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Effects of ultraviolet C, methyl jasmonate and salicylic acid, alone or in combination, on stilbene biosynthesis in cell suspension cultures of Vitis vinifera L. cv. Cabernet Sauvignon

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Abstract

Vitis vinifera L. cv. Cabernet Sauvignon cell suspension cultures were treated with ultraviolet C (UV-C), methyl jasmonate (MeJA) and salicylic acid (SA), alone or in combination, to investigate the effects on stilbene biosynthesis. The application of elicitors at the proper dosage or concentration did not exert a negative effect on cell growth. All treatments enhanced both stilbene production inside the cells and trans-resveratrol accumulation in the culture medium. UV-C irradiation for 20 min or MeJA at 100 μM was efficient in promoting stilbene accumulation. The combined treatment of UV-C and MeJA highly induced total intracellular stilbene production to the maximum of 2005.05 ± 63.03 μg g−1 DW, and showed a synergistic effect on extracellular trans-resveratrol accumulation to 3.96 ± 0.2 mg l−1. SA at 100 μM was less efficient than UV-C and MeJA in promoting stilbene production. However, the combined elicitation of UV-C and SA further promoted intracellular stilbene production to the maximum of 1630.93 ± 44.17 μg g−1 DW, and markedly increased extracellular trans-resveratrol accumulation to 2.33 ± 0.15 mg l−1. Intracellular total phenolics and total flavonoids contents also significantly increased after elicitations. Relative expression of genes involved in stilbene and flavonoid biosynthesis was up-regulated, and there was a synergistic effect of UV-C together with MeJA or SA on STS expression. The results suggested that the combined treatment of UV-C together with MeJA or SA can be used as an efficient method to enhance stilbene production in V. vinifera cell cultures.

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Abbreviations

4CL:

4-Coumarate:CoA ligase

C4H:

Cinnamate 4-hydroxylase

CHS:

Chalcone synthase

DW:

Dry weight

FW:

Fresh weight

JA:

Jasmonic acid

MeJA:

Methyl jasmonate

PAL:

Phenylalanine ammonia lyase

qPCR:

Quantitative real-time polymerase chain reaction

SA:

Salicylic acid

STS:

Stilbene synthase

UV-C:

Ultraviolet C

References

  • Ali M, Abbasi BH, Ali GS (2015) Elicitation of antioxidant secondary metabolites with jasmonates and gibberellic acid in cell suspension cultures of Artemisia absinthium L. Plant Cell Tissue Organ Cult 120:1099–1106. doi:10.1007/s11240-014-0666-2

    Article  CAS  Google Scholar 

  • Almagro L, Gutierrez J, Pedreño MA, Sottomayor M (2014) Synergistic and additive influence of cyclodextrins and methyl jasmonate on the expression of the terpenoid indole alkaloid pathway genes and metabolites in Catharanthus roseus cell cultures. Plant Cell Tissue Organ Cult 119:543–551. doi:10.1007/s11240-014-0554-9

    Article  CAS  Google Scholar 

  • Belchí-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreño MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyljasmonate. Plant Cell Rep 31:81–99. doi:10.1007/s00299-011-1141-8

    Article  PubMed  Google Scholar 

  • Belhadj A, Saigne C, Telef N, Cluzet S, Bouscaut J, Corio-Costet MF, Mérillon JM (2006) Methyl jasmonate induces defense responses in grapevine and triggers protection against Erysiphe necator. J Agric Food Chem 54:9119–9125. doi:10.1021/jf0618022

    Article  CAS  PubMed  Google Scholar 

  • Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon JM (2008) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem 46:493–499. doi:10.1016/j.plaphy.2007.12.001

    Article  CAS  PubMed  Google Scholar 

  • Bulgakov VP, Tchernoded GK, Mischenko NP, Khodakovskaya MV, Glazunov VP, Radchenko SV, Zvereva EV, Fedoreyev SA, Zhuravlev YN (2002) Effect of salicylic acid, methyl jasmonate, ethephon and cantharidin on anthraquinone production by Rubia cordifolia callus cultures transformed with the rolB and rolC genes. J Biotechnol 97:213–221. doi:10.1016/S0168-1656(02)00067-6

    Article  CAS  PubMed  Google Scholar 

  • Cai ZZ, Kastell A, Mewis I, Knorr D, Smetanska I (2012) Polysaccharide elicitors enhance anthocyanin and phenolic acid accumulation in cell suspension cultures of Vitis vinifera. Plant Cell Tissue Organ Cult 108:401–409. doi:10.1007/s11240-011-0051-3

    Article  CAS  Google Scholar 

  • Chen JY, Wen PF, Kong WF, Pan QH, Zhan JC, Li JM, Wan SB, Huang WD (2006) Effect of salicylic acid on phenylpropanoids and phenylalanine ammonia-lyase in harvested grape berries. Postharvest Biol Technol 40:64–72. doi:10.1016/j.postharvbio.2005.12.017

    Article  CAS  Google Scholar 

  • Chung IM, Park MR, Chun JC, Yun SJ (2003) Resveratrol accumulation and resveratrol synthase gene expression in response to abiotic stresses and hormones in peanut plants. Plant Sci 164:103–109. doi:10.1016/S0168-9452(02)00341-2

    Article  CAS  Google Scholar 

  • Crupi P, Pichierri A, Basile T, 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.2013.03.055

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097. doi:10.1105/tpc.7.7.1085

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266–274. doi:10.1016/S1360-1385(97)86349-2

    Article  Google Scholar 

  • Fang F, Huang WD (2013) Salicylic acid modulated flavonol biosynthesis in three key phases during grape berry development. Eur Food Res Technol 237:441–448. doi:10.1007/s00217-013-2008-8

    Article  CAS  Google Scholar 

  • Fernández-Marín MI, Puertas B, Guerrero RF, García-Parrilla MC, Cantos-Villar E (2014) Preharvest methyl jasmonate and postharvest UVC treatments: increasing stilbenes in wine. J Food Sci 79:310–317. doi:10.1111/1750-3841.12368

    Article  Google Scholar 

  • Gadzovska S, Maury S, Delaunay A, Spasenoski M, Hagège D, Courtois D, Joseph C (2013) The influence of salicylic acid elicitation of shoots, callus, and cell suspension cultures on production of naphtodianthrones and phenylpropanoids in Hypericum perforatum L. Plant Cell Tissue Organ Cult 113:25–39. doi:10.1007/s11240-012-0248-0

    Article  CAS  Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158. doi:10.1016/0014-4827(68)90403-5

    Article  CAS  PubMed  Google Scholar 

  • Guerrero RF, Puertas B, Fernández MI, Palma M, Cantos-Villar E (2010) Induction of stilbenes in grapes by UV-C Comparison of different subspecies of Vitis. Innov Food Sci Emerg Technol 11:231–238. doi:10.1016/j.ifset.2009.10.005

    Article  CAS  Google Scholar 

  • Hu YH, Yu YT, Piao CH, Liu JM, Yu HS (2011) Methyl jasmonate- and salicylic acid-induced D-chiro-inositol production in suspension cultures of buckwheat (Fagopyrum esculentum). Plant Cell Tissue Organ Cult 106:419–424. doi:10.1007/s11240-011-9938-2

    Article  CAS  Google Scholar 

  • Jeandet P, Douillt-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agric Food Chem 50:2731–2741. doi:10.1021/jf011429s

    Article  CAS  PubMed  Google Scholar 

  • Krzyzanowska J, Czubacka A, Pecio L, Przybys M, Doroszewska T, Stochmal A, Oleszek W (2012) The effects of jasmonic acid and methyl jasmonate on rosmarinic acid production in Mentha × piperita cell suspension cultures. Plant Cell Tissue Organ Cult 108:73–81. doi:10.1007/s11240-011-0014-8

    Article  CAS  Google Scholar 

  • Langcake P, Pryce RJ (1977) The production of resveratrol and viniferins by grapevines in response to ultraviolet irradiation. Phytochemistry 16:1193–1196. doi:10.1016/S0031-9422(00)94358-9

    Article  CAS  Google Scholar 

  • Larkin PJ (1976) Purification and viability determinations of plant protoplasts. Planta 128:213–216. doi:10.1007/BF00393231

    Article  CAS  PubMed  Google Scholar 

  • Larronde F, Krisa S, Decendit A, Cheze C, Merillon JM (1998) Regulation of polyphenol production in Vitis vinifera cell suspension cultures by sugars. Plant Cell Rep 17:946–950. doi:10.1007/s002990050515

    Article  CAS  Google Scholar 

  • Liu W, Liu CY, Yang CX, Wang LJ, Li SH (2010) Effect of grape genotype and tissue type on callus growth and production of resveratrols and their piceids after UV-C irradiation. Food Chem 122:475–481. doi:10.1016/j.foodchem.2010.03.055

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. doi:10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Logemann E, Tavernaro A, Schulz WG, Somssich IE, Hahlbrock K (2000) UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proc Natl Acad Sci USA 97:1903–1907. doi:10.1073/pnas.97.4.1903

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Morales M, Bru R, García-Carmona F, Barceló AR, Pedreño MA (1998) Effect of dimethyl-β-cyclodextrins on resveratrol metabolism in Gamay grapevine cell cultures before and after inoculation with Xylophilus ampelinus. Plant Cell Tissue Organ Cult 53:179–187. doi:10.1023/A:1006027410575

    Article  CAS  Google Scholar 

  • Nopo-Olazabal C, Condori J, Nopo-Olazabal L, Medina-Bolivar F (2014) Differential induction of antioxidant stilbenoids in hairy roots of Vitis rotundifolia treated with methyl jasmonate and hydrogen peroxide. Plant Physiol Biochem 74:50–69. doi:10.1016/j.plaphy.2013.10.035

    Article  CAS  PubMed  Google Scholar 

  • Palomer X, Capdevila-Busquets E, Álvarez-Guardia D, Barroso E, Pallàs M, Camins A, Davidson MM, Planavila A, Villarroya F, Vázquez-Carrera M (2013) Resveratrol induces nuclear factor-κB activity in human cardiac cells. Int J Cardiol 167:2507–2516. doi:10.1016/j.ijcard.2012.06.006

    Article  PubMed  Google Scholar 

  • Pastrana-Bonilla E, Akoh CC, Sellappan S, Krewer G (2003) Phenolic content and antioxidant capacity of muscadine grapes. J Agric Food Chem 51:5497–5503. doi:10.1021/jf030113c

    Article  CAS  PubMed  Google Scholar 

  • Pezet R, Perret C, Jean-Denis JB, Tabacchi R, Gindro K, Viret O (2003) δ-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

    Article  CAS  PubMed  Google Scholar 

  • Pezet R, Gindro K, Viret O, Spring JL (2004) 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

    Article  CAS  Google Scholar 

  • Qu JG, Zhang W, Yu XJ (2011) A combination of elicitation and precursor feeding leads to increased anthocyanin synthesis in cell suspension cultures of Vitis vinifera. Plant Cell Tissue Organ Cult 107:261–269. doi:10.1007/s11240-011-9977-8

    Article  CAS  Google Scholar 

  • Riha J, Brenner S, Böhmdorfer M, Giessrigl B, Pignitter M, Schueller K, Thalhammer T, Stieger B, Somoza V, Szekeres T, Jäger W (2014) Resveratrol and its major sulfated conjugates are substrates of organic anion transporting polypeptides (OATPs): impact on growth of ZR-75-1 breast cancer cells. Mol Nutr Food Res 58:1830–1842. doi:10.1002/mnfr.201400095

    Article  CAS  PubMed  Google Scholar 

  • Sansanelli S, Zanichelli D, Filippini A, Ferri M, Tassoni A (2014) Production of free and glycosylated isoflavones in in vitro soybean (Glycine max L.) hypocotyl cell suspensions and comparison with industrial seed extracts. Plant Cell Tissue Organ Cult 119:301–311. doi:10.1007/s11240-014-0534-0

    Article  CAS  Google Scholar 

  • Santamaria AR, Innocenti M, Mulinacci N, Melani F, Valletta A, Sciandra I, Pasqua G (2012) Enhancement of viniferin production in Vitis vinifera L. cv. Alphonse Lavallée cell suspensions by low-energy ultrasound alone and in combination with methyl jasmonate. J Agric Food Chem 60:11135–11142. doi:10.1021/jf301936u

    Article  CAS  PubMed  Google Scholar 

  • Shumakova OA, Manyakhin AY, Kiselev KV (2011) Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in cell cultures of Vitis amurensis treated with coumaric acid. Appl Biochem Biotechnol 165:1427–1436. doi:10.1007/s12010-011-9361-5

    Article  CAS  PubMed  Google Scholar 

  • Silja PK, Gisha GP, Satheeshkumar K (2014) Enhanced plumbagin accumulation in embryogenic cell suspension cultures of Plumbago rosea L. following elicitation. Plant Cell Tissue Organ Cult 119:469–477. doi:10.1007/s11240-014-0547-8

    Article  CAS  Google Scholar 

  • Soleas GJ, Diamandis EP, Goldberg DM (1997) Resveratrol: a molecule whose time has come and gone. Clin Biochem 30:91–113. doi:10.1016/S0009-9120(96)00155-5

    Article  CAS  PubMed  Google Scholar 

  • Tassoni A, Fornale S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (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

    Article  CAS  PubMed  Google Scholar 

  • Tassoni A, Durante L, Ferri M (2012) Combined elicitation of methyl-jasmonate and red light on stilbene and anthocyanin biosynthesis. J Plant Physiol 169:775–781. doi:10.1016/j.jplph.2012.01.017

    Article  CAS  PubMed  Google Scholar 

  • Vang O, Ahmad N, Baile CA, Baur JA, Brown K, Csiszar A, Das DK, Delmas D, Gottfried C, Lin HY, Ma QY, Mukhopadhyay P, Nalini N, Pezzuto JM, Richard T, Shukla Y, Surh YJ, Szekeres T, Szkudelski T, Walle T, Wu JM (2011) What is new for an old molecule? Systematic review and recommendations on the use of resveratrol. PLoS One 6:e19881. doi:10.1371/journal.pone.0019881

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang CY, Chen CT, Wang SY (2009) Changes of flavonoid content and antioxidant capacity in blueberries after illumination with UV-C. Food Chem 117:426–431. doi:10.1016/j.foodchem.2009.04.037

    Article  CAS  Google Scholar 

  • Wang HL, Wang W, Zhang P, Pan QH, Zhan JC, Huang WD (2010a) Gene transcript accumulation, tissue and subcellular localization of anthocyanidin synthase (ANS) in developing grape berries. Plant Sci 179:103–113. doi:10.1016/j.plantsci.2010.04.002

    Article  CAS  Google Scholar 

  • Wang W, Tang K, Yang HR, Wen PF, Zhang P, Wang HL, Huang WD (2010b) Distribution of resveratrol and stilbene synthase in young grape plants (Vitis vinifera L. cv. Cabernet Sauvignon) and the effect of UV-C on its accumulation. Plant Physiol Biochem 48:142–152. doi:10.1016/j.plaphy.2009.12.002

    Article  CAS  PubMed  Google Scholar 

  • Wang LJ, Ma L, Xi HF, Duan W, Wang JF, Li SH (2013) Individual and combined effects of CaCl2 and UV-C on the biosynthesis of resveratrols in grape leaves and berry skins. J Agric Food Chem 61:7135–7141. doi:10.1021/jf401220m

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Guo LP, Xie T, Yang J, Tang JF, Li X, Wang X, Huang LQ (2014) Different secondary metabolic responses to MeJA treatment in shikonin-proficient and shikonin-deficient cell lines from Arnebia euchroma (Royle) Johnst. Plant Cell Tissue Organ Cult 119:587–598. doi:10.1007/s11240-014-0558-5

    Article  CAS  Google Scholar 

  • Wasternack C, Parthier B (1997) Jasmonate-signalled plant gene expression. Trends Plant Sci 2:302–307. doi:10.1016/S1360-1385(97)89952-9

    Article  Google Scholar 

  • Waterhouse AL, Lamuela-Raventós RM (1994) The occurrence of piceid, a stilbene glucoside in grape berries. Phytochemistry 37:571–573. doi:10.1016/0031-9422(94)85102-6

    Article  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493. doi:10.1104/pp.126.2.485

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wolfe K, Wu XZ, Liu RH (2003) Antioxidant activity of apple peels. J Agric Food Chem 51:609–614. doi:10.1021/jf020782a

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Zhu WH, Hu Q (2001) Enhanced catharanthine production in Catharanthus roseus cell cultures by combined elicitor treatment in shake flasks and bioreactors. Enzyme Microb Technol 28:673–681. doi:10.1016/S0141-0229(01)00306-4

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was funded by the National Natural Science Foundation of China (No. 31471835) and the National “Twelfth Five-Year” Plan for Science and Technology Support (2012BAD31B07).

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The authors declare that they have no conflict of interest.

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  1. College of Food Science and Nutritional Engineering, Beijing Key Laboratory of Viticulture and Enology, China Agricultural University, Beijing, 100083, People’s Republic of China

    Ai Xu, Ji-Cheng Zhan & Wei-Dong Huang

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  1. Ai Xu
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  2. Ji-Cheng Zhan
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Correspondence to Ji-Cheng Zhan or Wei-Dong Huang.

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Xu, A., Zhan, JC. & Huang, WD. Effects of ultraviolet C, methyl jasmonate and salicylic acid, alone or in combination, on stilbene biosynthesis in cell suspension cultures of Vitis vinifera L. cv. Cabernet Sauvignon. Plant Cell Tiss Organ Cult 122, 197–211 (2015). https://doi.org/10.1007/s11240-015-0761-z

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