A wheat superoxide dismutase gene TaSOD2 enhances salt resistance through modulating redox homeostasis by promoting NADPH oxidase activity

Plant Molecular Biology

Volumn 91, Issue 1-2, 2016, Pages 115-130

  Wang, Mengcheng ^a   Zhao, Xin ^a   Xiao, Zhen ^a   Yin, Xunhao ^a   Xing, Tian ^a   Xia, Guangmin ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

NADPH oxidase; Redox homeostasis; ROS; Salinity resistance; Superoxide dismutase; Wheat

Indexed keywords

HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM CHLORIDE; SUPEROXIDE DISMUTASE;

AMINO ACID SEQUENCE; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; OXIDATION REDUCTION REACTION; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; WHEAT;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; HYDROGEN PEROXIDE; NADPH OXIDASE; OXIDATION-REDUCTION; PHYLOGENY; REACTIVE OXYGEN SPECIES; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; TRITICUM;

EID: 84957648350     PISSN: 01674412     EISSN: 15735028     Source Type: Journal    
DOI: 10.1007/s11103-016-0446-y     Document Type: Article

References (62)

1. Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054
2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
3. Asselbergh B, Curvers K, França SC, Audenaert K, Vuylsteke M, Van Breusegem F, Höfte M (2007) Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol 144:1863–1877
4. Attia H, Karray N, Msilini N, Lachaâl M (2011) Effect of salt stress on gene expression of superoxide dismutases and copper chaperone in Arabidopsis thaliana. Biol Plant 55:159–163
5. Baxter A, Mittler R, Suzuki N (2013) ROS as key players in plant stress signalling. J Exp Bot ert375
6. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
8. Chen Z, Pan YH, An LY, Yang WJ, Xu LG, Zhu C (2013) Heterologous expression of a halophilic archaeon manganese superoxide dismutase enhances salt tolerance in transgenic rice. Russ J Plant Physiol 60:359–366
9. +-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
11. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc Natl Acad Sci USA 83:3811–3815
12. Evans NH, McAinsh MR, Hetherington AM, Knight MR (2005) ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41:615–626
13. Foreman J et al (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446
14. Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18
15. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112
16. Gibon Y, Larher F (1997) Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium. Anal Biochem 251:153–157
17. Gill SS et al (2015) Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res 22:10375–10394
18. Grace SC, Logan BA (1996) Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. Plant Physiol 112:1631–1640
19. Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791
20. Hao FS, Wang XC, Chen J (2006) Involvement of plasma-membrane NADPH oxidase in nickel-induced oxidative stress in roots of wheat seedlings. Plant Sci 170:151–158
21. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
22. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
23. Kwak JM et al (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633
24. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
25. Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51:185–197
26. Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 60:3221–3238
27. Liu C, Li S, Wang M, Xia G (2012) A transcriptomic analysis reveals the nature of salinity tolerance of a wheat introgression line. Plant Mol Biol 78:159–169
28. Liu S, Liu S, Wang M, Wei T, Meng C, Wang M, Xia G (2014) A wheat SIMILAR TO RCD-ONE gene enhances seedling growth and abiotic stress resistance by modulating redox homeostasis and maintaining genomic integrity. Plant Cell 26:164–180
29. −ΔΔCT Method. Methods 25:402–408
30. + homeostasis in Arabidopsis under salt stress. J Exp Bot err280
31. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15
32. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittle R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:ra45
33. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
34. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
35. Mittler R et al (2011) ROS signaling: the new wave? Trends in Plant Sci 16:300–309
36. Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase scavenges hydrogen peroxide photoproduced: photoreduction of monodehydroascorbate radical. Kluwer, Dordrecht
37. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
38. Noctor G, Foyer CH (2000) Homeostasis of adenylate status during photosynthesis in a fluctuating environment. J Exp Bot 51:347–356
39. Okamura M (1980) An improved method for determination of l-ascorbic acid and l-dehydroascorbic acid in blood plasma. Clin Chim Acta 103:259–268
40. Peng Z, Wang M, Li F, Lv H, Li C, Xia G (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteom 8:2676–2686
41. Pitcher LH, Brennan E, Hurley A, Dunsmuir P, Tepperman JM, Zilinskas BA (1991) Overproduction of petunia copper/zinc superoxide dismutase does not confer ozone tolerance in transgenic tobacco. Plant Physiol 97:452–455
42. Posé D et al (2009) Identification of the Arabidopsis dry2/sqe1-5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species. Plant J 59:63–76
43. Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165
44. Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290
45. Sebastiani M, Giordano C, Nediani C, Travaglini C, Borchi E, Zani M, Feccia M, Mancini M, Petrozza V, Cossarizza A, Gallo P, Taylor RW, d’Amati G (2007) Induction of mitochondrial biogenesis is a maladaptive mechanism in mitochondrial cardiomyopathies. J Am Coll Cardiol 50:1362–1369
46. Sen Gupta A, Webb RP, Holaday AS, Allen RD (1993) Over-expression of superoxide dismutase protects plants from oxidative stress: induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants. Plant Physiol 103:1067–1073
47. Sierla M, Rahikainen M, Salojärvi J, Kangasjärvi J, Kangasjärvi S (2013) Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid Redox Sign 18:2220–2239
48. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699
49. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell Environ 35:259–270
50. Suzuki N, Miller G, Salazar C, Mondal HA, Shulaev E, Cortes DF, Shuman JL, Luo X, Shah J, Schlauch K, Shulaev V, Mittler R (2013) Temporal–spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25:3553–3569
51. Takahashi MA, Asada K (1983) Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Arch Biochem Biophys 226:558–566
52. 2 stress. Mol Biol Cell 24:2876–2884
53. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403
54. Wang MC, Peng ZY, Li CL, Li F, Liu C, Xia GM (2008) Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8:1470–1489
55. Wang X et al (2015) The plasma membrane NADPH oxidase OsRbohA plays a crucial role in developmental regulation and drought-stress response in rice. Physiol Plant. doi:10.1111/ppl.12389
56. Wi SJ, Ji NR, Park KY (2012) Synergistic biosynthesis of biphasic ethylene and reactive oxygen species in response to hemibiotrophic Phytophthora parasitica in tobacco plants. Plant Physiol 159:251–265
57. Xia GM (2009) Progress of chromosome engineering mediated by asymmetric somatic hybridization. J Genet Genomics 36:547–556
58. Xia GM, Xiang FN, Zhou AF, Wang H, Chen HM (2003) Asymmetric somatic hybridization between wheat (Triticum aestivum L.) and Agropyron elongatum (Host) Nevishi. Theor Appl Genet 107:299–305
59. Xie YJ et al (2011) Evidence of Arabidopsis salt acclimation induced by upregulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292
60. Yoo S-D, Cho Y-H, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Prot 2:1565–1572
61. 2 and NO production and antioxidant defences. Plant, Cell Environ 32:509–519
62. Zhao TJ, Zhao SY, Chen HM, Zhao QZ, Hu ZM, Hou BK, Xia GM (2006) Transgenic wheat progeny resistant to powdery mildew generated by Agrobacterium inoculum to the basal portion of wheat seedling. Plant Cell Rep 25:1199–1204