Mechanisms of salt tolerance in halophytes: current understanding and recent advances

Xiaoqian Meng 1 , Jun Zhou 1 ,  and Na Sui 1
  • 1 College of Life Science, Shandong Normal University, Shandong, Jinan, China
Xiaoqian Meng, Jun Zhou and Na Sui

Abstract

Halophytes are plants that exhibit high salt tolerance, allowing them to survive and thrive under extremely saline conditions. The study of halophytes advances our understanding about the important adaptations that are required for survival in high salinity conditions, including secretion of salt through the salt glands, regulation of cellular ion homeostasis and osmotic pressure, detoxification of reactive oxygen species, and alterations in membrane composition. To explore the mechanisms that contribute to tolerance to salt stress, salt-responsive genes have been isolated from halophytes and expressed in non-salt tolerant plants using targeted transgenic technologies. In this review, we discuss the mechanisms that underpin salt tolerance in different halophytes.

1 Introduction

Plants face many environmental abiotic stresses. These stresses induce a wide variety of survival and tolerance responses, including enhanced accumulation of osmolytes, reduced photosynthesis, closure of stomata, and induction of stress-responsive genes [1, 2, 3, 4, 5, 6, 7, 8]. Salinity represents a major abiotic stress that has been associated with significant economic impacts due to loss of arable land and reduced agricultural productivity. More than 950 million hectares of land are affected by elevated salt levels worldwide. Most plants are sensitive to salt stress, and salinity can inhibit plant growth by triggering ionic toxicity and osmotic and oxidative stress [9, 10, 11, 12, 13]. Reactive oxygen species (ROS) can also be produced in response to salt exposure, resulting in damage to DNA, proteins, and lipids [14]. In addition, salt stress can negatively affect chloroplast structure, leading to decreases in chlorophyll content and photosynthesis [15, 16].

Plants have developed complex defenses to resist salt stress that rely on a variety of mechanisms, such as osmolyte biosynthesis, alterations in ion homeostasis, intracellular compartmentalization of toxic ions, and ROS scavenging systems [17]. Induction of these pathways through brief exposure to low levels of salt stress, a process called salt acclimation, can improve a plants resistance to salinity [18, 19, 20]. However, tolerance to soil salinity levels varies between plant species, and plants can be characterized as halophytes or glycophytes. Halophytes are salt-resistant or salt-tolerant and can complete their life cycles in soil containing more than 200mM NaCl, while glycophytes cannot [17, 21, 22]. Generally, halophytes follow three mechanisms of salt tolerance; reduction of the Na+ influx, compartmentalization, and excretion of sodium ions [17]. Pseudo-halophytes intercept ions in roots and minimize transport to the shoot parts of the plant to protect the main metabolic tissues [23]. Euhalophytes can dilute salt within their succulent leaves or stems and thus have high salt tolerance [17]. Recretohalophytes can actively excrete absorbed salt to theoutside via a typical salt excretory structure in the epidermis [24].

Growth of some obligate halophytes requires high salt concentrations, so salinity may restrict the distributions of some halophyte populations to saline environments [25, 26, 27, 28]. Halophytes have developed distinct morphological, structural, and physiological strategies to survive in these high salt environments. To investigate the molecular mechanisms underlying tolerance to salt stress, salt-responsive genes have been isolated from certain halophytes and expressed in glycophytes to validate their function in salt tolerance [29, 30]. Halophytes represent promising models to characterize salt tolerance mechanisms. Suaeda salsa is a euhalophytic herb that occurs both on inland saline soils and in intertidal zones [31] . S. salsa has succulent leaves and is highly salt tolerant. Halophytes, such as Aeluropus, Mesembryanthemum, Suaeda, Atriplex, Thellungiella, Cakile, and Salicornia, serve as model plants for the identification of potential candidates for salt-responsive genes and promoters [32]. In this review, we will focus on recent advances in our understanding of salinity tolerance mechanisms used by halophytes to resist salt stress.

2 Salt secretion through specialized salt glands

A small group of halophytes have evolved specific salt excretory structures, termed salt glands, which can excrete excess salt from plant tissues to enhance salinity tolerance [33]. Halophytes with salt glands are collectively termed recretohalophytes. Salt glands have originated from the epidermis of these plant species, however the structure and mechanism of salt exclusion differs between recretohalophytic species. According to the structural similarities, salt glands can be categorized into 4 groups: salt bladders, multicellular salt glands, bicellular salt glands and unicellular vacuolated secretory hairs [34]. Salt bladders consisting of a large vacuolated cell with or without 1 or 2 stalk cells are only found in Aizoaceae and Amaranthaceae, in which salt is sequestered in the bladder cell vacuole upon salt stress [35]. A mutant M. crystallinum plant deficient in bladder cells was highly sensitive to salt under salt stress compared to the wild type M. crystallinum, which indicates the critical importance of salt bladders for salt compartmentalization and ion homeostasis [36]. Most salt glands consist of multiple cells (varying from 4-40 cells) which have cell types differentiated into basal collecting cells and distal secretory cells. The secretory cells have numerous plasmodesmata connections with surrounding mesophyll cells. Thus it appears that salt is actively transported through the collecting cells into the secretory cells [34]. The outer surface of the secretory cells is covered with cuticle. Research by Feng et al. [37] in Limonium bicolar showed that each of the secretory cells has a pore in the center of the cuticle and observed salt crystals located above the pores. In addition to secretion from the pore, extra salt also could be stored in the cuticular chamber on top of the secretory cells as observed in Aeluropus littoralis [38]. The bicellular salt gland with a basal cell and a cap cell is found in Chloridoid grasses. The continuous cuticle on the epidermis in some species thickens on top of the cap cell and forms a cuticular chamber that stores secreted salts [39]. The unicellular hairs are found in the wild rice species Porteresia coarctata, and appear to lack specific organelles and be completely filled with vacuoles [34].

Molecular genetic studies of salt glands have been limited in the past. However, new methods are increasing our ability to study the detailed function of salt glands at the cellular and molecular level. For instance, scanning electron microscopy has identified a potentially important feature of L. bicolor salt glands showing that salt glands in these plants emit fluorescence under UV excitation (330–380 nm) [33]. This autofluorescence arises from ferulic acid localized in the cuticle, which plays an crucial role in salt secretion [40]. Salt secretion is an energy-intensive process that is associated with high levels of water efflux. To recover from water loss, aquaporins play an critical role in re-uptake of water into cells [33, 41]. Inorganic elements extruded through the salt glands include a variety of cations and anions, but high selectivity for Na+ and Cl- compared to other ions has been observed [42]. Additionally, recent transcriptomic [24, 43, 44, 45], proteomic [46, 47], and metabolomic [48] analyses have reported many candidate genes, proteins and metabolites expressed specifically in salt glands; these candidate genes, proteins and metabolites may play key roles in salt gland development and salt secretion. For example, genes related to ion transport, vesicles, reactive oxygen species scavenging, the abscisic acid-dependent signaling pathway and transcription factors were found to be highly expressed under NaCl treatment in Limonium bicolor [43]. In salt bladders cells of M. crystallinum, active metabolic changes related to energy generation, UV protection, organic osmolyte accumulation and stress signaling have been identified to be regulated by a number of genes of unknown function in response to salt stress [46, 47, 48]. In addition, recretohalophyte L. bicolor mutants exhibiting altered salt secretion can be obtained by physical and chemical methods and used to identify potentially critical genes that contribute to salt secretion pathways [49, 50]. The functions of these genes can then be validated by combining established transformation protocols with the leaf disk secretion model [51].

3 Alterations in ion homeostasis and osmotic pressure contribute to salt tolerance

Intracellular compartmentalization of toxic ions using specific transporters represents another key pattern used by halophytes to maintain a moderate cytosolic K+/Na+ ratio in the cytosol. Thus, membrane ATPases and ion transporters play essential roles in salinity tolerance in some halophytes. Expression and activity of plasma membrane and vacuolar membrane H+-ATPases significantly increased in Suaeda salsa in response to NaCl treatment [52, 53]. ATPase activity is required to establish the proton gradient that maintains electrochemical and pH differences across the membrane. Membrane transporters can couple this electrochemical gradient to movement of substrates against their concentration gradients [54]. Thus, the activities of ion transporters or antiporters localized in the plasma membrane and vacuolar membrane are tightly regulated and essential for plant growth and development [55, 56]. Many such ion transporters, including the vacuolar Ca2+/H+ antiporter [57], the vacuolar H+/Ca2+ transporter [58], the K+ transporter [59], and others [32, 60] have been cloned and shown to reduce concentrations of Na+ and Cl- in the cytosol. Over expression of these transporters can improve salt tolerance by maintaining cytosolic ion homeostasis during salt stress [61, 62].

Under salt stress conditions the osmotic pressure is also severely compromised due to the influx of high concentrations of salt ions. Halophytes have evolved a defense mechanism involving accumulation of osmoprotectants, such as proline, glycine betaine, polyphenols, and soluble sugars, in the cytosol to reduce and balance the osmotic pressure. Overexpression of halophyte genes for enzymes involved in the synthesis of glycine betaine or raffinose, such as choline monooxygenase (CMO) [63], betaine aldehyde dehydrogenase (BADH) [64] and galactinol synthase (GOLS) [65], have been shown to enhance salt stress tolerance in glycophytic plants. Furthermore, expression of these genes is also induced in response to cold, drought, and heat, in addition to salinity, resulting in a concomitant increase in galactinol, raffinose, and a-ketoglutaric acid in transgenic plants [65].

4 Detoxification of ROS and alterations in membrane composition

ROS detoxification pathways play a protective role in the response to salt stress by scavenging toxic radicals generated from the electron transport chains of mitochondria and chloroplasts. Antioxidative defense systems include both non-enzymatic and enzymatic components. One such system is termed theascorbate-glutathione pathway and acts in chloroplasts. A series of enzymes belonging to this system, including monodehydroascorbate reductase (Am-MDAR) [66], glutathione transferases (SbGST, SsGST) [67, 68], ascorbate peroxidases (SssAPX and PtcAPX) [69, 70] and superoxide dismutases (TaSOD) [71], have been identified in several kinds of halophytes and have been shown to play important roles in protecting against salt-induced oxidative stress in higher plants. Overexpression of these genes leads to enhanced NaCl tolerance under salt stress. Overexpression of the SssAPX gene, that normally encodes the stromal APX in S. salsa, can increase the germination rate, cotyledon growth, survival rate, and salt tolerance of transgenic Arabidopsis [72].

In addition to enzymes that scavenge ROS directly certain other types of proteins/enzymes have also been shown to improve a plants antioxidative capacity. Metallothioneins (MTs) can bind to heavy metals and are involved in the homeostasis of essential metals (Cu and Zn), as well as cellular detoxification of nonessential metals (Cd and Hg). For example, cloning of the Salicornia brachiata metallothionein gene sbMT-2 and expression in tobacco resulted in significantly enhanced salt tolerance, a higher membrane stability index, and decreased levels of H2O2 and lipid peroxidation (MDA), implicating sbMT-2 in H2O2 detoxification. Furthermore, mechanistic analysis revealed elevated expression of key antioxidant enzymes, specifically SOD, POD, and APX, in sbMT-2-expressing transgenic plants, further confirming the role of the SbMT-2 gene and its protein product in ROS scavenging/detoxification [73]. In addition to metallothioneins, S-adenosylmethionine synthetase [74], glycosyltransferase [75], At Fes1A [76] and CCCH-type zinc finger protein have also been shown to participate in salt tolerance by limiting oxidative stress and, additionally, helping to maintain the ionic and osmotic balance [77].

Membrane structure and fluidity regulated by varying the composition and degree of fatty acid saturation of membrane lipids affects membrane permeability and contributes to plant resistance to environmental stressors [78, 79]. Comparative analysis of the membrane lipid and fatty acid composition in the halophyte Thellungiella halophila and the glycophyte Arabidopsis thaliana under high salinity conditions revealed higher levels of phosphatidylglycerol (PG) and unsaturated fatty acids, as well as a higher double-bond index for monogalactosyldiacylglycerols and PGs in T. halophila [80]. Consistent with these observations, transgenic Arabidopsis plants expressing the S. salsa gene that encodes glycerol-3-phosphate acyltransferase (GPAT), anacyl-esterifying enzyme required for PG synthesis expressed under high-salt conditions, exhibit tolerance to NaCl [81]. Additional studies have revealed that increased levels of unsaturated fatty acids in membrane lipids can protect photosystem II (PSII) and photosystem I (PSI) and enhance photosystem tolerance to salt stress [23, 82]. Furthermore, a nonspecific lipid transfer protein TsnsLTP4 has been shown to be involved in stress tolerance [83].

5 Conclusion

Different types of halophytes have different strategies to cope with high ionic concentrations. For example, small molecules, such as nitric oxide (NO) and hydrogen sulfide (H2S), have been identified as endogenous gasotransmitters involved in alleviating salt or other kind of stress [84, 85, 86]. Genome-wide identification of microRNAs has also revealed putative roles for microRNAs in the salt stress response [87]. Based on results showing that genes cloned from halophytes promote stress tolerance when expressed in glycophytes, expression of these genes could be used to produce transgenic crops with higher levels of salt tolerance suitable for sustainable agriculture in saline-affected areas. Identification of additional salinity-responsive genes from these and other halophytes could help us to better understand salt-tolerance mechanisms and these advances may be applied to the development of hardier transgenic crops.

Conflict of interest: Authors state no conflict of interest.

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (31101034) and Natural Science Foundation of Shandong Province (ZR2016CM28).

References

  • [1]

    Pang C.H., Li K., Wang B.S., Overexpression of SsCHLAPXs confers protection against oxidative stress induced by high light in transgenic Arabidopsis thaliana, Physiol. Plantarum, 2011, 143, 355-366

  • [2]

    Landi S., Hausman J.F., Guerriero G., Esposito S., Poaceae vs. Abiotic Stress: Focus on Drought and Salt Stress, Recent Insights and Perspectives, Front. Plant Sci., 2017, 8, 1214

  • [3]

    Wang J.S., Zhang Q., Cui F., Hou L., Zhao S.Z., Xia H., et al., Genome-Wide Analysis of Gene Expression Provides New Insights into Cold Responses in Thellungiella salsuginea, Front. Plant Sci., 2017, 8, 713

  • [4]

    Wang P.F., Song H., Li C.S., Li P.C., Li A.Q., Guan H.S., et al., Genome-Wide Dissection of the Heat Shock Transcription Factor Family Genes in Arachis, Front. Plant Sci., 2017, 6, 106

  • [5]

    Zhang J.X., Wang C., Yang C.Y., Wang J.Y., Chen L., Bao X.M., et al., The role of arabidopsis AtFes1A in cytosolic Hsp70 stability and abiotic stress tolerance, Plant J., 2010, 62, 539-548

  • [6]

    Chen M., Zhang W.H., Lv Z.W., Zhang S.L., Hidema J., Shi F.M., et al., Abscisic acid is involved in the response of Arabidopsis mutant sad2-1 to ultraviolet-B radiation by enhancing antioxidant enzymes, S. Afr. J. Bot., 2013, 85, 79-86

  • [7]

    Zhao S.S., Jiang Y.X., Zhao Y., Huang S.J., Yuan M., Zhao Y.X., et al., CASEIN KINASE1-LIKE PROTEIN2 Regulates Actin Filament Stability and Stomatal Closure via Phosphorylation of Actin Depolymerizing Factor, Plant Cell., 2016, 28, 1422-1439

  • [8]

    Wang F.R., Zhang C.Y., Liu G.D., Chen Y., Zhang J.X., Qiao Q.H., et al., Phenotypic variation analysis and QTL mapping for cotton (Gossypium hirsutum L.) fiber quality grown in different cotton-producing regions, Euphytica, 2016, 211, 169-183

  • [9]

    Guo Y.H., Jia W.J., Song J., Wang D.A., Chen M., Wang B.S., Thellungilla halophila is more adaptive to salinity than Arabidopsis thaliana at stages of seed germination and seedling establishment, Acta. Physiol. Plant, 2012, 34, 1287-1294

  • [10]

    Munns R., Tester M., Mechanism of salinity tolerance, Annu. Rev. Plant Biol., 2008, 59, 651-681

  • [11]

    Zhao K.F., Song J., Fan H., Zhou S., Zhao M., Growth response to ionic and osmotic stress of NaCl in salt-tolerant and salt-sensitive maize, J. Integ. Plant Biol., 2010, 52, 468-475

  • [12]

    Guo J.R., Suo S.S., Wang B.S., Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa, Seed Sci. Res., 2015, 25, 335-344

  • [13]

    Zhang S.R., Song J., Wang H., Feng G., Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia, J. Plant Ecol., 2010, 3, 259-267

  • [14]

    Gill S.S., Tuteja N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 2010, 48, 909-930

  • [15]

    Ma Q., Yue L.J., Zhang J.L., Wu G.Q., Bao A.K., Wang S.M., sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum, Tree Physiol., 2012, 32, 4-13

  • [16]

    Feng Z.T., Deng Y.Q., Fan H., Sun Q.J., Sui N., Wang B.S., Effects of NaCl stress on the growth and photosynthetic characteristics of Ulmus pumila L. seedlings in sand culture, Photosynthetica, 2014, 52, 313-320

  • [17]

    Flowers T.J., Colmer T.D., Salinity tolerance in halophytes, New Phytol., 2008, 179, 945-963

  • [18]

    Shen X.Y., Wang Z.L., Song X.F., Xu J.J., Jiang C.Y., Zhao Y.X., et al., Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis, Plant Mol.Biol., 2014, 86, 303-317

  • [19]

    Song J., Shi W.W., Liu R.R., Xu Y.G., Sui N., Zhou J.C., et al., The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity, Plant Spec. Biol., 2017, 32, 107-114

  • [20]

    Song J., Zhou J.C., Zhao W.W., Xu H.L., Wang F.X., Xu Y.G., et al., Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa, Plant Spec. Biol., 2016, 31, 19-28

  • [21]

    Santos J., Al-Azzawi M., Aronson J., Flowers T.J., eHALOPH a Database of Salt-Tolerant Plants: Helping put Halophytes to Work., Plant Cell Physiol., 2016, 57, e10

  • [22]

    Zhang T., Song J., Fan J.L., Feng G., Effects of salinewaterlogging and dryness/moist alternations on seed germination of halophyte and xerophyte, Plant Spec. Biol., 2015, 30, 231-236

  • [23]

    Sui N., Li M., Li K., Song J., Wang B.S., Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity, Photosynthetica, 2010, 48, 623-629

  • [24]

    Yuan F., Lyu M.J.A., Leng B.Y., Zheng G.Y., Feng Z.T., Li P.H., et al., Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation, Plant Cell Environ., 2015, 38, 1637-1657

  • [25]

    Song J., Shi G.W., Gao B., Fan H., Wang B.S., Waterlogging and salinity effects on two Suaeda salsa populations, Physiol. Plantarum, 2011, 141, 343-351

  • [26]

    Li X., Liu Y., Chen M., Song Y.P., Song J., Wang B.S., et al., Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations, Plant Biosyst., 2012, 146, 142-149

  • [27]

    Wang F.X., Xu Y.G., Wang S., Shi W.W., Liu R.R., Feng G., et al., Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa, Plant Physiol. Biochem., 2015, 95, 41-48

  • [28]

    Zhou J.C., Zhao W.W., Yin C.H., Song J., Wang B.S., Fan J.L., et al., The role of cotyledons in the establishment of Suaeda physophora seedlings, Plant Biosyst., 2014, 148, 584-590

  • [29]

    Hou L., Liu W., Li Z., Huang C., Fang X.L., Wang Q., et al., Identification and expression analysis of genes responsive to drought stress in peanut, Russ. J. Plant Physiol., 2014, 61, 842-852

  • [30]

    Zhao L., Ding Q., Zeng J., Wang F.R., Zhang J., Fan S.J., et al., An Improved CTAB-Ammonium Acetate Method for Total RNA Isolation from Cotton, Phytochem. Anal., 2012, 23, 647-650

  • [31]

    Song J., Wang B.S., Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model, Ann. Bot., 2015, 115, 541-553

  • [32]

    Mishra A., Tanna B., Halophytes: Potential Resources for Salt Stress Tolerance Genes and Promoters, Front. Plant Sci., 2017, 8, 829

  • [33]

    Yuan F., Leng B.Y., Wang B.S., Progress in Studying Salt Secretion from the Salt Glands in Recretohalophytes: How Do Plants Secrete Salt?, Front. Plant Sci., 2016, 7

  • [34]

    Dassanayake M., Larkin M.D., Making plants break a sweat: the structure, function, and evolution of plant salt glands., Front. Plant Sci., 2017, 8, 406

  • [35]

    Park J., Okita T.W., Edwards G.E., Salt tolerant mechanisms in single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae), Plant Sci., 2009, 176, 616-626

  • [36]

    Agarie S., Shimoda T., Shimizu Y., Baumann K., Sunagawa H., Kondo A., et al., Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum, J. Exp. Bot., 2007, 58, 1957-1967

  • [37]

    Feng Z.T., Sun Q.J., Deng Y.Q., Sun S.F., Zhang J.G., Wang B.S., Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor, Acta. Physiol. Plant, 2014, 36, 2729-2741

  • [38]

    Barhoumi Z., Djebali W., Abdelly C., Chaïbi W., Smaoui A., Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress, Protoplasma, 2008, 233, 195-202

  • [39]

    Amarasinghe V., Watson L., Comparative ultrastructure of microhairs in grasses, Bot. J. Linn. Soc., 1988, 98, 303-319

  • [40]

    Deng Y.Q., Feng Z.T., Yuan F., Guo J.R., Suo S.S., Wang B.S., Identification and functional analysis of the autofluorescent substance in Limonium bicolor salt glands, Plant Physiol. Biochem., 2015, 97, 20-27

  • [41]

    Tan W.K., Lin Q., Lim T.M., Kumar P., Loh C.S., Dynamic secretion changes in the salt glands of the mangrove tree species Avicennia officinalis in response to a changing saline environment., Plant Cell Environ., 2013, 36, 1410-1422

  • [42]

    Feng Z.T., Deng Y.Q., Zhang S.C., Liang X., Yuan F., Hao J.L., et al., K+ accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS, Plant Sci., 2015, 238, 286-296

  • [43]

    Yuan F., Lyu M.J.A., Leng B.Y., Zhu X.G., Wang B.S., The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland, Plant Mol. Biol., 2016, 91, 241-256

  • [44]

    Dang Z.H., Qi Q., Zhang H.R., Yu L.H., Wu S.B., Wang Y.C., Identification of salt-stress-induced genes from the RNA-Seq data of Reaumuria trigyna using differential-display reverse transcription PCR., Int. J. Genomics, 2014, 2014, 381501

  • [45]

    Yamamoto N., Takano T., Tanaka K., Ishige T., Terashima S., Endo C., et al., Comprehensive analysis of transcriptome response to salinity stress in the halophytic turf grass Sporobolus virginicus., Front. Plant Sci., 2015, 6, 241

  • [46]

    Barkla B.J., Vera-Estrella R., Pantoja O., Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum, Proteomics, 2012, 12, 2862-2865

  • [47]

    Barkla B.J., Vera-Estrella R., Raymond C., Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins, BMC. Plant Bio., 2016, 16, 110

  • [48]

    Barkla B.J., Vera-Estrella R., Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum, Fron.Plant Sci., 2015, 6, 435

  • [49]

    Yuan F., Chen M., Leng B.Y., Wang B.S., An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion, S. Afr. J. Bot., 2013, 88, 110-117

  • [50]

    Yuan F., Chen M., Yang J.C., Song J., Wang B.S., the optimal dosage of co-60 gamma irradiation for obtaining salt gland mutants of exo-recretohalophyte limonium bicolor (bunge) o. Kuntze, Pak. J. Bot., 2015, 47, 71-76

  • [51]

    Yuan F., Chen M., Yang J.C., Leng B.Y., Wang B.S., A system for the transformation and regeneration of the recretohalophyte Limonium bicolor, In Vitro Cell Dev-Pl., 2014, 50, 610-617

  • [52]

    Chen M., Song J., Wang B.S., NaCl increases the activity of the plasma membrane H+-ATPase in C-3 halophyte Suaeda salsa callus, Acta. Physiol. Plant, 2010, 32, 27-36

  • [53]

    Yang M.F., Song J., Wang B.S., Organ-Specific Responses of Vacuolar H+-ATPase in the Shoots and Roots of C-3 Halophyte Suaeda salsa to NaCl, J. Integr. Plant Biol., 2010, 52, 308-314

  • [54]

    Palmgren M.G., Plant plasma membrane H+-ATPase: powerhouses for nutrient uptake, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, 52, 817-861

  • [55]

    Ren X.L., Qi G.N., Feng H.Q., Zhao S., Zhao S.S., Wang Y., et al., Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis, Plant J., 2013, 74, 258-266

  • [56]

    Lu M., Zhang Y.Y., Tang S.K., Pan J.B., Yu Y.K., Han J., et al., AtCNGC2 is involved in jasmonic acid-induced calcium mobilization, J. Exp. Bot., 2016, 67, 809-819

  • [57]

    Han N., Shao Q., Bao H.Y., Wang B.S., Cloning and Characterization of a Ca2+/H+ Antiporter from Halophyte Suaeda salsa L, Plant Mol. Biol. Rep., 2011, 29, 449-457

  • [58]

    Han N., Lan W.J., He X., Shao Q., Wang B.S., Zhao X.J., Expression of a Suaeda salsa Vacuolar H+/Ca2+ Transporter Gene in Arabidopsis Contributes to Physiological Changes in Salinity, Plant Mol. Biol. Rep., 2012, 30, 470-477

  • [59]

    Shao Q., Han N., Ding T.L., Zhou F., Wang B.S., SsHKT1;1 is a potassium transporter of the C-3 halophyte Suaeda salsa that is involved in salt tolerance, Funct. Plant Biol., 2014, 41, 790-802

  • [60]

    Kong X.Q., Gao X.H., Sun W., An J., Zhao Y.X., Zhang H., Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1, Plant Mol.Biol., 2011, 75, 567-578

  • [61]

    Patel M.K., Joshi M., Mishra A., Jha B., Ectopic expression of SbNHX1 gene in transgenic castor (Ricinus communis L.) enhances salt stress by modulating physiological process, Plant Cell Tiss. Organ Cult., 2015, 122, 477-490

  • [62]

    Pandey S., Patel M.K., Mishra A., Jha B., In planta transformed cumin (Cuminum cyminum L.) plants, overexpressing the SbNHX1 gene showed enhanced salt endurance, PLoS ONE, 2016, 11, e0159349

  • [63]

    Wu S.B., Su Q., An L.J., Isolation of choline monooxygenase (CMO) gene from Salicornia europaea and enhanced salt tolerance of transgenic tobacco with CMO genes, Ind. J. Biochem. Biophys., 2010, 47, 298-305

  • [64]

    Li Q.L., Gao X.R., Yu X.H., Wang X.Z., An L.J., 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., 2003, 25, 1431-1436

  • [65]

    Sun Z.B., Qi X.Y., Wang Z.L., Li P.H., Wu C.X., Zhang H., et al., Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses, Plant Physiol. Biochem., 2013, 69, 82-89

  • [66]

    Kavitha K., George S., Venkataraman G., Parida A., A salt-inducible chloroplastic monodehydroascorbate reductase from halophyte Avicennia marina confers salt stress tolerance on transgenic plants, Biochimie, 2010, 92, 1321-1329

  • [67]

    Jha B., Sharma A., Mishra A., Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicorniabrachiata in tobacco for salt tolerance, Mol. Biol. Rep., 2011, 38, 4823-4832

  • [68]

    Qi Y.C., Liu W.Q., Qiu L.Y., Zhang S.M., Ma L., Zhang H., Overexpression of glutathione S-transferase gene increases salt tolerance of arabidopsis, Russ. J. Plant Physiol., 2010, 57, 233-240

  • [69]

    Li K., Pang C.H., Ding F., Sui N., Feng Z.T., Wang B.S., Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis chloroplasts enhances salt tolerance of plants, S. Afr. J. Bot., 2012, 78, 235-245

  • [70]

    Cao S., Du X.H., Li L.H., Liu Y.D., Zhang L., Pan X., et al., Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants, Russ. J. Plant Physiol., 2017, 64, 224-234

  • [71]

    Wang Y.C., Qu G.Z., Li H.Y., Wu Y.J., Wang C., Liu G.F., et al., Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii, Mol. Biol. Rep., 2010, 37, 1119-1124

  • [72]

    Li K., Pang C.H., Ding F., Sui N., Feng Z.T., Wang B.S., Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis, S. Afr. J. Bot., 2012, 78, 235-245

  • [73]

    Chaturvedi A.K., Patel M.K., Mishra A., Tiwari V., Jha B., The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco, PLoS ONE, 2014, 9, e111379

  • [74]

    Qi Y.C., Wang F.F., Zhang H., Liu W.Q., Overexpression of suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco, Acta. Physiol. Plant, 2010, 32, 263-269

  • [75]

    Zheng Y., Liao C.C., Zhao S.S., Wang C.W., Guo Y., The Glycosyltransferase QUA1 Regulates Chloroplast-Associated Calcium Signaling During Salt and Drought Stress in Arabidopsis, Plant Cell Physiol., 2017, 58, 329-341

  • [76]

    Fu C., Zhang J.X., Liu X.X., Yang W.W., Yu H.B., Liu J., AtFes1A is Essential for Highly Efficient Molecular Chaperone Function in Arabidopsis, J. Plant Biol., 2015, 58, 366-373

  • [77]

    Han G.L., Wang M.J., Yuan F., Sui N., Song J., Wang B.S., The CCCH zinc finger protein gene AtZFP1 improves salt resistance in Arabidopsis thaliana, Plant Mol.Biol., 2014, 86, 237-253

  • [78]

    Mikami K., Murata N., Membrane fluidity and the perception of environmental signals in cyanobacteria and plants, Prog. Lipid. Res., 2003, 42, 527-543

  • [79]

    Tang G.Y., Wei L.Q., Liu Z.J., Bi Y.P., Shan L., Ectopic expression of peanut acyl carrier protein in tobacco alters fatty acid composition in the leaf and resistance to cold stress, Biol. Plant, 2012, 56, 493-501

  • [80]

    Sui N., Han G.L., Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids, Acta. Physiol. Plant, 2014, 36, 983-992

  • [81]

    Sui N., Tian S.S., Wang W.Q., Wang M.J., Fan H., Overexpression of Glycerol-3-Phosphate Acyltransferase from Suaeda salsa Improves Salt Tolerance in Arabidopsis, Front. Plant Sci., 2017, 8

  • [82]

    Sun Y.L., Li F., Sui N., Sun X.L., Zhao S.J., Meng Q.W., The increase in unsaturation of fatty acids of phosphatidylglycerol in thylakoid membrane enhanced salt tolerance in tomato, Photosynthetica, 2010, 48, 400-408

  • [83]

    Sun W., Li Y., Zhao Y.X., Zhang H., The TsnsLTP4, a Nonspecific Lipid Transfer Protein Involved in Wax Deposition and Stress Tolerance, Plant Mol. Biol. Rep., 2015, 33, 962-974

  • [84]

    Deng Y.Q., Bao J., Yuan F., Liang X., Feng Z.T., Wang B.S., Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content, Plant Growth Regul., 2016, 79, 391-399

  • [85]

    Chen T.S., Yuan F., Song J., Wang B.S., Nitric oxide participates in waterlogging tolerance through enhanced adventitious root formation in the euhalophyte Suaeda salsa, Funct. Plant Biol., 2016, 43, 244-253

  • [86]

    Kong X.Q., Wang T., Li W.J., Tang W., Zhang D.M., Dong H.Z., Exogenous nitric oxide delays salt-induced leaf senescence in cotton (Gossypium hirsutum L.), Acta. Physiol. Plant, 2016, 38

  • [87]

    Zhang Q., Zhao C.Z., Li M., Sun W., Liu Y., Xia H., et al., Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response, BMC. Plant Biol., 2013, 13

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  • [1]

    Pang C.H., Li K., Wang B.S., Overexpression of SsCHLAPXs confers protection against oxidative stress induced by high light in transgenic Arabidopsis thaliana, Physiol. Plantarum, 2011, 143, 355-366

  • [2]

    Landi S., Hausman J.F., Guerriero G., Esposito S., Poaceae vs. Abiotic Stress: Focus on Drought and Salt Stress, Recent Insights and Perspectives, Front. Plant Sci., 2017, 8, 1214

  • [3]

    Wang J.S., Zhang Q., Cui F., Hou L., Zhao S.Z., Xia H., et al., Genome-Wide Analysis of Gene Expression Provides New Insights into Cold Responses in Thellungiella salsuginea, Front. Plant Sci., 2017, 8, 713

  • [4]

    Wang P.F., Song H., Li C.S., Li P.C., Li A.Q., Guan H.S., et al., Genome-Wide Dissection of the Heat Shock Transcription Factor Family Genes in Arachis, Front. Plant Sci., 2017, 6, 106

  • [5]

    Zhang J.X., Wang C., Yang C.Y., Wang J.Y., Chen L., Bao X.M., et al., The role of arabidopsis AtFes1A in cytosolic Hsp70 stability and abiotic stress tolerance, Plant J., 2010, 62, 539-548

  • [6]

    Chen M., Zhang W.H., Lv Z.W., Zhang S.L., Hidema J., Shi F.M., et al., Abscisic acid is involved in the response of Arabidopsis mutant sad2-1 to ultraviolet-B radiation by enhancing antioxidant enzymes, S. Afr. J. Bot., 2013, 85, 79-86

  • [7]

    Zhao S.S., Jiang Y.X., Zhao Y., Huang S.J., Yuan M., Zhao Y.X., et al., CASEIN KINASE1-LIKE PROTEIN2 Regulates Actin Filament Stability and Stomatal Closure via Phosphorylation of Actin Depolymerizing Factor, Plant Cell., 2016, 28, 1422-1439

  • [8]

    Wang F.R., Zhang C.Y., Liu G.D., Chen Y., Zhang J.X., Qiao Q.H., et al., Phenotypic variation analysis and QTL mapping for cotton (Gossypium hirsutum L.) fiber quality grown in different cotton-producing regions, Euphytica, 2016, 211, 169-183

  • [9]

    Guo Y.H., Jia W.J., Song J., Wang D.A., Chen M., Wang B.S., Thellungilla halophila is more adaptive to salinity than Arabidopsis thaliana at stages of seed germination and seedling establishment, Acta. Physiol. Plant, 2012, 34, 1287-1294

  • [10]

    Munns R., Tester M., Mechanism of salinity tolerance, Annu. Rev. Plant Biol., 2008, 59, 651-681

  • [11]

    Zhao K.F., Song J., Fan H., Zhou S., Zhao M., Growth response to ionic and osmotic stress of NaCl in salt-tolerant and salt-sensitive maize, J. Integ. Plant Biol., 2010, 52, 468-475

  • [12]

    Guo J.R., Suo S.S., Wang B.S., Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa, Seed Sci. Res., 2015, 25, 335-344

  • [13]

    Zhang S.R., Song J., Wang H., Feng G., Effect of salinity on seed germination, ion content and photosynthesis of cotyledons in halophytes or xerophyte growing in Central Asia, J. Plant Ecol., 2010, 3, 259-267

  • [14]

    Gill S.S., Tuteja N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants, Plant Physiol. Biochem., 2010, 48, 909-930

  • [15]

    Ma Q., Yue L.J., Zhang J.L., Wu G.Q., Bao A.K., Wang S.M., sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum, Tree Physiol., 2012, 32, 4-13

  • [16]

    Feng Z.T., Deng Y.Q., Fan H., Sun Q.J., Sui N., Wang B.S., Effects of NaCl stress on the growth and photosynthetic characteristics of Ulmus pumila L. seedlings in sand culture, Photosynthetica, 2014, 52, 313-320

  • [17]

    Flowers T.J., Colmer T.D., Salinity tolerance in halophytes, New Phytol., 2008, 179, 945-963

  • [18]

    Shen X.Y., Wang Z.L., Song X.F., Xu J.J., Jiang C.Y., Zhao Y.X., et al., Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis, Plant Mol.Biol., 2014, 86, 303-317

  • [19]

    Song J., Shi W.W., Liu R.R., Xu Y.G., Sui N., Zhou J.C., et al., The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity, Plant Spec. Biol., 2017, 32, 107-114

  • [20]

    Song J., Zhou J.C., Zhao W.W., Xu H.L., Wang F.X., Xu Y.G., et al., Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa, Plant Spec. Biol., 2016, 31, 19-28

  • [21]

    Santos J., Al-Azzawi M., Aronson J., Flowers T.J., eHALOPH a Database of Salt-Tolerant Plants: Helping put Halophytes to Work., Plant Cell Physiol., 2016, 57, e10

  • [22]

    Zhang T., Song J., Fan J.L., Feng G., Effects of salinewaterlogging and dryness/moist alternations on seed germination of halophyte and xerophyte, Plant Spec. Biol., 2015, 30, 231-236

  • [23]

    Sui N., Li M., Li K., Song J., Wang B.S., Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity, Photosynthetica, 2010, 48, 623-629

  • [24]

    Yuan F., Lyu M.J.A., Leng B.Y., Zheng G.Y., Feng Z.T., Li P.H., et al., Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation, Plant Cell Environ., 2015, 38, 1637-1657

  • [25]

    Song J., Shi G.W., Gao B., Fan H., Wang B.S., Waterlogging and salinity effects on two Suaeda salsa populations, Physiol. Plantarum, 2011, 141, 343-351

  • [26]

    Li X., Liu Y., Chen M., Song Y.P., Song J., Wang B.S., et al., Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations, Plant Biosyst., 2012, 146, 142-149

  • [27]

    Wang F.X., Xu Y.G., Wang S., Shi W.W., Liu R.R., Feng G., et al., Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa, Plant Physiol. Biochem., 2015, 95, 41-48

  • [28]

    Zhou J.C., Zhao W.W., Yin C.H., Song J., Wang B.S., Fan J.L., et al., The role of cotyledons in the establishment of Suaeda physophora seedlings, Plant Biosyst., 2014, 148, 584-590

  • [29]

    Hou L., Liu W., Li Z., Huang C., Fang X.L., Wang Q., et al., Identification and expression analysis of genes responsive to drought stress in peanut, Russ. J. Plant Physiol., 2014, 61, 842-852

  • [30]

    Zhao L., Ding Q., Zeng J., Wang F.R., Zhang J., Fan S.J., et al., An Improved CTAB-Ammonium Acetate Method for Total RNA Isolation from Cotton, Phytochem. Anal., 2012, 23, 647-650

  • [31]

    Song J., Wang B.S., Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model, Ann. Bot., 2015, 115, 541-553

  • [32]

    Mishra A., Tanna B., Halophytes: Potential Resources for Salt Stress Tolerance Genes and Promoters, Front. Plant Sci., 2017, 8, 829

  • [33]

    Yuan F., Leng B.Y., Wang B.S., Progress in Studying Salt Secretion from the Salt Glands in Recretohalophytes: How Do Plants Secrete Salt?, Front. Plant Sci., 2016, 7

  • [34]

    Dassanayake M., Larkin M.D., Making plants break a sweat: the structure, function, and evolution of plant salt glands., Front. Plant Sci., 2017, 8, 406

  • [35]

    Park J., Okita T.W., Edwards G.E., Salt tolerant mechanisms in single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae), Plant Sci., 2009, 176, 616-626

  • [36]

    Agarie S., Shimoda T., Shimizu Y., Baumann K., Sunagawa H., Kondo A., et al., Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum, J. Exp. Bot., 2007, 58, 1957-1967

  • [37]

    Feng Z.T., Sun Q.J., Deng Y.Q., Sun S.F., Zhang J.G., Wang B.S., Study on pathway and characteristics of ion secretion of salt glands of Limonium bicolor, Acta. Physiol. Plant, 2014, 36, 2729-2741

  • [38]

    Barhoumi Z., Djebali W., Abdelly C., Chaïbi W., Smaoui A., Ultrastructure of Aeluropus littoralis leaf salt glands under NaCl stress, Protoplasma, 2008, 233, 195-202

  • [39]

    Amarasinghe V., Watson L., Comparative ultrastructure of microhairs in grasses, Bot. J. Linn. Soc., 1988, 98, 303-319

  • [40]

    Deng Y.Q., Feng Z.T., Yuan F., Guo J.R., Suo S.S., Wang B.S., Identification and functional analysis of the autofluorescent substance in Limonium bicolor salt glands, Plant Physiol. Biochem., 2015, 97, 20-27

  • [41]

    Tan W.K., Lin Q., Lim T.M., Kumar P., Loh C.S., Dynamic secretion changes in the salt glands of the mangrove tree species Avicennia officinalis in response to a changing saline environment., Plant Cell Environ., 2013, 36, 1410-1422

  • [42]

    Feng Z.T., Deng Y.Q., Zhang S.C., Liang X., Yuan F., Hao J.L., et al., K+ accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS, Plant Sci., 2015, 238, 286-296

  • [43]

    Yuan F., Lyu M.J.A., Leng B.Y., Zhu X.G., Wang B.S., The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland, Plant Mol. Biol., 2016, 91, 241-256

  • [44]

    Dang Z.H., Qi Q., Zhang H.R., Yu L.H., Wu S.B., Wang Y.C., Identification of salt-stress-induced genes from the RNA-Seq data of Reaumuria trigyna using differential-display reverse transcription PCR., Int. J. Genomics, 2014, 2014, 381501

  • [45]

    Yamamoto N., Takano T., Tanaka K., Ishige T., Terashima S., Endo C., et al., Comprehensive analysis of transcriptome response to salinity stress in the halophytic turf grass Sporobolus virginicus., Front. Plant Sci., 2015, 6, 241

  • [46]

    Barkla B.J., Vera-Estrella R., Pantoja O., Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum, Proteomics, 2012, 12, 2862-2865

  • [47]

    Barkla B.J., Vera-Estrella R., Raymond C., Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins, BMC. Plant Bio., 2016, 16, 110

  • [48]

    Barkla B.J., Vera-Estrella R., Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum, Fron.Plant Sci., 2015, 6, 435

  • [49]

    Yuan F., Chen M., Leng B.Y., Wang B.S., An efficient autofluorescence method for screening Limonium bicolor mutants for abnormal salt gland density and salt secretion, S. Afr. J. Bot., 2013, 88, 110-117

  • [50]

    Yuan F., Chen M., Yang J.C., Song J., Wang B.S., the optimal dosage of co-60 gamma irradiation for obtaining salt gland mutants of exo-recretohalophyte limonium bicolor (bunge) o. Kuntze, Pak. J. Bot., 2015, 47, 71-76

  • [51]

    Yuan F., Chen M., Yang J.C., Leng B.Y., Wang B.S., A system for the transformation and regeneration of the recretohalophyte Limonium bicolor, In Vitro Cell Dev-Pl., 2014, 50, 610-617

  • [52]

    Chen M., Song J., Wang B.S., NaCl increases the activity of the plasma membrane H+-ATPase in C-3 halophyte Suaeda salsa callus, Acta. Physiol. Plant, 2010, 32, 27-36

  • [53]

    Yang M.F., Song J., Wang B.S., Organ-Specific Responses of Vacuolar H+-ATPase in the Shoots and Roots of C-3 Halophyte Suaeda salsa to NaCl, J. Integr. Plant Biol., 2010, 52, 308-314

  • [54]

    Palmgren M.G., Plant plasma membrane H+-ATPase: powerhouses for nutrient uptake, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, 52, 817-861

  • [55]

    Ren X.L., Qi G.N., Feng H.Q., Zhao S., Zhao S.S., Wang Y., et al., Calcineurin B-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis, Plant J., 2013, 74, 258-266

  • [56]

    Lu M., Zhang Y.Y., Tang S.K., Pan J.B., Yu Y.K., Han J., et al., AtCNGC2 is involved in jasmonic acid-induced calcium mobilization, J. Exp. Bot., 2016, 67, 809-819

  • [57]

    Han N., Shao Q., Bao H.Y., Wang B.S., Cloning and Characterization of a Ca2+/H+ Antiporter from Halophyte Suaeda salsa L, Plant Mol. Biol. Rep., 2011, 29, 449-457

  • [58]

    Han N., Lan W.J., He X., Shao Q., Wang B.S., Zhao X.J., Expression of a Suaeda salsa Vacuolar H+/Ca2+ Transporter Gene in Arabidopsis Contributes to Physiological Changes in Salinity, Plant Mol. Biol. Rep., 2012, 30, 470-477

  • [59]

    Shao Q., Han N., Ding T.L., Zhou F., Wang B.S., SsHKT1;1 is a potassium transporter of the C-3 halophyte Suaeda salsa that is involved in salt tolerance, Funct. Plant Biol., 2014, 41, 790-802

  • [60]

    Kong X.Q., Gao X.H., Sun W., An J., Zhao Y.X., Zhang H., Cloning and functional characterization of a cation-chloride cotransporter gene OsCCC1, Plant Mol.Biol., 2011, 75, 567-578

  • [61]

    Patel M.K., Joshi M., Mishra A., Jha B., Ectopic expression of SbNHX1 gene in transgenic castor (Ricinus communis L.) enhances salt stress by modulating physiological process, Plant Cell Tiss. Organ Cult., 2015, 122, 477-490

  • [62]

    Pandey S., Patel M.K., Mishra A., Jha B., In planta transformed cumin (Cuminum cyminum L.) plants, overexpressing the SbNHX1 gene showed enhanced salt endurance, PLoS ONE, 2016, 11, e0159349

  • [63]

    Wu S.B., Su Q., An L.J., Isolation of choline monooxygenase (CMO) gene from Salicornia europaea and enhanced salt tolerance of transgenic tobacco with CMO genes, Ind. J. Biochem. Biophys., 2010, 47, 298-305

  • [64]

    Li Q.L., Gao X.R., Yu X.H., Wang X.Z., An L.J., 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., 2003, 25, 1431-1436

  • [65]

    Sun Z.B., Qi X.Y., Wang Z.L., Li P.H., Wu C.X., Zhang H., et al., Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses, Plant Physiol. Biochem., 2013, 69, 82-89

  • [66]

    Kavitha K., George S., Venkataraman G., Parida A., A salt-inducible chloroplastic monodehydroascorbate reductase from halophyte Avicennia marina confers salt stress tolerance on transgenic plants, Biochimie, 2010, 92, 1321-1329

  • [67]

    Jha B., Sharma A., Mishra A., Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicorniabrachiata in tobacco for salt tolerance, Mol. Biol. Rep., 2011, 38, 4823-4832

  • [68]

    Qi Y.C., Liu W.Q., Qiu L.Y., Zhang S.M., Ma L., Zhang H., Overexpression of glutathione S-transferase gene increases salt tolerance of arabidopsis, Russ. J. Plant Physiol., 2010, 57, 233-240

  • [69]

    Li K., Pang C.H., Ding F., Sui N., Feng Z.T., Wang B.S., Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis chloroplasts enhances salt tolerance of plants, S. Afr. J. Bot., 2012, 78, 235-245

  • [70]

    Cao S., Du X.H., Li L.H., Liu Y.D., Zhang L., Pan X., et al., Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants, Russ. J. Plant Physiol., 2017, 64, 224-234

  • [71]

    Wang Y.C., Qu G.Z., Li H.Y., Wu Y.J., Wang C., Liu G.F., et al., Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii, Mol. Biol. Rep., 2010, 37, 1119-1124

  • [72]

    Li K., Pang C.H., Ding F., Sui N., Feng Z.T., Wang B.S., Overexpression of Suaeda salsa stroma ascorbate peroxidase in Arabidopsis, S. Afr. J. Bot., 2012, 78, 235-245

  • [73]

    Chaturvedi A.K., Patel M.K., Mishra A., Tiwari V., Jha B., The SbMT-2 gene from a halophyte confers abiotic stress tolerance and modulates ROS scavenging in transgenic tobacco, PLoS ONE, 2014, 9, e111379

  • [74]

    Qi Y.C., Wang F.F., Zhang H., Liu W.Q., Overexpression of suadea salsa S-adenosylmethionine synthetase gene promotes salt tolerance in transgenic tobacco, Acta. Physiol. Plant, 2010, 32, 263-269

  • [75]

    Zheng Y., Liao C.C., Zhao S.S., Wang C.W., Guo Y., The Glycosyltransferase QUA1 Regulates Chloroplast-Associated Calcium Signaling During Salt and Drought Stress in Arabidopsis, Plant Cell Physiol., 2017, 58, 329-341

  • [76]

    Fu C., Zhang J.X., Liu X.X., Yang W.W., Yu H.B., Liu J., AtFes1A is Essential for Highly Efficient Molecular Chaperone Function in Arabidopsis, J. Plant Biol., 2015, 58, 366-373

  • [77]

    Han G.L., Wang M.J., Yuan F., Sui N., Song J., Wang B.S., The CCCH zinc finger protein gene AtZFP1 improves salt resistance in Arabidopsis thaliana, Plant Mol.Biol., 2014, 86, 237-253

  • [78]

    Mikami K., Murata N., Membrane fluidity and the perception of environmental signals in cyanobacteria and plants, Prog. Lipid. Res., 2003, 42, 527-543

  • [79]

    Tang G.Y., Wei L.Q., Liu Z.J., Bi Y.P., Shan L., Ectopic expression of peanut acyl carrier protein in tobacco alters fatty acid composition in the leaf and resistance to cold stress, Biol. Plant, 2012, 56, 493-501

  • [80]

    Sui N., Han G.L., Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids, Acta. Physiol. Plant, 2014, 36, 983-992

  • [81]

    Sui N., Tian S.S., Wang W.Q., Wang M.J., Fan H., Overexpression of Glycerol-3-Phosphate Acyltransferase from Suaeda salsa Improves Salt Tolerance in Arabidopsis, Front. Plant Sci., 2017, 8

  • [82]

    Sun Y.L., Li F., Sui N., Sun X.L., Zhao S.J., Meng Q.W., The increase in unsaturation of fatty acids of phosphatidylglycerol in thylakoid membrane enhanced salt tolerance in tomato, Photosynthetica, 2010, 48, 400-408

  • [83]

    Sun W., Li Y., Zhao Y.X., Zhang H., The TsnsLTP4, a Nonspecific Lipid Transfer Protein Involved in Wax Deposition and Stress Tolerance, Plant Mol. Biol. Rep., 2015, 33, 962-974

  • [84]

    Deng Y.Q., Bao J., Yuan F., Liang X., Feng Z.T., Wang B.S., Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content, Plant Growth Regul., 2016, 79, 391-399

  • [85]

    Chen T.S., Yuan F., Song J., Wang B.S., Nitric oxide participates in waterlogging tolerance through enhanced adventitious root formation in the euhalophyte Suaeda salsa, Funct. Plant Biol., 2016, 43, 244-253

  • [86]

    Kong X.Q., Wang T., Li W.J., Tang W., Zhang D.M., Dong H.Z., Exogenous nitric oxide delays salt-induced leaf senescence in cotton (Gossypium hirsutum L.), Acta. Physiol. Plant, 2016, 38

  • [87]

    Zhang Q., Zhao C.Z., Li M., Sun W., Liu Y., Xia H., et al., Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response, BMC. Plant Biol., 2013, 13

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