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Journal of soil science and plant nutrition

versión On-line ISSN 0718-9516

J. Soil Sci. Plant Nutr. vol.17 no.1 Temuco mar. 2017

http://dx.doi.org/10.4067/S0718-95162017005000015 

 

Enhancing NO3- supply confers NaCl tolerance by adjusting Cl- uptake and transport in G. max & G. soja

 

J.S. Guo1, Q. Zhou2, X.J. Li1, B.J. Yu1*, Q.Y. Luo3*

 

1Lab of Plant Stress Biology, College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, P.R.China.
2Lab of Plant Resource Conservation and Utilization, Jishou University, Jishou 416000, P.R.China.
3College of Horticuture, Nanjing Agricultural University, Nanjing 210095, P.R.China.
*Corresponding authors: bjyu@njau.edu.cn and qyluo@njau.edu.cn

 


Abstract

The objective of this work was to elucidate NO3- supply, Cl- toxicity, and Cl-/NO3-interaction in Glycine max and Glycine soja under salt stress. G. max cultivars (Lee68 and Jackson) and G. soja accessions (BB52 and N23227) with different salt tolerance were chosen as the experimental materials. Effects of low (0.75 mmol/L), normal (7.5 mmol/L), and high (15 mmol/L) NO3- supply on growth, relative electrolytic leakage, and contents of Cl-, NO3-, Na+, K+ in roots and leaves of NaCl (50 and 100 mmol/L)-stressed plants were investigated. Results showed that, low NO3- supply led to serious salt damage on G. max and G. soja plants. While enhanced NO3- supply could significantly reduce relative electrolytic leakage and contents of Na+ and Cl- in roots and leaves accompanying with obvious NO3- increase and K+ maintenance. Thus, finally an improved growth and alleviated salt injury by reducing Cl-/NO3- and Na+/K+ ratios, especially forthe relatively salt-sensitive Jackson and N23227 were obtained. Moreover, Cl-/NO3- and Na+/K+ ratios were significant or extreme significant positively correlated with relative electrolytic leakage, and significant or extreme significant negatively correlated with root vigor or plant fresh weight. It suggests that Cl-/NO3- ratio can be used as vital reference indexes as Na+/K+ for evaluating soybean salt tolerance.

Keywords: Salt stress, nitrate supply, cultivated soybean, wild soybean, Cl-/NO3-interaction


1. Introduction

Soil salinization is one of major abiotic stress factors that adversely affects plant growth and development thus reduce crop quality and yield (Munns and Tester, 2008). Ionic toxicity, osmotic stress, nutritional imbalance and oxidative damage are the main causes inducing plants or crops salt injury, and ionic toxicity is the primary and fundamental factor (Adem et al., 2014). NaCl is the major form of salt stress to crop plants, so Na+ and Cl- are the main toxic salty ions damaging crop plants as exposed to saline environment. At present, Na+ toxicity or adaptation for salt-stressed crop plants has been deeply and widely understood. Under salt stress, the toxicity to plants is mainly caused by Cl- and excess Cl- causes negative effects on many physiological processes, such as nitrogen absorption and transport, cell water potential, photosynthetic oxygen generation. Also stomatal closure and reactive oxygen species (ROS) accumulation in chloroplasts, finally affects crop growth, yield and quality. It is a pity that the study on Cl- toxicity to crops under salt stress is far from being enough, and therefore is called "the forgotten enemy" (Teakle and Tyerman, 2010). However, it is encouraging that Cl- accumulation or transport and Cl-/salt tolerance in stressed plants have been received much attention in recent years (Nguyen et al., 2015, Qiu et al., 2016, Wei et al., 2016 ).

Nitrogen, as a necessary component of many important organic compounds in plants, is an essential element to plant growth and development (Jung and McCouch, 2013). The absorbed nitrogen for plants utilization includes various N forms (nitrate, ammonium, amino acids, and peptides), and nitrate (NO3-) is the most important nitrogen source for plants (Chen et al., 2012), and is also the main mineral and univalent anions in plant tissues and cells except Cl-, 2010). Studies have showed that, tobacco, grape, potato, citrus and soybean, whose salt stress effects are mainly caused by Cl-, are known as the "chloride-hating plants" (Zhang et al., 2011, Abbaspour et al., 2013, Henderson et al., 2014). Cultivated soybean (G. max) is one of the important grain and oil crops in the world, wild soybean (G. soja) is the relative of G. max, and is often regarded as an important genetic germplasm resource for high yield and good quality of G. max breeding (Zhang et al., 2011). As one kind of legume, soybean has its unique nitrogen absorption characteristics, and can meet its nitrogen requirements about 36% ~ 82% through biological nitrogen fixation directly using free nitrogen in the atmosphere, the remaining nitrogen is supplemented through absorbing soil mineral nitrogen or fertilizer nitrogen by roots (Salvagiotti et al., 2008). Under salt stress, NO3- absorption and transport through plant roots is disrupted (Shi et al.,2015, Gallegos-Cedillo et al., 2016.), especially NO3- reallocation from shoots to roots is strengthened, which resulted in NO3- deficiency in plant aerial parts as leaves (Chen et al., 2012). Higher NO3- content is often showed in old leaves than the young (Wang, et al., 2012a). Thus, enhancing NO3- supply for crop plants under salt stress can significantly reduce Cl- content and increase NO3- level in leaves and alleviate crop salt injury or enhance its salt tolerance (Abdolzadeh et al., 2008).

In terms of both NO3- and Cl- in organs or tissues of salt-treated plants, the increased NO3-/Cl- ratio in shoots plays a positive role in regulation of plant Cl-/salt tolerance (Qiu et al., 2016). However,the alleviative effects of enhancing NO3- supply on salt-stressed G. max and G. soja seedlings have not been reported until now. In this study, G. max cultivars (Lee68 and Jackson) and G. soja accessions (BB52 and N23227) with different salt tolerance were used as the experimental materials. Effects of different NO3- supply on seedlings growth, relative electrolytic leakage (REL), and contents of Na+, K+, Cl-, NO3- in roots and leaves of soybeans under NaCl stress were compared, and correlations between Cl-/NO3-, Na+/K+ ratio and different salt sensitivity of G. max and G. soja were also investigated. The objective of this work is to provide essential scientific basis for future nutrient management or fertilizer applications and variety breeding in soybean or other crops salt tolerance on aspect of Cl-/NO3-interaction.

2. Materials and Methods

2.1. Plant material and culture

Soybeans used in this study were G. max Lee68 and Jackson cultivars (USA), G. soja BB52 and N23227 accessions (respectively from Shandong and Jiangsu, China). Seeds surface-sterilization, germination, and seedlings culture were done according to our previous work (Wei et al., 2015). When the first pair of unifoliolate leaves was fully expanded, the seedlings were randomly separated into 7 groups. One was continually cultured in 1/2 Hoagland solution (expressed as S0N7.5, "S" means NaCl treatment levels, "N" means NO3- supply levels), the others were treated in 1/2 Hoagland solution with 0.75, 7.5, or 15 mmol/L NO3- plus 50 or 100 mmol/L NaCl (expressed as S50N0.75, S50N7.5, S50N15, S100N0.75, S100N7.5, and S100N15). The different NO3- supply levels were adjusted by KNO3 or Ca(NO3)2. When treated for 5 days (the culture solutions were renewed once during this period), the seedlings were photographed and sampled to measure root vigor (for G. max Lee68 and Jackson), plant fresh weight (for G. soja BB52 and N23227), REL, and Na+, K+, Cl- and NO3- contents in roots and leaves of all seedlings.

2.2. Plant sampling and analysis

Root vigor of G. max Lee68 and Jackson seedlings was determined according to triphenyltetrazolium chloride (TTC) method (Wang et al., 2012b).G. soja BB52 and N23227 seedlings (each ten) were selected randomly and fully rinsed in distilled water, then were dried with blotting paper for measurement of fresh weight per plant. REL values in roots and leaves of the above-mentioned 4 kinds of soybean plants were assayed as the method described by Luo et al. (2005). Extraction and assay of Na+, K+, Cl- and NO3- in roots and leaves of soybean plants were performed according to our previous methods (Wei et al., 2015, Zhang et al., 2011, Zhou and Yu, 2009).

2.3. Statistical analysis

All data were analyzed and presented as means ± SD for each treatment (n=3, except in measurement of plant fresh weight, where n=10), and the correlation analysis was conducted using SPSS software (ver. 20.0), and data were subjected to analysis of variance (ANOVA) and Duncan,s multiple range tests were employed to detect differences between means at P < 0.05.

3. Results

3.1. Effects of different NO3- supply on growth and REL in roots and leaves of salt-stressed G. max and G. soja seedlings

Under low NO3- supply and low NaCl concentration stress (S50N0.75), when compared with the control (S0N7.5), G. max cultivar Lee68 and Jackson seedlings were slightly damaged, REL values in roots and leaves were increased within a narrow range, but their roots became sparse and root vigor decreased significantly. Under low NO3- supply and high NaCl concentration stress (S100N0.75), growth of two G. max seedlings were obviously inhibited, leaves became yellow and even wilted, roots became more sparse and black, REL values in leaves and roots were risen remarkably, especially for the salt-sensitive Jackson cultivar. Under low or high concentration of NaCl stress, when NO3-level was added from N0.75 to N7.5 or N15, respectively, REL values in leaves and roots of Lee68 and Jackson seedlings were greatly reduced, and root vigor was clearly restored, the salt injury on soybean seedlings was effectively alleviated, and more apparent ameliorative effect was displayed for Jackson (Figure 1). Under low or high concentration of salt stress, influence of improving NO3- supply on growth (plant fresh weight), REL in leaves and roots of salt-stressed G. soja accession BB52 and N23227 seedlings were similar with those on the above-mentioned G. max cultivar Lee68 and Jackson,and the ameliorative effect on N23227 accession was more obvious (Figure 2).

Figure 1. Effects of different NO3- supplyon (A, from left to right, represent treatments of S0N7.5, S50N0.75, S50N7.5, S50N15, S100N0.75, S100N7.5 and S100N15, respectively) growth, (B) root vigor, and (C) REL in leaves and roots of G. max Lee68 and Jackson seedlings under NaCl stress. Means in bars followed by different letters show significant difference (P < 0.05). The same as belows.

Figure 2. Effects of different NO3- supplyon (A, from left to right, represent treatments of S0N7.5, S50N0.75, S50N7.5, S50N15, S100N0.75, S100N7.5 and S100N15, respectively) growth, (B) FW per plant, and (C) REL in leaves and roots of G. soja BB52 and N23227 seedlings under NaCl stress

3.2. Changes in Na+, K+ contents and Na+/K+ ratios in roots and leaves of NaCl-stressed G. max and G. soja seedlings under different NO3- supply

Whether under low (S50) or high (S100) salt stress plus low NO3- supply (N0.75), Na+ contents in roots or leaves of G. max Lee68 and Jackson, and G. soja BB52 and N23227 seedlings were significantly increased compared with the control (S0N7.5), huger rises were observed under high salt stress, and more obvious in G. soja. In comparison, in addition to K+ contents in leaves of Lee68, Jackson and N23227 remaining relatively stable, K+ contents in roots of Jackson and N23227, and leaves or roots of BB52 were decreased only under high salt stress. However, Na+/K+ ratios in leaves or roots of the above 4 salt-stressed soybean plants were significantly increased as compared with the control, especially under low NO3- supply and high salt stress (S100N0.75). Improvement of NO3- supply level (N7.5 or N15) could obviously reduce Na+ contents in leaves or roots of the other three soybean plants except Jackson under high salt stress, maintain or enhance K+ contents in leaves or roots of all soybean plants, and finaly result in low Na+/K+ ratio. Moreover, these effects showed more obvious under high salt stress (Figure 3, Figure 4).

Figure 3. Changes in (A) Na+,(B) K+contents and (C) Na+/K+ ratios in leaves and roots of G. max Lee68 and Jackson seedlings under NaCl stress plus different NO3- supply

Figure 4. Changes in (A) Na+, (B) K+contents and (C) Na+/K+ ratios in leaves and roots of G. soja BB52 and N23227 seedlings under NaCl stress plus different NO3- supply

3.3. Changes in Cl-, NO3- contents and Cl-/NO3- ratios in roots and leaves of NaCl-stressed G. max and G. soja seedlings under different NO3- supply

Under the condition of low salt stress and low NO3- supply (S50N0.75), Cl- contents in leaves of G. max Lee68 and Jackson seedlings were invisibly changed when compared with the control (S0N7.5), but Cl- contents in roots were sharply raised. Under high salt stress (S100), Cl- contents in roots and leaves of Lee68 and Jackson seedlings were significantly increased, while NO3- contents in roots and leaves were evidently decreased under both low and high salt stress. Under low or high salt stress,when NO3- supply was increased from N0.75 to N7.5 or N15, Cl- contents in roots and leaves of Lee68 seedlings were significantly decreased, while NO3 contents increased obviously, and especially Cl- and NO3- contents in leaves had been restored to control levels, and NO3- content in roots had exceeded the control. Although the reducing effects of enhancing NO3-supply on Cl- contents in leaves and roots of Jackson seedlings under low or high salt stress were not found, the obvious recovery on reduced NO3- content in leaves and roots under salt stress were showed. As a result, increasing NO3 supply showed apparent down-regulation effect on Cl -/NO3-ratios in leaves and roots of G. max Lee68 and Jackson seedlings under low NaCl (S50) or high NaCl (S100) stress (Figure 5). As for G. soja BB52 and N23222 plants and in comparison with the control (S0N7.5), underlow NO3-(N0.75) and low NaCl (S50) or high NaCl (S100) stress, Cl- contents in leaves and roots were significantly increased, NO3- contents decreased obviously and Cl-/NO3- ratios were enlarged, the higher the salt concentration, the greater the increase or decrease. When NO3- supply was increased to N7.5 or N15 under low or high NaCl stress, apparent up-regulation on NO3- contents, and down-regulation on Cl- contents or Cl-/NO3- ratios in leaves and roots of G. soja BB52 and N23222 seedlings were displayed, the effects were more obvious especially under high NaCl stress and high NO3- supply (Figure 6).

Figure 5. Changes in (A) Cl-,(B) NO3- contents and (C) Cl-/NO3- ratios in leaves and roots of G. max Lee68 and Jackson seedlings under NaCl stress plus different NO3- supply

Figure 6. Changes in (A) Cl-,(B) NO3-contents and (C) Cl-/NO3- ratios in leaves and roots of G. soja BB52 and N23227 seedlings under NaCl stress plus different NO3- supply

3.4. Correlations between Cl-/NO3- or Na+/K+ ratios in roots and leaves of NaCl-stressed G. max and G. soja seedlings, and the morphological and physiological parameters

When correlation analysis was carried out between Cl-/NO3- or Na+/K+ ratios and REL values in roots and leaves, root vigor of NaCl-stressed G. max Lee68 and Jackson seedlings and REL values in roots and leaves, plant fresh weight of NaCl-stressed G. soja BB52 and N23227 seedlings, we could find that, Cl-/NO3- and Na+/K+ ratio were significant or extreme significant positively correlated with REL values. Significant or extreme significant negatively correlated Cl-/NO3- or Na+/K+ ratios with root vigor or plant fresh weight were found. Moreover, the extreme significant positive or negative correlations displayed the vast majority, and Cl-/NO3- ratio, roughly equal to Na+/K+ ratio in terms of correlation intensity (Table 1).

Table 1. Correlations between Cl-/NO3- or Na+/K+ and REL in roots and leaves, root vigor or FW per plant of G. max Lee68, Jackson, and G. soja BB52, N23227 seedlings under NaCl stress plus different NO3- supply

Note* show significant correlation, ** show extremely significant correlation.)

4. Discussion

High concentrations of Na+ and Cl- in soil environments will produce osmotic stress on plants at the early stage of salt treatment, then following by ionic Na+ stress with additional Cl- stress on plants as a result of absorbing and accumulating too much Na+ and Cl- in plants (Munns and Tester, 2008;). In saline soils, salt and fertilizer interaction resulted plant nitrogen deficiency has been existed but has yet not been properly investigated, and suitable nutrient management or fertilizer applications on crop plants is the very practical way for alleviating salt injury (Hussain et al., 2016, Ma et al., 2016). In terms of nutrient imbalance for plants under salt stress condition, the competitive inhibition of K+ by Na+ and the resulted K+ loss or deficiency are often firstly focused by the researchers (Jiang et al., 2013). Therefore, contents of Na+, K+ and Na+/K+ ratio (especially the latter) are often used as the most valuable indicators for evaluating plant salt tolerance. On aspects of ionic toxicity or nutrition balance, maintenance of low Na+/K+ ratio is the important prerequisite for most plants to live and grow under saline circumstance (Nemati et al., 2011; Zhang et al., 2011). However, also studies pointed out that high concentration of Cl- in salty soil will competitively inhibit or antagonize plants to absorb NO3-from external environment, and cause nitrogen starvation or deficiency, which negatively affect cellular nitrate assimilation and protein synthesis, leaf growth and photosynthesis (Abbaspour et al., 2014). In addition, soil salinity could cause the strengthening of NO3-reallocation from plant shoots (such as leaves) to roots, which resulted in insufficient NO3-supply for shoots, and negatively affected plant normal nitrogen metabolism, growth and development (Chen et al., 2012). NO3-content in leaves of tomato plants under NaCl stress were dropped greater than roots, and NaCl negatively affected the enzymes activity (such as nitrate reductase and glutamine synthetase located in cytoplasm, and glutamate synthase in plasmids or chloroplasts). NaCl has been shown to inhibit NO3-reduction, NH4+assimilation, and growth of the plants, especially for leaves (Debouba et al., 2007). Taking the above-mentioned "chloride-hating plant", grape for example maintain a lower Cl-content in shoots (mainly leaves) and higher ratio of root/shoot Cl-concentration. A reduction of Cl-distribution in main roots through efflux outside cells or compartmentalization in vacuoles are the important physical characteristics of the salt-tolerant varieties, and these differences may be related with the anion transporters or channel proteins in cellular or intracellular membranes (Gong et al., 2011; Abbaspour et al., 2013; Henderson et al., 2014).

In this study, in comparison with low NO3- (N0.75) supply, enhancement of NO3- (N7.5, N15) supply for 4 kinds of G. max and G. soja plants under low (S50) or high (S100) NaCl stress could obviously increase NO3- content and maintain steady K+content in leaves and roots. A reduction in Cl-and Na+contents (except Jackson), resulted in the evident drops of leaf and root Cl-/NO3- and Na+/K+ratios, especially the drops of Cl-/NO3- ratio under high salt stress were more remarkable (Figure 3, Figure 4, Figure 5, Figure 6). Corresponding to these changes, the increased root and leaf REL values of salt-stressed G. max and G. soja plants were significantly reduced. Root vigor of G. max, plant biomass (fresh weight) of G. soja, and leaf yellowing and growth inhibition of G. max and G. soja plants were obviously restored by enhancing NO3- supply. The mitigating effects on the relatively salt-sensitive G. max Jackson cultivar and G. soja N23227 accession showed more apparent (Figure 1, Figure 2). Correlation analyses between REL values in roots and leaves, or root vigorof NaCl-stressed G. max Lee68 and Jackson seedlings, plant fresh weight of NaCl-stressed G. soja BB52 and N23227 seedlings under different concentration of salt stress and NO3- supply levels, were positively or negatively correlated with Cl-/NO3- or Na+/K+ ratios at the extremely significant level. Also Cl-/NO3- ratio was roughly equal to Na+/K+ ratio in terms of correlation intensity (Table 1). Therefore, Cl- toxicity should not be ignored for the salt-stressed crop plants, especially for the "chloride-hating plants" such as soybean, grape, citrus, etc. Cl-/NO3- ratio should also be looked and used as a vital reference index as Na+/K+ ratio for evaluating crop salt injury or salt tolerance (Teakle and Tyerman, 2010; Abbaspour et al., 2014). The improvement of NO3- uptake and transport in G. max and G. soja plants under NaCl stress, resulted from enhancing NO3- supply. This result might be related to low- and high-affinity nitrate transporter (NRT) located in plasma membrane(Fan et al., 2009, Chen et al., 2012) and H+/NO3-antiporter at tonoplast (Migocka et al., 2013), and this needs further study in future.

5. Conclusion

The enhanced NO3- supply could obviously reduce relative electrolytic leakage values, Cl-/NO3- and Na+/K+ ratios in roots and leaves, restore growth and confer salt tolerance of G. max and G. soja seedlings, especially for the relatively salt-sensitive soybean species. Moreover, Cl-/NO3- ratio should also be used as a vital reference index as Na+/K+ratio for evaluating crop salt tolerance in practice.

Acknowledgments

This work was funded by the National Natural Science Foundation of China (No. 30400280, 31671604).

References

Abbaspour, N., Kaiser, B., Tyerman, S. 2013. Chloride transport and compartmentation within main and lateral roots of two grapevine rootstocks differing in salt tolerance. Trees. 7, 1317–1325.         [ Links ]

Abbaspour, N., Kaiser, B., Tyerman, S. 2014. Root apoplastic transport and water relations cannot account for differences in Cl- transport and Cl-/NO3- interactions of two grapevine rootstocks differing in salt tolerance. Acta Physiol. Plant. 36, 687–698.         [ Links ]

Abdolzadeh, A., Shima, K., Lambers, H., Chiba, K. 2008. Change in uptake, transport and accumulation of ions in Nerium oleander (Rosebay) as affected by different nitrogen sources and salinity. Ann. Bot. 102, 735–746.         [ Links ]

Adem, G.D., Roy, S.J., Zhou, M., Bowman, J.P., Shabala, S. 2014. Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biol. 14, 1-13.         [ Links ]

Chen, C.Z., Lv, X.F., Li, J.Y., Yi, H.Y., Gong, J.M. 2012. Arabidopsis NRT1.5 is another essential component in the regulation of nitrate reallocation and stress tolerance. Plant Physiol. 159, 1582–1590.         [ Links ]

Debouba, M., Maâroufi-Dghimi, H., Suzuki, A., Ghorbel, M.H., Gouta, H. 2007. Changes in growth and activity of enzymes involved in nitrate reduction and ammonium assimilation in tomato seedlings in response to NaCl stress. Ann. Bot. 99, 1143–1151.         [ Links ]

Fan, S.C., Lin, C.S., Hsu, P.K., Lin, S.H., and Tsay, Y.F. 2009. The arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell. 21, 2750–2761.         [ Links ]

Gallegos-Cedillo, V.M., Urrestarazu, M., Álvaro, J.E. 2016. Influence of salinity on transport of nitrates and potassium by means of the xylem sap content between roots and shoots in young tomato plants. J. Soil Sci. Plant Nutr. 16(4), 991-998.         [ Links ]

Gimeno, V., Syvertzen, J.P., Nieves, M., Simon, I., Martinez, F., Garcia-Sanchez, F. 2009. Additional nitrogen fertilization affects salt tolerance of lemon trees on different root stocks. Sci. Hortic. 121, 298–305.         [ Links ]

Gong, H., Blackmore, D., Clingeleffer, P., Sykes, S., Jha, D., Tester, M., Walker, R. 2011. Contrast in chloride exclusion between two grapevine genotypes and its variation in their hybrid progeny. J. Exp. Bot. 62, 989–999.         [ Links ]

Henderson, S.W., Baumann, U., Blackmore, D.H., Walker, A.R., Walker, R.R., Gilliham, M. 2014.Shoot chloride exclusion and salt tolerance in grapevine is associated with differential ion transporter expression in roots. BMC Plant Biol. 14, 273. doi:10.1186/s12870-014-0273-8.         [ Links ]

Hussain, Z., Khattak, R.A., Irshad, M., Mahmood, Q., An, P. 2016. Effect of saline irrigation water on the leachability of salts, growth and chemical composition of wheat (Triticum aestivum L.) in saline-sodic soil supplemented with phosphorus and potassium. J. Soil Sci.Plant Nutr. 16 (3), 604-620.         [ Links ]

Jung, J.K.H., McCouch, S. 2013. Getting to the roots of it: genetic and hormonal control of root architecture. Front. Plant Sci. 4, 57–60.         [ Links ]

Luo, Q.Y., Yu, B.J., Liu, Y.L. 2005.Differential sensitivity to chloride and sodium ions in seedlings of Glycine max and Glycine soja under NaCl stress. J. Plant Physiol. 162, 1003–1012.         [ Links ]

Ma, T., Zeng, W., Li, Q., Wu, J., Huang, J. 2016. Effects of water, salt and nitrogen stress on sunflower (Helianthus annuus L.) at different growth stages. J. Soil Sci. Plant Nutr. http://dx.doi.org/10.4067/S0718-95162016005000075.         [ Links ]

Migocka, M., Warzybok, A., Papierniak, A., Kłobus, G. 2013. NO3-/H+ antiport in the tonoplast of cucumber root cells is stimulated by nitrate supply: evidence for a reversible nitrate-induced phosphorylation of vacuolar NO3-/H+ antiport. PLoS ONE. 8, e73972.         [ Links ]

Munns, R., Tester, M. 2008. Mechanisms of salinity tolerance. Ann. Rev. Plant Biol. 59, 651–681.         [ Links ]

Nemati, I., Moradi, F., Gholizadeh, S., Esmaeili, M.A., Bihamta, M.R. 2011. The effect of salinity stress on ions and soluble sugars distribution in leaves, leaf sheaths and roots of rice (Oryza sativa L.) seedlings. Plant Soil Environ. 57, 26-33.         [ Links ]

Nguyen, C.T., Agorio, A., Jossier, M., Depré, S., Thomine, S., Filleur, S. 2015. Characterization of the chloride channel-like, AtCLCg, involved in chloride tolerance in Arabidopsis thaliana. Plant Cell Physiol. 57, 764–775.         [ Links ]

Nie, L., Feng, J., Fan, P., Chen, X., Guo, J., Lv, S., Bao, H., Jia, W., Tai, F., Jiang, P., Wang, J., Li, Y. 2015. Comparative proteomics of root plasma membrane proteins reveals the involvement of calcium signalling in NaCl-facilitated nitrate uptake in Salicornia europaea. J. Exp. Bot. 66, 4497–4510.         [ Links ]

Qiu, J., Henderson, S.W., Tester, M., Roy, S.J., Gilliham, M. 2016. SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl- accumulation and salt tolerance in Arabidopsis thaliana. J. Exp. Bot. 67., 4495-4505.         [ Links ]

Salvagiotti, F., Cassman, K.G., Specht, J.E., Walters, D.T., Weiss, A., Dobermann, A.R. 2008. Nitrogen uptake, fixation and response to fertilizer N in soybean: a review. Field Crop. Res. 108, 1–13.         [ Links ]

Shi, L., Ma, S., Fang, Y., Xu, J. 2015. Crucial variations in growth and ion homeostasis of Glycine gracilis seedlings under two types of salt stresses. J. Soil Sci. Plant Nutr. 15(4), 1007-1023.         [ Links ]

Teakle, N.L., Tyerman, S.D. 2010. Mechanisms of Cl- transport contributing to salt tolerance. Plant Cell Environ. 33, 566–589.         [ Links ]

Wang, H., Zhang, M., Guo, R., Shi, D., Liu, B., Lin, X., Yang, C. 2012a. Effects of salt stress on ion balance and nitrogen metabolism of old and young leaves in rice (Oryza sativa L.). BMC Plant Biol. 12,194.         [ Links ]

Wang, C.J., Yang, W., Wang, C., Gu, C., Niu, D.D., Liu, H.X., Wang, Y.P., Guo, J.H. 2012b. Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE. 7, e52565.         [ Links ]

Wei, P., Wang, L., Liu, A., Yu, B., Lam, H-M. 2016. Gm CLC1 confers enhanced salt tolerance through regulating chloride accumulation in soybean. Front. Plant Sci. doi: 10.3389/fpls.2016.01082.         [ Links ]

Wei, P.P., Chen, D.M., Jing, R.N., Zhao, C.R., Yu, B.J. 2015. Ameliorative effects of foliar methanol spraying on salt injury to soybean seedlings differing in salt tolerance. Plant Growth Regul. 75, 133–141.         [ Links ]

Zhang, X.K., Zhou, Q.H., Cao, J.H., Yu, B.J. 2011. Differential Cl-/salt tolerance and NaCl-induced alternations of tissue and cellular ion fluxes in Glycine max, Glycine soja and their hybrid seedlings. J. Agron. Crop Sci. 197, 329–339.         [ Links ]

Zhou, Q., Yu, B.J. 2009. Accumulation of inorganic and organic osmolytes and its role in osmotic adjustment in NaCl-stressed vetiver grass seedlings. Russ. J. Plant Physiol. 56, 678–685.         [ Links ]

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