Biologia plantarum 57:675-683, 2013 | DOI: 10.1007/s10535-013-0346-9

Peroxiredoxins are involved in two independent signalling pathways in the abiotic stress protection in Vitis vinifera

P. Vidigal1, R. Carvalho1, S. Amâncio1, L. Carvalho1,*
1 DRAT/CBAA, Instituto Superior de Agronomia, Universidade Técnica de Lisboa, Lisboa, Portugal

Peroxiredoxins (Prxs) play major roles in preventing oxidative damage and their function is consistent with the presence of Prx isoforms in most, if not all, cellular compartments and their expression is dependent on environmental conditions. The aim of this study was to identify and characterize genes encoding Prxs in Vitis vinifera. Quantitative real time polymerase chain reaction (qRT PCR) was used to determine their response to irradiance, heat, and water stress. We identified seven vvprx genes, two of which were especially responsive to water stress, followed by heat stress, but no major changes were observed after high irradiance. The vvprxIIF targeted to mitochondria was the most responsive to water stress and it might be involved in drought tolerance through H2O2 signalling. The vvprxII-2, a putative PrxII, is targeted to the chloroplasts and was the most responsive to heat stress. It might be related with abscisic acid-dependent thermotolerance. Additional key words: abscisic acid, antioxidants, grapevine, heat stress, photosynthesis, qRT PCR, water stress.

Subjects: peroxiredoxins; abscisic acid; antioxidants; temperature - high; water stress; catalase; ascorbate peroxidase; superoxide dismutase; glutathione reductase; net photosynthetic rate; chlorophyll fluorescence; grapevine

Received: November 20, 2012; Accepted: March 21, 2013; Published: December 1, 2013Show citation

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Vidigal, P., Carvalho, R., Amâncio, S., & Carvalho, L. (2013). Peroxiredoxins are involved in two independent signalling pathways in the abiotic stress protection in Vitis vinifera. Biologia plantarum57(4), 675-683. doi: 10.1007/s10535-013-0346-9.
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References

  1. Aragón, C., Carvalho, L.C., González, J., Escalona, M., Amâncio, S.: Sugarcane (Saccharum sp. hybrid) propagated in headspace renovating systems shows autotrophic characteristics and develops improved anti-oxidative response. - Trop. Plant Biol. 2: 38-50, 2008. Go to original source...
  2. Asada, K.: The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 601-639, 1999. Go to original source...
  3. Baier, M., Dietz, K.J.: Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. - Plant Physiol. 119: 1407-1414, 1999. Go to original source...
  4. Baier, M., Noctor, G., Foyer, C.H., Dietz, K.J.: Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. - Plant Physiol. 124: 823-832, 2000. Go to original source...
  5. Baier, M., Stroher, E., Dietz, K.J.: The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. - Plant Cell Physiol. 45: 997-1006, 2004. Go to original source...
  6. Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Sayers, E.W.: GenBank. - Nucl. Acids Res. 39(Suppl.): D32-D37, 2011. Go to original source...
  7. Bradford, M.M.: 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, 1976. Go to original source...
  8. Broin, M., Cuine, S., Eymery, F., Rey, P.: The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. - Plant Cell 14: 1417-1432, 2002. Go to original source...
  9. Carvalho, L.C., Vilela, B.J., Mullineaux, P.M., Amâncio, S.: Comparative transcriptomic profiling of Vitis vinifera under high light using a custom-made array and the Affymetrix gene chip. - Mol. Plant 4: 1038-1051, 2011. Go to original source...
  10. Carvalho, L.C., Vilela, B.J., Vidigal, P., Mullineaux, P.M., Amâncio, S.: Activation of the ascorbate-glutathione cycle is an early response of micropropagated Vitis vinifera L. explants transferred to ex vitro. - Int. J. Plant Sci. 167: 759-770, 2006. Go to original source...
  11. Coito, J.L., Rocheta, M., Carvalho, L.C., Amâncio, S.: Microarray-based uncovering reference genes for quantitative real time PCR in grapevine under abiotic stress. - BMC Res. Notes 5: 220, 2012. Go to original source...
  12. Dietz, K.J.: The dual function of plant peroxiredoxins in antioxidant defence and redox signaling. - Subcell. Biochem. 44: 267-294, 2007. Go to original source...
  13. Dietz, K.J.: Peroxiredoxins in plants and cyanobacteria. - Antioxid. Redox Signal 15: 1129-1159, 2011. Go to original source...
  14. Dietz, K.J., Horling, F., Konig, J., Baier, M.: The function of the chloroplast 2-cysteine peroxiredoxin in peroxide detoxification and its regulation. - J. exp. Bot. 53: 1321-1329, 2002.
  15. Dietz, K.J., Jacob, S., Oelze, M.L., Laxa, M., Tognetti, V., De Miranda, S.M., Baier, M., Finkemeier, I.: The function of peroxiredoxins in plant organelle redox metabolism. - J. exp. Bot. 57: 1697-1709, 2006. Go to original source...
  16. Felsenstein, J.: Confidence limits on phylogenies: an approach using the bootstrap. - Evolution 39: 783-791, 1985. Go to original source...
  17. Gama, F., Keech, O., Eymery, F.O., Finkemeier, I., Gelhaye, E., Gardestrom, P., Dietz, K.J., Rey, P., Jacquot, J.P., Rouhier, N.: The mitochondrial type II peroxiredoxin from poplar. - Physiol. Plant. 129: 196-206, 2007. Go to original source...
  18. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D., Bairoch, A.: Protein identification and analysis tools on the ExPASy server. - In: Walker, J.M. (ed.): The Proteomics Protocols Handbook. Pp. 571-607. Humana Press, Totowa 2005. Go to original source...
  19. Geuna, F., Hartings, H., Scienza, A.: A new method for rapid extraction of high quality RNA from recalcitrant tissues of grapevine. - Plant mol. Biol. Rep. 16: 61-67, 1998. Go to original source...
  20. Haslekas, C., Stacy, R.A., Nygaard, V., Culianez-Macia, F.A., Aalen, R.B.: The expression of a peroxiredoxin antioxidant gene, AtPer1, in Arabidopsis thaliana is seed-specific and related to dormancy. - Plant mol. Biol. 36: 833-845, 1998. Go to original source...
  21. Haslekas, C., Viken, M.K., Grini, P.E., Nygaard, V., Nordgard, S.H., Meza, T.J., Aalen, R.B.: Seed 1-cysteine peroxiredoxin antioxidants are not involved in dormancy, but contribute to inhibition of germination during stress. - Plant Physiol. 133: 1148-1157: 2003. Go to original source...
  22. Horling, F., Konig, J., Dietz, K.J.: Type II peroxiredoxin C, a member of the peroxiredoxin family of Arabidopsis thaliana: its expression and activity in comparison with other peroxiredoxins. - Plant Physiol. Biochem. 40: 491-499, 2002. Go to original source...
  23. Horling, F., Lamkemeyer, P., Konig, J., Finkemeier, I., Kandlbinder, A., Baier, M., Dietz, K.J.: Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. - Plant Physiol. 131: 317-325, 2003. Go to original source...
  24. Horton, P., Park, K.J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C.J., Nakai, K.: WoLFPSORT: protein localization predictor. - Nucl. Acids Res. 35(Suppl.): W585-W587, 2007. Go to original source...
  25. Hossain, M.A., Fujita, M.: Regulatory role of components of ascorbate-glutathione (AsA-GSH) pathway in plant tolerance to oxidative stress. - In: Anjum, N.A., Umar, S., Ahmed, A. (ed.): Oxidative Stress in Plants: Causes, Consequences and Tolerance. Pp. 81-147. IK International Publishing House, New Delhi 2011.
  26. Huang, L., McCluskey, M.P., Ni, H., LaRossa, R.A.: Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. - J. Bacteriol. 184: 6845-6858, 2002. Go to original source...
  27. Jing, L.W., Chen, S.H., Guo, X.L., Zhang, H., Zhao, Y.X.: Overexpression of a chloroplast-located peroxiredoxin Q gene, SsPrxQ, increases the salt and low-temperature tolerance of Arabidopsis. - J. Integr. Plant Biol. 48: 1244-1249, 2006. Go to original source...
  28. Konig, J., Baier, M., Horling, F., Kahmann, U., Harris, G., Schurmann, P., Dietz, K.J.: The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. - Proc. nat. Acad. Sci. USA 99: 5738-5743, 2002. Go to original source...
  29. Lamkemeyer, P., Laxa, M., Collin, V., Li, W., Finkemeier, I., Schottler, M.A., Holtkamp, V., Tognetti, V.B., Issakidis-Bourguet, E., Kandlbinder, A., Weis, E., Miginiac-Maslow, M., Dietz, K.J.: Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. - Plant J. 45: 968-981, 2006. Go to original source...
  30. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G.: Clustal W and Clustal X version 2.0. - Bioinformatics 23: 2947-2948, 2007. Go to original source...
  31. Li, H., Singh, A.K., McIntyre, L.M., Sherman, L.A.: Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803. - J. Bacteriol. 186: 3331-3345, 2004. Go to original source...
  32. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C., Fong, J.H., Geer, L.Y., Geer, R.C., Gonzales, N.R., Gwadz, M., Hurwitz, D.I., Jackson, J.D., Ke, Z., Lanczycki, C.J., Lu, F., Marchler, G.H., Mullokandov, M., Omelchenko, M.V., Robertson, C.L., Song, J.S., Thanki, N., Yamashita, R.A., Zhang, D., Zhang, N., Zheng, C., Bryant, S.H.: CDD: a conserved domain database for the functional annotation of proteins. - Nucl. Acids Res. 39(Suppl.): D225-D229, 2011. Go to original source...
  33. Mittler, R.: Oxidative stress, antioxidants, and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
  34. Mowla, S.B., Thomson, J.A., Farrant, J.M., Mundree, S.G.: A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. - Planta 215: 716-726, 2002. Go to original source...
  35. Parsonage, D., Karplus, P.A., Poole, L.B.: Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. - Proc. nat. Acad. Sci. USA 105: 8209-8214, 2008. Go to original source...
  36. Perez-Perez, M.E., Mata-Cabana, A., Sanchez-Riego, A.M., Lindahl, M., Florencio, F.J.: A comprehensive analysis of the peroxiredoxin reduction system in the cyanobacterium Synechocystis sp. strain PCC 6803 reveals that all five peroxiredoxins are thioredoxin dependent. - J. Bacteriol. 191: 7477-7489, 2009. Go to original source...
  37. Petersson, U.A., Kieselbach, T., Garcia-Cerdan, J.G., Schroder, W.P.: The Prx Q protein of Arabidopsis thaliana is a member of the luminal chloroplast proteome. - FEBS Lett. 580: 6055-6061, 2006. Go to original source...
  38. Pulido, P., Cazalis, R., Cejudo, F.J.: An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. - Plant J. 57: 132-145, 2009. Go to original source...
  39. Pulido, P., Spinola, M.C., Kirchsteiger, K., Guinea, M., Pascual, M.B., Sahrawy, M., Sandalio, L.M., Dietz, K.J., Gonzalez, M., Cejudo, F.J.: Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. - J. exp. Bot. 61: 4043-4054, 2010. Go to original source...
  40. Rhee, S.G., Kang, S.W., Jeong, W., Chang, T.S., Yang, K.S., Woo, H.A.: Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. - Curr. Opin. Cell Biol. 17: 183-189, 2005. Go to original source...
  41. Rhue R.D., Grogan C.O., Stockmeyer E.W., Evert H.L.: Genetic control of aluminium tolerance in corn. - Crop Sci. 18: 1063-1067, 1978. Go to original source...
  42. Romero-Puertas, M.C., Laxa, M., Matte, A., Zaninotto, F., Finkemeier, I., Jones, A.M., Perazzolli, M., Vandelle, E., Dietz, K.J., Delledonne, M.: S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. - Plant Cell 19: 4120-4130, 2007. Go to original source...
  43. Rouhier, N., Jacquot, J.P.: The plant multigenic family of thiol peroxidases. - Free Rad. Biol. Med. 38: 1413-1421, 2005. Go to original source...
  44. Saitou, N., Nei, M.: The neighbor-joining method: a new method for reconstructing phylogenetic trees. - Mol. Biol. Evol. 4: 406-425, 1987.
  45. Schwarz, R., Dayhoff, M.: Matrices for detecting distant relationships. - In: Dayhoff, M. (ed.): Atlas of Protein sequences. Pp. 353-358. Nat. Biomed. Res. Found., Washington 1979.
  46. Song, Y., Lin, Y., Tong, S., Hou, H.: Molecular cloning, promoter analysis, and expression profile of VvERF3b gene in Vitis vinifera. - Biol. Plant. 56: 31-36, 2012. Go to original source...
  47. Sweetlove, L.J., Heazlewood, J.L., Herald, V., Holtzapffel, R., Day, D.A., Leaver, C.J., Millar, A.H.: The impact of oxidative stress on Arabidopsis mitochondria. - Plant J. 32: 891-904, 2002. Go to original source...
  48. Tamura, K., Dudley, J., Nei, M., Kumar, S.: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. - Mol. Biol. Evol. 24: 1596-1599, 2007. Go to original source...
  49. Tripathi, B.N., Bhatt, I., Dietz, K.J.: Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. - Protoplasma 235: 3-15, 2009. Go to original source...
  50. Upadhyay, A., Upadhyay, A.K., Bhirangi, R.A.: Expression of Na+/H+ antiporter gene in response to water and salinity stress in grapevine rootstocks. - Biol. Plant. 56: 762-766, 2012. Go to original source...
  51. Vandenabeele, S., Vanderauwera, S., Vuylsteke, M., Rombauts, S., Langebartels, C., Seidlitz, H.K., Zabeau, M., Van Montagu, M., Inzé, D., Van Breusegem, F.: Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. - Plant J. 39: 45-58, 2004. Go to original source...
  52. Vilela, B.J., Carvalho, L.C., Ferreira, J., Amâncio, S.: Imaging of photooxidative stress symptoms and stomatal functioning in Vitis vinifera L. transferred from in vitro to ex vitro under increased light. - Plant Cell Rep. 26: 2149-2157, 2007. Go to original source...
  53. Wang, L.J., Huang, W.D., Liu, Y.P., Zhan, J.C.: Changes in salicylic and abscisic acid contents during heat treatment and their effect on thermotolerance of grape plants. - Russ. J. Plant Physiol. 52: 516-520, 2005. Go to original source...
  54. Wood Z.A., Schroder E., Harris J.R., Poole L.B.: Structure, mechanism and regulation of peroxiredoxins. - Trends Biochem. Sci. 28: 32-40, 2003. Go to original source...