Transcriptomic and metabolomic networks in the grape berry illustrate that it takes more than flavonoids to fight against ultraviolet radiation

Frontiers in Plant Science

Volumn 7, Issue AUG2016, 2016, Pages

  Matus, José Tomás ^a  

^a CSIC   (Spain)

Author keywords

Anthocyanins; Flavonols; HY5; Light; MYB; Ripening; Stilbene; Terpenes

Indexed keywords

EID: 84986578185     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01337     Document Type: Review

References (57)

1. Adrian, M., Jeandet, P., Douillet-Breuil, A. C., Tesson, L., and Bessis, R. (2000). Stilbene content of mature Vitis vinifera berries in response to UV-C elicitation. J. Agric. Food Chem. 12, 6103-6105. doi: 10.1021/jf0009910
2. Almagro, L., Carbonell-Bejerano, P., Belchí-Navarro, S., Bru, R., Martínez-Zapater, J. M., Lijavetzky, D., et al. (2014). Dissecting the transcriptional response to elicitors in Vitis vinifera cells. PLoS ONE 9: e109777. doi: 10.1371/journal.pone.0109777
3. Berli, F. J., Fanzone, M., Piccoli, P., and Bottini, R. (2011). Solar UV-B and ABA are involved in phenol metabolism of Vitis vinifera L. increasing biosynthesis of berry skin polyphenols. J. Agric. Food Chem. 59, 4874-4884. doi: 10.1021/jf200040z
4. Bohlmann, J., and Keeling, C. I. (2008). Terpenoid biomaterials. Plant J. 4, 656-669. doi: 10.1111/j.1365-313X.2008.03449.x
5. Brown, B. A., Cloix, C., Jiang, G. H., Kaiserli, E., Herzyk, P., Kliebenstein, D. J., et al. (2005). AUV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U.S.A. 102, 18225-18230. doi: 10.1073/pnas.0507187102
6. Carbonell-Bejerano, P., Diago, M. P.,Martínez-Abaigar, J.,Martínez-Zapater, J. M., Tardáguila, J., and Núñez-Olivera, E. (2014). Solar ultraviolet radiation is necessary to enhance grapevine fruit ripening transcriptional and phenolic responses. BMC Plant Biol. 14: 183. doi: 10.1186/1471-2229-14-183
7. Cavallini, E.,Matus, J. T., Finezzo, L., Zenoni, S., Loyola, R., Guzzo, F., et al. (2015). The phenylpropanoid pathway is controlled at different branches by a set of R2R3-MYB C2 repressors in grapevine. Plant Physiol. 167, 1448-1470. doi: 10.1104/pp.114.256172
8. Chen, X., Yao, Q., Gao, X., Jiang, C., Harberd, N. P., and Fu, X. (2016). Shoot-toroot mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26, 640-646. doi: 10.1016/j.cub.2015.12.066
9. Crupi, P., Pichierri, A., Basile, T., and Antonacci, D. (2013). Postharvest stilbenes and flavonoids enrichment of table grape cv Redglobe (Vitis vinifera L.) as affected by interactive UV-C exposure and storage conditions. Food Chem. 141, 802-808. doi: 10.1016/j.foodchem.03.055
10. Demkura, P. V., and Ballaré, C. L. (2012). UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation. Mol. Plant. 5, 642-652. doi: 10.1093/mp/sss025
11. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., and Lepiniec, L. (2010). MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573-581. doi: 10.1016/j.tplants.2010.06.005
12. Frohnmeyer, H., and Staiger,D. (2003). Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol. 133, 1420-1428. doi: 10.1104/pp.103.030049
13. Gil, M., Pontin, M., Berli, F., Bottini, R., and Piccoli, P. (2012). Metabolism of terpenes in the response of grape (Vitis vinifera L.) leaf tissues to UV-B radiation. Phytochemistry. 77, 89-98. doi: 10.1016/j.phytochem.2011. 12.011
14. Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S., and Lauvergeat, V. (2011). Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 62, 2465-2483. doi: 10.1093/jxb/erq442
15. Höll, J., Vannozzi, A., Czemmel, S., D’Onofrio, C., Walker, A. R., Rausch, T., et al. (2013). The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera. Plant Cell 25, 4135-4149. doi: 10.1105/tpc.113.117127
16. Jenkins, G. I. (2009). Signal transduction in responses to UV-B radiation. Annu. Rev. Plant Biol. 60, 407-431. doi: 10.1146/annurev.arplant.59.032607. 092953
17. Jiang, L., Wang, Y., Björn, L. O., He, J. X., and Li, S. (2012). Sensing of UV-B radiation by plants. Plant Signal. Behav. 7, 999-1003. doi: 10.4161/psb.20815
18. Jordan, B. R. (2002). Molecular response of plant cells to UV-B stress. Funct. Plant Biol. 29, 909-916. doi: 10.1071/FP02062
19. Joubert, C., Young, P. R., Eyeghe-Bickong, H. A., and Vivier, M. A. (2016). Field-grown grapevine berries use carotenoids and the associated xanthophyll cycles to acclimate to UV exposure differentially in high and low light (shade) conditions. Front. Plant Sci. 7: 786. doi: 10.3389/fpls.2016.00786
20. Kolb, C. A., Käser, M. A., Kopecký, J., Zotz, G., Riederer, M., and Pfündel, E. E. (2001). Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. Plant Physiol. 127, 863-875. doi: 10.1104/pp.010373
21. Kolb, C. A., Kopecky, J., Riederer, M., and Pfundel, E. E. (2003). UV screening by phenolics in berries of grapevine (Vitis vinifera). Funct. Plant Biol. 30, 1177-1186. doi: 10.1071/FP03076
22. Liu, L., Gregan, S., Winefield, C., and Jordan, B. (2014). From UVR8 to flavonol synthase: UV-B-induced gene expression in Sauvignon blanc grape berry. Plant Cell Environ. 38, 905-919. doi: 10.1111/pce.12349
23. Llorente, B., D’Andrea, L., and Rodríguez-Concepción, M. (2016). Evolutionary recycling of light signaling components in fleshy fruits: new insights on the role of pigments to monitor ripening. Front. Plant. Sci. 7: 263. doi: 10.3389/fpls.2016.00263
24. Loyola, R., Herrera, D., Mas, A., Wong, D. C. J., Höll, J., Cavallini, E., et al. (2016). The photomorphogenic factors UV-B RECEPTOR 1, ELONGATED HYPOCOTYL 5 and HY5 HOMOLOGUE are part of the UV-B signalling pathway in grapevine and mediate flavonol accumulation in response to the environment. J. Exp. Bot. doi: 10.1093/jxb/erw307 [Epub ahead of print].
25. Luan, F., and Wüst, M. (2002). Differential incorporation of 1-deoxy-Dxylulose into (3S)-linalool and geraniol in grape berry exocarp and mesocarp. Phytochemistry 60, 451-459. doi: 10.1016/S0031-9422(02) 00147-4
26. Mackerness, S. (2000). Plant responses to ultraviolet-B (UV-B: 280-320 nm) stress: what are the key regulators? Plant Growth Regul. 32, 27-39. doi: 10.1023/A: 1006314001430
27. Madronich, S., McKenzie, R. L., Björn, L. O., and Caldwell, M. M. (1998). Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J. Photochem. Photobiol. B 46, 5-19. doi: 10.1016/S1011-1344(98)00182-1
28. Malacarne, G., Coller, E., Czemmel, S., Vrhovsek, U., Engelen, K., Goremykin, V., et al. (2016). The grapevine VvibZIPC22 transcription factor is involved in the regulation of flavonoid biosynthesis. J. Exp. Bot. 67, 3509-3522. doi: 10.1093/jxb/erw181
29. Martin, D. M., Aubourg, S., Schouwey, M. B., Daviet, L., Schalk, M., Toub, O., et al. (2010). Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol. 10: 226. doi: 10.1186/1471-2229-10-226
30. Martínez-Lüscher, J., Sánchez-Díaz, M., Delrot, S., Aguirreolea, J., Pascual, I., and Gomès, E. (2014). Ultraviolet-B radiation and water deficit interact to alter flavonol and anthocyanin profiles in grapevine berries through transcriptomic regulation. Plant Cell Physiol. 55, 1925-1936. doi: 10.1093/pcp/pcu121
31. Matus, J. T., Aquea, F., and Arce-Johnson, P. (2008). Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol. 8: 83. doi: 10.1186/1471-2229-8-83
32. Matus, J. T., Loyola, R., Vega, A., Peña-Neira, A., Bordeu, E., Arce-Johnson, P., et al. (2009). Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. J. Exp. Bot. 60, 853-867. doi: 10.1093/jxb/ern336
33. McKenzie, R. L., Björn, L. O., Bais, A., and Ilyasad, M. (2003). Changes in biologically active ultraviolet radiation reaching the Earth’s surface. Photochem. Photobiol. Sci. 2, 5-15.
34. Neves, A. R., Lucio, M., Lima, J. L., and Reis, S. (2012). Resveratrol in medicinal chemistry: a critical review of its pharmacokinetics, drugdelivery, and membrane interactions. Curr. Med. Chem. 19, 1663-1681. doi: 10.2174/092986712799945085
35. Parage, C., Tavares, R., Réty, S., Baltenweck-Guyot, R., Poutaraud, A., Renault, L., et al. (2012). Structural, functional, and evolutionary analysis of the unusually large stilbene synthase gene family in grapevine. Plant Physiol. 160, 1407-1419. doi: 10.1104/pp.112.202705
36. 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
37. Pezet, R., Perret, C., Jean-Denis, J. B., Tabacchi, R., Gindro, K., and Viret, O. (2003). Delta-viniferin, a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves. J. Agric. Food Chem. 51, 5488-5492. doi: 10.1021/jf030227o
38. Pontin, M., Piccoli, P., 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
39. Rizzini, L., Favory, J. J., Cloix, C., Faggionato, D., O’Hara, A., Kaiserli, E., et al. (2011). Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103-106. doi: 10.1126/science.1200660
40. Robson, T. M., Klem, K., Urban, O., and Jansen, M. A. (2015). Re-interpreting plant morphological responses to UV-B radiation. Plant Cell Environ. 38, 856-866. doi: 10.1111/pce.12374
41. Sasaki, K., Takase, H., Matsuyama, S., Kobayashi, H., Matsuo, H., Ikoma, G., et al. (2016). Effect of light exposure on linalool biosynthesis and accumulation in grape berries. Biosci. Biotechnol. Biochem. 4, 1-7. doi: 10.1080/09168451.2016.1217148
42. Savoi, S., Wong, D. C., Arapitsas, P., Miculan, M., Bucchetti, B., Peterlunger, E., et al. (2016). Transcriptome and metabolite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes (Vitis vinifera L.). BMC Plant Biol. 16: 67. doi: 10.1186/s12870-016-0760-1
43. Shin, D. H., Choi, M., Kim, K., Bang, G., Cho, M., Choi, S. B., et al. (2013). HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett. 587, 1543-1547. doi: 10.1016/j.febslet.2013.03.037
44. Shirley, B. W. (1996). Flavonoid biosynthesis: ʼnew’ functions for an ‘old’ pathway. Trends Plant Sci. 1, 377-382. doi: 10.1016/S1360-1385(96)80312-8
45. Song, J., Smart, R., Wang, H., Dambergs, B., Sparrow, A., and Qian, M. C. (2015). Effect of grape bunch sunlight exposure and UV radiation on phenolics and volatile composition of Vitis vinifera L. cv. Pinot noir wine. Food Chem. 173, 424-431. doi: 10.1016/j.foodchem.2014.09.150
46. Stapleton, A. E. (1992). Ultraviolet radiation and plants: burning questions. Plant Cell 4, 1353-1358. doi: 10.1105/tpc.4.11.1353
47. Stracke, R., Favory, J. J., Gruber, H., Bartelniewoehner, L., Bartels, S., Binkert, M., et al. (2010). The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ. 33, 88-103. doi: 10.1111/j.1365-3040.2009.02061.x
48. Suzuki, M., Nakabayashi, R., Ogata, Y., Sakurai, N., Tokimatsu, T., Goto, S., et al. (2015). Multiomics in grape berry skin revealed specific induction of the stilbene synthetic pathway by ultraviolet-C irradiation. Plant Physiol. 168, 47-59. doi: 10.1104/pp.114.254375
49. Tattini, M., Loreto, F., Fini, A., Guidi, L., Brunetti, C., Velikova, V., et al. (2015). Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus × acerifolia plants during Mediterranean summers. New Phytol. 207, 613-626. doi: 10.1111/nph.13380
50. Ulm, R., Baumann, A., Oravecz, A., Máté, Z., Adám, E., Oakeley, E. J., et al. (2004). Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 1397-1402. doi: 10.1073/pnas.0308044100
51. Vannozzi, A., Dry, I. B., Fasoli, M., Zenoni, S., and Lucchin, M. (2012). Genomewide 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
52. Vezzulli, S., Civardi, S., Ferrari, F., and Bavaresco, L. (2007). Methyl jasmonate treatment as a trigger of resveratrol synthesis in cultivated grapevine. Am. J. Enol. Vitic. 58, 530-533.
53. Wen, Y. Q., Zhong, G. Y., Gao, Y., Lan, Y. B., Duan, C. Q., and Pan, Q. H. (2015). Using the combined analysis of transcripts and metabolites to propose key genes for differential terpene accumulation across two regions. BMC Plant Biol. 15: 240. doi: 10.1186/s12870-015-0631-1
54. Wolf, L., Rizzini, L., Stracke, R., Ulm, R., and Rensing, S. A. (2010). The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiol. 153, 1123-1134. doi: 10.1104/pp.110.154658
55. Wong, D. C. J., Schlechter, R., Vannozzi, A., Höll, J., Hmmam, I., Bogs, J., et al. (2016). A systems-oriented analysis of the grapevine R2R3-MYB transcription factor family uncovers new insights into the regulation of stilbene accumulation. DNA Res. doi: 10.1093/dnares/dsw028 [Epub ahead of print].
56. Young, P. R., Eyeghe-Bickong, H. A., du Plessis, K., Alexandersson, E., Jacobson, D. A., Coetzee, Z., et al. (2016). Grapevine plasticity in response to an altered microclimate: sauvignon blanc modulates specific metabolites in response to increased berry exposure. Plant Physiol. 170, 1235-1254. doi: 10.1104/pp.15.01775
57. Zhang, Z. Z., Che, X. N., Pan, Q. H., Li, X. X., and Duan, C. Q. (2013). Transcriptional activation of flavan-3-ols biosynthesis in grape berries by UV irradiation depending on developmental stage. Plant Sci. 208, 64-74. doi: 10.1016/j.plantsci.2013.03.013