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BioMed Research International
Volume 2017, Article ID 4049534, 15 pages
https://doi.org/10.1155/2017/4049534
Research Article

Overexpression of CaAPX Induces Orchestrated Reactive Oxygen Scavenging and Enhances Cold and Heat Tolerances in Tobacco

1Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Zhejiang Provincial Key Laboratory of Tree Breeding, Hangzhou, Zhejiang 311400, China
2Lianyungang Academy of Agricultural Sciences, Flower Research Center, Lianyungang, Jiangsu 222000, China
3School of Marine Sciences, Ningbo University, Ningbo, Zhejiang 315211, China
4College of Horticulture and Landscape Architecture, Hunan Agricultural University, Changsha, Hunan 410128, China

Correspondence should be addressed to Hengfu Yin; nc.ca.sbis@niyfh, Libo He; ten.uanuh@obileh, and Jiyuan Li; moc.621@il_nauyij

Received 7 September 2016; Accepted 6 February 2017; Published 13 March 2017

Academic Editor: Atanas Atanassov

Copyright © 2017 Jiangying Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. S. Karpinski, G. Wingsle, B. Karpinska, and J. Hallgren, “Low-temperature stress and antioxidant defense mechanisms in higher plants,” in Oxidative Stress in Plants, pp. 69–103, Taylor & Francis, 2002. View at Google Scholar
  2. N. Suzuki and R. Mittler, “Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction,” Physiologia Plantarum, vol. 126, no. 1, pp. 45–51, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. R. D. Allen, “Dissection of oxidative stress tolerance using transgenic plants,” Plant Physiology, vol. 107, no. 4, pp. 1049–1054, 1995. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Asada, “The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons,” Annual Review of Plant Biology, vol. 50, pp. 601–639, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Mittler, S. Vanderauwera, M. Gollery, and F. Van Breusegem, “Reactive oxygen gene network of plants,” Trends in Plant Science, vol. 9, no. 10, pp. 490–498, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Mittler, “Abiotic stress, the field environment and stress combination,” Trends in Plant Science, vol. 11, no. 1, pp. 15–19, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Azarabadi, H. Abdollahi, M. Torabi, Z. Salehi, and J. Nasiri, “ROS generation, oxidative burst and dynamic expression profiles of ROS-scavenging enzymes of superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX) in response to Erwinia amylovora in pear (Pyrus communis L),” European Journal of Plant Pathology, vol. 147, no. 2, pp. 279–294, 2017. View at Publisher · View at Google Scholar · View at Scopus
  8. L. Pnueli, H. Liang, M. Rozenberg, and R. Mittler, “Growth suppression, altered stomatal responses, and augmented induction of heat shock proteins in cytosolic ascorbate peroxidase (Apx1)-deficient Arabidopsis plants,” Plant Journal, vol. 34, no. 2, pp. 187–203, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. W. R. Swindell, M. Huebner, and A. P. Weber, “Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways,” BMC Genomics, vol. 8, article no. 125, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Baxter, R. Mittler, and N. Suzuki, “ROS as key players in plant stress signalling,” Journal of Experimental Botany, vol. 65, no. 5, pp. 1229–1240, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Marino, C. Dunand, A. Puppo, and N. Pauly, “A burst of plant NADPH oxidases,” Trends in Plant Science, vol. 17, no. 1, pp. 9–15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. I. I. Panchuk, R. A. Volkov, and F. Schöffl, “Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis,” Plant Physiology, vol. 129, no. 2, pp. 838–853, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Davletova, L. Rizhsky, H. Liang et al., “Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis,” Plant Cell, vol. 17, no. 1, pp. 268–281, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Asada, “Ascorbate peroxidase—a hydrogen peroxide-scavenging enzyme in plants,” Physiologia Plantarum, vol. 85, no. 2, pp. 235–241, 1992. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Noctor and C. H. Foyer, “Ascorbate and glutathione: keeping active oxygen under control,” Annual Review of Plant Biology, vol. 49, pp. 249–279, 1998. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Shigeoka, T. Ishikawa, M. Tamoi et al., “Regulation and function of ascorbate peroxidase isoenzymes,” Journal of Experimental Botany, vol. 53, no. 372, pp. 1305–1319, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Lu, D. Liu, and S. Liu, “Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis,” Plant Cell Reports, vol. 26, no. 10, pp. 1909–1917, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. S. S. Gill and N. Tuteja, “Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants,” Plant Physiology and Biochemistry, vol. 48, no. 12, pp. 909–930, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. Guan, Z. Wang, X. Wang, T. Takano, and S. Liu, “A peroxisomal APX from Puccinellia tenuiflora improves the abiotic stress tolerance of transgenic Arabidopsis thaliana through decreasing of H2O2 accumulation,” Journal of Plant Physiology, vol. 175, pp. 183–191, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. C. H. Foyer and B. Halliwell, “The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism,” Planta, vol. 133, no. 1, pp. 21–25, 1976. View at Publisher · View at Google Scholar · View at Scopus
  21. P. P. Jablonski and J. W. Anderson, “Light-dependent reduction of hydrogen peroxide by ruptured pea chloroplasts,” Plant Physiology, vol. 69, no. 6, pp. 1407–1413, 1982. View at Publisher · View at Google Scholar
  22. M. A. Hossain and K. Asada, “Purification of dehydroascorbate reductase from spinach and its characterization as a thiol enzyme,” Plant and Cell Physiology, vol. 25, pp. 85–92, 1984. View at Google Scholar · View at Scopus
  23. S.-H. Lee, N. Ahsan, K.-W. Lee et al., “Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses,” Journal of Plant Physiology, vol. 164, no. 12, pp. 1626–1638, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Kavitha, G. Venkataraman, and A. Parida, “An oxidative and salinity stress induced peroxisomal ascorbate peroxidase from Avicennia marina: molecular and functional characterization,” Plant Physiology and Biochemistry, vol. 46, no. 8-9, pp. 794–804, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Ahmad, Y.-H. Kim, M.-D. Kim et al., “Simultaneous expression of choline oxidase, superoxide dismutase and ascorbate peroxidase in potato plant chloroplasts provides synergistically enhanced protection against various abiotic stresses,” Physiologia Plantarum, vol. 138, no. 4, pp. 520–533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Moon, B. Lee, G. Choi et al., “NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 1, pp. 358–363, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. Y.-H. Kim, S. Lim, K.-S. Yang et al., “Expression of arabidopsis NDPK2 increases antioxidant enzyme activities and enhances tolerance to multiple environmental stresses in transgenic sweetpotato plants,” Molecular Breeding, vol. 24, no. 3, pp. 233–244, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Sato, T. Murakami, H. Funatsuki, S. Matsuba, H. Saruyama, and M. Tanida, “Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings,” Journal of Experimental Botany, vol. 52, no. 354, pp. 145–151, 2001. View at Google Scholar · View at Scopus
  29. S. Lim, Y.-H. Kim, S.-H. Kim et al., “Enhanced tolerance of transgenic sweetpotato plants that express both CuZnSOD and APX in chloroplasts to methyl viologen-mediated oxidative stress and chilling,” Molecular Breeding, vol. 19, no. 3, pp. 227–239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Tang, S.-Y. Kwon, S.-H. Kim et al., “Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature,” Plant Cell Reports, vol. 25, no. 12, pp. 1380–1386, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. M. D. Kim, Y.-H. Kim, S.-Y. Kwon, D.-J. Yun, S.-S. Kwak, and H.-S. Lee, “Enhanced tolerance to methyl viologen-induced oxidative stress and high temperature in transgenic potato plants overexpressing the CuZnSOD, APX and NDPK2 genes,” Physiologia Plantarum, vol. 140, no. 2, pp. 153–162, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. S. B. Rosa, A. Caverzan, F. K. Teixeira et al., “Cytosolic APx knockdown indicates an ambiguous redox responses in rice,” Phytochemistry, vol. 71, no. 5-6, pp. 548–558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Bonifacio, M. O. Martins, C. W. Ribeiro et al., “Role of peroxidases in the compensation of cytosolic ascorbate peroxidase knockdown in rice plants under abiotic stress,” Plant, Cell and Environment, vol. 34, no. 10, pp. 1705–1722, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Caverzan, A. Bonifacio, F. E. L. Carvalho et al., “The knockdown of chloroplastic ascorbate peroxidases reveals its regulatory role in the photosynthesis and protection under photo-oxidative stress in rice,” Plant Science, vol. 214, pp. 74–87, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. R. B. Horsch, J. E. Fry, N. L. Hoffmann, D. Eichholtz, S. G. Rogers, and R. T. Fraley, “A simple and general method for transferring genes into plants,” Science, vol. 227, no. 4691, pp. 1229–1231, 1985. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Nakano and K. Asada, “Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts,” Plant and Cell Physiology, vol. 22, no. 5, pp. 867–880, 1981. View at Google Scholar · View at Scopus
  37. N. Arakawa, K. Tsutsumi, N. G. Sanceda, T. Kurata, and C. Inagaki, “A rapid and sensitive method for the determination of ascorbic acid using 4,7-diphenyl-l,10-phenanthroline,” Agricultural and Biological Chemistry, vol. 45, no. 5, pp. 1289–1290, 1981. View at Publisher · View at Google Scholar · View at Scopus
  38. H. S. Lee, The Principles and Techniques of the Plant Physiological and Biochemical, Higher Education Press, Beijing, China, 2000.
  39. R. L. Heath and L. Packer, “Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation,” Archives of Biochemistry and Biophysics, vol. 125, no. 1, pp. 189–198, 1968. View at Publisher · View at Google Scholar · View at Scopus
  40. X. Shi, D. C. Flynn, D. W. Porter, S. S. Leonard, V. Vallyathan, and V. Castranova, “Efficacy of taurine based compounds as hydroxyl radical scavengers in silica induced peroxidation,” Annals of Clinical and Laboratory Science, vol. 27, no. 5, pp. 365–374, 1997. View at Google Scholar · View at Scopus
  41. X. Z. Zhang, The Research Method of Physiology in the Crop, Agriculture Press, Beijing, China, 1992.
  42. H. M. Jespersen, I. V. H. Kjærsgård, L. Østergaard, and K. G. Welinder, “From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase,” Biochemical Journal, vol. 326, no. 2, pp. 305–310, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Mittler, “Oxidative stress, antioxidants and stress tolerance,” Trends in Plant Science, vol. 7, no. 9, pp. 405–410, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Shafi, V. Dogra, T. Gill, P. S. Ahuja, and Y. Sreenivasulu, “Simultaneous over-expression of PaSOD and RaAPX in transgenic Arabidopsis thaliana confers cold stress tolerance through increase in vascular lignifications,” PLoS ONE, vol. 9, no. 10, Article ID e110302, 14 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Koussevitzky, N. Suzuki, S. Huntington et al., “Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination,” Journal of Biological Chemistry, vol. 283, no. 49, pp. 34197–34203, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. C. H. Padaria, H. Vishwakarma, K. Biswas, R. S. I. Jasrotia, and G. P. R. Singh, “Molecular cloning and in-silico characterization of high temperature stress responsive pAPX gene isolated from heat tolerant Indian wheat cv. Raj 3765,” BMC Research Notes, vol. 7, pp. 713–714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. K.-H. Baek and D. Z. Skinner, “Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines,” Plant Science, vol. 165, no. 6, pp. 1221–1227, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. H.-C. Liu, D.-Q. Tian, J.-X. Liu, G.-Y. Ma, Q.-C. Zou, and Z.-J. Zhu, “Cloning and functional analysis of a novel ascorbate peroxidase (APX) gene from Anthurium andraeanum,” Journal of Zhejiang University: Science B, vol. 14, no. 12, pp. 1110–1120, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Zhang, Q. Zhang, J. Wu et al., “Gene knockout study reveals that cytosolic ascorbate peroxidase 2(OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses,” PLOS ONE, vol. 8, no. 2, Article ID e57472, pp. 1–13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. K.-H. Lin, H.-C. Huang, and C.-Y. Lin, “Cloning, expression and physiological analysis of broccoli catalase gene and Chinese cabbage ascorbate peroxidase gene under heat stress,” Plant Cell Reports, vol. 29, no. 6, pp. 575–593, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Kornyeyev, A. L. Barry, P. Payton, R. D. Allen, and A. Scott Holaday, “Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of photosystem II in cotton overexpressing genes encoding chloroplast-targeted antioxidant enzymes,” Physiologia Plantarum, vol. 113, no. 3, pp. 323–331, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. K. Asada, “Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress,” in Photoinhibition of Photosynthesis. From Molecular Mechanisms to the Field, N. R. Baker and J. R. Bowyer, Eds., pp. 129–142, Bios Scientific Publishers, Oxford, UK, 1994. View at Google Scholar
  53. R. Zhou, X. Yu, K. H. Kjær, E. Rosenqvist, C.-O. Ottosen, and Z. Wu, “Screening and validation of tomato genotypes under heat stress using Fv/Fm to reveal the physiological mechanism of heat tolerance,” Environmental and Experimental Botany, vol. 118, pp. 1–11, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Bartwal and S. Arora, “Drought stress-induced enzyme activity and mdar and apx gene expression in tolerant and susceptible genotypes of Eleusine coracana (L.),” In Vitro Cellular & Developmental Biology—Plant, pp. 1–9, 2016. View at Publisher · View at Google Scholar
  55. A. Harb, D. Awad, and N. Samarah, “Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare l.) under controlled severe drought,” Journal of Plant Interactions, vol. 10, no. 1, pp. 109–116, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. Z. Wang, Z. Q. Jin, J. S. Wang et al., “Cloning and characterization of an ascorbate peroxidase gene regulated by ethylene and abscisic acid during banana fruit ripening,” African Journal of Biotechnology, vol. 11, no. 43, pp. 10089–10097, 2012. View at Google Scholar
  57. W.-H. Sun, M. Duan, D.-F. Shu, S. Yang, and Q.-W. Meng, “Over-expression of StAPX in tobacco improves seed germination and increases early seedling tolerance to salinity and osmotic stresses,” Plant Cell Reports, vol. 29, no. 8, pp. 917–926, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Faize, E. Nicolás, L. Faize, P. Díaz-Vivancos, L. Burgos, and J. A. Hernández, “Cytosolic ascorbate peroxidase and Cu, Zn-superoxide dismutase improve seed germination, plant growth, nutrient uptake and drought tolerance in tobacco,” Theoretical and Experimental Plant Physiology, vol. 27, no. 3-4, pp. 215–226, 2015. View at Publisher · View at Google Scholar · View at Scopus