HUANG Rui-dong

College of Agronomy, Shenyang Agricultural University, Shenyang 110866, P.R.China

1. Introduction

Saline-alkaline soil accounts for a considerable share,nearly 1 billion hectares, of the world’s total land resources according to the incomplete statistics of the United Nations Educational, Scientific and Cultural Organization (UNESCO)and the Food and Agriculture Organization (FAO). The total area of saline-alkaline soil in China is approximately 100 million hectares and represents an important land resource (Wanget al. 1993). Improvement and utilization of saline-alkaline land has been brought to the attention of the government, and remarkable achievements have been made, such as in the ecological environment governance of tens of millions of acres of saline-alkaline land in the Huang-Huai-Hai Plain. However, due to the complexity of the factors that affect saline-alkaline soil formation, coupled with the action of the secondary salinization, there is an increasing trend of regional salt accumulation, and across the country, especially in North China, the area of salinealkaline soil is increasing. In addition, the widespread inappropriate use of fertilization and irrigation is also a cause of soil salinization (Zhaoet al. 2007). Soil salinization is always a practical ecological problem of agricultural production in China and the world.

Sorghum is one of the world’s five major cereal crops and is widely grown in arid, semiarid tropical, subtropical,and temperate regions. It is an important source of food,feed, and raw material for brewing and is expected to be a promising bioenergy crop. Sorghum was once one of the most important food crops in North China; however, in recent decades it has gradually changed from being mainly used for food consumption to being mainly used as raw material for brewing, and it is now mainly grown in Northeast and Southwest China. Sorghum is famous for its strong stress resistances and wide adaptability, and salt tolerance is one of its main characteristics (Igartuaet al. 1994). Enhancing sorghum production on saline-alkaline land is one of the best choices for effective use of this marginal soil. Domestic and overseas studies on plant tolerance to soil salinity and alkalinity in sorghum have led to many achievements. These mainly include the improvements in genetics and breeding,physiology, production, and evaluation of saline-alkaline resistance.

2. Genetic research in sorghum saline-alkaline tolerance

Plants under salt stress show a series of physiological and ecological adaptabilities (Liet al. 2012). These adaptive responses are induced by environmental factors and hormones and are regulated by the relevant genes. The expression of many important plant functional genes is induced or suppressed by salt stress, and gene expression regulation has become a hot research topic in recent years. These studies have focused on the transcriptional regulation of genes encoding proteins that are involved in the synthesis of osmotic regulation substances, ion transport,cell detoxification, and antioxidant defense, and protecting cells against stress damage, salt-stress signal transduction,and expression regulation.

2.1. Genetics of sorghum saline-alkaline tolerance

Plant tolerance to soil salinity and alkalinity has been shown to be genetically determined in many plant species(Tal 1985). A strong genotype×salinity interaction was observed while evaluating salt tolerance of sorghum(Azhar and McNeilly 1987; Krishnamurthyet al. 2003).Salt tolerance in sorghum is inherited mainly along the male line and is controlled by several non-allelic genes that condition dominant or overdominant expression of resistance (Spivakov 1990). Similarly, Igartuaet al. (1994)also reported that salt tolerance in sorghum is a very complex quantitative trait controlled by polygenes. They observed substantial genetic variation for salt tolerance during sorghum germination and emergence. In the tested hybrids, these differences in salt tolerance were due to special combining ability (SCA) and female general combining ability (GCA) for emergence, and female GCA for germination, although the male GCA was also significant for both characters. Lineper seperformance was significantly correlated with individual GCA estimates for emergence,but not for germination. Heterosis was also detected in some crosses for germination and final emergence. Wang H Let al. (2014) studied the quantitative trait loci (QTLs)for three traits (germination vigor, germination percentage,and relative salt-injury rate) at the germination stage and nine traits (salt injury index, root dry weight, total dry weight,shoot height, root length, shoot fresh weight, root fresh weight, total fresh weight, and shoot dry weight) at the seedling stage of sorghum and identified 12 and 29 QTLs at the germination and seedling stages, respectively. Six major QTLs and five chromosome regions were found to play a crucial role in salt tolerance of sorghum and could be applied in marker-assisted selection and in further investigations of salt tolerance.

2.2. Genes and proteins related to sorghum saline-alkaline tolertance

The osmolyte proline accumulates when plants are subjected to abiotic stress (Tripathiet al. 2007). Delta 1-pyrroline-5-carboxylate synthetase (P5CS) is a key regulatory enzyme that plays a crucial role in proline biosynthesis. Suet al.(2011) isolated two closely relatedP5CSgenes from sweet sorghum, designatedSbP5CS1(GenBank accession number: GQ377719) andSbP5CS2(GenBank accession number: GQ377720), which are located on chromosomes 3 and 9 and encode 729 and 716 amino acid polypeptides,respectively. Expression analysis revealed thatSbP5CS1andSbP5CS2transcripts were up-regulated after drought and salt treatment of 10-day-old sweet sorghum seedlings.Under high salt treatment,SbP5CS1andSbP5CS2expression peaked in roots at 4 and 8 h, respectively, and the level ofSbP5CS1up-regulation was higher than that ofSbP5CS2. Proline concentration increased after stress application and was correlated with the expression of bothSbP5CSgenes. These findings suggest that these two genes could potentially be used in improving stress tolerance of sweet sorghum.

Dalalet al. (2013) identified four genes encoding LEA3 proteins in the sorghum genome and further classified them into LEA3A and LEA3B subgroups based on the conservation of LEA3 specific motifs. The changes in the expression levels of theSbLEA3genes in response to abiotic stresses, such as soil moisture deficit and osmotic,salt and temperature stress suggest that theLEA3genes have non-redundant functions in stress tolerance in sorghum. Wanget al. (2013) characterized a member of the stress-associated protein (SAP) gene family fromSorghum bicolor(SbSAP14) with A20 and AN1 zinc-finger domains. Expression profiling revealed thatSbSAP14is specifically induced in response to dehydration, salt, and oxidative stress as well as abscisic acid treatment. They proposed thatSbSAP14may play a key role in antioxidant defense systems and possibly be involved in the induction of antioxidant genes in plants, suggesting a possible role of theSAPgene family in stress defense response.

In halophytic plants, the high-affinity potassium transporterHKTgene family can selectively uptake K+in the presence of toxic concentrations of Na+. Wang T Tet al. (2014) described the characterization ofSbHKT1;4,a member of theHKTgene family from sorghum. Upon Na+stress,SbHKT1;4expression was more strongly upregulated in a salt-tolerant sorghum accession and was correlated with a more balanced Na+/K+ratio and enhanced plant growth.

Calcineurin B-like protein interacting protein kinases(CIPKs) are critical components in various stress signal transduction pathways. Guoet al. (2013) identified 32 putative CIPK genes (SbCIPKs) in sweet sorghum and were the first to characterize the role of the CIPK family proteins in response to alkali stress. Real-time polymerase chain reaction (PCR) analysis revealed that the 32SbCIPKgenes had different expression patterns under Na2CO3stress, and sixSbCIPKswere up-regulated >10-fold at the transcriptional level.

Changes in the leaf proteome of sorghum grown under salt stress in hydroponic cultures were studied (Swamiet al.2011). Based on 2-D gel electrophoresis and subsequent mass spectrometric identification 2-DE/MS, it was found that salinity treatment induced changes in the levels of 21 proteins. Majority of the differentially expressed proteins belonged to the functional category of signal transduction mechanisms and inorganic ion transport and metabolism.

3. Sorghum breeding for saline-alkaline tolerance

There are two main ways to utilize saline-alkaline land in agriculture: (1) physical or chemical methods, such as reasonable irrigation, fresh water irrigation and soil amendments, can be used to create a soil environment suitable for crop growth; and (2) genetic engineering or genetic breeding techniques can be used to develop new varieties that are salt tolerant (Wanget al. 2012).Several salt-, drought-, and cold-tolerant lines have been developed through breeding and are being maintained in different locations all over the world (Maqboolet al. 2001).Field trials of a few sorghum genotypes have shown that hybrids have better salt tolerance than their respective parents (Penget al. 1994; Azharet al. 1998). In a study of F1, F2, F1BC1, and F1BC2hybrids from crosses involving 20 sorghum varieties (9 Kafir corn, 6 Bantu corn and 5 Durra-type varieties), Spivakov (1990) found that the most resistant parents were the Bantu corn and Durra types. The most useful hybrids were identified in the F1, and the best recombinants were selected in the F2. Overall, progress in the improvement of sorghum salt tolerance through conventional breeding programs has been limited (Shahbaz and Ashraf 2013). Perhaps this is due to the problem of providing an optimal selection environment. For example, a breeder has to determine whether to improve a trait for the whole target environment (breeding for wide adaptation),or for a specific homogeneous sub-environment (breeding for specific adaptation) (Igartua 1995).

In recent years, with the rapid development in the fields of molecular biology and biotechnology, employing transgenic technology has become the main focus of salt-tolerant plant research. Researchers have identified and cloned salttolerant genes from a variety of salt-tolerant microorganisms and plants by using gene silencing and site-directed mutagenesis and molecular cloning techniques (Sunet al.2001). At the same time, by studying the transcriptional regulation of gene expression in salt-tolerant plants and using this information to improve the expression levels of these genes, the salinity tolerance of transgenic plants could be enhanced. For example, some researchers have used transgenic technology to introduce genes involved in salt tolerance into many types of crops to improve their resistance to salt, and many research results have been obtained (Guoet al. 2015). Molecular biological technology has also been used to increase the synthesis of proline and glycinebetaine, which is an effective way to increase the antioxidant activity of crops and to breed new stress-tolerant varieties (Wang and Li 2001).

Despite these technological advances, little progress has been made in marker-assisted selection for salinity tolerance in sorghum, although some scientists have identified some molecular markers associated with salinity tolerance (Raoet al. 2007). Similarly, there is little information available in the literature about improving salt tolerance in sorghum through genetic engineering, in part due to slow progress in developing transformation protocols (Shahbaz and Ashraf 2013). Progress in making transgenic sorghum has trailed behind other cereals due to tissue culture limitations, lack of model genotypes, low regeneration frequency, and lack of sustainability of regeneration through sub-cultures(Madhusudhanaet al. 2015). However, there have been some successful attempts to generate salt-tolerant sorghumviagenetic engineering. Sorghumcv. SPV462 was transformed with themtlDgene, which encodes mannitol-1-phosphate dehydrogenase fromEscherichia coli, with the aim of enhancing tolerance to NaCl stress (Maheswariet al.2010). Transgene (pCAM mtlD) integration and expression were successfully confirmed by PCR, RT-PCR, and Southern and Western blot analysis. ThemtlDtransgenic plants maintained a 1.7- to 2.8-fold higher shoot and root growth, respectively, under NaCl stress (200 mmol L–1) when compared to untransformed controls, which demonstrates that introducing the mannitol biosynthetic pathway into sorghum can impart enhanced tolerance to salinity. Bihaniet al. (2011) reported the identification of a dehydration response element binding (DREB) transcription factor gene from sorghum,SbDREB2, which was induced specifically under drought/salt stress.

4. Physiological research in sorghum saline-alkaline tolerance

Different sorghum germplasms show different physiological responses to salinity stress and have different resistances to salinity. Physiological research in sorghum saline-alkaline resistance has mainly focused on osmotic regulation,membrane peroxidation and protective enzyme activity, and photosynthesis and fluorescent properties.

4.1. Osmotic regulation substances

Plant cell water deficit, namely osmotic stress, occurs under salinity and alkalinity stress due to the low external osmotic potential. In order to avoid water deficit under abiotic stress, plants must produce the appropriate adaptive response. Under stress conditions, plant cells will take the initiative to accumulate soluble solutes to reduce cell osmotic potential and prevent water loss. There are two categories of osmoregulation substances in plants: (1)inorganic ions such as Na+, Cl–, and K+, which move from the external environment into the cell, and (2) synthetic organic solutes, which mainly consist of multivariate alcohol and nitrogen compounds. Osmotic regulation substances play an important role in improving plant stress resistance;however, the relative contribution of different osmotic regulation substances differs according to plant type, growth period, environment, and the degree and duration of stress.Osmotic regulation substances also affect the creation and clearance of reactive oxygen species (ROS). For example,proline and mannitol have the ability to remove ROS, and Ca2+can enhance the activity of the antioxidant enzymes(Shenet al. 1997; Guan 1999; Jiang 1999; Wang and Li 2001).

Salinity was found to reduce the osmotic potential (Ys)of the cellular sap of leaves and roots in both salt-tolerant and salt-sensitive sorghum genotypes, but this reduction was higher in the salt-sensitive genotype (Lacerdaet al.2003). The higher decrease in the Ys of the salt-sensitive genotype was mostly due to the higher accumulation of Na+and Cl–, which probably exceeded the amount needed for osmotic adjustment. Among the inorganic solutes, K+contributed the most to Ys in control unstressed seedlings,but its contribution decreased as salt stress increased,especially in the salt-sensitive genotype (Lacerdaet al.2003). Under salt (NaCl) stress, the Na+content of sorghum tissue increases, and significantly higher Na+content is found in the roots than in the leaves (Lacerdaet al. 2004;Sun 2012; Almodareset al. 2014). The Na+content in roots of a salt-tolerant hybrid was found to increase more than in a salt-sensitive hybrid, but adverse result was found in the leaves, indicating that maintaining a low concentration of Na+in the leaves is more advantageous for improving salt tolerance (Sun 2012; Almodareset al. 2014). Under salt stress, the levels of K+and Ca2+and the ratios of K+/Na+and Ca2+/Na+in the leaves and roots of sorghum decrease.A salt-tolerant hybrid was found to have a lower reduction in K+and Ca2+than a salt-sensitive hybrid, indicating that under salt stress, the salt-tolerant hybrid has higher ion selective absorption than the salt-sensitive hybrid (Lacerdaet al. 2003; Baveiet al. 2011; Sun 2012). Under mixed alkali(NaHCO3and Na2CO3molar ratio of 9:1) stress conditions,the behavior of alkali-resistant and -sensitive hybrids was similar to that reported under salt stress (Shanget al. 2015).Under salt stress, Na+was mainly retained in the roots,preventing the distribution of excess Na+to leaves, but the root dry weight was increased by salt stress (Chaugoolet al.2013). It is therefore believed that thicker leaf blades and increases in root dry weight are the main contributors to the maintenance of dry matter yield and enhancing growth of sorghum cultivars under NaCl treatment.

Under salt (NaCl) stress conditions, sorghum leaf proline, soluble sugar, reducing sugar, soluble protein,and free amino acid content were found to increase, and a salt-tolerant hybrid showed a higher increase in these substances under salt stress than the salt-sensitive hybrid(Sun 2012). Among organic solutes, soluble carbohydrates and amino acids are believed to contribute the most to leaf and root Ys, respectively. However, the contribution of these solutes to root Ys was found to be higher in the salt-tolerant genotype, especially at higher NaCl concentrations (Lacerdaet al. 2003). A similar result was reported by Shanget al.(2015) under mixed alkali (NaHCO3and Na2CO3molar ratio of 9:1) stress conditions. It was also reported that increasing salinity had an adverse effect on the leaf and root soluble protein content, which decreased with increasing salinity(Baveiet al. 2011).

4.2. Membrane peroxidation and protective enzyme activity

Wang and Li (2001) reported the positive role of proline in removing ROS and the effects of Ca2+and glycinebetaine on protective enzyme activity and antioxidant content. Foliar application of the growth regulator, salicylic acid (SA), was found to increase leaf SOD and POD activities (Noreenet al. 2009). Yanet al. (2015) reported that salt priming enhanced osmotic resistance, as proline levels and relative water content in the leaf were higher in pretreated plants under salt stress. Salt priming can alleviate salt-induced oxidative damage; however, it is not by improving antioxidant protection due to lower increase in leaf MDA content and no extra induction occurs on APX, CAT, SOD, ascorbic acid,and reduced glutathione in pretreated plants.

4.3. Photosynthesis and fluorescence properties

Chlorophyll plays a key role in plant photosynthesis. Baveiet al. (2011) reported that the concentrations of chlorophylla,b, and (a+b) decreased with increasing salinity. Sunet al. (2012) studied the impacts of salt stress on the photosynthesis and chlorophyll fluorescence parameters of sorghum seedlings. A low NaCl concentration (50 mmol L–1) increased the chlorophyll content, whereas high NaCl concentrations (100–200 mmol L–1) substantially reduced chlorophyll content. Salt stress reduced net photosynthetic rate (Pn), stomatal conductance (Gs), transpiration rate (Tr),the maximum fluorescence (Fm), potential photochemical efficiency (Fv/Fo), the maximum photochemical efficiency(Fv/Fm), effective photochemical quantum yield (Fv′/Fm′), and photochemical quenching coefficient (qP), and increased initial fluorescence (Fo) and non-photochemical quenching coefficient (NPQ). Intercellular CO2concentration (Ci)increased with a low NaCl concentration (50 mmol L–1) but decreased under high NaCl concentrations (100–200 mmol L–1). The small reduction in netPncaused by 50 mmol L–1NaCl stress was considered to be the result of non-stomatal restriction, but the increased stomatal restriction with increased NaCl concentration resulted in a more severe reduction inPn. Under salt stress, the photosynthetic organs were more effectively protected in the salt-tolerant cultivars than in salt-sensitive ones.

Exogenously applied SA could increase POD activity and promote sorghum growth and photosynthetic capacity under salt stress (Noreenet al. 2009). The decreases inPnandTrunder salt stress were found to be alleviated by silicon application (Liuet al. 2015). Sorghum plants pretreated with salt maintained a higherPnduring salt stress, suggesting that salt priming can enhance salt tolerance (Yanet al. 2015).

5. Research on agronomic technologies for enhancing saline-alkaline resistance of sorghum

Improvement of saline-alkaline land is the basis for its effective utilization. The methods and techniques used to improve saline-alkaline land utilization mainly include water conservancy engineering, agronomic technology, chemical modification, and biological measures. This article will focus only on the research progress in agronomic technologies of sorghum planting in saline-alkalien land.

Several crop species can be cultivated in saline-alkaline soil, including rice, cotton, sunflower, and sorghum.Because it has resistance to multiple stresses, such as drought, waterlogging, malnutrition, salinity, and alkalinity,sorghum is the best choice in some circumstances.Screening for salt-tolerant sorghum cultivars is an effective method for successful plantation in saline-alkaline soil, and some tolerant varieties have been identified (Sunet al. 2012;Liet al. 2013; Almodareset al. 2014).

Sorghum production in saline-alkaline soil has become more popular with the application of some agronomic approaches (Wang H Yet al. 2014; Liet al. 2015; Wanget al. 2015). However, more systematic and comprehensive researches on the technologies are still insufficient. A set of cultivation methods for growing high-yielding sweet sorghum in saline-alkaline fields that includes variety selection, soil preparation, planting method, and plant management was summarized (Wang H Yet al. 2014). Sowing depth should be shallower compared with non-saline soil, and plastic film mulching and furrow planting are recommended (Liet al. 2015).

Application of specific chemical compounds could also help to alleviate the negative effects of salt in saline-alkaline soils. For example, a high Ca2+concentration in the nutrient solution was found to partially reduce the impacts of salt,mainly in the shoots, of a salt-tolerant genotype (Lacerdaet al. 2004). Silicon application could alleviate the decrease in root hydraulic conductance by mediating aquaporin activity, leading to increased water uptake and resistance to salt-induced osmotic stress (Liuet al. 2015). SA can be used to promote plant growth under stress and non-stress conditions (Noreenet al. 2009). As previously mentioned,salt priming can improve salt tolerance in sweet sorghum by enhancing osmotic resistance and reducing root Na+uptake (Yanet al. 2015).

6. Research on the evaluation of saline-alkaline tolerance in sorghum

Progress has been made in identifying traits that are good indicators of salt tolerance in sorghum. The responses of 42 sorghum cultivars to salt stress were compared,and sorghum cultivars with tolerance to salinity during germination were identified based on the relevant parameters (Sunet al. 2012). In this study, the optimal concentration of NaCl for screening sorghum cultivars during germination was determined to be 150 mmol L–1. Principal component analysis revealed that root length, leaf weight, and germination rate, which were the largest loads in the root,leaf, and germination factors, respectively, could be used as the main indexes to screen for sorghum salt tolerance.Five of the 42 cultivars were highly salt tolerant (e.g., Liaoza 15), 14 cultivars were salt tolerant (e.g., Shenshi 104), 12 cultivars were moderately salt sensitive (e.g., Aoza 1), 8 cultivars were salt sensitive (e.g., Tieza 17), and 3 were highly salt sensitive (e.g., Longza 10). Liet al. (2013) reported that root length, germination index, and leaf dry weight were the most significant factors and were recommended as the main indexes to identify alkaline tolerance of sorghum at germination. They classified 35 sorghum cultivars; 7 were strongly tolerant to alkaline conditions (e.g., Siza 25), 22 were moderately tolerant (e.g., Jiza 319 and Chiza 28), and 6 were sensitive (e.g., Longza 9).

Some individual parameters have also been reported to be useful as indicators for identifying sorghum cultivars with tolerance to salt stress. A novel 50 kDa polypeptide that is expressed under NaCl stress was suggested to be a marker protein for salt adaptation (Baveiet al. 2011).Because the K+/Na+ratio increases in salt-tolerant cultivars and decreases in salt-sensitive ones, it seems that this ratio is a good indicator for selection of salt-tolerant cultivars(Almodareset al. 2014).

7. Pay more attention to salt-tolerant research in sorghum for increasing its productivity in saline-alkaline soil

To summarize, many studies on sorghum salinity and alkalinity tolerance have been done in China and throughout the world, and many successful results have been obtained, as mentioned above. However, much of the research is still in the elementary stage, and relatively few findings have been applied to production practices,so it is necessary to further strengthen the salinity and alkalinity tolerance research in sorghum. One approach is to strengthen the work on screening salinity- and alkalinitytolerant sorghum germplasm and the excellent germplasm innovation. Sorghum is an old crop that originated from stressful environments and thus has many inheritable stress-tolerant traits. More screening and identification of tolerant germplasm should be done using the existing technologies. By making full use of the new achievements in biotechnology, scientists may create new salinity- and alkalinity-tolerant breeding materials. New varieties with high yield, good quality, and salinity and alkalinity tolerance can then be bred through a combination of conventional breeding and biotechnology. The second approach is to strengthen the research on comprehensive farming techniques for growing sorghum on saline-alkaline land. In addition, by employing the saline-alkaline land cultivation technologies from other crops, more suitable sorghum farming technologies can be developed to improve the utilization efficiency of this marginal land.

The current development of sorghum production has many advantages, especially in saline-alkaline land, and sorghum production will have a good developing space and prospect. The National Crop Structure Adjustment Planning (NCSAP) (2016–2020) compiled by the Ministry of Agriculture of China pointed out that under the new background of agriculture, the main problem facing agriculture in China has changed from insufficient production to structural unbalance. So currently, and in the near future,boosting the structural reforms in agricultural “supply-side”is the most important task in improving agriculture and the rural economy. For the structural adjustment in grain crop species, NCSAP clearly proposed to increase the production of side grain crops and beans. As sorghum is both an important side grain crop and a drought-resistant crop, it is also one of the preferential options for water-saving cultivation. Because the saline-alkaline land area in China is large and continues to increase, sorghum as a salinity- and alkalinity-tolerant crop will also be advantageous in terms of saline-alkaline land utilization. Moreover, in recent years,a large amount of sorghum has been imported into China.The biggest import occurred in 2015, when 10.7 million tons,nearly four times the amount of the domestic production,was imported. Expanding sorghum planting area is going to reduce the amount of sorghum imports.

Acknowledgements

This work was supported by the earmarked fund for China Agriculture Research System (CARS-06).

Almodares A, Hadi M R, Kholdebarin B, Samedani B, Kharazian Z A. 2014. The response of sweet sorghum cultivars to salt stress and accumulation of Na+, Cl–and K+ions in relation to salinity.Journal of Environmental Biology, 35, 733–739.

Azhar F M, Hussain S S, Mahomood I. 1998. Heterotic response of F1sorghum hybrids to NaCl salinity at early stage of plant growth.Pakistan Journal of Science and Industrial Research, 41, 50–53.

Azhar F M, McNeilly T. 1987. Variability for salt tolerance inSorghum bicolor(L.) Moench under hydroponic condition.Journal of Agronomy and Crop Science, 159, 269–277.

Bavei V, Shiran B, Khodambashi M, Ranjbar A. 2011. Protein electrophoretic profiles and physiochemical indicators of salinity tolerance in sorghum (Sorghum bicolorL.).African Journal of Biotechnology, 10, 2683–2697.

Bihani P, Char B, Bhargava S. 2011. Transgenic expression of sorghumDREB2in rice improves tolerance and yield under water limitation.Journal of Agricultural Science,149, 95–101.

Chaugool J, Naito H, Kasuga S, Ehara H. 2013. Comparison of young seedling growth and sodium distribution among sorghum plants under salt stress.Plant Production Science,16, 261–270.

Cheng J D, An Y L, Sun Y F, Liu L P, Zhang Q C. 2006. Progress on drought, salt gene types and acting mechanisms.Acta Agriculturae Boreali-Sinica, 21, 116–120. (in Chinese)

Dalal M, Kumar G S, Mayandi K. 2013. Identification and expression analysis of group 3LEAfamily genes in sorghum [Sorghum bicolor(L.) Moench].Acta Physiologiae Plantarum, 35, 979–984.

Fu Y S, Cui J Z, Chen G D, Liu J, Mi X J, Zhang H B. 2012.Expression of Na+/H+antiporter geneKsNHX1inKochia sieversianaunder saline-alkali stress.Chinese Journal of Applied Ecology, 23, 1629–1634. (in Chinese)

Guan J F. 1999. Effects of calcium ion on ell membrane permeability, activities of protectives enzymes and content of protective substances in apple fruits.Chinese Bulletin of Botany, 16, 72–74. (in Chinese)

Guo M, Liu Q, Yu H, Zhou T T, Zou J, Zhang H, Bian M D, Liu X M. 2013. Characterization of alkali stress-responsive genes of the CIPK family in sweet sorghum [Sorghum bicolor(L.)Moench].Crop Science, 55, 1254–1263.

Guo W F, Nong W T, Li G Q, Liu D H. 2015. Research progress of genetic engineering on plant salt tolerance.Biotechnology Bulletin, 31, 11–17. (in Chinese)

Igartua E. 1995. Choice of selection environment for improving crop yields in saline areas.Theoretical and Applied Genetics, 91, 1016–1021.

Igartua E, Gracia M P, Lasa J M. 1994. Characterization and genetic control of germination-emergence responses of grain sorghum to salinity.Euphytica, 76, 185–193.

Jiang M Y. 1999. Generation of hydroxyl radicals and its relation to cellular oxidative damage in plants subjected to water stress.Acta Botanica Sinica, 41, 229–234. (in Chinese)

Krishnamurthy L, Reddy B V S, Serraj R. 2003. Screening sorghum germplasm for tolerance to soil salinity.International Sorghum and Millets Newsletter, 44, 90–92.

Lacerda C F, Cambraia J, Oliva M A, Ruiz H A. 2003. Osmotic adjustment in roots and leaves of two sorghum genotypes under NaCl stress.Brazilian Journal of Plant Physiology,15, 113–118.

Lacerda C F, Cambraia J, Oliva M A, Ruiz H A. 2004. Calcium effects on growth and solute contents of sorghum seedlings under NaCl stress.Revista Brasileira de Ciência do Solo,28, 289–295. (in Portuguese)

Li C H, Zhang P T, Guo W Q, Tang S Y, Xie Q, Yin J M, Han X Y, Wang L. 2015. Breeding and cultivation techniques of salt resistant sweet sorghum hybrid Zhongketian 3.Jiangsu Agricultural Sciences, 43, 95–96. (in Chinese)

Li F X, Zhou Y F, Wang Y T, Sun L, Bai W, Yan T, Xu W J,Huang R D. 2013. Screening and identification of sorghum cultivars for alkali tolerance during germination.Scientia Agricultura Sinica, 46, 1762–1771. (in Chinese)

Li M, Zhang J, Li Y J, Tan F, Cong X L. 2012. Research progress of plant salt-tolerant physiology and salt-tolerant genes.Jiangsu Agricultural Sciences, 40, 45–49. (in Chinese)

Liu P, Yin L N, Wang S W, Zhang M J, Deng X P, Zhang S Q,Tanaka K. 2015. Enhanced root hydraulic conductance by aquaporin regulation accounts for silicon alleviated saltinduced osmotic stress inSorghum bicolorL.Environmental and Experimental Botany, 111, 42–51.

Madhusudhana R, Rajendrakumar P, Patil J V. 2015.Sorghum Molecular Breeding. Springer, India.

Maheswari M, Varalaxmi Y, Vijayalakshmi A, Yadav S K,Sharmila P, Venkateswarlu B, Vanaja M, Saradhi P P.2010. Metabolic engineering usingmtlDgene enhances tolerance to water deficit and salinity in sorghum.Biological Plantarum, 54, 647–652.

Maqbool S B, Devi P, Sticklen M B. 2001. Biotechnology:Genetic improvement of sorghum (Sorghum bicolor(L.)Moench).In Vitro Cellular & Developmental Biology-Plant,37, 504–515.

Noreen S, Ashraf M, Hussain M, Jamil A. 2009. Exogenous application of salicylic acid enhances antioxidative capacity in salt stressed sunflower (Helianthus annuusL.) plants.Pakistan Journal of Botany, 41, 473–479.

Peng J, Lill H, Li J, Tan Z. 1994. Screening Chinese sorghum cultivars for tolerance to salinity.International Sorghum and Millets Newsletter, 35, 124.

Rao M V S, Kumari P K, Manga V, Mani N S. 2007. Molecular markers for screening salinity response in sorghum.Indian Journal of Biotechnology, 6, 271–273.

Shahbaz M, Ashraf M. 2013. Improving salinity tolerance in cereals.Critical Reviews in Plant Sciences, 32, 237–249.

Shang P P, Li F X, Zhou Y F, Peng Z, Gao M Y, Han Y, Xu W J, Huang R D. 2015. Effects of mixed alkaline (NaHCO3and Na2CO3) stress on osmotic regulation and ion balance of sorghum seedlings.Chinese Journal of Ecology, 34,1924–1929.

Shen B, Jensen R G, Bohnert H J. 1997. Mannitol protects against oxidation by hydroxyl radicals.Plant Physiology,115, 527–532.

Spivakov N S. 1990. Genetic nature and inheritance of salt resistance in sorghum.Soviet Agricultural Sciences, 4,25–28.

Su M, Li X F, Ma X Y, Peng X J, Zhao A G, Cheng L Q, Chen S Y, Liu G S. 2011. Cloning twoP5CSgenes from bioenergy sorghum and their expression profiles under abiotic stresses and MeJA treatment.Plant Science, 181, 652–659.

Sun L. 2012. Salt-tolerant sorghum screening and the mechanisms of salt tolerances. Ph D thesis, Shenyang Agricultural University, China. (in Chinese)

Sun L, Huang R D. 2014. Responses to salt stress of protective enzyme system in sorghum seedlings.Journal of Shenyang Agricultural University, 45, 134–137. (in Chinese)

Sun L, Zhou Y F, Li F X, Xiao M J, Tao Y, Xu W J, Huang R D. 2012. Impacts of salt stress on characteristics of photosynthesis and chlorophyll fluorescence of sorghum seedlings.Scientia Agricultura Sinica, 45, 3265–3272. (in Chinese)

Sun L, Zhou Y F, Wang C, Xiao M J, Tao Y, Xu W J, Huang R D. 2012. Screening and identification of sorghum cultivars for salinity tolerance during germination.Scientia Agricultura Sinica, 45, 1714–1722. (in Chinese)

Sun L J, Yue G F, Wang J X, Zhou B C. 2001. Mechanism of salt stress tolerance in plants.Marine Sciences, 25, 28–31.(in Chinese)

Swami A K, Alam S I, Sengupta N, Sarin R. 2011. Differential proteomic analysis of salt stress response inSorghum bicolorleaves.Environmental and Experimental Botany,71, 321–328.

Tal M. 1985. Genetics of salt tolerance in higher plants:Theoretical and practical considerations.Plant and Soil,89, 199–226.

Tripathi S B, Gurumurthi K, Panigrahi A K, Shaw B P. 2007.Salinity induced changes in proline and betaine contents and synthesis in two aquatic macrophytes differing in salt tolerance.Biologia Plantarum, 51, 110–115.

Wang H L, Chen G L, Zhang H W, Liu B, Yang Y B, Qin L,Chen E Y, Guan Y A. 2014. Identification of QTLs for salt tolerance at germination and seedling stage ofSorghum bicolorL. Moench.Euphytica, 196, 117–127.

Wang H Y, Wang W, Chen J P, Cai L W, Wang Y H, Qi Y K,Shi Q H, Gao J, Pan Z J. 2014. Sweet sorghum high yield cultivation techniques in Jiangsu coastal shoal saline-alkali land.Barley and Cereal Science, 3, 33–34. (in Chinese)

Wang J, Li D Q. 2001. The accumulation of plant osmoticum and activated oxygen metabolism under stress.Chinese Bulletin of Botany, 18, 459–465. (in Chinese)

Wang T T, Ren Z J, Liu Z Q, Feng X, Guo R Q, Li B G, Li L G,Jing H C. 2014.SbHKT1;4, a member of the high-affinity potassium transporter gene family fromSorghum bicolor,functions to maintain optimal Na+/K+balance under Na+stress.Journal of Integrative Plant Biology, 56, 315–332.

Wang W, He X L, Pan Z J, Wang H Y, Guo S W, Zhang D Y,Gao J, Cai L W, Wang Y H, Chen J P, Wang B H. 2015.Adaptability research of Yajin sweet sorghum cultivars in coastal saline soil in Jiangsu.Southwest China Journal of Agricultural Sciences, 28, 1851–1853. (in Chinese)

Wang Y, Ren X, Yu Z J, Cai Q A, Lin X X, Ma R. 2012. Advances in the transformation of salt tolerance gene into maize.Journal of Anhui Agricultural Science, 40, 3908–3911. (in Chinese)

Wang Y H, Zhang L R, Zhang L L, Xing T, Peng J Z, Sun S L,Chen G, Wang X J. 2013. A novel stress-associated proteinSbSAP14fromSorghum bicolorconfers tolerance to salt stress in transgenic rice.Molecular Breeding, 32, 437–449.Wang Z Q, Zhu S Q, Yu R P, Li L Q, Shan G Z, You W R, Zeng X X, Zhang C W, Zhang L J, Song R H. 1993.Saline Soil in China. Science Press, China. (in Chinese)

Yan K, Xu H L, Cao W, Chen X B. 2015. Salt priming improved salt tolerance in sweetsorghum by enhancing osmotic resistance and reducing root Na+uptake.Acta Physiologiae Plantarum, 37, 203.

Zhao L, Luo J X, Huang H L, Xiao Q L. 2007. The cause and control of soils secondary salinization in protected land.Crop Research, 21, 547–554.