http://informahealthcare.com/bty ISSN: 0738-8551 (print), 1549-7801 (electronic) Crit Rev Biotechnol, Early Online: 1–13 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/07388551.2014.889080

REVIEW ARTICLE

Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology Critical Reviews in Biotechnology Downloaded from informahealthcare.com by University Library Utrecht on 06/11/14 For personal use only.

Xiaoli Tang1,2, Xingmin Mu3,4, Hongbo Shao1,3,4,5, Hongyan Wang1,2, and Marian Brestic1,6 1

Key Laboratory of Coastal Biology & Bioresources Utilization, Yantai Institute of Coastal Zone Research (YIC), Chinese Academy of Sciences (CAS), Yantai, China, 2University of Chinese Academy of Sciences, Beijing, China, 3Institute of Soil and Water Conservation, Northwest A&F University, Yangling, China, 4Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling, China, 5 Institute for Life Sciences, Qingdao University of Science & Technology (QUST), Qingdao, China, and 6Department of Plant Physiology, Slovak Agricultural University, Nitra, Slovak Republic Abstract

Keywords

The increasing seriousness of salinization aggravates the food, population and environmental issues. Ameliorating the salt-resistance of plants especially the crops is the most effective measure to solve the worldwide problem. The salinity can cause damage to plants mainly from two aspects: hyperosmotic and hyperionic stresses leading to the restrain of growth and photosynthesis. To the adverse effects, the plants derive corresponding strategies including: ion regulation and compartmentalization, biosynthesis of compatible solutes, induction of antioxidant enzymes and plant hormones. With the development of molecular biology, our understanding of the molecular and physiology knowledge is becoming clearness. The complex signal transduction underlying the salt resistance is being illuminated brighter and clearer. The SOS pathway is the central of the cell signaling in salt stress. The accumulation of the compatible solutes and the activation of the antioxidant system are the effective measures for plants to enhance the salt resistance. How to make full use of our understanding to improve the output of crops is a huge challenge for us, yet the application of the genetic engineering makes this possible. In this review, we will discuss the influence of the salt stress and the response of the plants in detail expecting to provide a particular account for the plant resistance in molecular, physiological and transgenic fields.

Antioxidant system, eco-environment, genetic engineering, photosynthesis, salinization, SOS pathway

Introduction All over the world, soil salinity is becoming an increasing threaten to plant growth (Rengasamy, 2010; Zhu, 2001). According to FAO (2008), there are at least 800 million hectares land subjected to salinity in the world, accounting for as much as 6% of the world‘s total land area. Although some of the salt-affected influences are the result of the natural causes, the considerable rest is derived from the degraded cultivated agricultural land (Lee et al., 2004; Munns & Tester, 2008). At present, the world’s cultivated land affected by salinity has achieved 20% (Rhoades & Loveday, 1990). Currently, food is basically enough but there are approximately 800 million people undernourished (Conway, 1998). It was reported that food production is needed to increase to 150% to meet the over-growing population by 2050 (FAO, 2008; Rengasamy, 2006). On the one hand, the cultivated agricultural land is narrowed with the increasingly serious salinization, more and more food is demanded with the increase of the population on the other hand. To meet these

Address for correspondence: Xingmin Mu and Hongbo Shao. Tel: +86 029 87012411. Fax: +86 029 87012210. E-mail: [email protected] (XM MU); [email protected] (HB SHAO)

History Received 5 November 2013 Revised 28 December 2013 Accepted 13 January 2014 Published online 16 April 2014

challenges, to survive abiotic stress and to maximize performance under less favoring conditions crops seem to be the major topics for research (Brown, 2008; Abreu et al., 2013). Generally, the so-called saline soil is soil with a high concentration of soluble salts. The soils are regarded as saline on the basis of the soil solution ECs reaching 4 dS/m or more. The solution concentration is equivalent to 40 mM NaCl, generating an osmotic pressure at 0.2 MPa and reducing significantly the yields of most cereal crops (Munns & Tester, 2008). However, the deleterious effects vary according to several related factors including climatic conditions, plant species and soil regime. For instance, rice is the most sensitive species among the grain crops, while barley displays a pronounced resistance relatively (Aslam et al., 1993; Colmer et al., 2006). The salinity can threaten plants from two aspects: hyperosmotic stress and hyperionic stress. (Tu¨rkan & Demiral, 2009). Based on the capacity of plants to grow on highly saline environments, plants are classified into two types: glycophytes and halophytes (Flowers et al., 1977). Some of the halophytes have the ability to exclude salts from their roots and shoots, some are able to endure high concentrations of salt, and the others adopt measures such as ion compartmentation, synthesis of the compatible solute and osmotic adjustment (Flowers & Colmer, 2008). Yet with most

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plants, almost all the crops are glycophytes. Thus, two key measures (producing salt-tolerant lines/cultivars through conventional breeding or genetic engineering) to overcome this peril have been put forward for a long time (Ashraf & Akram, 2009). Growing halophytes and salt-tolerant crops on saline soil is regarded as the ‘‘biotic approach’’, which is similar to the idea of the ‘‘biosaline agriculture’’ (Ashraf & Wu, 1994; Kingsbury & Epstein, 1984). As we all know, other than animals, plants maintain a sessile lifestyle subjected to various environmental stresses (Sarwat et al., 2013). Modern-day plants are all the products of primal livings, and experienced eons of evolution with abiotic and biotic changes. Thus, they have acquired various adaptive mechanisms to optimize growth and development under stresses (Xue et al., 2010). Sodium chloride is the most common and widespread salt in soil, so the evolved mechanisms of plants are all to regulate its accumulation and distribution (Munns, 2005). For glycophytes, high concentration salts can produce ionic stress, osmotic stress and secondary stresses (Zhu, 2002). In order to guarantee survival under such a detrimental circumstance, plants have evolved a series of biochemical and molecular processes to acclimatize themselves to the environment (Dufty et al., 2002; Glombitza et al., 2004; Jaleel et al., 2009; Yan et al., 2013). The specific biochemical strategy contains: (1) ion regulation and compartmentalization, (2) induced biosynthesis of compatible solutes, (3) induction of antioxidant enzymes, (4) induction of plant hormones and (5) changes in photosynthetic pathway (Parida & Das, 2005). The molecular mechanism includes: (1) the SOS pathway for ion homeostasis, (2) the protein kinase pathway for stress signaling, (3) the phytohormone signaling pathway under high salt stress (Zhu, 2002) and (4) the associated genes encoding salt-stress proteins, such as genes for photosynthetic enzymes, synthesis of compatible solutes, vacuolar-sequestering enzymes and for radicalscavenging enzymes (Winicov, 1998). In recent years, tremendous advances have achieved in salt stress studies. Plant breeders have fostered some salt-tolerant lines of crops by conventional breeding, moreover a transgenic approach is employed to improve the crop salt tolerance and a number of transgenic lines have been testified to be effective under control conditions (Ashraf & Akram, 2009). Metabolomics is becoming a tool to understand the cellular mechanism to abiotic stress and acts as a viable option for the biotechnological improvement of halophytes (Ruan & Teixeira da Silva, 2011). Small non-coding RNAs mainly coming down to microRNAs and siRNAs (short interfering RNAs) can regulate gene expression by silencing of the genes (Carrington & Ambros, 2003). MiR393 has been discovered to be strongly up-regulated by drought, high-salinity treatments (Dharmasiri et al., 2005; Kepinski & Leyser, 2005). In the nearest, the ribosomal RNA methylation was discovered to respond to abiotic stress (Baldridge & Contreras, 2013). In addition, the mitogen-activated protein kinase (MAPK) signaling pathways, which are involved in stress responses, are the highly conserved and important regulating system in plants (Colcombet & Hirt, 2008; Sinha et al., 2011). Reviews on salinity responses arose three decades ago, and new reports appeared continuous (Flowers et al., 1977; Munns & Tester, 2008; Parida & Das, 2005; Tu¨rkan & Demiral,

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2009; Zhu, 2001, 2003). The molecular, cellular and holistic mechanisms of plant salt tolerance were discussed in detail (Munns & Tester, 2008). Flowers & Colmer (2008) chose to stand at the point of uptake and transport of ions to review the concrete mechanisms of salt-tolerance. Tu¨rkan & Demiral (2009) described how the plants manage to control ion homeostasis by sensing, transduction and responding salt stress signaling. Thanks to the rapid development of life science, our understanding of the salinity tolerance in both physiological and molecular fields has experienced a qualitative leap. In this review, we will focus on the molecular, cellular and physiological mechanisms of the salt-tolerance in detail especially the latest findings in this sphere.

Growth and photosynthesis Environmental stresses can trigger various plant responses from gene expression, metabolism all the way to growth rate and productivity (Shao et al., 2009). Salinity which is the common and comprehensive negative influence can lead to apparent stunting of plant growth (Gorai et al., 2011; Tarchoune et al., 2011). From another point of view, slower growth is an available measure for plant survival under stress (Zhu, 2001). That is to say, the adverse environments affect plants and plants take the necessary measures to fit it. Actually, all the physiological performances are the adaptive strategies for plants under salt stress. Research on Arabidopsis revealed a link between stress and cell division illustrating the mechanisms at the molecular level (Wang et al., 1998). ICK1 (cyclin-dependent-protein-kinase inhibitor), which is induced by ABA, can reduce the activities of cyclin-dependent protein kinase to restrain cell division and ABA is a central plant hormone under abiotic stress, involved in cellular signaling, regulation of plant growth and stomatal conductance (Davies et al., 2005; Zhu, 2003). Yet, studies in barley displayed that ABA concentration increased transiently under salt stress and returned to normal after 24 h with the leaf growth rate reduced (Fricke et al., 2004). Recent research shows that it is DELLA protein which is a common negative factor in plant growth and a key component in GA signal transduction that integrate signals from hormones and abiotic stress to plant growth (Achard et al., 2006). The accumulated Na+ within plants also can produce ionic toxicity. With a few exceptions, the glycophytes in a large proportion of crops cannot tolerate Na+ concentrations at 50 mM or higher (Munns & Tester, 2008). The excess salt can inhibit enzyme activity and lead to the death of leaves (Munns, 2005). Salt may also build up in the chloroplast exerting a toxic effect on photosynthetic processes and photosynthetic components directly (Munns & Tester, 2008). The MPK6 has been demonstrated to play an important role in sodium detoxification through phosphorylating the Na+/H+ antiporters and inducing the efflux of sodium (Davies et al., 2005). Biomass is only a broad and morphological parameter, while photosynthesis is one of the most direct and conclusive elements in deciding plant growth and crop yields. Photosynthetic rate would decrease if any part of its process was affected (Yan et al., 2013). For instance, the stresses can reduce stomatal and mesophyll conductance

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DOI: 10.3109/07388551.2014.889080

and decreased CO2 availability lowering photosynthesis in end (Davies et al., 2005). The CO2 can be destroyed by salt stress directly, for example, the Rubisco activity that is the key enzyme in photosynthesis (Brugnoli & Bjo¨rkman, 1992; Tarchoune et al., 2011; Yang et al., 2008). Gas exchange and chlorophyll fluorescence are used to monitor the photosynthesis to reflect the disadvantage influences (Jedmowski et al., 2013). In order to resist the disadvantageous impact, some plants choose to change the photosynthetic pathway in order to cope with it (Parida & Das, 2005). The M. crystallinum adopted to transform C3 pathway to CAM to reduce water loss (Cushman et al., 1989). The halophytic plant Atriplex lentiformis is able to shift from C3 to C4 to respond to the salt stress (Meinzer & Zhu, 1999). Some transgenic C3 plants displayed higher photosynthetic efficiency and improved growth characteristics (Ruan et al., 2012). Moreover, salt stress can also weaken photosynthesis indirectly by reducing chlorophyll and total carotenoid content. It was reported that the content of total chlorophyll and carotene was decreased by NaCl stress in leaves of the tomato and B. parviflora (Khavari-Nejad & Mostofi, 1998; Parida et al., 2002). All in all, salinity is accompanied by a significant reduction in photosynthesis.

Osmotic stress effects and tolerance As is mentioned earlier, there are two aspects of salt tolerance: osmotic stress and ionic stress. Osmotic stress is not only confined to drought, but it is also the result of salinity. The abundant amount of ions in the saline soil lower the flow of water causing difficulties for water uptake or even loss of intracellular water (Yan et al., 2013). On this occasion, the resistant measure of plants is to accumulate many metabolites which are usually called ‘‘compatible solutes’’ to increase the osmotic tolerance (Tu¨rkan & Demiral, 2009). The compatible solutes include sugars (fructose, sucrose and glucose), complex sugars (trehalose, raffinose and fructans), quaternary amino acid derivatives, tertiary amines, sulfonium compounds and so on (Munns & Tester, 2008). They can not only counteract the ions but also balance the osmotic potential of Na+ and Cl being sequestered into the vacuole. Among the compatible solutes, proline (Pro) and glycine betaine (GB) are the most common and efficient. Several decades ago, Flowers et al. (1977) has reported that the Pro or GB is able to accumulate at a high concentration as much as 0.1 MPa in osmotic pressure. With research, their vital functions in salt-stress are increasingly in-depth and becoming clearer. Pro is able to act as a molecular chaperone to stabilize the protein conformation, buffer cytosolic pH and balance cell redox condition (Maggio et al., 2002). Under stresses, the accumulation of the Pro is due to increased biosynthesis and decreased degradation. In leaves of two rice cultivars with different salinity tolerance, the accumulative rate of proline is quicker in the tolerant line (Demiral & Tu¨rkan, 2004). Research on sorghum also illustrated that the proline concentration is at a higher level subjected to salt stress (Yan et al., 2012). Now, it is known that there are two pathways and three enzymes involved in the synthesis of Pro (Verbruggen & Hermans, 2008). For the three synthetic

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enzymes (P5CS, P5CR and OAT), P5CS is the rate-limiting enzyme and is adjusted by feed-back and transcriptional regulation (Savoure´ et al., 1995; Zhang et al., 1995). In Arabidopsis, the signaling pathway for the induction of P5CS1 expression during salt stress depends on phospholipase C (PLC) and ABA responsive (ABRE) element (Abraha´m et al., 2003; Parre et al., 2007). The development of molecular mechanisms of Pro metabolism is accompanied by the progress of the transgenic engineering. The first transgenic plant with accumulated Pro was acquired in 1995 (Kavi et al., 1995). In Arabidopsis, overexpression of P5CS antisense or the insertional mutant of this gene can reduce the salt tolerance of the transgenic plants (Nanjo et al., 1999; Sze´kely et al., 2008). Meanwhile, we may reduce the degradation of the Pro to maintain its concentration, so the key enzyme PDH during degradation is also manipulated. However, in PDH antisense lines, higher stress tolerance emerged at times but not always (Mani et al., 2002; Nanjo et al., 1999). Glycine betaine is synthesized and accumulated under a variety of abiotic stress and acts as an osmolyte to protect PSII during salinity (Jagendorf & Takabe, 2001). It can also protect the integrity of membrane and the activity of enzymes against osmotic stress (Ma¨kela¨ et al., 2000). Generally, high concentration salt is able to increase GB concentration in many crop plants, such as sugar beet, spinach, barley, wheat and sorghum (Fallon & Phillips, 1989; Weimberg et al., 1984; Yang et al., 2003). In view of its powerful features, transgenic engineering was also employed to operate the GB concentration. Transgenic Arabidopsis expressing the N-methyltransferase gene, which is one of the three key enzymes in GB synthesis, possess improved seed yield compared to the control under salt stress (Waditee et al., 2005). Similarly, overexpression of GOLS2, a GB synthase, enhanced tolerance to high salinity in Arabidopsis (Sun et al., 2013). In fact, there are many more other compatible solutes. For example, in Arabidopsis, overexpression of mannose6-phosphate reductase was reported to increase growth and photosynthesis in saline treatment (Sickler et al., 2007). Some plants, which are able to bear Na+ at high level such as barley, tend to adapt and maintain turgor in the face of high soil salinities by Na+ directly. In addition, there are a part of plants adopted to accumulate carbohydrates such as sugars and starch to cope with salt stress (Parida et al., 2002). In conclusion, to tolerate salt stress successfully, plants have to accumulate high concentrations of compatible solutes to maintain low water potential in cells.

Ion toxicity and ion homeostasis Duo to their similarity in physicochemical properties, Na+ competes with K+ to bind to the active site of the enzymes causing the inactivation or degeneration of the enzymes and the disorder of protein synthesis and ribosome functions (Munns & Tester, 2008). The toxic position of Na+ is mainly in leaf blade, since Na+ in the transpiration stream is deposited here not in the roots (Munns, 2002). Slabu et al. (2009) indicated that the functions of chloroplast were disturbed when K+ was replaced by Na+, resulting in

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uncontrolled water losses. Although Cl is a necessary micronutrient for cells in regulating enzyme activity, maintaining membrane protein and pH gradients, it is toxic to cells at high levels (White & Broadley, 2001; Xu et al., 1999). Accumulated Na+ in shoots is associated with a decline in stomatal conductance, while high concentrations of Cl can damage chlorophyll and inhibit PS II (Tavakkoli et al., 2011). More seriously, the toxic effects of Na+ and Cl have a cumulative effect. Hence, balancing intracellular ion concentrations by maintaining high K+ and low Na+ concentration in the cytosol are the foremost for plants (Yan et al., 2013). Fortunately, during the lengthy evolution, most plants have acquired capabilities to regulate ion accumulation and to uptake ions selectively. Plants can exclude the toxic excess Na+ ions from cytosol (Janicka-Russak et al., 2013) and almost all the plants are able to take up water and exclude Na+ and Cl from soil effectively (Munns, 2005). Some plants, especially halophytes, have succulent leaves and stems in order to dilute the concentration of the toxic ions and others evolve salt glands or bladders to secret excess ions (Yan et al., 2013). Studies with wheat and wild soybean, with better salttolerance, demonstrated that the Na+ concentration in shoots is kept lower through withholding it in the roots (Islam et al., 2007; Luo et al., 2005). That is to say, to exclude Na+ from the cytoplasm and to accumulate Na+ in the vacuoles are the most important steps to maintain ion homeostasis in cells (Silva & Gero´s, 2009). Either exclusion by roots or compartmentalization into the vacuoles, the transport of ions is mediated by H+-ATPase, ion channels and co-transporters in plants. The plasma membrane Na+/H+ antiporter SOS1 and the tonoplast membrane antiporters NHXs are the most important transporters in salt stress and are investigated extensively and thoroughly (Zhu, 2003). Salinity exposure triggers complicated signaling events, so how the stresses are sensed and transported by salt-stress signaling provides us with a clue to understand the regulation mechanism of plants. The SOS signaling pathway is elucidated at the earliest and it consists of three key components: SOS3, SOS2 and SOS1. SOS3 is a Ca2+ sensor (Liu & Zhu, 1998). SOS2 is a serine/threonine protein kinase (Liu et al., 2000). The SOS3 can sense the perturbation of Ca2+ levels in cytoplast caused by salt stress and then bind to the SOS2. This SOS3/SOS2 complex phosphorylates and activates SOS1, hence the activated SOS1 has the ability to export excess ions and contribute to Na+ ion homeostasis (Liu & Zhu, 1998; Liu et al., 2000; Quintero et al., 2002). SOS1 was discovered to be the downstream target of MPK6 by GST-pull-down assay (Sme´kalova´ et al., 2013). Moreover, during salt stress the phosphorylation degree of SOS1 increases (Davies et al., 2005). Many other researches attested that the components of the signaling pathway may be regulated by salt stress directly or have a hand in other signaling pathways of the stress in order to affect responses indirectly (Mahajan & Tuteja, 2005; Qiu et al., 2002; Shabala et al., 2005). The NHXs are the vacuolar Na+/H+ antiporters. In a review published recently, NHXs were demonstrated to play roles in cell expansion, cell volume regulation, ion homeostasis, osmotic adjustment, pH regulation, protein processing and so on (Rengasamy, 2010). In genetic engineering, the

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hypersensitive phenotype of sos1 demonstrated the key position of the SOS signaling pathway during salt-stress. Compared to control leaves, the H+-ATPase in tonoplast vesicles increased 2-fold in salt-treated leaves (Qiu et al., 2007). Overexpression of NHX may reduce the cytosolic Na+ concentration and improve salt tolerance by efficient sequestration (Apse et al., 1999). Its overexpression confers salt tolerance to a wide range of plants (Yang et al., 2009). In Table 1, transgenic plants with different ion transporters with enhanced ion homeostasis are listed. In addition, the HKT family also plays vital functions in maintaining ion homeostasis. The HKT proteins act as Na+/K+ symporters and Na+-selective transporters, involved in balancing of Na+ and K+. Most recently, the AtHKT1 was demonstrated to take charge of the resorption of Na+ from xylem to reduce the amount of Na+ reaching shoots in Arabidopsis (Davenport et al., 2007). In durum wheat, TmHKT1 is correlated with Na+ exclusion and a high K+/ Na+ rate in the leaves (Huang et al., 2006). In rice, OsHKT1 appears to have the same function as AtHKT1 (Horie et al., 2007), yet much more work is required to clarify the multiple functions of the gene family. Recently, maintaining an intracellular high cytosolic K+/Na+ ratio is accepted as the key determinant of salinity tolerance (Munns & Tester, 2008). K+ possesses a significant important role in activating enzymes, regulating osmotic pressure, regulating stoma movement and balancing turgor (Che´rel, 2004). In wheat cells, the content of K+ and Na+ are kept at 150 and 30 mM, respectively, so the K+/Na+ ratio is 5 (Carden et al., 2003). Indeed, increasingly reports show that it should be the cytosolic K+/Na+ ratio that determines the plant salt tolerance. Neid & Biesboer (2005) put forward that the low level of KNO3 could alleviate NaCl-induced stress. Zheng et al. (2008) further acclaimed that the NaCl stress symptoms can be alleviated by simultaneously applied KNO3 and the optimal K+/Na+ ratio should be 100:16 for both the salt-tolerant and the salt-sensitive cultivar. Similarly, overexpression of LeENH1 (a tomato enhancer of SOS3-1) in tobacco enhanced salinity tolerance by excluding Na+ from cytosol and retained high K+ levels in the cytosol (Li et al., 2013). Studies on NHXs also attest to this point. Recently, mineral analysis of the transgenic plants with over expressed NHXs seems to indicate that the salt resistance is offered by a high K+/Na+ ratio through K+ retention rather than Na+ exclusion (Hueras et al., 2013). In Arabidopsis, the phenotype of sos mutants may be alleviated by an exogenous supply of K+ (Zhu, 2003). Compared to Arabidopsis, the Thellungiella possess stronger adapt ability to saline soil. One of the reasons is that the cytosolic K+ concentration in Thellungiella is higher. Leidi et al. (2010) testified that the transgenic tomato with high resistance depended on cytosolic K+ homeostasis rather than on vacuolar Na+ accumulation.

Oxidative stress and antioxidant defense responses Besides osmotic stress and ion toxicity, salinity can also induce the generation of ROS and lead to oxidative stress. ROS derive from the excitation of O2 including singlet oxygen (1O2), superoxide anion (O 2 ), hydrogen peroxide (H2O2) and hydroxyl radical (OH), respectively (Yan et al.,

A. thaliana

Alfalfa Aeluropus littoralis A. thaliana A. thaliana Salsola soda

Vacuolar Na+/H+ antiporter MsNHX1

Vacuolar Na+/H+ antiporter AlNHXI

Vacuolar H+ pyrophosphatase AVP1

Vacuolar Na+/H+ antiporter AtNHX1

Vacuolar Na+/H+ antiporter SsNHX1

A. thaliana Ammopiptanthus mongolicus Yeast

Vacuolar Na+/H+ antiporter AtNHX1

Vacuolar Na+/H+ antiporter NHX1

Thellungiella halophila Thellungiella halophila A. thaliana A. thaliana A. thaliana Yeast

H+-pyrophosphatase (PPase) gene TsVP

H+-pyrophosphatase (PPase) gene TsVP

H+-pyrophosphatase (PPase) gene AVP1

H+-pyrophosphatase (PPase) gene AVP1

Plasma membrane Na+/H+ antiporter SOS1

Plasma membrane Na+/H+ antiporter sodium2 (SOD2)

Plasma membrane Na+/H+ antiporter sodium2 (SOD2)

Malus

Vacuolar Na /H antiporter MdNHX1

+

Rice

Vacuolar Na+/H+ antiporter OsNHX1

+

Pennisetum glaucum

Vacuolar Na /H antiporter PgNHX1

+

Vacuolar Na+/H+ antiporter AtNHX1

+

A. thaliana

Vacuolar Na+/H+ antiporter AtNHX1

Donor A. thaliana

+

Vacuolar Na /H antiporter AtNHX1

+

Gene symbol

Table 1. Improving plant salt tolerance by bioengineering ion homeostasis.

A. thaliana

A. thaliana

Cotton

Alfalfa

Cotton

Tobacco

Rice

A. thaliana

Groundnut

Apple

Alfalfa

Kiwifruit

Alfalfa

Tobacco

A. thaliana

Perennial ryegrass

Rice

Tall fescue

Tall fescue

Wheat

Acceptor +

Gene function Na /H antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ + + Na /H antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ + + Na /H antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ + + Na /H antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ Na+/H+ antiporters in tonoplast, exchange Na+ or Li+ for H+ + + Na /H antiporters in plasma membrane, exchange Na+ or Li+ for H+ Pumping H+ from the cytoplasm into vacuoles to form the pH gradient Pumping H+ from the cytoplasm into vacuoles to form the pH gradient Pumping H+ from the cytoplasm into vacuoles to form the pH gradient Pumping H+ from the cytoplasm into vacuoles to form the pH gradient Na+/H+ antiporters in plasma membrane, exchange Na+ or Li+ for H+ Na+/H+ antiporters in plasma membrane, exchange Na+ or Li+ for H+

+

Accumulating less Na+ in the xylem transpirational stream and in the shoot Accumulating less Na+ and more K+ in the symplast

More vigorous growth in the presence of 200 mM NaCl

Accumulating more Na+, K+ Ca2+, Cl2 and soluble sugars in their root and leaf tissues Accumulating more Na+, K+ and Ca2+ in leaves and roots

Greater dry weight at 300 mM NaCl

Enhanced net photosynthetic rate, higher K+, lower Na+

Growth in high concentrations of NaCl over 50 days A relatively high K+/Na+ ratio in the leaves Resistant to high concentration of salt Lower Na+ content in leaves

A relative high K+/Na+ ratio in the leaves and roots Increased content of Na+, K+ and Ca2+ in leaves and roots Improved salt tolerance

Elevated concentration of Na+, K+ and proline Increased osmotic adjustment

Advanced root system

Biomass production, grain output and leaf K+ accumulation Activity of vacuolar Na+/H+ antiporter Better growth at 200 mM NaCl

Elevated character

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Global plant-responding mechanisms to salt stress (continued )

Gao et al. (2003)

Shi et al. (2003)

Pasapula et al. (2011)

Bao et al. (2008)

Lv et al. (2009)

Gao et al. (2006)

Zhao et al. (2006)

Wei et al. (2011)

Asif et al. (2011)

Li et al. (2010)

Li et al. (2010)

Tian et al. (2011)

Bao et al. (2009)

Zhang et al. (2008)

Bao-Yan et al. (2008)

Wu et al. (2005)

Verma et al. (2007)

Tian et al. (2006)

Zhao et al. (2007)

Xue et al. (2004)

Reference

DOI: 10.3109/07388551.2014.889080

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Ma et al. (2013)

Huertas et al. (2012)

Active loading of Na+ into the xylem, and Na+ and K+ compartmentalization Superior growth and accumulated less Na+ and more K+ in roots after 350 mM NaCl treatment

Increased salt tolerance

Na /H antiporters in plasma membrane, exchange Na+ or Li+ for H+ Na+/H+ antiporters in plasma membrane, exchange Na+ or Li+ for H+ Na+/H+ antiporters in plasma membrane, exchange Na+ or Li+ for H+

Elevated character

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Tall fescue A. thaliana Plasma membrane Na+/H+ antiporter SOS1, SOS2, SOS3

Tomato Tomato Plasma membrane Na+/H+ antiporter SISOS

A. thaliana A. thaliana Plasma membrane Na /H antiporter SOS

Gene symbol

Table 1. Continued

+

+

Donor

Acceptor

+

+

Gene function

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Yang et al. (2009)

X. Tang et al.

Reference

6

2013). Unlike atmospheric oxygen, ROS has the ability to oxidize the various cellular components unrestrictedly leading to the oxidative destruction to plant cells (Mittler, 2002). Actually, ROS are the common byproducts of the metabolic pathways such as photosynthetic electron transport, respiration and photorespiration processes (Ahmad et al., 2010). For example, the salt stress limits the supply of CO2 causing over-reduction of photosynthetic electron transport chain and a vast production of ROS (Tu¨rkan & Demiral, 2009). The overmuch ROS can oxidize cellular components, hinder metabolic activities and affect organelle integrity (Suzuki et al., 2012). The destructive effect of ROS is the lipid peroxidation estimated by the content of MDA (Herna´ndez & Almansa, 2002). Generally, under normal conditions, the production and elimination of ROS are in an equilibrium state (Jaleel et al., 2009). However, under salt stress conditions, the generation rate of ROS overwhelms the scavenging of antioxidant system, and then oxidative damage would occur leading to oxidation to lipids, proteins and nucleic acids. It is precisely because that these biomacromolecules are the components of the plasma membrane, thus the membrane system is the main subject of the ROS (Yan et al., 2013). In higher plants, the ROS removal system includes ROSscavenging antioxidant enzymes and small non-enzymatic molecules such as ascorbate, glutathione, flavonoids, anthocyanines and carotenoids (Tu¨rkan & Demiral, 2009). The non-enzymatic molecules are able to donate electron or hydrogen to scavenge free radicals (Jaleel et al., 2009). The antioxidant enzyme system consists of superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase (APX), glutathione peroxidases (GPX), glutathione reductase (GR), catalase (CAT) and ascorbate-glutathione cycle (Ashraf & Akram, 2009). The SOD, APX and GR are reported to scavenge H2O2 in chloroplasts and mitochondria, and the others are believed to be capable of removing H2O2, neutralizing or scavenging free radicals (Karpinski & Muhlenbock, 2007). Among them, SOD and CAT are the most efficient enzymes. Under salt stress, the second metabolites increased more quickly than the increase of antioxidant enzyme activities in Swertia chirata (Abrol et al., 2012). The levels and contents of superoxide and hydrogen peroxide can be decreased by most of the antioxidant obviously, so in many species the antioxidant capacity is associated with salinity tolerance tightly. For example, the antioxidant enzyme activities of SOD, APX and GR increased 10–18 times after salt stress in P. popularis (Chen & Polle, 2010). The correlation between antioxidant capacity and salinity tolerance is being discovered in more and more species, containing cotton, citrus, foxtail millet, purslane, sugar beet, pea and plantago (Tu¨rkan & Demiral, 2009). During the last few decades, engineering the genes of some antioxidant enzymes has been employed to ameliorate plants exposed to stresses. By observing the changes of the related genes expression level, transgenic plants were produced to probe the effects. Finally, the transgenic plants overexpression of antioxidant enzymes such as SOD, CAT and APX displayed elevated tolerance to oxidative stress (Tu¨rkan & Demiral, 2009). The transgenic Arabidopsis and L. esculentum possess a significant increase in salt tolerance with the overexpression of a Mn-SOD (Wang et al., 2004, 2007).

Tobacco

Tobacco Tobacco

A. thaliana Tobacco Tobacco Tobacco A. thaliana

Rice

Tobacco

A. thaliana

Escherichia coli

Avicennia marina

Tobacco

Tomato

Suaeda salsa

Avicennia marina

Populus Tobacco

Wheat

Ascorbate peroxidase (APX), Superoxide dismutase (SOD) and Dehydroascorbate reductase (DHAR) Monodehydroascorbate reductase (MDAR) Catalase (CAT)

Superoxide dismutase (SOD)

Superoxide dismutase (SOD)

Ascorbate peroxidase (APX)

Suaeda salsa glutathione S_transferase gene (GST) Monodehydroascorbate reductase (MDAR) Ascorbate peroxidase (APX) Ascorbate peroxidase (APX), Superoxide dismutase (SOD) Glutathione peroxidases (GPXs)

Plums

A. thaliana

Rice

Dehydroascorbate reductase (DHAR) Ascorbate peroxidase (APX)

Ascorbate peroxidase (APX), Superoxide dismutase (SOD)

A. thaliana

Pea

Ascorbate peroxidase (APX)

Plums

Tobacco

Pepper

Rice

Tobacco

A. thaliana

A. thaliana

Superoxide dismutase (SOD)

Tobacco

Acceptor

A. thaliana

Donor

Ascorbate peroxidase (APX)

Gene symbol

Gene functions

Involved in the reduction of most active oxygen radicals generated due to stress Crucial for Ascorbate (AsA) regeneration and essential for maintaining a reduced pool of AsA Primary H2O2 scavenging enzyme Primary H2O2 scavenging enzyme; the first enzyme in the enzymatic antioxidative pathway Reducing H2O2 and organic hydroperoxides to water and correspondingly alcohols Primary H2O2 scavenging enzyme; the first enzyme in the enzymatic antioxidative pathway

Primary H2O2 scavenging enzyme; A critical enzyme eliminating reactive oxygen species (ROS) in plant cells; A critical enzyme for ascorbate recycling Crucial for Ascorbate (AsA) regeneration and essential for maintaining a reduced pool of AsA Catalyze the dismutation of H2O2 into water and oxygen The first enzyme in the enzymatic antioxidative pathway The first enzyme in the enzymatic antioxidative pathway Primary H2O2 scavenging enzyme

Primary H2O2 scavenging enzyme

A critical enzyme for ascorbate recycling

A critical enzyme eliminating reactive oxygen species (ROS) in plant cells Primary H2O2 scavenging enzyme

Primary H2O2 scavenging enzyme

Table 2. Genetic transformation of antioxidant enzymes for enhancing salt tolerance.

Higher contents of non-enzymatic antioxidants glutathione and Ascorbate and lower accumulation of hydrogen peroxide

Enhanced redox state of ascorbate and reduced levels of malondialdehyde Resistance to methyl viologen and salt stress Improved seed longevity and germination under various environmental stress Strong tolerance to salt, H2O2 and ABA treatment

Higher seed germination rate and elevated stress tolerance during post-germination Higher photosynthesis rate and the fresh weight

Higher net photosynthesis rates and greater PSII effective quantum yield under salt stress Increased the resistance of the chloroplast’s translational machinery under salt stress More tolerant to methyl viologen mediated oxidative stress Increased resistance to oxidative damage

Longer root length and higher total chlorophyll content More resistant to paraquat-induced stress and enhanced tolerance to NaCI

Enhanced tolerance to the active oxygen-generating paraquat and sodium sulphite Lower content of malondialdehyde (MDA) and better growth than control under salt stress Higher germination rate and minimized leaf damage under salt stress Enhanced resistance to salt stress

Elevated character

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Diaz-Vivanco et al. (2013)

Zhai et al. (2013)

Li et al. (2009) Lee et al. (2010)

Kavitha et al. (2010)

Qi et al. (2010)

Chatzidimitriadou et al. (2009) Sun et al. (2010)

Prashanth et al. (2008)

Al-Taweel et al. (2007)

Eltayeb et al. (2007)

Lee et al. (2007)

Lu et al. (2007)

Ushimaru et al. (2006)

Wang et al. (2005)

Wang et al. (2004)

Badawi et al. (2004)

References

DOI: 10.3109/07388551.2014.889080

Global plant-responding mechanisms to salt stress 7

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X. Tang et al.

The detail is shown in Table 2. More importantly, most of the transgenic plants with some over expressed antioxidant enzymes acquire an elevated tolerance to almost all abiotic stresses instead of a specific stress. In our opinion, the possible reason is that oxidative stress is the result of almost all the abiotic stresses, so the enhancement of the antioxidative capacity is able to boost resistance in general. Although the transgenic plants with over expressed antioxidant enzymes acquire enhanced tolerance, there exist contradictions inevitable. The Arabidopsis mutants, with the loss of either or both cytosolic and chloroplastic APX, on the contrary showed enhanced tolerance (Miller et al., 2007). Likewise, there was a decline in CAT activity in A. doliolum under NaCl stress (Srivastava et al., 2005). In Glycyrrhiza uralensis seedlings, the CAT activity was also decreased by salt and drought stress (Pan et al., 2006). In conclusion, the ROS pathway is plastic and redundancy, more strategies and principles remain to be seen. ROS act as a dual role in plants. Superfluous ROS are detrimental to plant cells, yet moderate ROS components are necessarily playing important roles in signaling transduction and cell homeostasis (Sme´kalova´ et al., 2013). In fact, the up-regulation of the enzyme genes expression levels or the enhancement of the enzyme activities are the result of the cell signaling. Ahead of their detoxification, they have initiated a series signaling in cells. MAK3 and MAK6 can be activated by the elevated content of ROS (Lumbreras et al., 2010), and the activated MAK3 and MAK6 were relocated in the nucleus to strengthen or lessen gene expression triggering plant responses to ROS. Nevertheless, the MAPK phosphatase 2 (MKP2) which is induced by oxidative stress is able to dephosphorylate MPK3 and MPK6 to promote oxidative stress tolerance (Sme´kalova´ et al., 2013). Therefore, the signal regulatory pathways are intricate.

Crit Rev Biotechnol, Early Online: 1–13

of ABA in antioxidant defense responses is that ABA induces antioxidant defense. During the ABA-induced antioxidant defense, H2O2, NO and MAPK are major components (Hu et al., 2005; Miller et al., 2010; Ye et al., 2011; Zhang et al., 2006, 2007). Zhang et al. (2012) reported that the zinc finger protein ZFP182 also mediated the ABA-induced antioxidant defense. In rice, ABA can significantly induce the expression and activity of OsCAT to control the accumulation of H2O2 under stress (Ye et al., 2011). Recently, ABA was discovered to induce the production of primary and secondary metabolites, photosynthetic capacity, antioxidant ability and antioxidant enzymes (Ibrahim & Jaafar, 2013). In recent years, the phytohormone – SA was also repeatedly reported to take part in the salt stress responses (Davies et al., 2005). The exogenously SA can ameliorate toxicity stress induced by salt stress and its vital function under salt stress manifests in its enhancement on antioxidant system. In periwinkle, non-enzymatic and enzymatic antioxidants can be induced by exogenous SA (Idrees et al., 2011). In mungbean, SA alleviates decreases in photosynthesis by means of enhancing antioxidant metabolism (Nazar et al., 2011). Furthermore, SA can lessen salt stress by maintaining ion homeostasis. Ion homeostasis, especially the optimum K+/Na+ ratio, is crucial for plant salt stress. Discoveries achieved by non-invasive microelectrode ion flux estimation (MIFE) techniques (Shabala et al., 1997) revealed that SA pretreatment can enhance K+ retention, increase H+-ATPase activity and reduce K+ loss under salt stress (Jayakannan et al., 2013). Generally speaking, the potential mechanism of SA to enhance salt tolerance lies in improving photosynthesis, enhancing antioxidant protection and maintaining the optimum K+/Na+ ratio (Horva´th et al., 2007; Jayakannan et al., 2013; Nazar et al., 2011).

Conclusions Phytohormone in salt stress Plant hormones take part in almost all the processes in plants including different positions, different tissues and different developmental stages. ABA is the foremost hormone and is induced by various stresses. It is able to regulate the adaption of the plants to stresses such as cold, drought, salinity, pathogen attacks, wounding and oxidative stress (Sme´kalova´ et al., 2013). It has been proven to be responsible for the changes in salt-stress-induced genes (De Bruxelles et al., 1996). Its powerful functions in salt stress reflected its involvement in photosynthesis and growth, osmotic tolerance, ion homeostasis and in the antioxidant defense responses discussed earlier. Two decades ago, Popova et al. (1995) has proposed that the inhibitory effect of salt stress on growth and photosynthesis can be alleviated by ABA. Moreover, ABA participates in regulating stress-related-gene expression. In an ABA-deficient mutant, the P5CS, which is the ratelimiting enzyme in the synthesis of Pro, is reduced or completely blocked (Xiong & Zhu, 2001). For ion homeostasis, ABA has the ability to reduce anion channels to reduce Cl transfer in saline conditions (Gilliham & Tester, 2005). The type 2C protein phosphatase ABI2, which acts as a vital component in ABA signaling, is able to bind to SOS2 directly and dephosphorylate it (Ohta et al., 2003). The involvement

Salt stress is one of the most common abiotic stresses. Its negative influences on plants are comprehensive. High concentration salt can profoundly interfere in the normal growth and development of plants and even lead to plant death. Fortunately, plants have acquired the abilities to ameliorate these adverse effects by physiological, molecular and genetic regulations. Plants reduce growth rate to guarantee survival and maintain regular photosynthesis by regulating enzyme activities under salt stress (Zhu, 2001). Facing osmotic stress produced by salt, plants accumulate compatible solute actively to reduce cell water potential (Munns & Tester, 2008). Different channels and transporters are activated or inhibited to regulate and maintain ion homeostasis. The clarified signaling pathways refer to the complicated regulatory mechanisms employed by plants under salt stress. The discovery of the SOS signaling pathway is the milestone of the signal pathway in salt stress (Liu & Zhu, 1998). The antioxidant system covering non-enzymatic and enzymatic antioxidant systems can help plants escape the problems of salt stress (Jaleel et al., 2009). Plant hormones are the growth regulators and they are involved in the processes in every regard and the salt stress is no exception. ABA plays a pivotal role in metabolomics, physiological and signal procedures. Thus, we can come to

Global plant-responding mechanisms to salt stress

DOI: 10.3109/07388551.2014.889080

Figure 1. The general pathway under salt stress.

9

SALINITY

Signal perception and transduction

Transcription factors Regulation of gene expression

Regulation of ion content and homeostasis

Adaptive growth and photosynthesis rate

Gene expression and responses Activation of antioxidant substance and enzyme

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Synthesis and accumulation of compatible solutes

RESISTANCE

the conclusion that the relationship between salt stress and plants are the processes of influences and adaptation. Exploring and understanding the regulatory mechanisms underlying salt stress can provide more methods and ideas to improve plant resistance. Based on the development of molecular biology and transgenic engineering, plants with enhanced tolerance are generating continuously. For example, over expression of the syntheses genes of Pro and GB can improve the content of Pro and GB obviously and endow the transgenic plants with enhanced tolerance (Kavi et al., 1995; Waditee et al., 2005). Similarly, the transgenic plants with more SOS1 or NHX1 transporters are able to regulate ion transport more quickly and effectively to grow well under salt stress (Liu et al., 2000; Quintero et al., 2002; Yang et al., 2009). Increasing the antioxidants through genetic engineering is widely adopted in breeding to produce crops with enhanced salt stress. Nevertheless, the salt tolerance trait is a multigenic property and the salt tolerance is related to physiological, biochemical and molecular processes, so genetic engineering to produce salt-tolerant crops is limited seriously in nature (Zhu, 2003). More energy, material and financial resources are needed to invest in research. Only in this way, can the mechanisms and principles be discovered and the corresponding solutions are proposed. In addition, there are other factors such as LEA proteins, WRKY and MYB transcriptional factors affecting salt tolerance of plants which should also arouse our attentions (Cheng et al., 2013; Gao et al., 2013; Scarpeci et al., 2013). The microorganisms in the soil is found to be involved in phytohormonal signaling to improve plant nutrition, photosynthesis and biomass production ameliorating crop salt tolerance (Dodd & Pe´rez-Alfocea, 2012). Finally, we summarize our points of view and future blueprint for salt stress as indicated in Figure 1.

Declaration of interest This work was jointly supported by the National Natural Science Foundation of China (41171216), One Hundred-Talent Plan of Chinese Academy of Sciences (CAS), the CAS Visiting

Professorship for Senior International Scientists (2012T1Z0010),the Major Program of the Chinese Academy of Sciences(KZZD-EW-04-03), the Science & Technology Development Plan of Shandong Province (2010GSF10208), the Science & Technology Development Plan of Yantai City (2011016; 20102450), European Community Project (no 26220220180)-Building Research Centre of ‘‘AgroBioTech’’, the CAS/SAFEA International Partnership Program for Creative Research Teams, Yantai Double-hundred High-end Talent Plan (XY–003–02) and 135 Development Plan of YICCAS. The authors report no declarations of interest.

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Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology.

The increasing seriousness of salinization aggravates the food, population and environmental issues. Ameliorating the salt-resistance of plants especi...
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