Abstract
Plant cell and tissue cultures are considered as a source of valuable secondary metabolites but usually produce insufficient level of the compounds, which is the limiting factor for their application in biotechnology. We obtained 18 callus cell cultures from different organs of wild grape Vitis amurensis Rupr. collected at different seasons and analyzed stilbene accumulation in combination with calli growth parameters. This analysis showed that temporal and tissue origin of the calli affected the rate of stilbene biosynthesis. Stem-derived calli accumulated higher stilbene levels and exhibited a higher expression of phenylalanine ammonia-lyase (PAL) and stilbene synthase (STS) genes than calli derived from the leaves and petioles. The highest content of stilbenes was detected in the calli initiated from grapevine stems collected in the autumn. In general, all “autumn” cell cultures contained more than 2 mg g− 1 dry wt (up to 11 mg g− 1 dry wt) and exhibited high PAL and STS genes expression in comparison with the calli initiated in the summer. The content of stilbenes in the “autumn” cell cultures were comparable to the highest stilbene contents detected in other plant sources described in the literature. Thus, selecting the most optimal explant source for cell culture establishment could be an effective approach towards developing plant cell cultures producing high stilbene levels.
Abbreviations
- HPLC:
-
High-performance liquid chromatography
- STS:
-
Stilbene synthase
- Wt:
-
Weight
References
Aleynova OA, Grigorchuk VP, Dubrovina AS, Rybin VG, Kiselev KV (2016) Stilbene accumulation in cell cultures of Vitis amurensis Rupr. overexpressing VaSTS1, VaSTS2, and VaSTS7 genes. Plant Cell Tissue Organ Cult 125:329–339.
Aleynova OA, Dubrovina AS, Kiselev KV (2017) Activation of stilbene synthesis in cell cultures of Vitis amurensis by calcium-dependent protein kinases VaCPK1 and VaCPK26. Plant Cell Tiss Organ Cult 130:141–152
Aleynova-Shumakova OA, Dubrovina AS, Manyakhin AY, Karetin YA, Kiselev KV (2014) VaCPK20 gene overexpression significantly increased resveratrol content and expression of stilbene synthase genes in cell cultures of Vitis amurensis Rupr.. Appl Microbiol Biotechnol 98:5541–5549
Arora J, Goyal S, Ramawat KG (2010) Enhanced stilbene production in cell cultures of Cayratia trifolia through co-treatment with abiotic and biotic elicitors and sucrose. In Vitro Cell Dev Biol Plant 46:430–436
Chang X, Seo M, Takebayashi Y, Kamiya Y, Riemann M, Nick P (2017) Jasmonates are induced by the PAMP flg22 but not the cell death-inducing elicitor Harpin in Vitis rupestris. Protoplasma 254:271–283
Chong J, Poutaraud A, Hugueney P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177:143–155
Dubrovina AS, Kiselev KV (2016) Age-associated alterations in the somatic mutation and DNA methylation levels in plants. Plant Biol (Stuttg) 18:185–196
Dubrovina AS, Kiselev KV (2017) Regulation of stilbene biosynthesis in plants. Planta 346:597–623
Dubrovina AS, Manyakhin AY, Zhuravlev YN, Kiselev KV (2010)) Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in rolC transgenic cell cultures of Vitis amurensis. Appl Microbiol Biotechnol 88:727–736
Giorcelli A, Sparvoli F, Mattivi F, Tava A, Balestrazzi A, Vrhovsek U, Calligari P, Bollini R, Confalonieri M (2004) Expression of the stilbene synthase (StSy) gene from grapevine in transgenic white poplar results in high accumulation of the antioxidant resveratrol glucosides. Transgenic Res 13:203–214
Huang KS, Lin M, Cheng GF (2001) Anti-inflammatory tetramers of resveratrol from the roots of Vitis amurensis and the conformations of the seven-membered ring in some oligostilbenes. Phytochemistry 58:357–362
Kawiak A, Krolicka A, Lojkowska E (2011) In vitro cultures of Drosera aliciae as a source of a cytotoxic naphthoquinone: ramentaceone. Biotechnol Lett 33:2309–2316
Keskin N, Kunter B (2008) Production of trans-resveratrol in ‘‘Cabernet Sauvignon’’ (Vitis vinifera L.) callus culture in response to ultraviolet-C irradiation. Vitis 47:193–196
Ketel DH, Breteler H, De Groot B (1985) Effect of explant origin on growth and differentiation of calli from Tagetes species. J Plant Physiol 118:327–333
Kiselev KV (2011) Perspectives for production and application of resveratrol. Appl Microbiol Biotechnol 90:417–425
Kiselev KV, Dubrovina AS, Veselova MV, Bulgakov VP, Fedoreyev SA, Zhuravlev YN (2007) The rolB gene-induced overproduction of resveratrol in Vitis amurensis transformed cells. J Biotechnol 128:681–692
Kiselev KV, Dubrovina AS, Isaeva GA, Zhuravlev YN (2010) The effect of salicylic acid on phenylalanine ammonia-lyase and stilbene synthase gene expression in Vitis amurensis cell culture. Russ J Plant Physiol 57:415–448
Kiselev KV, Tyunin AP, Manyakhin AY, Zhuravlev YN (2011) Resveratrol content and expression patterns of stilbene synthase genes in Vitis amurensis cells treated with 5-azacytidine. Plant Cell Tissue Organ Cult 105:65–72
Kiselev KV, Dubrovina AS, Shumakova OA, Karetin YA, Manyakhin AY (2013) Structure and expression profiling of a novel calcium-dependent protein kinase gene, CDPK3a, in leaves, stems, grapes, and cell cultures of wild-growing grapevine Vitis amurensis Rupr.. Plant Cell Rep 32:431–442
Kiselev KV, Aleynova OA, Grigorchuk VP, Dubrovina AS (2017a) Stilbene accumulation and expression of stilbene biosynthesis pathway genes in wild grapevine Vitis amurensis Rupr.. Planta 245:151–159
Kiselev KV, Aleynova OA, Tyunin AP (2017b) Expression of the R2R3 MYB transcription factors in Vitis amurensis Rupr. plants and cell cultures with different resveratrol content. Russ J Genet 53:465–471
Langcake P, Pryce RJ (1977) A new class of phytoalexins from grapevines. Experientia 33:151–152
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
Margara J, Piollat MT (1983) New observations on in vitro organogenesis from begonia x elator petals. Comptes Rendus de l’Académie des Sciences - Series III - Sciences de la Vie 297: 161–164
Martini AN, Papafotiou M, Vemmos SN (2013) Season and explant origin affect phenolic content, browning of explants, and micropropagation of X Malosorbus florentina (Zucc.) Browicz. Hortscience 48:102–107
Ochoa-Villarreal M, Howat S, Hong S, Jang MO, Jin YW, Lee EK, Loake GJ (2016) Plant cell culture strategies for the production of natural products. BMB Rep 49:149–158
Pezet R (1998) Purification and characterization of a 32-kDa laccase-like stilbene oxidase produced by Botrytis cinerea Pers.:Fr. FEMS Microbiol Lett 167:203–208
Santamaria AR, Mulinacci N, Valletta A, Innocenti M, Pasqua G (2011) Effects of elicitors on the production of resveratrol and viniferins in cell cultures of Vitis vinifera L. cv Italia. J Agric Food Chem 59:9094–9101
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
Schwekendiek A, Spring O, Heyerick A, Pickel B, Pitsch NT, Peschke F, Keukeleire DD, Weber G (2007) Constitutive expression of a grapevine stilbene synthase gene in transgenic hop (Humulus lupulus L.) yields resveratrol and its derivatives in substantial quantities. J Agric Food Chem 55:7002–7009
Shankar S, Nall D, Tang SN, Meeker D, Passarini J, Sharma J, Srivastava RK (2011) Resveratrol inhibits pancreatic cancer stem cell characteristics in human and kras(G12D) transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLoS ONE 6:e16530
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
Suwalsky M, Villena F, Gallardo MJ (2015) In vitro protective effects of resveratrol against oxidative damage in human erythrocytes. Biochim Biophys Acta 1848:76–82
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
Taurino M, Ingrosso I, D’amico L, De Domenico S, Nicoletti I, Corradini D, Santino A, Giovinazzo G (2015) Jasmonates elicit different sets of stilbenes in Vitis vinifera cv. Negramaro cell cultures. Springerplus 4:49
Tavares S, Vesentini D, Fernandes JC, Ferreira RB, Laureano O, Ricardo-Da-Silva JM, Amâncio S (2013) Vitis vinifera secondary metabolism as affected by sulfate depletion: diagnosis through phenylpropanoid pathway genes and metabolites. Plant Physiol Biochem 66:118–126
Tyunin AP, Kiselev KV (2016) Alternations in VaSTS gene cytosine methylation and t-resveratrol production in response to UV-C irradiation in Vitis amurensis Rupr. cells. Plant Cell Tissue Organ Cult 124:33–45
Wilson AG (2008) Epigenetic regulation of gene expression in the inflammatory response and relevance to common diseases. J Periodontol 79:1514–1519
Xu A, Zhan JC, Huang WD (2015) 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 Tissue Organ Cult 122:197–211
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This work was supported by a Grant from the Russian Science Foundation (17-74-10082).
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ASD and KKV were involved in research design, data analysis, and paper preparation. APT, ARS, and NNN were involved in plant cell cultures management and qRT-PCR. MAY performed HPLC. YAK: analyzed the data.
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Communicated by Klaus Eimert.
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Tyunin, A.P., Suprun, A.R., Nityagovsky, N.N. et al. The effect of explant origin and collection season on stilbene biosynthesis in cell cultures of Vitis amurensis Rupr.. Plant Cell Tiss Organ Cult 136, 189–196 (2019). https://doi.org/10.1007/s11240-018-1490-x
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DOI: https://doi.org/10.1007/s11240-018-1490-x