Oxidative stress homeostasis in grapevine (Vitis vinifera L.)

Frontiers in Environmental Science

Volumn 3, Issue MAR, 2015, Pages

  Carvalho, Luísa C ^a   Vidigal, Patrícia ^a   Amâncio, Sara ^a  

^a INSTITUTO SUPERIOR DE AGRONOMIA   (Portugal)

Author keywords

Ascorbate glutathione cycle; Biotic stress; Hormone stress signals; In vitro stress; Oxidative burst; Peroxiredoxins; ROS

Indexed keywords

EID: 84959292748     PISSN: None     EISSN: 2296665X     Source Type: Journal    
DOI: 10.3389/fenvs.2015.00020     Document Type: Review

References (115)

1. Aldini, G., Carini, M., Piccoli, A., Rossoni, G., and Facino, R. M. (2003). Procyanidins from grape seeds protect endothelial cells from peroxynitrite damage and enhance endothelium-dependent relaxation in human artery: new evidences for cardio-protection. Life Sci. 73, 2883-2898. doi: 10.1016/S0024-3205(03)00697-0
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.55.031903.141701
3. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396. doi: 10.1104/pp.106.082040
4. Avanci, N. C., Luche, D. D., Goldman, G. H., and Goldman, M. H. S. (2010). Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. GMR 9, 484-505. doi: 10.4238/vol9-1gmr754
5. Aziz, A., Heyraud, A., and Lambert, B. (2004). Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218, 767-774. doi: 10.1007/s00425-003-1153-x
6. Baier, M., Ströher, E., and Dietz, K. (2004). 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. doi: 10.1093/pcp/pch114
7. Baker, A., and Graham, I. (2002). Plant Peroxisomes. Biochemistry, Cell Biology and Biotechnological Applications. Dordrecht: Kluwer Academic Publishers.
8. Balbi, V., and Devoto, A. (2008). Jasmonate signaling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol. 177, 301-318. doi: 10.1111/j.1469-8137.2007.02292.x
9. Berli, F. J., Moreno, D., Piccoli, P., Hespanhol-Viana, L., Silva, M. F., Bressan-Smith, R., et al. (2010). Abscisic acid is involved in the response of grape (Vitis vinifera L.) cv. Malbec leaf tissues to ultraviolet-B radiation by enhancing ultraviolet-absorbing compounds, antioxidant enzymes and membrane sterols. Plant Cell Environ. 33, 1-10. doi: 10.1111/j.1365-3040.2009.02044.x
10. Bari, R., and Jonathan, J. (2009). Role of plant hormones in plant defence responses. Plant Mol. Biol. 69, 473-488. doi: 10.1007/s11103-008-9435-0
11. Bertamini, M., Zulini, L., Muthuchelian, K., and Nedunchezhian, N. (2006). Effect of water deficit on photosynthetic and other physiological responses in grapevine (Vitis vinifera L. cv. Riesling) plants. Photosynthetica 44, 151-154. doi: 10.1007/s11099-005-0173-0
12. Carvalho, C., and Amâncio, S. (2002). Antioxidant defence system in plantlets transferred from in vitro to ex vitro: effects of increasing light intensity and CO2 concentration. Plant Sci. 162, 33-40. doi: 10.1016/S0168-9452(01)00524-6
13. Carvalho, L. C., Coito, J. L., Colaço, S., Sangiogo, M., and Amâncio, S. (2014). Heat stress in grapevine: the pros and cons of acclimation. Plant. Cell Environ. doi: 10.1111/pce.12445. [Epub ahead of print].
14. Carvalho, L. C., Esquível, M. G., Martins, I., Pinto Ricardo, C., and Amâncio, S. (2005). Monitoring the stability of Rubisco in micropropagated grapevine (Vitis vinifera L.) by two-dimensional electrophoresis. J. Plant Physiol. 162, 365-374. doi: 10.1016/j.jplph.2004.09.013
15. Carvalho, L. C., Os, M. L., Chaves, M. M., and Amâncio, S. (2001). Chlorophyll fluorescence as an indicator of photosynthetic functioning of in vitro grapevine and chestnut plantlets under ex vitro acclimatization. Plant Cell. Tissue Organ Cult. 67, 271-280. doi: 10.1023/A:1012722112406
16. Carvalho, L. C., Vilela, B. J., Mullineaux, P. M., and Amâncio, S. (2011). Comparative transcriptomic profiling of Vitis vinifera under high light using a custom-made array and the affymetrix genechip. Mol. Plant 6, 1038-1051. doi: 10.1093/mp/ssr027
17. Carvalho, L. C., Vilela, B. J., Vidigal, P., Mullineaux, P. M., and Amâncio, S. (2006). 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. doi: 10.1086/503919
18. Chaves, M. M. (1994). "Environmental constrains to photosynthesis in ex vitro plants," in Physiology, Growth and Development of Plants in Culture, eds P. J. Lumsden, J. R. Nicholas, and W. J. Davies (Dordrecht, Kluwer Academic Publishers), 1-18.
19. Chervin, C., El-Kereamy, A., Roustan, J.-P., Latché, A., Lamon, J., and Bouzayen, M. (2004). Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci. 167, 1301-1305. doi: 10.1016/j.plantsci.2004.06.026
20. Conde, C., Silva, P., Fontes, N., Dias, A. C. P., Tavares, R. M., Sousa, M. J., et al. (2007). Biochemical changes throughout grape berry development and fruit and wine quality. Food 1, 1-22.
21. Conklin, P. L., and Loewus, F. A. (2001). Biosynthesis of ascorbic acid in plants: a renaiscance. Annu. Rev. Plant Biol. Plant Mol. Biol. 52, 437-467. doi: 10.1146/annurev.arplant.52.1.437
22. Conn, S., Curtin, C., Bézier, A., Franco, C., and Zhang, W. (2008). Purification, molecular cloning, and characterization of glutathione S-transferases (GSTs) from pigmented Vitis vinifera L. cell suspension cultures as putative anthocyanin transport proteins. J. Exp. Bot. 59, 3621-3634. doi: 10.1093/jxb/ern217
23. Corpas, F. J., Barroso, J. B., and del Río, L. (2001). Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci. 6, 145-150. doi: 10.1016/S1360-1385(01)01898-2
24. Costa, J. M., Ortuño, M. F., Lopes, C. M., and Chaves, M. M. (2012). Grapevine varieties exhibiting differences in stomatal response to water deficit. Func. Plant Biol. 39, 179-189. doi: 10.1071/FP11156
25. Cramer, G. R. (2010). Abiotic stress and plant responses from the whole vine to the genes. Aust. J. Grape Wine Res. 16, 86-93. doi: 10.1111/j.1755-0238.2009.00058.x
26. Cramer, G. R., Ergül, A., Grimplet, J., Tillett, R. L., Tattersall, E. A. R., Bohlman, M. C., et al. (2007). Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct. Integr. Genomics 7, 111-134. doi: 10.1007/s10142-006-0039-y
27. Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., and Abrams, S. R. (2010). Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679. doi: 10.1146/annurev-arplant-042809-112122
28. Del Río, L. A., Sandalio, L. M., Corpas, F. J., Palma, M., and Barroso, J. B. (2006). Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signalling. Plant Physiol. 141, 330-335. doi: 10.1104/pp.106.078204
29. Deluc, L. G., Quilici, D. R., Decendit, A., Grimplet, J., Wheatley, M. D., Schlauch, K., et al. (2009). Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics 10:212. doi: 10.1186/1471-2164-10-212
30. De Nisco, M., Manfra, M., Bolognese, A., Sofo, A., Scopa, A., Tenore, G. C., et al. (2013). Nutraceutical properties and polyphenolic profile of berry skin and wine of Vitis vinifera L. (cv. Aglianico). Food Chem. 140, 623-629. doi: 10.1016/j.foodchem.2012.10.123
31. Dietz, K.-J. (2003). Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107. doi: 10.1146/annurev.arplant.54.031902.134934
32. Dietz, K.-J. (2011). Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal. 15, 1129-1159. doi: 10.1089/ars.2010.3657
33. Dry, P., and Loveys, B. R. (1999). Grapevine shoot growth and stomatal conductance are reduced when part of the root system is dried. Vitis 38, 151-156.
34. Edge, R., McGarvey, D. J., and Truscott, T. G. (1997). The carotenoids as anti-oxidants-a review. J. Photochem. Photobiol. 41, 189-200. doi: 10.1016/S1011-1344(97)00092-4
35. Edwards, R., Dixon, D. P., and Walbot, V. (2000). Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5, 193-198. doi: 10.1016/S1360-1385(00)01601-0
36. Fang, J., Chai, C., Qian, Q., Li, C., Tang, J., Sun, L., et al. (2008). Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. Plant J. 54, 177-189. doi: 10.1111/j.1365-313X.2008.03411.x
37. Fasoli, M., Dal Santo, S., Zenoni, S., Tornielli, G. B., Farina, L., Zamboni, A., et al. (2012). The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24, 3489-3505. doi: 10.1105/tpc.112.100230
38. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., et al. (2006). Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9, 436-442. doi: 10.1016/j.pbi.2006.05.014
39. Gama, F., Keech, O., Eymery, F., Finkemeier, I., Gelhaye, E., Gardeström, P., et al. (2007). The mitochondrial type II peroxiredoxin from poplar. Physiol. Plant 129, 196-206. doi: 10.1111/j.1399-3054.2006.00785.x
40. Gambetta, G. A., Matthews, M. A., Shaghasi, T. H., McElrone, A. J., and Castellarin, S. D. (2010). Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232, 219-234. doi: 10.1007/s00425-010-1165-2
41. Giribaldi, M., Perugini, I., Sauvage, F.-X., and Schubert, A. (2007). Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 7, 3154-3170. doi: 10.1002/pmic.200600974
42. Grimplet, J., Deluc, L. G., Tillett, R. L., Wheatley, M. D., Schlauch, K. A., Cramer, G. R., et al. (2007). Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics 8:187. doi: 10.1186/1471-2164-8-187
43. Gunes, A., Soylemezoglu, G., Inal, A., Bagci, E. G., Coban, S., and Sahin, O. (2006). Antioxidant and stomatal responses of grapevine (Vitis vinifera L.) to boron toxicity. Sci. Hortic. 110, 279-284. doi: 10.1016/j.scienta.2006.07.014
44. Guo, X.-L., Cao, Y.-R., Cao, Z.-Y., Zhao, Y.-X., and Zhang, H. (2004). Molecular cloning and characterization of a stress-induced peroxiredoxin Q gene in halophyte Suaeda salsa. Plant Sci. 167, 969-975. doi: 10.1016/j.plantsci.2004.05.004
45. Horling, F., Lamkemeyer, P., Ko, J., Finkemeier, I., Kandlbinder, A., Baier, M., et al. (2003). Dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiol. 131, 317-325. doi: 10.1104/pp.010017
46. Ismail, A., Riemann, M., and Nick, P. (2012). The jasmonate pathway mediates salt tolerance in grapevines. J. Exp. Bot. 63, 2127-2139. doi: 10.1093/jxb/err426
47. Jeong, S., Goto-Yamamoto, N., Kobayashi, S., and Esaka, M. (2004). Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins. Plant Sci. 167, 247-252. doi: 10.1016/j.plantsci.2004.03.021
48. Jia, W., and Zhang, J. (1997). Comparison of exportation and metabolism of xylem-delivered ABA in maize leaves at different water status and xylem sap pH. Plant Growth Regul. 21, 43-49. doi: 10.1023/A:1005722121030
49. Jones, G. V., White, M. A., Cooper, O. R., and Storchmann, K. (2005). Climate change and global wine quality. Clim. Change 73, 319-343. doi: 10.1007/s10584-005-4704-2
50. Kim, K.-H., Alam, I., Lee, K.-W., Sharmin, S. A., Kwak, S.-S., Lee, S. Y., et al. (2010). Enhanced tolerance of transgenic tall fescue plants overexpressing 2-Cys peroxiredoxin against methyl viologen and heat stresses. Biotechnol. Lett. 32, 571-576. doi: 10.1007/s10529-009-0185-0
51. Kiyosue, T., Yoshiba, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1996). A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8, 1323-1335. doi: 10.1105/tpc.8.8.1323
52. König, J., Lotte, K., Plessow, R., Brockhinke, A., Baier, M., and Dietz, K.-J. (2003). Reaction mechanism of plant 2-Cys peroxiredoxin. Role of the C terminus and the quaternary structure. J. Biol. Chem. 278, 24409-24420. doi: 10.1074/jbc.M301145200
53. Kortekamp, A. (2006). Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiol. Biochem. 44, 58-67. doi: 10.1016/j.plaphy.2006.01.008
54. Kortekamp, A., and Zyprian, E. (2003). Characterization of Plasmopara-resistance in grapevine using in vitro plants. J. Plant Physiol. 160, 1393-1400. doi: 10.1078/0176-1617-01021
55. Koyama, Y. (1991). Structures and functions of carotenoids in photosynthetic systems. J. Photochem. Photobiol. 9, 265-280.
56. Krause, G. H., and Weis, E. (1991). Chlorophyll fluorescence and photosynthesis: the basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 313-349. doi: 10.1146/annurev.pp.42.060191.001525
57. Kvaratskhelia, M., Winkel, C., and Thorneley, R. N. F. (1997). Purification and characterization of a nove1 class 111 peroxidase isoenzyme from tea leaves. Plant Physiol. 1237-1245. doi: 10.1104/pp.114.4.1237
58. Lacampagne, S., Gagné, S., and Gény, L. (2009). Involvement of abscisic acid in controlling the proanthocyanidin biosynthesis pathway in grape skin: new elements regarding the regulation of tannin composition and leucoanthocyanidin reductase (LAR) and anthocyanidin reductase (ANR) activities and expression. J. Plant Growth Regul. 29, 81-90. doi: 10.1007/s00344-009-9115-6
59. Lamkemeyer, P., Laxa, M., Collin, V., Li, W., Finkemeier, I., Schöttler, M., et al. (2006). Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. Plant J. 45, 968-981. doi: 10.1111/j.1365-313X.2006.02665.x
60. Leon-Reyes, A., Van der Does, D., De Lange, E. S., Delker, C., Wasternack, C., Van Wees, S. C. M., et al. (2010). Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232, 1423-1432. doi: 10.1007/s00425-010-1265-z
61. Lijavetzky, D., Carbonell-Bejerano, P., Grimplet, J., Bravo, G., Flores, P., Fenoll, J., et al. (2012). Berry flesh and skin ripening features in Vitis vinifera as assessed by transcriptional profiling. PLoS ONE 7:e39547. doi: 10.1371/annotation/fd93800a-3b3c-484d-97a9-190043309e4b
62. Marrs, K. (1996). Functions and regulation of glutathione s-transferases in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 127-158. doi: 10.1146/annurev.arplant.47.1.127
63. Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11, 15-19. doi: 10.1016/j.tplants.2005.11.002
64. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498. doi: 10.1016/j.tplants.2004.08.009
65. Moutinho-Pereira, J., Magalhães, N., Gonçalves, B., Bacelar, E., Brito, M., and Correia, C. (2007). Gas exchange and water relations of three Vitis vinifera L. cultivars growing under Mediterranean climate. Photosynthetica 45, 202-207. doi: 10.1007/s11099-007-0033-1
66. Mullineaux, P. M., Karpinski, S., and Baker, N. R. (2006). Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol. 141, 346-350. doi: 10.1104/pp.106.078162
67. Munné-Bosch, S., Queval, G., and Foyer, C. H. (2013). The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol. 161, 5-19. doi: 10.1104/pp.112.205690
68. Negri, A. S., Prinsi, B., Rossoni, M., Failla, O., Scienza, A., Cocucci, M., et al. (2008). Proteome changes in the skin of the grape cultivar Barbera among different stages of ripening. BMC Genomics 9:378. doi: 10.1186/1471-2164-9-378
69. Neves, C., Sá, C., and Amâncio, S. (1998). Histochemical detection of H2O2 by tissue printing as a precocious marker of rhizogenesis in grapevine. Plant Physiol. Biochem. 36, 817-824. doi: 10.1016/S0981-9428(99)80019-9
70. Noctor, G., and Foyer, C. H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 249-279. doi: 10.1146/annurev.arplant.49.1.249
71. Noctor, G., Gomez, L., Vanacker, H., and Foyer, C. H. (2002). Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J. Exp. Bot. 53, 1283-1304. doi: 10.1093/jexbot/53.372.1283
72. Ozden, M., Demirel, U., and Kahraman, A. (2009). Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Sci. Hortic. 119, 163-168. doi: 10.1016/j.scienta.2008.07.031
73. Passardi, F., Cosio, C., Penel, C., and Dunand, C. (2005). Peroxidases have more functions than a Swiss army knife. Plant Cell Rep. 24, 255-265. doi: 10.1007/s00299-005-0972-6
74. Pastore, C., Zenoni, S., Fasoli, M., Pezzotti, M., Tornielli, G. B., and Filippetti, I. (2013). Selective defoliation affects plant growth, fruit transcriptional ripening program and flavonoid metabolism in grapevine. BMC Plant Biol. 13:30. doi: 10.1186/1471-2229-13-30
75. Peleg, Z., and Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14, 290-295. doi: 10.1016/j.pbi.2011.02.001
76. Peter, B., and Pryce, J. (1977). Oxidative dimerisation of 4-hydroxystilbenes in vitro: production of a grapevine phytoalexin mimic. J. Chem. Soc. Chem. Commun., 208-210.
77. Pezet, R., Gindro, K., Viret, O., and Richter, H. (2004a). Effects of resveratrol, viniferins and pterostilbene on Plasmopara viticola zoospore mobility and disease development. Vitis 43, 145-148.
78. Pezet, R., Gindro, K., Viret, O., and Spring, J.-L. (2004b). Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiol. Mol. Plant Pathol. 65, 297-303. doi: 10.1016/j.pmpp.2005.03.002
79. Pilati, S., Brazzale, D., Guella, G., Milli, A., Ruberti, C., Biasioli, F., et al. (2014). The onset of grapevine berry ripening is characterized by ROS accumulation and lipoxygenase-mediated membrane peroxidation in the skin. BMC Plant Biol. 14:87. doi: 10.1186/1471-2229-14-87
80. Pilati, S., Perazzolli, M., Malossini, A., Cestaro, A., Demattè, L., Fontana, P., et al. (2007). Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at veraison. BMC Genomics 8:428. doi: 10.1186/1471-2164-8-428
81. Pontin, M. A., Piccoli, P. N., Francisco, R., Bottini, R., Martinez-Zapater, J. M., and Lijavetzky, D. (2010). Transcriptome changes in grapevine (Vitis vinifera L.) cv. Malbec leaves induced by ultraviolet-B radiation. BMC Plant Biol. 10:224. doi: 10.1186/1471-2229-10-224
82. Potters, G., De Gara, L., Asard, H., and Horemans, N. (2002). Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol. Biochem. 40, 537-548. doi: 10.1016/S0981-9428(02)01414-6
83. Rabbani, M. A., Maruyama, K., Abe, H., Khan, M. A., Katsura, K., Ito, Y., et al. (2003). Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol. 133, 1755-1767. doi: 10.1104/pp.103.025742
84. Ramel, F., Birtic, S., Ginies, C., Soubigou-Taconnat, L., Triantaphylidès, C., and Havaux, M. (2012). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc. Natl. Acad. Sci. U.S.A. 109, 5535-5540. doi: 10.1073/pnas.1115982109
85. Raskin, I. (1992). Role of salicylic acid in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 439-463. doi: 10.1146/annurev.pp.43.060192.002255
86. Rey, P., Cuiné, S., Eymery, F., Garin, J., Court, M., Jacquot, J.-P., et al. (2005). Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J. 41, 31-42. doi: 10.1111/j.1365-313X.2004.02271.x
87. Rienth, M., Torregrosa, L., Kelly, M. T., Luchaire, N., Pellegrino, A., Grimplet, J., et al. (2014). Is transcriptomic regulation of berry development more important at night than during the day? PLoS ONE 9:e88844. doi: 10.1371/journal.pone.0088844
88. Rizhsky, L., Liang, H., and Mittler, R. (2003). The water-water cycle is essential for chloroplast protection in the absence of stress. J. Biol. Chem. 278, 38921-38925. doi: 10.1074/jbc.M304987200
89. Rocheta, M., Becker, J. D., Coito, J. L., Carvalho, L., and Amâncio, S. (2014). Heat and water stress induce unique transcriptional signatures of heat-shock proteins and transcription factors in grapevine. Funct. Integr. Genomics 14, 135-148. doi: 10.1007/s10142-013-0338-z
90. Rotter, A., Camps, C., Lohse, M., Kappel, C., Pilati, S., Hren, M., et al. (2009). Gene expression profiling in susceptible interaction of grapevine with its fungal pathogen Eutypa lata: extending MapMan ontology for grapevine. BMC Plant Biol. 9:104. doi: 10.1186/1471-2229-9-104
91. Santner, A., and Estelle, M. (2009). Recent advances and emerging trends in plant hormone signaling. Nature 459:1071-1078. doi: 10.1038/nature08122
92. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., et al. (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279-292. doi: 10.1046/j.1365-313X.2002.01359.x
93. Sgherri, C., Ranieri, A., and Quartacci, M. F. (2013). Antioxidative responses in Vitis vinifera infected by grapevine fanleaf virus. J. Plant Physiol. 170, 121-128. doi: 10.1016/j.jplph.2012.09.016
94. Skopelitis, D. S., Paranychianakis, N. V., Paschalidis, K., Pliakonis, E. D., Delis, I. D., Yakoumakis, D. I., et al. (2006). Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18, 2767-2781. doi: 10.1105/tpc.105.038323
95. Stoll, M., Loveys, B., and Dry, P. (2000). Hormonal changes induced by partial rootzone drying of irrigated grapevine. J. Exp. Bot. 51, 1627-1634. doi: 10.1093/jexbot/51.350.1627
96. Tassoni, A., Fornalè, S., Franceschetti, M., Musiani, F., Michael, A. J., Perry, B., et al. (2005). Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv. Barbera cell cultures. New Phytol. 166, 895-905. doi: 10.1111/j.1469-8137.2005.01383.x
97. Tattersall, E. (2006). Changes in Gene Expression in Response to Abiotic Stress in Grapevine (Vitis Vinifera). Ph.D. thesis, University of Reno, Nevada: ProQuest.
98. Tenore, G. C., Troisi, J., Di Fiore, R., Manfra, M., and Novellino, E. (2011). Nutraceutical value and toxicological profile of selected red wines from Morocco. Food Chem. 129, 792-798. doi: 10.1016/j.foodchem.2011.05.022
99. Terrier, N., Glissant, D., Grimplet, J., Barrieu, F., Abbal, P., Couture, C., et al. (2005). Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222, 832-847. doi: 10.1007/s00425-005-0017-y
100. Triantaphylidès, C., and Havaux, M. (2009). Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci. 14, 219-228. doi: 10.1016/j.tplants.2009.01.008
101. Vannozzi, A., Dry, I. B., Fasoli, M., Zenoni, S., and Lucchin, M. (2012). Genome-wide analysis of the grapevine stilbene synthase multigenic family: genomic organization and expression profiles upon biotic and abiotic stresses. BMC Plant Biol. 12:130. doi: 10.1186/1471-2229-12-130
102. Vergara, R., Parada, F., Rubio, S., and Pérez, F. J. (2012). Hypoxia induces H2O2 production and activates antioxidant defence system in grapevine buds through mediation of H2O2 and ethylene. J. Exp. Bot. 63, 4123-4131. doi: 10.1093/jxb/ers094
103. Vidigal, P., Carvalho, R., Amâncio, S., and Carvalho, L. (2013). Peroxiredoxins are involved in two independent signaling pathways in the abiotic stress protection in Vitis vinifera. Biol. Plant. 57, 675-683. doi: 10.1007/s10535-013-0346-9
104. Vidigal, P., Martin-Hernandez, A. M., Guiu-Aragonés, V., Amâncio, S., and Carvalho, L. C. (2014). Selective silencing of 2Cys and type-IIB Peroxiredoxins discloses their roles in cell redox state and stress signaling. J. Integr. Plant Biol. doi: 10.1111/jipb.12296. [Epub ahead of print].
105. Vilela, B. J., Carvalho, L. C., and Amâncio, S. (2008). Integration of stress produced reactive oxygen species in the stomatal regulation of micropropagated Vitis vinifera L. plantlets impaired in ABA signaling. Plant Signal. Behav. 3, 558-559. doi: 10.1007/s00299-007-0427-3
106. Vilela, B. J., Carvalho, L. C., Ferreira, J., and Amâncio, S. (2007). Gain of function of stomatal movements in rooting Vitis vinifera L. plants: regulation by H2O2 is independent of ABA before the protruding of roots. Plant Cell Rep. 26, 2149-2157. doi: 10.1007/s00299-007-0427-3
107. Wang, D., Pajerowska-Mukhtar, K., Culler, A. H., and Dong, X. (2007). Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17, 1784-1790. doi: 10.1016/j.cub.2007.09.025
108. Wang, L.-J., Fan, L., Loescher, W., Duan, W., Liu, G.-J., Cheng, J.-S., et al. (2010). Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol. 10:34. doi: 10.1186/1471-2229-10-34
109. Wang, L., and Li, S. (2006). Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci. 170, 685-694. doi: 10.1016/j.plantsci.2005.09.005
110. Wen, P.-F., Chen, J.-Y., Kong, W.-F., Pan, Q.-H., Wan, S.-B., and Huang, W.-D. (2005). Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci. 169, 928-934. doi: 10.1016/j.plantsci.2005.06.011
111. Werner, T., and Schmülling, T. (2009). Cytokinin action in plant development. Curr. Opin. Plant Biol. 12, 527-538. doi: 10.1016/j.pbi.2009.07.002
112. Wetztein, H. I., and Sommer, H. E. (1982). Leaf anatomy of tissue cultured Liquidambar styraciflua (Hamamelidaceae) during acclimatization. Am. J. Bot. 69, 1579-1586. doi: 10.2307/2442913
113. Yang, Y., He, M., Zhu, Z., Li, S., Xu, Y., Zhang, C., et al. (2012). Identification of the dehydrin gene family from grapevine species and analysis of their responsiveness to various forms of abiotic and biotic stress. BMC Plant Biol. 12:140. doi: 10.1186/1471-2229-12-140
114. Yoshida, K., Terashima, I., and Noguchi, K. (2007). Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol. 48, 606-614. doi: 10.1093/pcp/pcm033
115. Zenoni, S., Ferrarini, A., Giacomelli, E., Xumerle, L., Fasoli, M., Malerba, G., et al. (2010). Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol. 152, 1787-1795. doi: 10.1104/pp.109.149716