[Home ] [Archive]   [ فارسی ]  
:: Main :: About :: Current Issue :: Archive :: Search :: Submit :: Contact ::
Main Menu
Home::
Journal Information::
Articles archive::
For Authors::
For Reviewers::
Registration::
Contact us::
Site Facilities::
Indexing and Abstracting::
Reviewers::
Publication Ethics::
Copyright and Licensing::
Fees and Charges::
Open Access Statement::
::
Search in website

Advanced Search
..
Receive site information
Enter your Email in the following box to receive the site news and information.
..
:: Volume 8, Issue 1 (Spring and Summer 2023) ::
FOP 2023, 8(1): 183-200 Back to browse issues page
The eelgrass Zostera marina antiporter gene (ZmNa+/H+) confers salt stress tolerance to ornamental tobacco (Nicotiana alata)
Soheila Khorsandy , Parastoo Ehsani , Abolfazl Jowkar * , Abbas Alemzadeh
Shiraz University
Abstract:   (1115 Views)
Salinity stress is a main restricting factor for plants’ growth and development, resulting from climate change. The ornamental tobacco (Nicotiana alata) from the Solanaceae family is a bedding plant with attractive flowers suitable for semi-arid and arid lands. In order to obtain salt tolerance, the Na+/H+ antiporter gene was transferred from the halophyte eelgrass (Z. marina) grown in saltwater lake Urmia to N. alata. For gene transformation, leaf explants were immersed in liquid medium containing Agrobacterium tumefaciens containing the vacuolar gene ZmNHX1. The explants were subcultured on MS medium supplemented with 1 mg L-1 benzyl amino purine, 0.1 mg L−1 naphthalene acetic acid, 200 mg L-1 cefotaxime and 10 mg L-1 kanamycin. After regeneration, salinity stress was applied by 0, 210, 230 and 240 mM NaCl in a completely randomized design with three replications. For the first time, vacuolar Na+/H+ antiporter gene ZmNHX1 was successfully transferred to ornamental tobacco. Compared to the wild type plants, the transgenic plants showed higher content of leaf chlorophyll, leaf carotenoid, fresh weight and dry weight of the whole plant, leaf proline content and leaf catalase activity. After salinity stress, the T revealed greater chlorophyll, carotenoid, anthocyanin, K+: Na+ ratio, fresh weight, dry weight, proline amount, catalase and ascorbate peroxidase activity. The T also demonstrated a lower decline in relative water content and a lesser increase of leaves electrolyte leakage, compared to the WT. The stable expression of ZmNHX1 obtained from eelgrass confer salinity stress tolerance in ornamental tobacco providing a new window for cultivation of this species in areas exposed to salinity stress and the resulting transgenic ornamental tobacco is suggested for garden flower cultivation in areas exposed to salinity stress.
Keywords: Antiporter gene, Nicotina alata, Ornamental tobacco, Salt stress tolerance, ZmNHX1, Zostera marina.
Full-Text [PDF 614 kb]   (400 Downloads)    
Type of Study: Research | Subject: Special
Received: 2023/01/15 | Accepted: 2023/02/6 | Published: 2024/01/5
References
1. رفرنس های متنی مثل خروجی کراس رف را در اینجا وارد کرده و تایید کنید -------------Alemzadeh, A., Fujie, M., Usami, S., Yoshizaki, T., Oyama, K., Kawabata, T., Yamada, T. (2006). ZMVHA-B1, the gene for subunit B of vacuolar H+-ATPase from the eelgrass Zostera marina L. Can replace vma2 in a yeast null mutant. Journal of Bioscience and Bioengineering, 102(5), 390-395. ‌ [DOI:10.1263/jbb.102.390]
2. Apse, M. P., Sottosanto, J. B., Blumwald, E. (2003). Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T‐DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. The Plant Journal, 36(2), 229-239. ‌ [DOI:10.1046/j.1365-313X.2003.01871.x]
3. Ayadi, M., Martins, V., Ben Ayed, R., Jbir, R., Feki, M., Mzid, R., Hanana, M. (2020). Genome-wide identification, molecular characterization, and gene expression analyses of grapevine NHX antiporters suggest their involvement in growth, ripening, seed dormancy, and stress response. Biochemical Genetics, 58, 102-128. [DOI:10.1007/s10528-019-09930-4]
4. Bao-Yan, A. N., Yan, L. U. O., Jia-Rui, L. I., Wei-Hua, Q. I. A. O., ZHANG, X. S., Xin-Qi, G. A. O. (2008). Expression of a vacuolar Na+/H+ antiporter gene of alfalfa enhances salinity tolerance in transgenic Arabidopsis. Acta Agronomica Sinica, 34(4), 557-564. ‌ [DOI:10.1016/S1875-2780(08)60022-X]
5. Barrs, H. D., Weatherley, P. E. (1962). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences, 15(3), 413-428. [DOI:10.1071/BI9620413]
6. Bassil, E., Zhang, S., Gong, H., Tajima, H., Blumwald, E. (2019). Cation specificity of vacuolar NHX-type cation/H+ antiporters. Plant Physiology, 179(2), 616-629. ‌ [DOI:10.1104/pp.18.01103]
7. Bates, L. S., Waldren, R. A., Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205-207. ‌ [DOI:10.1007/BF00018060]
8. Blumwald, E., Aharon, G. S., Apse, M. P. (2000). Sodium transport in plant cells. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1465(1-2), 140-151. ‌ [DOI:10.1016/S0005-2736(00)00135-8]
9. Brini, F., Hanin, M., Mezghani, I., Berkowitz, G. A., Masmoudi, K. (2007). Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt and drought-stress tolerance in Arabidopsis thaliana plants. Journal of Experimental Botany, 58(2), 301-308. ‌ [DOI:10.1093/jxb/erl251]
10. Cao, D., Hou, W., Liu, W., Yao, W., Wu, C., Liu, X., Han, T. (2011). Overexpression of TaNHX2 enhances salt tolerance of 'composite' and whole transgenic soybean plants. Plant Cell, Tissue and Organ Culture (PCTOC), 107, 541-552. [DOI:10.1007/s11240-011-0005-9]
11. Chapman, H. D., Pratt, F. P. (1982). Determination of minerals by titration method. Methods of Analysis for Soils, Plants and Water, 2nd ed. Oakland, CA: Agriculture Division, California University, 169-170.
12. Chance, B., Maehly, A.C. (1955) Assay of Catalase and Peroxidase. Methods in Enzymology, 2, 764-775. [DOI:10.1016/S0076-6879(55)02300-8]
13. Chauhan, S., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D. E., Bohnert, H. J. (2000). Na+/myo‐inositol symporters and Na+/H+‐antiport in Mesembryanthemum crystallinum. The Plant Journal, 24(4), 511-522. ‌ [DOI:10.1046/j.1365-313x.2000.00903.x]
14. Chen, H. T., Xin, C. H. E. N., Wu, B. Y., Yuan, X. X., Zhang, H. M., Cui, X. Y., Liu, X. Q. (2015). Whole-genome identification and expression analysis of K+ efflux antiporter (KEA) and Na+/H+ antiporter (NHX) families under abiotic stress in soybean. Journal of Integrative Agriculture, 14(6), 1171-1183. ‌ [DOI:10.1016/S2095-3119(14)60918-7]
15. Chen, S., Wu, F., Li, Y., Qian, Y., Pan, X., Li, F., Yang, A. (2019). NtMYB4 and NtCHS1 are critical factors in the regulation of flavonoid biosynthesis and are involved in salinity responsiveness. Frontiers in Plant Science, doi: /10.3389/fpls.2019.00178. [DOI:10.3389/fpls.2019.00178]
16. Doblin, M. S., de Melis, L., Read, S., Newbigin, E. J., Bacic, A. (2000). The cloning of two putative ß-glucan synthase genes from pollen tubes of Nicotiana alata. Plant Biology ‌(Abstract no. 310).
17. Dong, J., Liu, C., Wang, Y., Zhao, Y., Ge, D., Yuan, Z. (2021). Genome-wide identification of the NHX gene family in Punica granatum L. and their expressional patterns under salt stress. Agronomy, 11(2), 264. ‌ [DOI:10.3390/agronomy11020264]
18. Fukuda, A., Nakamura, A., Tanaka, Y. (1999). Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1446(1-2), 149-155. ‌ [DOI:10.1016/S0167-4781(99)00065-2]
19. Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P., Alper, S. L., Fink, G. R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences, 96(4), 1480-1485. ‌ [DOI:10.1073/pnas.96.4.1480]
20. Habibi, F., Ramezanian, A. (2017). Vacuum infiltration of putrescine enhances bioactive compounds and maintains the quality of blood orange during cold storage. Food Chemistry, 227, 1-8. ‌ [DOI:10.1016/j.foodchem.2017.01.057]
21. Hasegawa, P. M., Bressan, R. A., Zhu, J. K., Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annual Review of Plant Biology, 51(1), 463-499. [DOI:10.1146/annurev.arplant.51.1.463]
22. ‌ Himabindu, Y., Chakradhar, T., Reddy, M. C., Kanygin, A., Redding, K. E., Chandrasekhar, T. (2016). Salt-tolerant genes from halophytes are potential key players of salt tolerance in glycophytes. Environmental and Experimental Botany, 124, 39-63. ‌ [DOI:10.1016/j.envexpbot.2015.11.010]
23. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., Bourguignon, J. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Molecular & Cellular Proteomics, 6(3), 394-412. ‌ [DOI:10.1074/mcp.M600250-MCP200]
24. Jha, B., Mishra, A., Jha, A., Joshi, M. (2013). Developing transgenic Jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS One, 8(8), e71136. ‌ [DOI:10.1371/annotation/89bc2c6f-2799-4a5b-9f57-8e2fa3e14fc9]
25. Khan, M. S., Ahmad, D., Khan, M. A. (2015). Trends in genetic engineering of plants with (Na+/H+) antiporters for salt stress tolerance. Biotechnology & Biotechnological Equipment, 29(5), 815-825. ‌ [DOI:10.1080/13102818.2015.1060868]
26. Knapp, S., Chase, M. W., Clarkson, J. J. (2004). Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon, 53(1), 73-82. ‌ [DOI:10.2307/4135490]
27. Lan, T., Duan, Y., Wang, B., Zhou, Y., Wu, W. (2011). Molecular cloning and functional characterization of a Na+/H+ antiporter gene from halophyte Spartina anglica. Turkish Journal of Agriculture and Forestry, 35(5), 535-543. ‌ [DOI:10.3906/tar-1003-2]
28. Leidi, E. O., Barragán, V., Rubio, L., El‐Hamdaoui, A., Ruiz, M. T., Cubero, B., Fernandez, J., Berresan, R., Quintero, F., Pardo, J. M. (2010). The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomatoes. The Plant Journal, 61(3), 495-506. [DOI:10.1111/j.1365-313X.2009.04073.x]
29. ‌ Li, J., Jiang, G., Huang, P., Ma, J., Zhang, F. (2007). Overexpression of the Na+/H+ antiporter gene from Suaeda salsa confers cold and salt tolerance to transgenic Arabidopsis thaliana. Plant cell, Tissue and Organ Culture, 90, 41-48. ‌ [DOI:10.1007/s11240-007-9246-z]
30. Li, T., Zhang, Y., Liu, H., Wu, Y., Li, W., Zhang, H. (2010). Stable expression of Arabidopsis vacuolar Na+/H+ antiporter gene AtNHX1, and salt tolerance in transgenic soybean for over six generations. Chinese Science Bulletin, 55, 1127-1134. ‌ [DOI:10.1007/s11434-010-0092-8]
31. Li, W., Zhao, F. A., Fang, W., Xie, D., Hou, J., Yang, X., Lv, S. (2015). Identification of early salt stress-responsive proteins in seedling roots of upland cotton (Gossypium hirsutum L.) employing the iTRAQ-based proteomic technique. Frontiers in Plant Science, 6, 732. ‌ doi: 10.3389/fpls.2015.00732. [DOI:10.3389/fpls.2015.00732]
32. Li, N., Wang, X., Ma, B., Du, C., Zheng, L., Wang, Y. (2017). Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte Reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. Journal of Plant Physiology, 218, 109-120. ‌ [DOI:10.1016/j.jplph.2017.07.015]
33. Li, C., Zhao, Y., Qi, Y., Duan, C., Zhang, H., Zhang, Q. (2022). The Eutrema EsMYB90 gene improves the growth and antioxidant capacity of transgenic wheat under salinity stress. Frontiers in Plant Science, 1126. doi: 10.3389/fpls.2022.856163. ‌ [DOI:10.3389/fpls.2022.856163]
34. Long, L., Zhao, J. R., Guo, D. D., Ma, X. N., Xu, F. C., Yang, W. W., Gao, W. (2020). Identification of NHXs in Gossypium species and the positive role of GhNHX1 in salt tolerance. BMC Plant Biology, 20, 1-13. ‌ [DOI:10.1186/s12870-020-02345-z]
35. Lu, W., Guo, C., Li, X., Duan, W., Ma, C., Zhao, M., Xiao, K. (2014). Overexpression of TaNHX3, a vacuolar Na+/H+ antiporter gene in wheat, enhances salt stress tolerance in tobacco by improving related physiological processes. Plant Physiology and Biochemistry, 76, 17-28. ‌ [DOI:10.1016/j.plaphy.2013.12.013]
36. Marriboina, S., Sekhar, K. M., Subramanyam, R., Reddy, A. R. (2022). Physiological, biochemical, and root proteome networks revealed new insights into salt tolerance mechanisms in Pongamia pinnata (L.) Pierre. Frontiers in Plant Science, 12, 3253. ‌ doi: 10.3389/fpls.2021.771992. [DOI:10.3389/fpls.2021.771992]
37. Mirzadeh Vaghefi, S. S., Jalili, A. (2020). Native plants with ornamental potential for planting in urban green space of Tehran. Flower and Ornamental Plants, 4(2), 131-142 (in Persian). [DOI:10.29252/flowerjournal.4.2.131]
38. Mirzaei, S., Dastoory, M. (2018). Effect of drought and salt stress on physiological and morphological characteristics of the green covers (Phyla nodiflora L. and Frankenia thymifolia Desf.). Flower and Ornamental Plants, 3(1), 61-74 (in Persian). ‌
39. Mishra, A., Tanna, B. (2017). Halophytes: potential resources for salt stress tolerance genes and promoters. Frontiers in Plant Science, 8, 829. ‌ doi: 10.3389/fpls.2017.00829 [DOI:10.3389/fpls.2017.00829]
40. Moghaieb, R. E. A., Tanaka, N., Saneoka, H., Hussein, H. A., Yousef, S. S., Ewada, M. A. F., Fujita, K. (2000). Expression of betaine aldehyde dehydrogenase gene in transgenic tomato hairy roots leads to the accumulation of glycine betaine and contributes to the maintenance of the osmotic potential under salt stress. Soil Science and Plant Nutrition, 46(4), 873-883. ‌ [DOI:10.1080/00380768.2000.10409153]
41. Munns, R., Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review in Plant Biology, 59, 651-681. [DOI:10.1146/annurev.arplant.59.032607.092911]
42. ‌ Murray, M. G., & Thompson, W. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8(19), 4321-4326. ‌ [DOI:10.1093/nar/8.19.4321]
43. Mushke, R., Yarra, R., Kirti, P. B. (2019). Improved salinity tolerance and growth performance in transgenic sunflower plants via ectopic expression of a wheat antiporter gene (TaNHX2). Molecular Biology Reports, 46(6), 5941-5953. [DOI:10.1007/s11033-019-05028-7]
44. ‌Nakano, Y., Asada, K. (1981) Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant and Cell Physiology, 22, 867-880.
45. Niu, X., Bressan, R. A., Hasegawa, P. M., Pardo, J. M. (1995). Ion homeostasis in NaCl stress environments. Plant Physiology, 109(3), 735. ‌ [DOI:10.1104/pp.109.3.735]
46. Nefissi Ouertani, R., Arasappan, D., Ruhlman, T. A., Ben Chikha, M., Abid, G., Mejri, S., Jansen, R. K. (2022). Effects of salt stress on transcriptional and physiological responses in barley leaves with contrasting salt tolerance. International Journal of Molecular Sciences, 23(9), 5006. [DOI:10.3390/ijms23095006]
47. ‌ Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A., Tanaka, A., Nakamura, T., Hayakawa, T. (2002). Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS letters, 532(3), 279-282. ‌ [DOI:10.1016/S0014-5793(02)03679-7]
48. Qiu, Q. S. (2012). Plant and yeast NHX antiporters: Roles in membrane trafficking F. Journal of Integrative Plant Biology, 54(2), 66-72. ‌ [DOI:10.1111/j.1744-7909.2012.01097.x]
49. Sambrook, J., Russell, D. W. (2001). Molecular cloning: a laboratory manual., 3rd ed. (Cold Spring Harbor Laboratory Press: New York). ‌
50. Saxena, S.C., Kaur, H., Verma, P., Petla, B.P., Andugula, V.R., Majee, M. (2013). Osmoprotectants: Potential for Crop Improvement Under Adverse Conditions. In: Tuteja, N., Singh Gill, S. (eds) Plant Acclimation to Environmental Stress (pp 197-232). Springer, New York, NY. [DOI:10.1007/978-1-4614-5001-6_9]
51. Shabala, S., Cuin, T. A. (2008). Potassium transport and plant salt tolerance. Physiologia Plantarum, 133(4), 651-669. ‌ [DOI:10.1111/j.1399-3054.2007.01008.x]
52. Shoaf, W. T., Lium, B. W. (1976). Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnology and Oceanography, 21(6), 926-928. ‌ [DOI:10.4319/lo.1976.21.6.0926]
53. Soliman, S. O., Sallah, A. A., Alkader Y, G. E. D. (2009). Transformation and expression of Na+/H+ antiporter vacuolar AtNHX1 gene in tobacco plants under salt stress. ‌ Journal of Biotechnology, 12, 99-108.
54. Vijayvargiya, S., Kumar, A. (2011). Influence of salinity stress on plant growth and productivity: Salinity stress influences on plant growth. Lap Lambert Academic Publishers, Germany.‌
55. Wang, J., Zuo, K., Wu, W., Song, J., Sun, X., Lin, J., Tang, K. (2004). Expression of a novel antiporter gene from Brassica napus resulted in enhanced salt tolerance in transgenic tobacco plants. Biologia Plantarum, 48, 509-515. ‌ [DOI:10.1023/B:BIOP.0000047145.18014.a3]
56. Wang, B., Zhai, H., He, S., Zhang, H., Ren, Z., Zhang, D., Liu, Q. (2016). A vacuolar Na+/H+ antiporter gene, IbNHX2, enhances salt and drought tolerance in transgenic sweet potatoes. Scientia Horticulturae, 201, 153-166. [DOI:10.1016/j.scienta.2016.01.027]
57. ‌Wang, H., Ding, Q., Wang, H. (2018). A new Na+/H+ antiporter gene KvNHX1 isolated from the halophyte Kosteletzkya virginica improves salt tolerance in transgenic tobacco. Biotechnology & Biotechnological Equipment, 32(6), 1378-1386. ‌ [DOI:10.1080/13102818.2018.1522972]
58. Wu, C. A., Yang, G. D., Meng, Q. W., Zheng, C. C. (2004). The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant and Cell Physiology, 45(5), 600-607. [DOI:10.1093/pcp/pch071]
59. Wu, G. Q., Wang, J. L., Li, S. J. (2019). Genome-wide identification of Na+/H+ antiporter (NHX) genes in sugar beet (Beta vulgaris L.) and their regulated expression under salt stress. Genes, 10(5), 401. ‌ doi: 10.3390/genes10050401. [DOI:10.3390/genes10050401]
60. Xue, Z. Y., Zhi, D. Y., Xue, G. P., Zhang, H., Zhao, Y. X., Xia, G. M. (2004). Enhanced salt tolerance of transgenic wheat (Triticum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Science, 167(4), 849-859. ‌ [DOI:10.1016/j.plantsci.2004.05.034]
61. Yamaguchi, T., Apse, M. P., Shi, H., Blumwald, E. (2003). Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity. Proceedings of the National Academy of Sciences, 100(21), 12510-12515. ‌ [DOI:10.1073/pnas.2034966100]
62. Yin, X. Y., Yang, A. F., Zhang, K. W., Zhang, J. R. (2004). Production and analysis of transgenic maize with improved salt tolerance by the introduction of the AtNHX1 gene. Acta Botanica Sinica-English-Edition, 46(7), 854-861. ‌
63. Yu, J. N., Huang, J., Wang, Z. N., Zhang, J. S., Chen, S. Y. (2007). A Na+/H+ antiporter gene from wheat plays an important role in stress tolerance. Journal of Biosciences, 32, 1153-1161. ‌ [DOI:10.1007/s12038-007-0117-x]
64. Zhang, H. X., Blumwald, E. (2001). Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology, 19(8), 765-768. ‌ [DOI:10.1038/90824]
65. Zhang, H. X., Hodson, J. N., Williams, J. P., Blumwald, E. (2001). Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proceedings of the National Academy of Sciences, 98(22), 12832-12836. ‌ [DOI:10.1073/pnas.231476498]
66. Zhang, H., Liu, Y., Xu, Y., Chapman, S., Love, A. J., Xia, T. (2012). A newly isolated Na+/H+ antiporter gene, DmNHX1, confers salt tolerance when expressed transiently in Nicotiana benthamiana or stably in Arabidopsis thaliana. Plant Cell, Tissue and Organ Culture (PCTOC), 110, 189-200. ‌ [DOI:10.1007/s11240-012-0142-9]
67. Zhang, L. Q., Niu, Y. D., Huridu, H., Hao, J. F., Qi, Z., Hasi, A. (2014). Salicornia europaea L. Na+/H+ antiporter gene improves salt tolerance in transgenic alfalfa (Medicago sativa L.). Genetic and Molecular Research, 13(3), 5350-5360. ‌ [DOI:10.4238/2014.July.24.14]
68. Zhao, F. Y., Zhang, X. J., Li, P. H., Zhao, Y. X., Zhang, H. (2006). Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Molecular Breeding, 17, 341-353. ‌ [DOI:10.1007/s11032-006-9005-6]
69. Zhu, J. K. (2001). Plant salt tolerance. Trends in Plant Science, 6(2), 66-71. ‌ [DOI:10.1016/S1360-1385(00)01838-0]
70. Zörb, C., Noll, A., Karl, S., Leib, K., Yan, F., Schubert, S. (2005). Molecular characterization of Na+/H+ antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. Journal of Plant Physiology, 162(1), 55-66. ‌ [DOI:10.1016/j.jplph.2004.03.010]
71. Alemzadeh, A., Fujie, M., Usami, S., Yoshizaki, T., Oyama, K., Kawabata, T., Yamada, T. (2006). ZMVHA-B1, the gene for subunit B of vacuolar H+-ATPase from the eelgrass Zostera marina L. Can replace vma2 in a yeast null mutant. Journal of Bioscience and Bioengineering, 102(5), 390-395. ‌ [DOI:10.1263/jbb.102.390]
72. Apse, M. P., Sottosanto, J. B., Blumwald, E. (2003). Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T‐DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. The Plant Journal, 36(2), 229-239. ‌ [DOI:10.1046/j.1365-313X.2003.01871.x]
73. Ayadi, M., Martins, V., Ben Ayed, R., Jbir, R., Feki, M., Mzid, R., Hanana, M. (2020). Genome-wide identification, molecular characterization, and gene expression analyses of grapevine NHX antiporters suggest their involvement in growth, ripening, seed dormancy, and stress response. Biochemical Genetics, 58, 102-128. [DOI:10.1007/s10528-019-09930-4]
74. Bao-Yan, A. N., Yan, L. U. O., Jia-Rui, L. I., Wei-Hua, Q. I. A. O., ZHANG, X. S., Xin-Qi, G. A. O. (2008). Expression of a vacuolar Na+/H+ antiporter gene of alfalfa enhances salinity tolerance in transgenic Arabidopsis. Acta Agronomica Sinica, 34(4), 557-564. ‌ [DOI:10.1016/S1875-2780(08)60022-X]
75. Barrs, H. D., Weatherley, P. E. (1962). A re-examination of the relative turgidity technique for estimating water deficits in leaves. Australian Journal of Biological Sciences, 15(3), 413-428. [DOI:10.1071/BI9620413]
76. Bassil, E., Zhang, S., Gong, H., Tajima, H., Blumwald, E. (2019). Cation specificity of vacuolar NHX-type cation/H+ antiporters. Plant Physiology, 179(2), 616-629. ‌ [DOI:10.1104/pp.18.01103]
77. Bates, L. S., Waldren, R. A., Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205-207. ‌ [DOI:10.1007/BF00018060]
78. Blumwald, E., Aharon, G. S., Apse, M. P. (2000). Sodium transport in plant cells. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1465(1-2), 140-151. ‌ [DOI:10.1016/S0005-2736(00)00135-8]
79. Brini, F., Hanin, M., Mezghani, I., Berkowitz, G. A., Masmoudi, K. (2007). Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt and drought-stress tolerance in Arabidopsis thaliana plants. Journal of Experimental Botany, 58(2), 301-308. ‌ [DOI:10.1093/jxb/erl251]
80. Cao, D., Hou, W., Liu, W., Yao, W., Wu, C., Liu, X., Han, T. (2011). Overexpression of TaNHX2 enhances salt tolerance of 'composite' and whole transgenic soybean plants. Plant Cell, Tissue and Organ Culture (PCTOC), 107, 541-552. [DOI:10.1007/s11240-011-0005-9]
81. Chapman, H. D., Pratt, F. P. (1982). Determination of minerals by titration method. Methods of Analysis for Soils, Plants and Water, 2nd ed. Oakland, CA: Agriculture Division, California University, 169-170.
82. Chance, B., Maehly, A.C. (1955) Assay of Catalase and Peroxidase. Methods in Enzymology, 2, 764-775. [DOI:10.1016/S0076-6879(55)02300-8]
83. Chauhan, S., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D. E., Bohnert, H. J. (2000). Na+/myo‐inositol symporters and Na+/H+‐antiport in Mesembryanthemum crystallinum. The Plant Journal, 24(4), 511-522. ‌ [DOI:10.1046/j.1365-313x.2000.00903.x]
84. Chen, H. T., Xin, C. H. E. N., Wu, B. Y., Yuan, X. X., Zhang, H. M., Cui, X. Y., Liu, X. Q. (2015). Whole-genome identification and expression analysis of K+ efflux antiporter (KEA) and Na+/H+ antiporter (NHX) families under abiotic stress in soybean. Journal of Integrative Agriculture, 14(6), 1171-1183. ‌ [DOI:10.1016/S2095-3119(14)60918-7]
85. Chen, S., Wu, F., Li, Y., Qian, Y., Pan, X., Li, F., Yang, A. (2019). NtMYB4 and NtCHS1 are critical factors in the regulation of flavonoid biosynthesis and are involved in salinity responsiveness. Frontiers in Plant Science, doi: /10.3389/fpls.2019.00178. [DOI:10.3389/fpls.2019.00178]
86. Doblin, M. S., de Melis, L., Read, S., Newbigin, E. J., Bacic, A. (2000). The cloning of two putative ß-glucan synthase genes from pollen tubes of Nicotiana alata. Plant Biology ‌(Abstract no. 310).
87. Dong, J., Liu, C., Wang, Y., Zhao, Y., Ge, D., Yuan, Z. (2021). Genome-wide identification of the NHX gene family in Punica granatum L. and their expressional patterns under salt stress. Agronomy, 11(2), 264. ‌ [DOI:10.3390/agronomy11020264]
88. Fukuda, A., Nakamura, A., Tanaka, Y. (1999). Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1446(1-2), 149-155. ‌ [DOI:10.1016/S0167-4781(99)00065-2]
89. Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P., Alper, S. L., Fink, G. R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences, 96(4), 1480-1485. ‌ [DOI:10.1073/pnas.96.4.1480]
90. Habibi, F., Ramezanian, A. (2017). Vacuum infiltration of putrescine enhances bioactive compounds and maintains the quality of blood orange during cold storage. Food Chemistry, 227, 1-8. ‌ [DOI:10.1016/j.foodchem.2017.01.057]
91. Hasegawa, P. M., Bressan, R. A., Zhu, J. K., Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annual Review of Plant Biology, 51(1), 463-499. [DOI:10.1146/annurev.arplant.51.1.463]
92. ‌ Himabindu, Y., Chakradhar, T., Reddy, M. C., Kanygin, A., Redding, K. E., Chandrasekhar, T. (2016). Salt-tolerant genes from halophytes are potential key players of salt tolerance in glycophytes. Environmental and Experimental Botany, 124, 39-63. ‌ [DOI:10.1016/j.envexpbot.2015.11.010]
93. Jaquinod, M., Villiers, F., Kieffer-Jaquinod, S., Hugouvieux, V., Bruley, C., Garin, J., Bourguignon, J. (2007). A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Molecular & Cellular Proteomics, 6(3), 394-412. ‌ [DOI:10.1074/mcp.M600250-MCP200]
94. Jha, B., Mishra, A., Jha, A., Joshi, M. (2013). Developing transgenic Jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS One, 8(8), e71136. ‌ [DOI:10.1371/annotation/89bc2c6f-2799-4a5b-9f57-8e2fa3e14fc9]
95. Khan, M. S., Ahmad, D., Khan, M. A. (2015). Trends in genetic engineering of plants with (Na+/H+) antiporters for salt stress tolerance. Biotechnology & Biotechnological Equipment, 29(5), 815-825. ‌ [DOI:10.1080/13102818.2015.1060868]
96. Knapp, S., Chase, M. W., Clarkson, J. J. (2004). Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon, 53(1), 73-82. ‌ [DOI:10.2307/4135490]
97. Lan, T., Duan, Y., Wang, B., Zhou, Y., Wu, W. (2011). Molecular cloning and functional characterization of a Na+/H+ antiporter gene from halophyte Spartina anglica. Turkish Journal of Agriculture and Forestry, 35(5), 535-543. ‌ [DOI:10.3906/tar-1003-2]
98. Leidi, E. O., Barragán, V., Rubio, L., El‐Hamdaoui, A., Ruiz, M. T., Cubero, B., Fernandez, J., Berresan, R., Quintero, F., Pardo, J. M. (2010). The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomatoes. The Plant Journal, 61(3), 495-506. [DOI:10.1111/j.1365-313X.2009.04073.x]
99. ‌ Li, J., Jiang, G., Huang, P., Ma, J., Zhang, F. (2007). Overexpression of the Na+/H+ antiporter gene from Suaeda salsa confers cold and salt tolerance to transgenic Arabidopsis thaliana. Plant cell, Tissue and Organ Culture, 90, 41-48. ‌ [DOI:10.1007/s11240-007-9246-z]
100. Li, T., Zhang, Y., Liu, H., Wu, Y., Li, W., Zhang, H. (2010). Stable expression of Arabidopsis vacuolar Na+/H+ antiporter gene AtNHX1, and salt tolerance in transgenic soybean for over six generations. Chinese Science Bulletin, 55, 1127-1134. ‌ [DOI:10.1007/s11434-010-0092-8]
101. Li, W., Zhao, F. A., Fang, W., Xie, D., Hou, J., Yang, X., Lv, S. (2015). Identification of early salt stress-responsive proteins in seedling roots of upland cotton (Gossypium hirsutum L.) employing the iTRAQ-based proteomic technique. Frontiers in Plant Science, 6, 732. ‌ doi: 10.3389/fpls.2015.00732. [DOI:10.3389/fpls.2015.00732]
102. Li, N., Wang, X., Ma, B., Du, C., Zheng, L., Wang, Y. (2017). Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte Reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. Journal of Plant Physiology, 218, 109-120. ‌ [DOI:10.1016/j.jplph.2017.07.015]
103. Li, C., Zhao, Y., Qi, Y., Duan, C., Zhang, H., Zhang, Q. (2022). The Eutrema EsMYB90 gene improves the growth and antioxidant capacity of transgenic wheat under salinity stress. Frontiers in Plant Science, 1126. doi: 10.3389/fpls.2022.856163. ‌ [DOI:10.3389/fpls.2022.856163]
104. Long, L., Zhao, J. R., Guo, D. D., Ma, X. N., Xu, F. C., Yang, W. W., Gao, W. (2020). Identification of NHXs in Gossypium species and the positive role of GhNHX1 in salt tolerance. BMC Plant Biology, 20, 1-13. ‌ [DOI:10.1186/s12870-020-02345-z]
105. Lu, W., Guo, C., Li, X., Duan, W., Ma, C., Zhao, M., Xiao, K. (2014). Overexpression of TaNHX3, a vacuolar Na+/H+ antiporter gene in wheat, enhances salt stress tolerance in tobacco by improving related physiological processes. Plant Physiology and Biochemistry, 76, 17-28. ‌ [DOI:10.1016/j.plaphy.2013.12.013]
106. Marriboina, S., Sekhar, K. M., Subramanyam, R., Reddy, A. R. (2022). Physiological, biochemical, and root proteome networks revealed new insights into salt tolerance mechanisms in Pongamia pinnata (L.) Pierre. Frontiers in Plant Science, 12, 3253. ‌ doi: 10.3389/fpls.2021.771992. [DOI:10.3389/fpls.2021.771992]
107. Mirzadeh Vaghefi, S. S., Jalili, A. (2020). Native plants with ornamental potential for planting in urban green space of Tehran. Flower and Ornamental Plants, 4(2), 131-142 (in Persian). [DOI:10.29252/flowerjournal.4.2.131]
108. Mirzaei, S., Dastoory, M. (2018). Effect of drought and salt stress on physiological and morphological characteristics of the green covers (Phyla nodiflora L. and Frankenia thymifolia Desf.). Flower and Ornamental Plants, 3(1), 61-74 (in Persian). ‌
109. Mishra, A., Tanna, B. (2017). Halophytes: potential resources for salt stress tolerance genes and promoters. Frontiers in Plant Science, 8, 829. ‌ doi: 10.3389/fpls.2017.00829 [DOI:10.3389/fpls.2017.00829]
110. Moghaieb, R. E. A., Tanaka, N., Saneoka, H., Hussein, H. A., Yousef, S. S., Ewada, M. A. F., Fujita, K. (2000). Expression of betaine aldehyde dehydrogenase gene in transgenic tomato hairy roots leads to the accumulation of glycine betaine and contributes to the maintenance of the osmotic potential under salt stress. Soil Science and Plant Nutrition, 46(4), 873-883. ‌ [DOI:10.1080/00380768.2000.10409153]
111. Munns, R., Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review in Plant Biology, 59, 651-681. [DOI:10.1146/annurev.arplant.59.032607.092911]
112. ‌ Murray, M. G., & Thompson, W. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8(19), 4321-4326. ‌ [DOI:10.1093/nar/8.19.4321]
113. Mushke, R., Yarra, R., Kirti, P. B. (2019). Improved salinity tolerance and growth performance in transgenic sunflower plants via ectopic expression of a wheat antiporter gene (TaNHX2). Molecular Biology Reports, 46(6), 5941-5953. [DOI:10.1007/s11033-019-05028-7]
114. ‌Nakano, Y., Asada, K. (1981) Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant and Cell Physiology, 22, 867-880.
115. Niu, X., Bressan, R. A., Hasegawa, P. M., Pardo, J. M. (1995). Ion homeostasis in NaCl stress environments. Plant Physiology, 109(3), 735. ‌ [DOI:10.1104/pp.109.3.735]
116. Nefissi Ouertani, R., Arasappan, D., Ruhlman, T. A., Ben Chikha, M., Abid, G., Mejri, S., Jansen, R. K. (2022). Effects of salt stress on transcriptional and physiological responses in barley leaves with contrasting salt tolerance. International Journal of Molecular Sciences, 23(9), 5006. [DOI:10.3390/ijms23095006]
117. ‌ Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A., Tanaka, A., Nakamura, T., Hayakawa, T. (2002). Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS letters, 532(3), 279-282. ‌ [DOI:10.1016/S0014-5793(02)03679-7]
118. Qiu, Q. S. (2012). Plant and yeast NHX antiporters: Roles in membrane trafficking F. Journal of Integrative Plant Biology, 54(2), 66-72. ‌ [DOI:10.1111/j.1744-7909.2012.01097.x]
119. Sambrook, J., Russell, D. W. (2001). Molecular cloning: a laboratory manual., 3rd ed. (Cold Spring Harbor Laboratory Press: New York). ‌
120. Saxena, S.C., Kaur, H., Verma, P., Petla, B.P., Andugula, V.R., Majee, M. (2013). Osmoprotectants: Potential for Crop Improvement Under Adverse Conditions. In: Tuteja, N., Singh Gill, S. (eds) Plant Acclimation to Environmental Stress (pp 197-232). Springer, New York, NY. [DOI:10.1007/978-1-4614-5001-6_9]
121. Shabala, S., Cuin, T. A. (2008). Potassium transport and plant salt tolerance. Physiologia Plantarum, 133(4), 651-669. ‌ [DOI:10.1111/j.1399-3054.2007.01008.x]
122. Shoaf, W. T., Lium, B. W. (1976). Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnology and Oceanography, 21(6), 926-928. ‌ [DOI:10.4319/lo.1976.21.6.0926]
123. Soliman, S. O., Sallah, A. A., Alkader Y, G. E. D. (2009). Transformation and expression of Na+/H+ antiporter vacuolar AtNHX1 gene in tobacco plants under salt stress. ‌ Journal of Biotechnology, 12, 99-108.
124. Vijayvargiya, S., Kumar, A. (2011). Influence of salinity stress on plant growth and productivity: Salinity stress influences on plant growth. Lap Lambert Academic Publishers, Germany.‌
125. Wang, J., Zuo, K., Wu, W., Song, J., Sun, X., Lin, J., Tang, K. (2004). Expression of a novel antiporter gene from Brassica napus resulted in enhanced salt tolerance in transgenic tobacco plants. Biologia Plantarum, 48, 509-515. ‌ [DOI:10.1023/B:BIOP.0000047145.18014.a3]
126. Wang, B., Zhai, H., He, S., Zhang, H., Ren, Z., Zhang, D., Liu, Q. (2016). A vacuolar Na+/H+ antiporter gene, IbNHX2, enhances salt and drought tolerance in transgenic sweet potatoes. Scientia Horticulturae, 201, 153-166. [DOI:10.1016/j.scienta.2016.01.027]
127. ‌Wang, H., Ding, Q., Wang, H. (2018). A new Na+/H+ antiporter gene KvNHX1 isolated from the halophyte Kosteletzkya virginica improves salt tolerance in transgenic tobacco. Biotechnology & Biotechnological Equipment, 32(6), 1378-1386. ‌ [DOI:10.1080/13102818.2018.1522972]
128. Wu, C. A., Yang, G. D., Meng, Q. W., Zheng, C. C. (2004). The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant and Cell Physiology, 45(5), 600-607. [DOI:10.1093/pcp/pch071]
129. Wu, G. Q., Wang, J. L., Li, S. J. (2019). Genome-wide identification of Na+/H+ antiporter (NHX) genes in sugar beet (Beta vulgaris L.) and their regulated expression under salt stress. Genes, 10(5), 401. ‌ doi: 10.3390/genes10050401. [DOI:10.3390/genes10050401]
130. Xue, Z. Y., Zhi, D. Y., Xue, G. P., Zhang, H., Zhao, Y. X., Xia, G. M. (2004). Enhanced salt tolerance of transgenic wheat (Triticum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Science, 167(4), 849-859. ‌ [DOI:10.1016/j.plantsci.2004.05.034]
131. Yamaguchi, T., Apse, M. P., Shi, H., Blumwald, E. (2003). Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity. Proceedings of the National Academy of Sciences, 100(21), 12510-12515. ‌ [DOI:10.1073/pnas.2034966100]
132. Yin, X. Y., Yang, A. F., Zhang, K. W., Zhang, J. R. (2004). Production and analysis of transgenic maize with improved salt tolerance by the introduction of the AtNHX1 gene. Acta Botanica Sinica-English-Edition, 46(7), 854-861. ‌
133. Yu, J. N., Huang, J., Wang, Z. N., Zhang, J. S., Chen, S. Y. (2007). A Na+/H+ antiporter gene from wheat plays an important role in stress tolerance. Journal of Biosciences, 32, 1153-1161. ‌ [DOI:10.1007/s12038-007-0117-x]
134. Zhang, H. X., Blumwald, E. (2001). Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology, 19(8), 765-768. ‌ [DOI:10.1038/90824]
135. Zhang, H. X., Hodson, J. N., Williams, J. P., Blumwald, E. (2001). Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proceedings of the National Academy of Sciences, 98(22), 12832-12836. ‌ [DOI:10.1073/pnas.231476498]
136. Zhang, H., Liu, Y., Xu, Y., Chapman, S., Love, A. J., Xia, T. (2012). A newly isolated Na+/H+ antiporter gene, DmNHX1, confers salt tolerance when expressed transiently in Nicotiana benthamiana or stably in Arabidopsis thaliana. Plant Cell, Tissue and Organ Culture (PCTOC), 110, 189-200. ‌ [DOI:10.1007/s11240-012-0142-9]
137. Zhang, L. Q., Niu, Y. D., Huridu, H., Hao, J. F., Qi, Z., Hasi, A. (2014). Salicornia europaea L. Na+/H+ antiporter gene improves salt tolerance in transgenic alfalfa (Medicago sativa L.). Genetic and Molecular Research, 13(3), 5350-5360. ‌ [DOI:10.4238/2014.July.24.14]
138. Zhao, F. Y., Zhang, X. J., Li, P. H., Zhao, Y. X., Zhang, H. (2006). Co-expression of the Suaeda salsa SsNHX1 and Arabidopsis AVP1 confer greater salt tolerance to transgenic rice than the single SsNHX1. Molecular Breeding, 17, 341-353. ‌ [DOI:10.1007/s11032-006-9005-6]
139. Zhu, J. K. (2001). Plant salt tolerance. Trends in Plant Science, 6(2), 66-71. ‌ [DOI:10.1016/S1360-1385(00)01838-0]
140. Zörb, C., Noll, A., Karl, S., Leib, K., Yan, F., Schubert, S. (2005). Molecular characterization of Na+/H+ antiporters (ZmNHX) of maize (Zea mays L.) and their expression under salt stress. Journal of Plant Physiology, 162(1), 55-66. ‌ [DOI:10.1016/j.jplph.2004.03.010]
Send email to the article author

Add your comments about this article
Your username or Email:

CAPTCHA



XML   Persian Abstract   Print


Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Khorsandy S, Ehsani P, Jowkar A, Alemzadeh A. The eelgrass Zostera marina antiporter gene (ZmNa+/H+) confers salt stress tolerance to ornamental tobacco (Nicotiana alata). FOP 2023; 8 (1) :183-200
URL: http://flowerjournal.ir/article-1-268-en.html


Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Volume 8, Issue 1 (Spring and Summer 2023) Back to browse issues page
گل و گیاهان زینتی Flower and Ornamental Plants
Persian site map - English site map - Created in 0.05 seconds with 37 queries by YEKTAWEB 4660