Overexpression of copper/zinc superoxide dismutase from mangrove Kandelia candel in tobacco enhances salinity tolerance by the reduction of reactive oxygen species in chloroplast

Frontiers in Plant Science

Volumn 6, Issue JAN, 2015, Pages 1-13

  Jing, Xiaoshu ^a   Hou, Peichen ^b   Lu, Yanjun ^a   Deng, Shurong ^a   Li, Niya ^c   Zhao, Rui ^a   Sun, Jian ^d   Wang, Yang ^a   Han, Yansha ^a   Lang, Tao ^a   Ding, Mingquan ^e   Shen, Xin ^a   Chen, Shaoliang ^a  

^a BEIJING FORESTRY UNIVERSITY   (China)

^b NATIONAL ENGINEERING RESEARCH CENTER FOR INFORMATION TECHNOLOGY IN AGRICULTURE   (China)

^c HAINAN NORMAL UNIVERSITY   (China)

^d JIANGSU NORMAL UNIVERSITY   (China)

^e ZHEJIANG A F UNIVERSITY   (China)

Author keywords

Catalase; Hydrogen peroxide; Kandelia candel; Na+ flux; Salt; Superoxide anion; Superoxide dismutase

Indexed keywords

KANDELIA CANDEL; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

EID: 84922326846     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00023     Document Type: Article

References (53)

1. Aebi, H. (1984). Catalase in vitro. Meth. Enzymol. 105, 121-126.
2. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399. doi: 10.1146/annurev.arplant.55.03-1903.141701
3. Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. PlantBiol. 50, 601-639. doi: 10.1146/annurev.arplant.50.1.601
4. Beauchamp, C., and Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44, 276-287. doi: 10.1016/00032697-(71)90370-8
5. Bowler, C., Montagu, M. V., and Inze, D. (1992). Superoxide dismutase and stress tolerance. Ann. Rev. PlantBiol. 43, 83-116.
6. Chen, S., andPolle, A. (2010). Salinity tolerance of Populus. PlantBiol. 12, 317-333. doi: 10.1111/j.1438-8677.2009.00301.x
7. Cuin, T. A., Bose, J., Stefano, G., Jha, D., Tester, M., Mancuso, S., et al. (2011). Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods. Plant Cell Environ. 34, 947-961. doi: 10.1111/j.1365-3040.2011.02296.x
8. Desikan, R., Soheila, A. H., Hancock, J. T., and Neill, S. J. (2001). Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 127, 159-172. doi: 10.1104/pp.127.1.159
9. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C. H., et al. (2003). Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15, 1212-1226. doi: 10.1105/tpc.009464
10. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971. doi: 10.1038/nprot.2007.131
11. Emanuelsson, O., Nielsen, H., and Heijne, G. V. (1999). ChloroP, a neural network- based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8, 978-984.
12. Fridovich, I. (1995). Superoxide radical and superoxide dismutases. Annu. Rev. PlantBiochem. 64, 97-112. doi: 10.1146/annurev.biochem.64.1.97
13. Giannopolitis, C. N., and Ries, S. K. (1977). Superoxide dismutases II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol. 59, 315-318. doi: 10.1104/pp.59.2.315
14. Gutteridge, J., and Halliwell, B. (2010). Antioxidants: molecules, medicines, and myths. Biochem. Biophy. Res. Commun. 393, 561-564. doi: 10.1016/j.bbrc.2010.02.071
15. Han, Y., Wang, W., Sun, J., Ding, M., Zhao, R., Deng, S., et al. (2013). Populus euphratica XTH overexpression enhances salinity tolerance by the development of leaf succulence in transgenic tobacco plants. J. Exp. Bot. 64, 4225-4238. doi: 10.1093/jxb/ert229
16. Heath, R. L., and Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophy. 125, 189-198. doi: 10.1016/0003-9861(68)90654-1
17. Hoagland, D. R., and Arnon, D. I. (1950). The Water-Culture Method for Growing Plants Without Soil. Circular 347, 39. Berkeley, CA: California Agricultural Experiment Station.
18. Horsch, R. B., Fry, J. E., Hoffmann, N. L., Eichholtz, D., Rogers, S. A., and Fraley, R. T. (1985). A simple and general method for transferring genes into plants. Science 227, 1229-1231. doi: 10.1126/science.227.4691.1229
19. Hou, P. (2010). Microarray Analysis of Gene Expression Patterns and Putative Functions of Differentially Expressed Genes in Mangrove Kandelia Candel Under High-Salinity Stress. Ph.D. dissertation, 55-62, Beijing Forestry University, Beijing.
20. Huang, C. H., Kuo, W. Y., Weiss, C., and Jinn, T. L. (2012). Copper chaperone- dependent and-independent activation of three copper-zinc superoxide dismu- tase homologs localized in different cellular compartments in Arabidopsis. Plant Physiol. 158, 737-746. doi: 10.1104/pp.111
21. Jakob, B., and Heber, U. (1996). Photoproduction and detoxification of hydroxyl radicals in chloroplasts and leaves and relation to photoinactivation of photosystems I and II. PlantCell Physiol. 37, 629-635.
22. Kliebenstein, D. J., Monde, R. A., and Last, R. L. (1998). Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. PlantPhysiol. 118, 637-650. doi: 10.1104/pp.118.2.637
23. Lang, T., Sun, H., Li, N., Lu, Y., Shen, Z., Jing, X., et al. (2014). Multiple signaling networks of extracellular ATP, hydrogen peroxide, calcium, and nitric oxide in the mediation of root ion fluxes in secretor and non-secretor mangroves under salt stress. Aquat. Bot. 119, 33-43. doi: 10.1016/j.aquabot.2014.06.009
24. Li, N., Chen, S., Zhou, X., Li, C., Shao, J., Wang, R., et al. (2008). Effect of NaCl on photosynthesis, salt accumulation and ion compartmentation in two mangrove species, Kandelia candel and Bruguiera gymnorhiza. Aquat. Bot. 88, 303-310. doi: 10.1016/j.aquabot.2007.12.003
25. Li, N. (2009). Regulation of Ionic and Reactive Oxygen Species Homeostasis in Seedlings of Two Mangrove and the Relevance to Salinity. Ph.D. dissertation, 69-76, Beijing Forestry University, Beijing.
26. Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth. Enzymol. 148, 350-382.
27. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-AACt method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
28. Lu, Y., Li, N., Sun, J., Hou, P., Jing, X., Zhu, H., et al. (2013). Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non- secretor mangrove species subjected to NaCl stress. TreePhysiol. 33, 81-95. doi: 10.1093/treephys/tps119
29. Maxwell, K., andJohnson, G. N. (2000). Chlorophyll fluorescence-apractical guide. J. Exp. Bot. 51, 659-668. doi: 10.1093/jexbot/51.345.659
30. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497. doi: 10.1111/j.1399-3054.1962.tb08052.x
31. Nakano, Y., and Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate- specific peroxidase in spinach chloroplasts. Plant CellPhysiol. 22, 867-880.
32. Payton, P., Webb, R., Kornyeyev, D., Allen, R., and Holaday, A. S. (2001). Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity. J. Exp. Bot. 52, 2345-2354. doi: 10.1093/jexbot/52.365.2345
33. Polle, A., and Chen, S. (2014). On the saltyside oflife: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant Cell Environ. doi: 10.1111/pce.12440. [Epub ahead ofprint].
34. Prashanth, S. R., Sadhasivam, V., and Parida, A. (2008). Over expression ofcytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res. 281-291. doi: 10.1007/s11248-007-9099-6
35. Ramirez, L., Bartoli, C. G., and Lamattina, L. (2013). Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency. J. Exp. Bot. 64, 3169-3178. doi: 10.1093/jxb/ert153
36. Shen, Z., Ding, M., Sun, J., Deng, S., Zhao, R., Wang, M., et al. (2013). Overexpression of PeHSF mediates leaf ROS homeostasis in transgenic tobacco lines grownunder saltstressconditions. PlantCellTiss. Org. Cult. 115,299-308. doi: 10.1007/s11240-013-0362-7
37. Stepien, P., and Johnson, G. N. (2009). Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol. 149, 1154-1165. doi: 10.1104/pp.108
38. Sun, J., Chen, S., Dai, S., Wang, R., Li, N., Shen, X., et al. (2009a). NaCl- induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol. 149, 1141-1153. doi: 10.1104/pp.108
39. Sun, J., Dai, S., Wang, R., Chen, S., Li, N., Zhou, X., et al. (2009b). Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance. Tree Physiol. 29, 1175-1186. doi: 10.1093/treephys/tpp04
40. Sun, J., Li, L., Liu, M., Wang, M., Ding, M., Deng, S., et al. (2010a). Hydrogen peroxide and nitric oxide mediate K+/Na+ homeostasis and antioxidant defense in NaCl-stressed callus cells of two contrasting poplars. PlantCell Tiss. Org. Cult. 103, 205-215. doi: 10.1007/s11240-010-9768-7
41. Sun, J., Wang, M. J., Ding, M. Q., Deng, S. R., Liu, M. Q., Lu, C. F., et al. (2010b). H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells. PlantCellEnviron. 33, 943-958. doi: 10.1111/j.1365-3040.2010.02118.x
42. Sun, J., Zhang, X., Deng, S., Zhang, C., Wang, M., Ding, M., et al. (2012). Extracellular ATP signaling is mediated by H2O2 and cytosolic Ca2+ in the salt response of Populus euphratica cells. PLoS ONE 7:e53136. doi: 10.1371/jour-nal.pone.0053136
43. Thordal-Christensen, H., Zhang, Z., Wei, Y., and Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction. Plant J. 11, 1187-1194. doi: 10.1046/j.1365-313X.1997.11061187.x
44. Tseng, M. J., Liu, C. W., and Yiu, J. C. (2007). Enhanced tolerance to sulfur dioxide and salt stress of transgenic Chinese cabbage plants expressing both superoxide dismutase and catalase in chloroplasts. PlantPhysiol. Biochem. 45, 822-833. doi: 10.1016/j.plaphy.2007.07.011
45. Volkov, V., Wang, B., Dominy, P. J., Fricke, W., and Amtmann, A. (2004). Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ. 27, 1-14. doi: 10.1046/j.0016-8025.2003.01116.x
46. Vranova, E., Inze, D., and Van Breusegem, F. (2002). Signal transduction during oxidativestress. J. Exp. Bot. 53, 1227-1236. doi: 10.1093/jexbot/53.372.1227
47. Wan, C. Y., and Wilkins, T. A. (1994). A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal. Biochem. 223, 7-12. doi: 10.1006/abio.1994.1538
48. Wang, L., Liang, W., Xing, J., Tan, F., Chen, Y., Huang, L., et al. (2013). Dynamics of chloroplast proteome in salt-stressed mangrove Kandelia candel (L.) Druce. J. ProteomeRes.12, 5124-5136. doi: 10.1021/pr4006469
49. Wang, L., Liu, X., Liang, M., Tan, F., Liang, W., Chen, Y., et al. (2014). Proteomic analysis of salt-responsive proteins in the leaves of mangrove Kandelia candel during short-term stress. PLoS ONE 9:e83141. doi: 10.1371/jour-nal.pone.0083141
50. Wang, R., Chen, S., Deng, L., Fritz, E., Huttermann, A., and Polle, A. (2007). Leaf photosynthesis, fluorescence response to salinity and the relevance to chloro- plast salt compartmentation and anti-oxidative stress in two poplars. Trees 21, 581-591. doi: 10.1007/s00468-007-0154-y
51. Wang, R., Chen, S., Zhou, X., Shen, X., Deng, L., Zhu, H., et al. (2008). Ionic homeostasis and reactive oxygen species control in leaves and xylem sap of two poplars subjected to NaCl stress. Tree Physiol. 28, 947-957. doi: 10.1093/treep-hys/28.6.947
52. Wellburn, A. R. (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, usingvarious solvents with spectrophotometers of different resolution. J. PlantPhysiol. 144, 307-313. doi: 10.1016/S0176-1617(11)81192-2
53. Yoo, S. D., Cho, Y. H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protoc. 2, 1565-1572. doi: 10.1038/nprot.2007.199