Mishra 1,2,*, Bhakti Tanna 1,2
PMCID: PMC5435751  PMID: 28572812

Abstract

Halophytes have demonstrated their capability to thrive under extremely saline conditions and thus considered as one of the best germplasm for saline agriculture. Salinity is a worldwide problem, and the salt-affected areas are increasing day-by-day because of scanty rainfall, poor irrigation system, salt ingression, water contamination, and other environmental factors. The salinity stress tolerance mechanism is a very complex phenomenon, and some pathways are coordinately linked for imparting salinity tolerance. Though a number of salt responsive genes have been reported from the halophytes, there is always a quest for promising stress-responsive genes that can modulate plant physiology according to the salt stress. Halophytes such as Aeluropus, Mesembryanthemum, Suaeda, Atriplex, Thellungiella, Cakile, and Salicornia serve as a potential candidate for the salt-responsive genes and promoters. Several known genes like antiporters (NHX, SOS, HKT, VTPase), ion channels (Cl−, Ca2+, aquaporins), antioxidant encoding genes (APX, CAT, GST, BADH, SOD) and some novel genes such as USP, SDR1, SRP etc. were isolated from halophytes and explored for developing stress tolerance in the crop plants (glycophytes). It is evidenced that stress triggers salt sensors that lead to the activation of stress tolerance mechanisms which involve multiple signaling proteins, up- or down-regulation of several genes, and finally the distinctive or collective effects of stress-responsive genes. In this review, halophytes are discussed as an excellent platform for salt responsive genes which can be utilized for developing salinity tolerance in crop plants through genetic engineering.

Keywords: abiotic stress, halophytes, promoter, salinity, salt responsive genes, salt stress, stress tolerance, transgenic

Introduction

Salinization is a worldwide problem in which salts gradually accumulate in the soil. In this process, water-soluble salts are deposited in the soil to an extent that affects crop productivity, microbial community, and agricultural economics (FAO, 2016). The salinization eventually transforms a fertile land to barren. The process destroys all vegetation and other organisms living in the soil and thus it is detrimental to the environmental health. Most of the world's land is not cultivated, and over 2% of the total land is affected by salinity (FAO; Land and Plant Nutrition Management Service). A significant proportion of cultivated land is salt-affected, and out of the current 230 million ha of irrigated land, 45 million ha are salt-affected whereas 32 million are salt-affected to varying degrees (FAO, 2008).

Halophytes are salt-resistant or salt-tolerant plants and have remarkable ability to complete their life cycle in saline condition. During evolution, they have developed different morphological, anatomical, and physiological strategies to proliferate in high-salt environments (Flowers and Colmer, 2008; Grigore et al., 2014). Halophytes have occasionally been reviewed for their general physiology (Flowers, 1985), ecophysiology (Ball, 1988), photosynthesis (Rozema and Van Diggelen, 1991; Lovelock and Ball, 2002), response to oxidative stress (Jithesh et al., 2006), flooding tolerance (Colmer and Flowers, 2008), salinity tolerance (Flowers and Colmer, 2008), and adaptations (Flowers et al., 2015). Additionally, other researchers have also examined halophytes under special topics as sustainable cultivation, saline agriculture, and integrative anatomy (Rozema et al., 2013; Grigore et al., 2014; Flowers et al., 2015; Xu et al., 2016).

Halophytes that consistently require salt for their growth are referred to “obligate halophytes” (Braun-Blanquet, 1932), but some halophytes have the ability to grow on the soil devoid of salt are called as “facultative halophytes” (Polunin, 1960). Halophytes are obligate and facultative based upon salt demand and tolerance for sodium salts. Previously, a study has been carried out with some selected halophytes to investigate the salt requirement for growth and development (Grigore et al., 2012). Researchers concluded that salts are not compulsorily required for the development of halophytic species but the availability of water and nutrients are also key limiting factors for growth in natural saline habitats (Grigore et al., 2012). Further, they hypothesized that halophytes are mostly distributed in saline areas to avoid competition with glycophytic species.

Ecophysiological characteristics are used by Cushman (2001) to differentiate between obligate, facultative, and habitat-indifferent halophytes. Habitat-indifferent halophytes are undistinguished to their habitat, usually, prefer to live in a salt-free soil but have the ability to cope with the saline condition (Cushman, 2001). Recently, Grigore and Toma (2010) proposed a new type of classification of halophytes; extreme-halophyte (irreversible and reversible) and meso-halophytes, by integrating anatomy observations with ecological factors (salinity). Extreme-halophytes are well-adapted extreme halophytes and growing exclusively in saline environments. Furthermore, the habitat of these halophytes may be irreversible or reversible. They concluded that Chenopodiaceae (now included in the family Amaranthaceae) succulent species (Salicornia, Suaeda, Halimione, and Petrosimonia) are extreme halophytes and best adapted to high salinity conditions. Halophytes such as Atriplex, Bassia, and Camphorosma are not strictly related to increased salinity, therefore may be classified as reversible halophytes. There is always a difficulty with the distinct terminology of halophytes because the definition is still obscure and Grigore et al. (2010) discussed a short historical evolution of halophytes definition in chronological order.

Advanced and novel stress-tolerant mechanisms are difficult to study with the model plant Arabidopsis as some mechanisms are unique to halophytes. The comparative genomics of Mesembryanthemum crystallinum and Arabidopsis thaliana confirmed that some transcripts present in former and later do not have counterparts (Wang et al., 2004). Some other halophytes, Suaeda species, and Atriplex species have been investigated to unravel molecular mechanism of stress tolerance. Among all, Thellungiella halophila is one of the halophytes emerging as a model halophyte for the study of abiotic stress tolerance mechanism (Wang et al., 2004; Amtmann, 2009). Halophyte Cakile maritima and Suaeda maritima (Megdiche et al., 2009; Sahu and Shaw, 2009) are considered as model plants for the transcript profiling and Salicornia brachiata as a potential halophyte for new and useful salt-tolerant genes (Singh et al., 2016; Udawat et al., 2016, 2017). In this review, halophytes are discussed as resources for salt stress tolerance genes, which can be explored further for developing abiotic stress tolerance crops for sustainable agriculture.

Salt tolerance mechanism in halophytes: a glimpse

Halophytes are well-adapted and thrive under high salinity by using two strategies, salt tolerance, and salt avoidance. Generally, halophytes follow three mechanisms of salt tolerance; reduction of the Na+ influx, compartmentalization, and excretion of sodium ions (Flowers and Colmer, 2008, 2015). Adaptations involved in salt avoidance are secretion, shedding, and succulence (discussed in Waisel, 1972; Rozema, 1995; Aslam et al., 2011; Shabala et al., 2014). In brief, secretion is a complex mechanism, and salt-secreting structures (salt hairs or salt glands) are distributed in halophytes. Some halophytes are capable of excreting excess salt in the form of a liquid which becomes crystals in contact with air and may visible on the plant leaf surface. In some halophytes, shedding of the old leaves which are grown under high salt concentrations is another strategy to avoid the salt toxicity. Grigore et al. (2014) discussed the different aspects of the various adaptive structures of halophytes in an integrative way at the anatomy level.

The salt tolerance mechanism is coordinately linked (Figure 1) with signal transduction, ROS generation and detoxification pathways, osmoregulation or ion homeostasis through osmoprotectants, and differential expression of salt responsive genes and transcription factors (Flowers and Colmer, 2008; Rajalakshmi and Parida, 2012; Himabindu et al., 2016; Khan et al., 2016; Muchate et al., 2016). ROS detoxification pathways include antioxidative enzymes which play a protective role in scavenging toxic radicals (Das and Strasser, 2013). Salt sequestration into cell vacuoles through transporters is another key mechanism employed by halophytes to maintain a high cytosolic K+/Na+ ratio and thus control the salt concentrations in the cytosol (Kronzucker and Britto, 2011; Sreeshan et al., 2014). Accumulation of osmoprotectants such as proline, glycine betaine, polyphenols, soluble sugars, and inorganic ions is a conventional plant defense mechanism routinely used by halophytes to cope with stresses (Lokhande and Suprasanna, 2012; Patel et al., 2016). At the molecular level, halophytes impart salt tolerance by regulating stress-responsive genes through ABA-dependent or ABA-independent regulation mechanism. Overall, salt tolerance in a halophyte is a complex network that involves the interactions of multiple physiological responses directive by several genes and gene products (Figure 1). Overall, halophytic salt tolerance defense mechanism includes changes in ion homeostasis (both influx and efflux), the formation of osmoprotectants, activation of crosstalk genes, induction of antioxidants, and the development of salt gland or bladders (Shabala et al., 2014; Slama et al., 2015; Himabindu et al., 2016).

Figure 1.

Figure 1

Open in a new tab

A generalized schematic representation of salinity stress tolerance mechanism in a plant.

Salt responsive genes from halophytes: an overview

Halophytes have been studied extensively for their ecological, physiological, anatomical, and biochemical responses toward salinity (Flowers and Colmer, 2008; Aslam et al., 2011; Shabala, 2013; Ventura et al., 2015). Furthermore, halophytes were also explored for saline agriculture and examined as bioenergy crop (Rozema and Schat, 2013; Sharma et al., 2016). However, little information is available on well-defined molecular defense mechanism of halophytes against salt stress (Anjum et al., 2012; Joshi et al., 2015). Surprisingly, a non-tolerant plant, A. thaliana is widely explored as a model plant to investigate the molecular mechanism of salt stress tolerance (Sanders, 2000; Zhu, 2001). Additionally, this plant is also exploited for the gene mining of salt stress-responsive genes for the improvement of tolerance in transgenic crops (Zhu, 2000).

It is a general assumption that halophytes are salt resistant while glycophytes are sensitive, but there are several species considered traditionally as glycophytes are resistant or tolerant to salt and some halophytes may be sensitive to several environmental stresses. Recently, it is experimentally proven that halophytes are one of the most appropriate models for the studying different salt stress tolerance mechanisms (Shabala, 2013; Flowers and Colmer, 2015; Himabindu et al., 2016). A number of evidences suggest that all plants have almost similar salt tolerance regulatory mechanisms and there are quantitative differences rather than qualitative between halophyte and glycophyte (Anjum et al., 2012; Rai et al., 2012; Bartels and Dinakar, 2013; Sreeshan et al., 2014; Joshi et al., 2015; Volkov, 2015; Muchate et al., 2016). It may be because of higher expression of key genes involved in the salt stress tolerance mechanism, or halophytic proteins are intrinsically more active than the corresponding glycophytic proteins (Anjum et al., 2012; Das and Strasser, 2013; Himabindu et al., 2016; Muchate et al., 2016).

Different genomic and transcriptomics efforts have been made to isolate salt responsive genes from some halophytes followed by their functional validation through transgenic approaches. The overexpression of several halophytic genes, under the control of a non-specific 35SCaMV promoter, have been claimed to enhance abiotic stress tolerance in the glycophytic recipients (Table 1). A number of crops have been transformed with halophytic genes for the improvement of salt tolerance. Most of these genes encode for Na+/H+ antiporters (vacuolar or plasma membrane), vacuolar pyrophosphatase, potassium transporters, ion channels, antioxidants, ROS scavengers, and proteins that involve in protective function and signal transduction. Additionally, some novel salt responsive genes were also cloned and characterized from halophytes like S. brachiata (Udawat et al., 2014, 2017; Singh et al., 2016).

Table 1.

Abiotic stress responsive genes of halophytic origin reported to enhance salt tolerance in glycophytic hosts.

Halophytes Genes Description Recipient plants References
Aeluropus littoralis AlNHX1 Vacuolar Na+/H+ antiporter Nicotiana tabacum Zhang et al., 2008
Atriplex centralasiatica AcBADH Synthesis of glycine betaine Nicotiana tabacum Yin et al., 2002
Atriplex gmelini AgNHX1 Vacuolar Na+/H+ antiporter Oryza sativa Ohta et al., 2002
Atriplex hortensis AhBADH Synthesis of glycine betaine Tomato Jia et al., 2002
Atriplex hortensis AhProT1 Proline transport Arabidopsis Shen et al., 2002
Atriplex nummularia AmCMO Enhanced glycine betaine synthesis Nicotiana tabacum Tabuchi et al., 2005
Avicennia marina AmMDHAR Ascorbate regeneration and ROS scavenging Nicotiana tabacum Kavitha et al., 2010
Halostachys caspica HcNHX1 Vacuolar Na+/H+ antiporter Arabidopsis Guan et al., 2011
Halostachys caspica V-ATPase Vacuolar-H+-pyrophosphatase Arabidopsis Hu et al., 2012
Kalidium foliatum V-ATPase Vacuolar-H+-pyrophosphatase Arabidopsis Yao et al., 2012
Salicornia brachiata SbASR1 Abscisic acid stress ripening-1 Arachis hypogea Tiwari et al., 2015a
Salicornia brachiata SbGSTU Tau class glutathione transferases Nicotiana tabacum Jha et al., 2011
Salicornia brachiata SbMT-2 Metallothionein: ROS scavenger Nicotiana tabacum Chaturvedi et al., 2014
Salicornia brachiata SbNHX1 Vacuolar Na+/H+ antiporter Jatropha curcas Joshi et al., 2013
Salicornia brachiata SbNHX1 Vacuolar Na+/H+ antiporter Ricinus communis Patel et al., 2015
Salicornia brachiata SbNHX1 Vacuolar Na+/H+ antiporter Cuminum cyminum Pandey et al., 2016
Salicornia brachiata SbpAPX Peroxisomal ascorbate peroxidase Nicotiana tabacum Singh et al., 2014a
Salicornia brachiata SbpAPX Peroxisomal ascorbate peroxidase Arachis hypogea Singh et al., 2014b
Salicornia brachiata SbSDR1 Salt and drought responsive gene Nicotiana tabacum Singh et al., 2016
Salicornia brachiata SbSRP Salt responsive protein encoding gene Nicotiana tabacum Udawat et al., 2017
Salicornia brachiata SbUSP Cytosolic universal stress protein Nicotiana tabacum Udawat et al., 2016
Salicornia europaea SeCMO Enhanced glycine betaine synthesis Nicotiana tabacum Wu et al., 2010
Salsola soda SsNHX1 Vacuolar Na+/H+ antiporter Alfalfa Li et al., 2011
Spartina alterniflora SaVHAc1 Vacuolar H + -ATPase subunit c1 Oryza sativa Baisakh et al., 2012
Suaeda corniculata V-ATPase Vacuolar-H+-pyrophosphatase Arabidopsis Liu et al., 2011
Suaeda liaotungensis SlASR1 Abscisic acid stress ripening Arabidopsis Hu et al., 2014
Suaeda liaotungensis SlBADH Synthesis of glycine betaine Zea mays Wu et al., 2008
Suaeda liaotungensis SlBADH Synthesis of glycine betaine Nicotiana tabacum Li et al., 2003a
Suaeda liaotungensis SlCMO Enhanced glycine betaine synthesis Nicotiana tabacum Li et al., 2003b
Suaeda liaotungensis SlNAC NAC transcription factor Arabidopsis Yang et al., 2014
Suaeda salsa SsCAX1 Vacuolar H+/Ca2+ Transporter Arabidopsis Han et al., 2012
Suaeda salsa Ss.sAPX Stroma ascorbate peroxidase Arabidopsis Li et al., 2012
Suaeda salsa SsCHLAPX Chloroplastic ascorbate peroxidase Arabidopsis Pang et al., 2011
Suaeda salsa SsGST Glutathione S-transferase Oryza sativa Zhao and Zhang, 2006
Suaeda salsa SsPrxQ Chloroplast-located Peroxiredoxin Q Arabidopsis Jing et al., 2006
Suaeda salsa SsVP Vacuolar-H+-pyrophosphatase Arabidopsis Guo et al., 2006
Tamarix androssowii TaMnSOD Antioxidant: manganese superoxide dismutase Populus Wang et al., 2010
Thellungiella halophila ThNHX1 Vacuolar Na+/H+ antiporter Arabidopsis Wu et al., 2009
Thellungiella halophila ThSOS1 Salt overly sensitive gene Arabidopsis Oh et al., 2009
Thellungiella halophila TsVP H+-PPase gene Gossypium Lv et al., 2008
Thellungiella halophila TsVP H+-PPase gene Nicotiana tabacum Gao et al., 2006
Thellungiella salsuginea TsLEA1 Late embryogenesis abundant (LEA) Arabidopsis Zhang et al., 2012
Thellungiella salsuginea TsTIP1 Tonoplast AQP gene Arabidopsis Wang et al., 2014
Open in a new tab

A close relative of thoroughly explored glycophytic crucifer A. thaliana, Thellungiella salsuginea, which was earlier classified as T. halophila is a halophyte, exhibiting a high tolerance to salt and drought, considered as a potential model for abiotic stress tolerance studies by some researchers (Amtmann, 2009; Bartels and Dinakar, 2013). The genome sequence of T. salsuginea provides evidence about the genetic basis of abiotic stress defense mechanisms, and comparative genomics identified this plant as a gene resource for cation transporters, abscisic acid signaling genes, and other upregulated genes that showing a response to stressful environments (Wu et al., 2012). Furthermore, microarray analysis exhibited that only few genes were induced in Thellungiella compared to Arabidopsis under salt stress (Taji et al., 2004). Another study reveals that about 154 genes were differentially regulated in Thellungiella compared to Arabidopsis under varying stress (Wong et al., 2006).

Similarly, another halophytic relative of the model plant Arabidopsis, Lepidium crassifolium showed salt, osmotic and oxidative stresses tolerance. Random genes were transferred from L. crassifolium to A. thaliana, and it was observed that independent transgenic lines enhanced tolerance under several stress conditions (Rigó et al., 2016). Approximately 15% of functionally unknown genes were additionally expressed under salt stress compared to the non-stress conditions in M. crystallinum (Cushman and Bohnert, 2000; Kore-eda et al., 2004).

An extreme halophyte S. brachiata grows luxuriantly on salt marshes and also frequently encountered with different environmental stresses. Since, S. brachiata has unique opportunity to sustain adverse conditions and thus considered as a rich source of stress responsive genes and promoters (Jha et al., 2011; Chaturvedi et al., 2012; Singh et al., 2014a; Tiwari et al., 2014, 2016; Udawat et al., 2016). The salt responsive genes from S. brachiata have been utilized to develop salt stress tolerant transgenic crops such as jatropha, cumin, castor, and peanuts (Joshi et al., 2011; Singh et al., 2014b; Patel et al., 2015; Tiwari et al., 2015a; Jha et al., 2016; Pandey et al., 2016) using different genetic transformation methods (Singh et al., 2010; Joshi et al., 2012; Pandey et al., 2013; Tiwari et al., 2015b). Furthermore, Salicornia also owns unique oligosaccharides (Mishra et al., 2013), metabolites (Mishra et al., 2015), sulfur-rich seed-storage proteins (Jha et al., 2012) and thus considered as a functional food. Transcriptomics of Porteresia coarctata, a wild relative of rice showing high salinity and submergence tolerance revealed a total of 152,367 unique transcript sequences (Garg et al., 2014). A total of 15,158 genes, involved in salinity and submergence tolerance were identified to unravel key metabolic pathways. These genes can be explored further to understand and engineer salinity and submergence tolerance in rice (Garg et al., 2014).

Promoters of salt-responsive halophytic genes: at a glance

A strong and well-regulated promoter is required for the engineering of crop plants to achieve the desired level of expression of a transgene. A comparative transcriptome analysis revealed that many stress-related genes constitutively expressed at higher level in T. halophila compared to their homologs of A. thaliana (Taji et al., 2004, 2010). This report suggests an efficient transcriptional regulatory network for stress responsive genes in halophytes. Recently, cis-regulatory elements of different stress responsive genes from some halophytes have been studied, and the presence of various stress-inducible motifs was observed (Tiwari et al., 2014, 2016). Yin et al. (2002) found that the promoter of AcBADH gene from Atriplex centralasiatica is strongly induced by salt stress and possesses two salt-responsive enhancer regions (located from −1,115 to −890 and −462 to −230) and one silencer region (located between −890 and −641).

The SlBADH gene promoter fragment (−300 bp only) from Suaeda liaotungensis showed about 6.3-fold expression under salt stress (400 mmol/l NaCl) compared to control (non-stressed) condition (Zhang et al., 2008). The TsVP1 gene promoter from halophyte T. halophila contained 130 bp specific cis-acting element and showed a higher expression of GUS in transgenic Arabidopsis under salt stress (Sun et al., 2010). Similarly, an 897 bp promoter region of SlPEAMT gene (S. liaotungensis) showed an 18.6-fold increase in the GUS activity under NaCl stress (200 mmol/l) treatment (Li et al., 2016). These results suggest that even a small fragment of promoter can also contain essential cis-acting elements to regulate gene expression under stress. The promoters of CMO genes from S. liaotungensis and Salicornia europaea also possessed basic elements and demonstrated to be salt inducible (Li et al., 2007; Wu et al., 2011). Schaeffer et al. (1995) identified enhancer and silencer regions involved in the transcriptional activation of salt-responsive expression of CAM (Crassulacean Acid Metabolism) genes in the halophyte M. crystallinum.

An age-dependent, abiotic-stress-inducible, organ-specific, and tissue-specific promoter, AlSAP was reported from Aeluropus littoralis (Saad et al., 2011). Furthermore, gusA exhibited same expression level under the control of AlSAP gene promoter in transgenic rice as AlSAP transcript in A. littoralis (Ben-Saad et al., 2015). They also concluded that the regulatory regions of two orthologs AlSAP and OsSAP9 (from rice) have a different specificity of regulation and stress induction in rice. Sun et al. (2010) found a 130 bp specific cis-acting element in the promoter region of vacuolar H+-pyrophosphatase from a halophyte T. halophila (TsVP1) which enhances the expression of GUS in transgenic Arabidopsis under salt stress. The CBL1 gene promoter isolated from Ammopiptanthus mongolicust controlled the expression of the reporter gene under abiotic and biotic stress conditions (Guo et al., 2010). A model, proposed for transcriptional regulation of the SbpAPX gene (from S. brachiata) showed the presence of enhancer and repressor binding sites in the cis-regulatory elements along with stress-inducible motifs (Tiwari et al., 2014). Similarly, the SbGSTU promoter showed the presence of a number of abiotic stress responsive cis-regulatory motifs which regulate the expression of GSTU gene in S. brachiata (Tiwari et al., 2016). Therefore, based on different reports, halophytic promoters emerge as a promising candidate for engineering abiotic stress tolerance in crops for high-level expression of transgenes.

Salt tolerant genes from halophytes and glycophytes: a comparative analysis

Among different strategies; Na+ efflux, compartmentalization of Na+ in vacuoles and prevention of Na+ influx are the most common, governed by antiporters and regulated by a multigene family (Rajendran et al., 2009; Kronzucker and Britto, 2011). A number of antiporters isolated from both glycophytes and halophytes are functionally characterized (Kronzucker and Britto, 2011; Sreeshan et al., 2014). The overexpression of glycophytic transporters encoding genes (NHX, SOS, HKT, ATPase, etc.), under the control of non-specific CaMV35S promoter, showed tolerance in the range of 150–250 mM NaCl, however their halophytic homologs may provide tolerance up to 400 mM NaCl (reviewed in Kronzucker and Britto, 2011; Sreeshan et al., 2014; Volkov, 2015). In several previous studies, the effects of overexpression of halophytic genes were commonly observed under salt stress treatments, however, negligible differences were observed between wild-type plants and the transgenic lines under control (unstressed) conditions (Jha et al., 2011; Joshi et al., 2012; Volkov, 2015; Tiwari et al., 2015a; Singh et al., 2016; Udawat et al., 2016, 2017).

The glycophytic NHX gene from A. thaliana was widely explored for developing salt tolerance in many crops including tomato, brassica, maize, wheat, etc. (Zhang et al., 2001; Xue et al., 2004; Yin et al., 2004). Even, other glycophytic NHX1 genes such as BnNHX1 (Brassica napus), GhNHX1 (Gossypium hirsutum), and HbNHX1 (Hordeum brevisubulatum) have demonstrated to produce salt tolerance in the model plant tobacco (Wang et al., 2004; Wu et al., 2004; Lü et al., 2005). Thus, the NHX1 gene from halophyte and glycophyte both showed the salt tolerance activity, but there is a difference regarding salt tolerant intensity. The antiporter AgNHX1 (from halophyte Atriplex gmelini) showed 75% amino-acid sequence similarity with AtNHX1 (A. thaliana) and a higher salinity tolerance in Oryza sativa (Hamada et al., 2001; Ohta et al., 2002). Transgenic plants overexpressing AgNHX1 (A. gmelini), SaNHX1 (Spartina anglica) or SsNHX1 (Suaeda salsa) gene show tolerance up to 300–400 mM NaCl compared to glycophytic counterparts (Ohta et al., 2002; Zhao et al., 2006; Lan et al., 2011). The overexpression of SbNHX1 gene showed 200 mM salt tolerance in the model plant transgenic tobacco, but only 100 mM NaCl tolerance was observed in the transgenic jatropha and castor plants (Joshi et al., 2013; Patel et al., 2015).

Similar to NHX gene family, the overexpression of other halophytic genes such as SbpAPX, SbUSP, and SbGSTU showed better salinity tolerance (200–300 mM NaCl) in the transgenic plants compared to their glycophytic homologs (Jha et al., 2011; Singh et al., 2014a,b; Udawat et al., 2016). The transgenic Arabidopsis plants, overexpressing the TIP1 gene from the halophyte T. salsuginea exhibited better salt tolerance compared to the same gene from glycophyte Panax ginseng (Peng et al., 2007). Similarly, APX and GST from rice showed lower tolerance up to 150–200 mM compared to the same genes (200–300 mM NaCl) from halophyte S. brachiata in the transgenic plants (Lu et al., 2007; Jha et al., 2011; Sharma et al., 2014; Singh et al., 2014a). Recently, it was reported that over-expression of a stress-associated protein gene (AlSAP) from A. littoralis improves different abiotic stress tolerance in tobacco, wheat, and rice (Ben-Saad et al., 2015). They also demonstrated that AlSAP transcripts are induced by multiple abiotic stresses, but the ortholog gene of rice OsSAP9 is preferentially induced by cold and heat treatments.

A comparative transcript expression analysis revealed a higher expression of antiporter SOS1 gene in Thellungiella species compared to Arabidopsis (Oh et al., 2010). Similarly, several genes such as SOS2, NHX1, and HKT1 involved in Na+ excretion, compartmentation, and diffusion were also expressed at higher levels in Thellungiella compared to Arabidopsis (Taji et al., 2010). To compare the Na+ hypersensitivity response, Arabidopsis lines overexpressing either AtHKT1 (A. thaliana) or TsHKT1 (T. salsuginea) were analyzed and delayed root growth was observed in AtHKT1 compared with those expressing TsHKT1 (Ali et al., 2012). The shoot sensitivity was observed in transgenic lines expressing AtHKT1. They also demonstrated a strong salt-dependent up-regulation of TsHKT1 but a strong repression of AtHKT1 expression under salt stress (Ali et al., 2012).

Based on different reports, it may be concluded that halophytic genes are one of the promising candidates to be explored further for producing transgenic plants with a higher level of salt tolerance as compared to glycophytic counterpart genes. Further, halophytes also serve as valuable resources to discover novel abiotic stress responsive genes for improving stress tolerance of crop plants for sustainable agriculture in the saline affected areas.

Perspective and conclusion

Halophytes are more tolerant to abiotic stress because of high differential regulation of the same basic set of stress-responsive genes present among all plants. Furthermore, halophytes exhibited higher expression of a large number of stress-inducible genes under the non-stress condition, suggesting constitutive expression of genes in halophytes. Since different halophytes use different mechanisms to respond the salt stress, a single species cannot be considered as a model species. However, the emergence of a halophyte species as a model plant for the molecular elucidation of corresponding abiotic stress tolerance will enlighten our understanding of the salinity tolerance mechanisms. Identification and isolation of novel salt responsive genes and promoters from different halophytes can be explored for the genetic engineering of crop plants for abiotic stress tolerance using transgenic approach.

Author contributions

AM: Conceived the idea, collected literature and wrote the paper. BT: Helped in revisions. All authors approved this mini-review for the publication.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

CSIR-CSMCRI Communication No.: PRIS-001/2017. CSIR-Young Scientist (YSP-02/2016-17) and SERB-DST (EMR/2016/000538) projects are thankfully acknowledged. Junior and Senior Research Fellowship to BT is also duly acknowledged. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

References

  1. Ali Z., Park H. C., Ali A., Oh D. H., Aman R., Kropornicka A., et al. (2012). TsHKT1; 2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K+ specificity in the presence of NaCl. Plant Physiol. 158, 1463–1474. 10.1104/pp.111.193110 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amtmann A. (2009). Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol. Plant 2, 3–12. 10.1093/mp/ssn094 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Anjum N. A., Gill S. S., Ahmad I., Tuteja N., Soni P., Pareek A., et al. (2012). Understanding stress-responsive mechanisms in plants: an overview of transcriptomics and proteomics approaches, in Improving Crop Resistance to Abiotic Stress, Vols. 1, 2, eds Tuteja N., Gill S. S., Tiburcio A. F., Tuteja R. (Weinheim: Wiley-VCH Verlag GmbH and Co. KGaA; ), 337–355. [Google Scholar]
  4. Aslam R., Bostan N., Maria M., Safdar W. (2011). A critical review on halophytes: salt tolerant plants. J. Med. Plants Res. 5, 7108–7118. 10.5897/JMPRX11.009 [DOI] [Google Scholar]
  5. Baisakh N., RamanaRao M. V., Rajasekaran K., Subudhi P., Janda J., Galbraith D., et al. (2012). Enhanced salt stress tolerance of rice plants expressing a vacuolar H+-ATPase subunit c1 (SaVHAc1) gene from the halophyte grass Spartina alterniflora Löisel. Plant Biotechnol. J. 10, 453–464. 10.1111/j.1467-7652.2012.00678.x [DOI] [PubMed] [Google Scholar]
  6. Ball M. C. (1988). Ecophysiology of mangroves. Trees Struct. Funct. 2, 129–142. 10.1007/BF00196018 [DOI] [Google Scholar]
  7. Bartels D., Dinakar C. (2013). Balancing salinity stress responses in halophytes and non-halophytes: a comparison between Thellungiella and Arabidopsis thaliana. Funct. Plant Biol. 40, 819–831. 10.1071/fp12299 [DOI] [PubMed] [Google Scholar]
  8. Ben-Saad R., Meynard D., Ben-Romdhane W., Mieulet D., Verdeil J. L., Al-Doss A., et al. (2015). The promoter of the AlSAP gene from the halophyte grass Aeluropus littoralis directs a stress-inducible expression pattern in transgenic rice plants. Plant Cell Rep. 34, 1791–1806. 10.1007/s00299-015-1825-6 [DOI] [PubMed] [Google Scholar]
  9. Braun-Blanquet J. (1932). Plant sociology: the Study of Plant Communities. Transl. by G. D. Fuller and H. S. Conard. New York; NY: McGraw-Hill Book Co. [Google Scholar]
  10. Chaturvedi A. K., Mishra A., Tiwari V., Jha B. (2012). Cloning and transcript analysis of type 2 metallothionein gene (SbMT-2) from extreme halophyte Salicornia brachiata and its heterologous expression in E. coli. Gene 499, 280–287. 10.1016/j.gene.2012.03.001 [DOI] [PubMed] [Google Scholar]
  11. Chaturvedi A. K., Patel M. K., Mishra A., Tiwari V., Jha B. (2014). The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco. PLoS ONE 9:e111379. 10.1371/journal.pone.0111379 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Colmer T. D., Flowers T. J. (2008). Flooding tolerance in halophytes. New Phytol. 179, 964–974. 10.1111/j.1469-8137.2008.02483.x [DOI] [PubMed] [Google Scholar]
  13. Cushman J. C. (2001). Osmoregulation in plants: implications for agriculture. Am. Zool. 41, 758–769. 10.1668/0003-1569(2001)041[0758:OIPIFA]2.0.CO;2 [DOI] [Google Scholar]
  14. Cushman J. C., Bohnert H. J. (2000). Genomic approaches to plant stress tolerance. Curr. Opin. Plant Biol. 3, 117–124. 10.1016/S1369-5266(99)00052-7 [DOI] [PubMed] [Google Scholar]
  15. Das A. B., Strasser R. J. (2013). Salinity-induced genes and molecular basis of salt-tolerant strategies in Mangroves, in Molecular Stress Physiology of Plants, eds Rout G. R., Das A. B. (Springer; ), 53–86. [Google Scholar]
  16. FAO (2008). Land and Plant Nutrition Management Service. Rome: FAO. [Google Scholar]
  17. FAO (2016). Food and Agriculture: Key to Achieving the 2030, Agenda for Sustainable Development. Job No. I5499, Food and Agriculture Organization of the United Nations, Rome, 23. Available online at: http://www.fao.org/3/a-i5499e.pdf
  18. Flowers T. J. (1985). Physiology of halophytes. Plant Soil 89, 41–56. 10.1007/BF02182232 [DOI] [Google Scholar]
  19. Flowers T. J., Colmer T. D. (2008). Salinity tolerance in halophytes. New Phytol. 179, 945–963. 10.1111/j.1469-8137.2008.02531.x [DOI] [PubMed] [Google Scholar]
  20. Flowers T. J., Colmer T. D. (2015). Plant salt tolerance: adaptations in halophytes. Ann. Bot. 115, 327–331. 10.1093/aob/mcu267 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Flowers T. J., Munns R., Colmer T. D. (2015). Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann. Bot. 115, 419–431. 10.1093/aob/mcu217 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gao F., Gao Q., Duan X., Yue G., Yang A., Zhang J. (2006). Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. J. Exp. Bot. 57, 3259–3270. 10.1093/jxb/erl090 [DOI] [PubMed] [Google Scholar]
  23. Garg R., Verma M., Agrawal S., Shankar R., Majee M., Jain M. (2014). Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata, provides novel insights into the salinity and submergence tolerance factors. DNA Res. 21, 69–84. 10.1093/dnares/dst042 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Grigore M. N., Ivanescu L., Toma C. (2014). Halophytes: An Integrative Anatomical Study. New York, NY: Springer. [Google Scholar]
  25. Grigore M.-N., Toma C. (2010). A proposal for a new halophytes classification, based on integrative anatomy observations. Oltenia Stud. Comun. Ştiinţele Nat. (Oltenia J. Stud. Nat. Sci.) 26, 45–50. Available online at: http://biozoojournals.ro/oscsn/cont/26_1/B08-Grigore.pdf [Google Scholar]
  26. Grigore M.-N., Toma C., Boşcaiu M. (2010). Dealing with halophytes: an old problem, the same continuous exciting challenge. An. Şt. Univ. Al. I. Cuza Iaşi 56, 21–32. Available online at: http://www.bio.uaic.ro/publicatii/anale_vegetala/issue/2010F1/03-2010F1.pdf [Google Scholar]
  27. Grigore M. N., Villanueva M., Boscaiu M., Vicente O. (2012). Do halophytes really require salts for their growth and development? An experimental approach. Not. Sci. Biol. 4, 23–29. 10.15835/nsb427606 [DOI] [Google Scholar]
  28. Guan B., Hu Y., Zeng Y., Wang Y., Zhang F. (2011). Molecular characterization and functional analysis of a vacuolar Na+/H+ antiporter gene (HcNHX1) from Halostachys caspica. Mol. Biol. Rep. 38, 1889–1899. 10.1007/s11033-010-0307-8 [DOI] [PubMed] [Google Scholar]
  29. Guo L., Yu Y., Xia X., Yin W. (2010). Identification and functional characterisation of the promoter of the calcium sensor gene CBL1 from the xerophyte Ammopiptanthus mongolicus. BMC Plant Biol. 10:18. 10.1186/1471-2229-10-18 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Guo S., Yin H., Zhang X., Zhao F., Li P., Chen S., et al. (2006). Molecular cloning and characterization of a vacuolar H+-pyrophos-phatase gene, SsVP, from the halophyte Suaeda salsa and its overexpression increases salt and drought tolerance of Arabidopsis. Plant Mol. Biol. 60, 41–50. 10.1007/s11103-005-2417-6 [DOI] [PubMed] [Google Scholar]
  31. Hamada A., Shono M., Xia T., Ohta M., Hayashi Y., Tanaka A., et al. (2001). Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol. Biol. 46, 35–42. 10.1023/A:1010603222673 [DOI] [PubMed] [Google Scholar]
  32. Han N., Lan W., He X., Shao Q., Wang B., Zhao X. (2012). Expression of a Suaeda salsa vacuolar H+/Ca2+ transporter gene in Arabidopsis contributes to physiological changes in salinity. Plant Mol. Biol. Rep. 30, 470–477. 10.1007/s11105-011-0353-y [DOI] [Google Scholar]
  33. Himabindu Y., Chakradhar T., Reddy M. C., Kanygin A., Redding K. E., Chandrasekhar T. (2016). Salt-tolerant genes from halophytes are potential key players of salt tolerance in glycophytes. Environ. Exp. Bot. 124, 39–63. 10.1016/j.envexpbot.2015.11.010 [DOI] [Google Scholar]
  34. Hu Y. X., Yang X., Li X. L., Yu X. D., Li Q. L. (2014). The SlASR gene cloned from the extreme halophyte Suaeda liaotungensis K. enhances abiotic stress tolerance in transgenic Arabidopsis thaliana. Gene 549, 243–251. 10.1016/j.gene.2014.07.071 [DOI] [PubMed] [Google Scholar]
  35. Hu Y. Z., Zeng Y. L., Guan B., Zhang F. C. (2012). Overexpression of a vacuolar H+-pyrophosphatase and a B subunit of H+-ATPase cloned from the halophyte Halostachys caspica improves salt tolerance in Arabidopsis thaliana. Plant Cell Tiss. Organ Cult. 108, 63–71. 10.1007/s11240-011-0013-9 [DOI] [Google Scholar]
  36. Jha B., Mishra A., Chaturvedi A. K. (2016). Engineering stress tolerance in peanut (Arachis hypogaea L.), in Genetically Modified Organisms (GMO) Foods: Production, Regulation and Public Health, eds Watson R., Preedy V. R. (Philadelphia, PA: Elsevier; ), 305–311. 10.1016/B978-0-12-802259-7.00027-0 [DOI] [Google Scholar]
  37. Jha B., Sharma A., Mishra A. (2011). Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol. Biol. Rep. 38, 4823–4832. 10.1007/s11033-010-0625-x [DOI] [PubMed] [Google Scholar]
  38. Jha B., Singh N. P., Mishra A. (2012). Proteome profiling of seed storage proteins reveals the nutritional potential of Salicornia brachiata Roxb., an extreme halophyte. J. Agric. Food Chem. 60, 4320–4326. 10.1021/jf203632v [DOI] [PubMed] [Google Scholar]
  39. Jia G. X., Zhu Z. Q., Chang F. Q., Li Y. X. (2002). Transformation of tomato with the BADH gene from Atriplex improves salt tolerance. Plant Cell Rep. 21, 141–146. 10.1007/s00299-002-0489-1 [DOI] [Google Scholar]
  40. Jing L. W., Chen S. H., Guo X. L., Zhang H., Zhao Y. X. (2006). Overexpression of a chloroplast-located peroxiredoxin Q gene, SsPrxQ, increases the salt and low-temperature tolerance of Arabidopsis. J. Integr. Plant Biol. 48, 1244–1249. 10.1111/j.1744-7909.2006.00357.x [DOI] [Google Scholar]
  41. Jithesh M. N., Prashanth S. R., Sivaprakash K. R., Parida A. K. (2006). Antioxidative response mechanisms in halophytes: their role in stress defence. J. Genet. 85, 237–254. 10.1007/bf02935340 [DOI] [PubMed] [Google Scholar]
  42. Joshi M., Jha A., Mishra A., Jha B. (2013). Developing transgenic Jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS ONE 8:e71136. 10.1371/journal.pone.0071136 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Joshi M., Mishra A., Jha B. (2011). Efficient genetic transformation of Jatropha curcas L. by microprojectile bombardment using embryo axes. Ind. Crops Prod. 33, 67–77. 10.1016/j.indcrop.2010.09.002 [DOI] [Google Scholar]
  44. Joshi M., Mishra A., Jha B. (2012). NaCl plays a key role for in vitro micropropagation of Salicornia brachiata, an extreme halophyte. Ind. Crops Prod. 35, 313–316. 10.1016/j.indcrop.2011.06.024 [DOI] [Google Scholar]
  45. Joshi R., Mangu V. R., Bedre R., Sanchez L., Pilcher W., Zandkarimi H., et al. (2015). Salt adaptation mechanisms of halophytes: improvement of salt tolerance in crop plants, in Elucidation of Abiotic Stress Signaling in Plants, ed Pandey G. K. (New York, NY: Springer; ), 243–279. [Google Scholar]
  46. Kavitha K., George S., Venkataraman G., Parida A. (2010). A salt-inducible chloroplastic monodehydroascorbate reductase from halophyte Avicennia marina confers salt stress tolerance on transgenic plants. Biochimie 92, 1321–1329. 10.1016/j.biochi.2010.06.009 [DOI] [PubMed] [Google Scholar]
  47. Khan M. S., Khan M. A., Ahmad D. (2016). Assessing utilization and environmental risks of important genes in plant abiotic stress tolerance. Front. Plant Sci. 7:792. 10.3389/fpls.2016.00792 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Kore-eda S., Cushman M. A., Akselrod I., Bufford D., Fredrickson M., Clark E., et al. (2004). Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum. Gene 341, 83–92. 10.1016/j.gene.2004.06.037 [DOI] [PubMed] [Google Scholar]
  49. Kronzucker H. J., Britto D. T. (2011). Sodium transport in plants: a critical review. New Phytol. 189, 54–81. 10.1111/j.1469-8137.2010.03540.x [DOI] [PubMed] [Google Scholar]
  50. Lan T., Duan Y., Wang B., Zhou Y., Wu W. (2011). Molecular cloning and functional characterization of a Na+/H+ antiporter gene from halophyte Spartina anglica. Turk. J. Agric. For. 35, 535–543. 10.3906/tar-1003-2 [DOI] [Google Scholar]
  51. Li K., Pang C. H., Ding F., Sui N., Feng Z. T., Wang B. S. (2012). Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis chloroplasts enhances salt tolerance of plants. S. Afr. J. Bot. 78, 235–245. 10.1016/j.sajb.2011.09.006 [DOI] [Google Scholar]
  52. Li Q., Yin H., Li D., Zhu H., Zhang Y., Zhu W. (2007). Isolation and characterization of CMO gene promoter from halophyte Suaeda liaotungensis K. J. Genet. Genomics 34, 355–361. 10.1016/S1673-8527(07)60038-1 [DOI] [PubMed] [Google Scholar]
  53. Li Q.-L., Gao X.-R., Yu X.-H., Wang X.-Z., An L.-J. (2003a). Molecular cloning and characterization of betaine aldehyde dehydrogenase gene from Suaeda liaotungensis and its use in improved tolerance to salinity in transgenic tobacco. Biotechnol. Lett. 25, 1431–1436. 10.1023/A:1025003628446 [DOI] [PubMed] [Google Scholar]
  54. Li Q.-L., Liu D.-W., Gao X.-R., Su Q., An L.-J. (2003b). Cloning of cDNA encoding choline monooxygenase from Suaeda liaotungensis and salt tolerance of transgenic tobacco. Acta Bot. Sin. 45, 242–247. Available online at: http://www.jipb.net/pubsoft/content/2/2318/X010047(PS2).pdf [Google Scholar]
  55. Li Q.-L., Xie J.-H., Ma X.-Q., Li D. (2016). Molecular cloning of Phosphoethanolamine N-methyltransferase (PEAMT) gene and its promoter from the halophyte Suaeda liaotungensis and their response to salt stress. Acta Physiol. Plant. 38, 39 10.1007/s11738-016-2063-4 [DOI] [Google Scholar]
  56. Li W., Wang D., Jin T., Chang Q., Yin D., Xu S., et al. (2011). The vacuolar Na+/H+ antiporter gene SsNHX1 from the halophyte Salsola soda confers salt tolerance in transgenic alfalfa (Medicago sativa L.). Plant Mol. Biol. Rep. 29, 278–290. 10.1007/s11105-010-0224-y [DOI] [Google Scholar]
  57. Liu L., Wang Y., Wang N., Dong Y. Y., Fan X. D., Liu X. M., et al. (2011). Cloning of a vacuolar H+-pyrophosphatase gene from the halophyte Suaeda corniculata whose heterologous overexpression improves salt, saline-alkali and drought tolerance in Arabidopsis. J. Integr. Plant Biol. 53, 731–742. 10.1111/j.1744-7909.2011.01066.x [DOI] [PubMed] [Google Scholar]
  58. Lokhande V. H., Suprasanna P. (2012). Prospects of halophytes in understanding and managing abiotic stress tolerance, in Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change, eds Ahmad P., Prasad M. N. V. (New York, NY: Springer; ), 29–56. [Google Scholar]
  59. Lovelock C. E., Ball M. C. (2002). Influence of salinity on photosynthesis of halophytes, in Salinity: Environment-Plants-Molecules, eds Läuchli A., Lüttge U. (Netherlands: Springer; ), 315–339. [Google Scholar]
  60. Lü S. Y., Jing Y. X., Shen S. H., Zhao H. Y., Ma L. Q., Zhou X. J., et al. (2005). Antiporter gene from Hordum brevisubulatum (Trin.) link and its overexpression in transgenic tobaccos. J. Integr. Plant Biol. 47, 343–349. 10.1111/j.1744-7909.2005.00027.x [DOI] [Google Scholar]
  61. Lu Z., Liu D., Liu S. (2007). Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep. 26, 1909–1917. 10.1007/s00299-007-0395-7 [DOI] [PubMed] [Google Scholar]
  62. Lv S., Zhang K., Gao Q., Lian L., Song Y., Zhang J. (2008). Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol. 49, 1150–1164. 10.1093/pcp/pcn090 [DOI] [PubMed] [Google Scholar]
  63. Megdiche W., Passaquet C., Zourrig W., Fodil Y. Z., Abdelly C. (2009). Molecular cloning and characterization of novel cystatin gene in leaves Cakile maritima halophyte. J. Plant Physiol. 166, 739–749. 10.1016/j.jplph.2008.09.012 [DOI] [PubMed] [Google Scholar]
  64. Mishra A., Joshi M., Jha B. (2013). Oligosaccharide mass profiling of nutritionally important Salicornia brachiata, an extreme halophyte. Carbohyd. Polym. 92, 1942–1945. 10.1016/j.carbpol.2012.11.055 [DOI] [PubMed] [Google Scholar]
  65. Mishra A., Patel M. K., Jha B. (2015). Non targeted metabolomics and scavenging activity of reactive oxygen species reveal the potential of Salicornia brachiata as a functional food. J. Funct. Foods 13, 21–31. 10.1016/j.jff.2014.12.027 [DOI] [Google Scholar]
  66. Muchate N. S., Nikalje G. C., Rajurkar N. S., Suprasanna P., Nikam T. D. (2016). Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot. Rev. 82, 371–406. 10.1007/s12229-016-9173-y [DOI] [Google Scholar]
  67. Oh D. H., Dassanayake M., Haas J. S., Kropornika A., Wright C., d'Urzo M. P., et al. (2010). Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. Plant Physiol. 154, 1040–1052. 10.1104/pp.110.163923 [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Oh D. H., Leidi E., Zhang Q., Hwang S. M., Li Y., Quintero F. J., et al. (2009). Loss of halophytism by interference with SOS1 expression. Plant Physiol. 151, 210–222. 10.1104/pp.109.137802 [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Ohta M., Hayashi Y., Nakashima A., Hamada A., Tanaka A., Nakamura T., et al. (2002). Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett. 532, 279–282. 10.1016/S0014-5793(02)03679-7 [DOI] [PubMed] [Google Scholar]
  70. Pandey S., Mishra A., Patel M. K., Jha B. (2013). An efficient method for Agrobacterium-mediated genetic transformation and plant regeneration in cumin (Cuminum cyminum L.). App. Biochem. Biotechnol. 171, 1–9. 10.1007/s12010-013-0349-1 [DOI] [PubMed] [Google Scholar]
  71. Pandey S., Patel M. K., Mishra A., Jha B. (2016). In planta transformed cumin (Cuminum cyminum L.) plants, overexpressing the SbNHX1 gene showed enhanced salt endurance. PLoS ONE 11:e0159349. 10.1371/journal.pone.0159349 [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Pang C. H., Li K., Wang B. (2011). Overexpression of SsCHLAPXs confers protection against oxidative stress induced by high light in transgenic Arabidopsis thaliana. Physiol. Plant. 143, 355–366. 10.1111/j.1399-3054.2011.01515.x [DOI] [PubMed] [Google Scholar]
  73. Patel M. K., Joshi M., Mishra A., Jha B. (2015). Ectopic expression of SbNHX1 gene in transgenic castor (Ricinus communis L.) enhances salt stress by modulating physiological process. Plant Cell Tiss. Organ Cult. 122, 477–490. 10.1007/s11240-015-0785-4 [DOI] [Google Scholar]
  74. Patel M. K., Mishra A., Jha B. (2016). Untargeted metabolomics of halophytes, in Marine Omics: Principles and Applications, ed Kim S. (Boca Raton, FL: CRC Press; ), 309–325. 10.1201/9781315372303-18 [DOI] [Google Scholar]
  75. Peng Y., Lin W., Cai W., Arora R. (2007). Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226, 729–740. 10.1007/s00425-007-0520-4 [DOI] [PubMed] [Google Scholar]
  76. Polunin N. (1960). Introduction to Plant Geography. New York, NY: McGraw-Hill Book Company, Inc. [Google Scholar]
  77. Rai V., Tuteja N., Takabe T. (2012). Transporters and abiotic stress tolerance in plants, in Improving Crop Resistance to Abiotic Stress, Vols. 1, 2, eds Tuteja N., Gill S. S., Tiburcio A. F., Tuteja R. (Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA; ), 507–522. [Google Scholar]
  78. Rajalakshmi S., Parida A. (2012). Halophytes as a source of genes for abiotic stress tolerance. Plant Biochem. Biot. 21, 63–67. 10.1007/s13562-012-0146-x [DOI] [Google Scholar]
  79. Rajendran K., Tester M., Roy S. J. (2009). Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ. 32, 237–249. 10.1111/j.1365-3040.2008.01916.x [DOI] [PubMed] [Google Scholar]
  80. Rigó G., Valkai I., Faragó D., Kiss E., Van Houdt S., Van de Steene N., et al. (2016). Gene mining in halophytes: functional identification of stress tolerance genes in Lepidium crassifolium. Plant Cell Environ. 39, 2074–2084. 10.1111/pce.12768 [DOI] [PubMed] [Google Scholar]
  81. Rozema J. (1995). Biology of halophytes, in Halophytes and Biosaline Agriculture, eds Choukr-AllAh R., Malcolm C. V., Hamdy A. (New York, NY: Marcel Dekker Inc; ), 17–30. [Google Scholar]
  82. Rozema J., Muscolo A., Flowers T. (2013). Sustainable cultivation and exploitation of halophyte crops in a salinising world. Environ. Exp. Bot. 92, 1–3. 10.1016/j.envexpbot.2013.02.001 [DOI] [Google Scholar]
  83. Rozema J., Schat H. (2013). Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ. Exp. Bot. 92, 83–95. 10.1016/j.envexpbot.2012.08.004 [DOI] [Google Scholar]
  84. Rozema J., Van Diggelen J. (1991). A comparative study of growth and photosynthesis of four halophytes in response to salinity. Acta Oecol. 12, 673–681. [Google Scholar]
  85. Saad R. B., Romdhan W. B., Zouari N., Azaza J., Mieulet D., Verdeil J. L., et al. (2011). Promoter of the AlSAP gene from the halophyte grass Aeluropus littoralis directs developmental-regulated, stress-inducible, and organ-specific gene expression in transgenic tobacco. Transgenic Res. 20, 1003–1018. 10.1007/s11248-010-9474-6 [DOI] [PubMed] [Google Scholar]
  86. Sahu B. B., Shaw B. P. (2009). Isolation, identification and expression analysis of salt-induced genes in Suaeda maritima, a natural halophyte, using PCR-based suppression subtractive hybridization. BMC Plant Biol. 9:69. 10.1186/1471-2229-9-69 [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Sanders D. (2000). The salty tale of Arabidopsis. Curr. Biol. 10, R486–R488. 10.1016/S0960-9822(00)00554-6 [DOI] [PubMed] [Google Scholar]
  88. Schaeffer H. J., Forsthoefel N. R., Cushman J. C. (1995). Identification of enhancer and silencer regions involved in salt-responsive expression of crassulacean acid metabolism (CAM) genes in the facultative halophyte Mesembryanthemum crystallinum. Plant Mol. Biol. 28, 205–218. 10.1007/BF00020241 [DOI] [PubMed] [Google Scholar]
  89. Shabala S. (2013). Learning from halophytes: Physiological basis and strategies to improve abiotic stress tolerance in crops. Ann. Bot. 112, 1209–1221. 10.1093/aob/mct205 [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Shabala S., Bose J., Hedrich R. (2014). Salt bladders: do they matter? Trends. Plant Sci. 19, 687–691. 10.1016/j.tplants.2014.09.001 [DOI] [PubMed] [Google Scholar]
  91. Sharma R., Sahoo A., Devendran R., Jain M. (2014). Over-expression of a rice tau class glutathione s-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PloS ONE 9:e92900. 10.1371/journal.pone.0092900 [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Sharma R., Wungrampha S., Singh V., Pareek A., Sharma M. K. (2016). Halophytes as bioenergy crops. Front. Plant Sci. 7:1372. 10.3389/fpls.2016.01372 [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Shen Y.-G., Zhang W.-K., Yan D.-Q., Du B.-X., Zhang J.-S., Chen S.-Y. (2002). Overexpression of proline transporter gene isolated from halophyte confers salt tolerance in Arabidopsis. Acta Bot. Sin. 44, 956–962. Available online at: http://www.jipb.net/pubsoft/content/2/2313/X010587(PS2).pdf [Google Scholar]
  94. Singh N., Mishra A., Jha B. (2014a). Over-expression of the peroxisomal ascorbate peroxidase (SbpAPX) gene cloned from halophyte Salicornia brachiata confers salt and drought stress tolerance in transgenic tobacco. Mar. Biotechnol. 16, 321–332. 10.1007/s10126-013-9548-6 [DOI] [PubMed] [Google Scholar]
  95. Singh N., Mishra A., Jha B. (2014b). Ectopic over-expression of peroxisomal ascorbate peroxidase (SbpAPX) gene confers salt stress tolerance in transgenic peanut (Arachis hypogaea). Gene 547, 119–125. 10.1016/j.gene.2014.06.037 [DOI] [PubMed] [Google Scholar]
  96. Singh N., Mishra A., Joshi M., Jha B. (2010). Microprojectile bombardment mediated genetic transformation of embryo axis and plant regeneration in cumin (Cuminum cyminum L.). Plant Cell Tiss. Organ Cult. 103, 1–6. 10.1007/s11240-010-9746-0 [DOI] [Google Scholar]
  97. Singh V. K., Mishra A., Haque I., Jha B. (2016). A novel transcription factor-like gene SbSDR1 acts as a molecular switch and confers salt and osmotic endurance to transgenic tobacco. Sci. Rep. 6:31686 10.1038/srep31686 [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Slama I., Abdelly C., Bouchereau A., Flowers T., Savoure A. (2015). Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann. Bot. 115, 433–447. 10.1093/aob/mcu239 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. Sreeshan A., Meera S. P., Augustine A. (2014). A review on transporters in salt tolerant mangroves. Trees 28, 957–960. 10.1007/s00468-014-1034-x [DOI] [Google Scholar]
  100. Sun Q., Gao F., Zhao L., Li K., Zhang J. (2010). Identification of a new 130 bp cis-acting element in the TsVP1 promoter involved in the salt stress response from Thellungiella halophila. BMC Plant Biol. 10:90. 10.1186/1471-2229-10-90 [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Tabuchi T., Kawaguchi Y., Azuma T., Nanmori T., Yasuda T. (2005). Similar regulation patterns of choline monooxygenase, phosphoethanolamine N-methyltransferase and S-adenosyl-L-methionine synthetase in leaves of the halophyte Atriplex nummularia L. Plant Cell Physiol. 46, 505–513. 10.1093/pcp/pci050 [DOI] [PubMed] [Google Scholar]
  102. Taji T., Komatsu K., Katori T., Kawasaki Y., Sakata Y., Tanaka S., et al. (2010). Comparative genomic analysis of 1047 completely sequenced cDNAs from an Arabidopsis-related model halophyte, Thellungiella halophila. BMC Plant Biol. 10:261. 10.1186/1471-2229-10-261 [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Taji T., Seki M., Satou M., Sakurai T., Kobayashi M., Ishiyama K., et al. (2004). Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol. 135, 1697–1709. 10.1104/pp.104.039909 [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Tiwari V., Chaturvedi A. K., Mishra A., Jha B. (2014). The transcriptional regulatory mechanism of the peroxisomal ascorbate peroxidase (pAPX) gene cloned from an extreme halophyte, Salicornia brachiata. Plant Cell Physiol. 55, 1774–1471. 10.1093/pcp/pct172 [DOI] [PubMed] [Google Scholar]
  105. Tiwari V., Chaturvedi A. K., Mishra A., Jha B. (2015a). Introgression of the SbASR−1 gene cloned from a halophyte Salicornia brachiata enhances salinity and drought endurance in transgenic groundnut (Arachis hypogaea) and acts as a transcription factor. PLoS ONE 10:e0135541 10.1371/journal.pone.0131567 [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Tiwari V., Chaturvedi A. K., Mishra A., Jha B. (2015b). An efficient method of Agrobacterium mediated genetic transformation and regeneration in local Indian cultivar of Groundnut (Arachis hypogaea) using grafting. App. Biochem. Biotechnol. 175, 436–453. 10.1007/s12010-014-1286-3 [DOI] [PubMed] [Google Scholar]
  107. Tiwari V., Patel M. K., Chaturvedi A. K., Mishra A., Jha B. (2016). Functional characterization of the tau class Glutathione-S-Transferases gene (SbGSTU) promoter of Salicornia brachiata under salinity and osmotic Stress. PLoS ONE 11:e0148494. 10.1371/journal.pone.0148494 [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Udawat P., Jha R. K., Mishra A., Jha B. (2017). Overexpression of a plasma membrane-localized SbSRP-like protein enhances salinity and osmotic stress tolerance in transgenic tobacco. Front. Plant Sci. 8:582. 10.3389/fpls.2017.00582 [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Udawat P., Jha R. K., Sinha D., Mishra A., Jha B. (2016). Overexpression of a cytosolic abiotic stress responsive universal stress protein (SbUSP) mitigates salt and osmotic stress in transgenic tobacco plants. Front. Plant Sci. 7:518. 10.3389/fpls.2016.00518 [DOI] [PMC free article] [PubMed] [Google Scholar]
  110. Udawat P., Mishra A., Jha B. (2014). Heterologous expression of an uncharacterized universal stress protein gene (SbUSP) from the extreme halophyte, Salicornia brachiata, which confers salt and osmotic tolerance to E. coli. Gene 536, 163–170. 10.1016/j.gene.2013.11.020 [DOI] [PubMed] [Google Scholar]
  111. Ventura Y., Eshel A., Pasternak D., Sagi M. (2015). The development of halophyte-based agriculture: past and present. Ann. Bot. 115, 529–540. 10.1093/aob/mcu173 [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Volkov V. (2015). Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front. Plant Sci. 6:873. 10.3389/fpls.2015.00873 [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Waisel Y. (1972). Biology of Halophytes (New York, NY: Academic press; ). [Google Scholar]
  114. Wang L. L., Chen A. P., Zhong N. Q., Liu N., Wu X. M., Wang F., et al. (2014). The Thellungiella salsuginea tonoplast aquaporin TsTIP1; 2 functions in protection against multiple abiotic stresses. Plant Cell Physiol. 55, 148–161. 10.1093/pcp/pct166 [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. Wang Y. C., Qu G. Z., Li H. Y., Wu Y. J., Wang C., Liu G. F., et al. (2010). Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol. Biol. Rep. 37, 1119–1124. 10.1007/s11033-009-9884-9 [DOI] [PubMed] [Google Scholar]
  116. Wang Z., Li P., Fredricksen M., Gong Z., Kim C. S., Zhang C., et al. (2004). Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Sci. 166, 609–616. 10.1016/j.plantsci.2003.10.030 [DOI] [Google Scholar]
  117. Wong C. E., Li Y., Labbe A., Guevara D., Nuin P., Whitty B., et al. (2006). Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol. 140, 1437–1450. 10.1104/pp.105.070508 [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Wu C. A., Yang G. D., Meng Q. W., Zheng C. C. (2004). The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant Cell Physiol. 45, 600–607. 10.1093/pcp/pch071 [DOI] [PubMed] [Google Scholar]
  119. Wu C., Gao X., Kong X., Zhao Y., Zhang H. (2009). Molecular cloning and functional analysis of a Na+/H+ antiporter gene ThNHX1 from a halophytic plant Thellungiella halophila. Plant Mol. Biol. Rep. 27, 1–12. 10.1007/s11105-008-0048-1 [DOI] [Google Scholar]
  120. Wu H. J., Zhang Z., Wang J. Y., Oh D. H., Dassanayake M., Liu B., et al. (2012). Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl. Acad. Sci. U.S.A. 109, 12219–12224. 10.1073/pnas.1209954109 [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Wu S., Su Q., An L. J. (2010). Isolation of choline monooxygenase (CMO) gene from Salicornia europaea and enhanced salt tolerance of transgenic tobacco with CMO genes. Ind. J. Biochem. Biophys. 47, 298–305. [PubMed] [Google Scholar]
  122. Wu S., Su Q., An L., Ma S. (2011). A choline monooxygenase gene promoter from Salicornia europaea increases expression of the-glucuronidase gene under abiotic stresses in tobacco (Nicotiana tabacum L.). Indian J Biochem. Biophys. 48, 170–174. [PubMed] [Google Scholar]
  123. Wu W., Su Q., Xia X. Y., Wang Y., Luan Y. S., An L. J. (2008). The Suaeda liaotungensis kitag betaine aldehyde dehydrogenase gene improves salt tolerance of transgenic maize mediated with minimum linear length of DNA fragment. Euphytica 159, 17–25. 10.1007/s10681-007-9451-1 [DOI] [Google Scholar]
  124. Xu C., Tang X., Shao H., Wang H. (2016). Salinity tolerance mechanism of economic halophytes from physiological to molecular hierarchy for improving food quality. Curr. Genomics 17, 207–214. 10.2174/1389202917666160202215548 [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. Xue Z. Y., Zhi D. Y., Xue G. P., Zhang H., Zhao Y. X., Xia G. M. (2004). Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci. 167, 849–859. 10.1016/j.plantsci.2004.05.034 [DOI] [Google Scholar]
  126. Yang X., Hu Y. X., Li X. L., Yu X. D., Li Q. L. (2014). Molecular characterization and functional analysis of SlNAC2 in Suaeda liaotungensis K. Gene 543, 190–197. 10.1016/j.gene.2014.04.025 [DOI] [PubMed] [Google Scholar]
  127. Yao M., Zeng Y., Liu L., Huang Y., Zhao E., Zhang F. (2012). Overexpression of the halophyte Kalidium foliatum H+-pyrophosphatase gene confers salt and drought tolerance in Arabidopsis thaliana. Mol. Biol. Rep. 39, 7989–7996. 10.1007/s11033-012-1645-5 [DOI] [PubMed] [Google Scholar]
  128. Yin X.-Y., Yang A.-F., Zhang K.-W., Zhang J.-R. (2004). Production and analysis of transgenic maize with improved salt tolerance by the introduction of AtNHX1 gene. Acta Bot. Sin-Engl. 46, 854–861. Available online at: http://www.jipb.net/pubsoft/content/2/3522/x030020.pdf [Google Scholar]
  129. Yin X., Zhao Y., Luo D., Zhang H. (2002). Isolating the promoter of a stress-induced gene encoding betaine aldehyde dehydrogenase from the halophyte Atriplex centralasiatica Iljin. BBA Gene Struct. Expr. 1577, 452–456. 10.1016/S0167-4781(02)00495-5 [DOI] [PubMed] [Google Scholar]
  130. Zhang G. H., Su Q., An L. J., Wu S. (2008). Characterization and expression of a vacuolar Na+/H+ antiporter gene from the monocot halophyte Aeluropus littoralis. Plant Physiol. Biochem. 46, 117–126. 10.1016/j.plaphy.2007.10.022 [DOI] [PubMed] [Google Scholar]
  131. Zhang H. X., Hodson J. N., Williams J. P., Blumwald E. (2001). Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc. Natl. Acad. Sci. U.S.A. 98, 12832–12836. 10.1073/pnas.231476498 [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Zhang Y., Li Y., Lai J., Zhang H., Liu Y., Liang L., et al. (2012). Ectopic expression of a LEA protein gene TsLEA1 from Thellungiella salsuginea confers salt-tolerance in yeast and Arabidopsis. Mol. Biol. Rep. 39, 4627–4633. 10.1007/s11033-011-1254-8 [DOI] [PubMed] [Google Scholar]
  133. Zhao F. Y., Zhang X. J., Li P. H., Zhao Y. X., Zhang H. (2006). Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Mol. Breed. 17, 341–353. 10.1007/s11032-006-9005-6 [DOI] [Google Scholar]
  134. Zhao F., Zhang H. (2006). Salt and paraquat stress tolerance results from co-expression of the Suaeda salsa glutathione S-transferase and catalase in transgenic rice. Plant cell Tiss. Organ cult. 86, 349–358. 10.1007/s11240-006-9133-z [DOI] [Google Scholar]
  135. Zhu J. K. (2000). Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol. 124, 941–948. 10.1104/pp.124.3.941 [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Zhu J. K. (2001). Plant salt tolerance. Trends Plant Sci. 6, 66–71. 10.1016/S1360-1385(00)01838-0 [DOI] [PubMed] [Google Scholar]

Articles from Frontiers in Plant Science are provided here courtesy of Frontiers Media SA

RESOURCES