Table 1.
Induction of stilbene biosynthetic gene expression and stilbene accumulation by environmental factors.
| Species/Cultivar/Variety | Treatment/s | Metabolites | Results | Reference |
|---|---|---|---|---|
| Vitis vinifera cvs. Alphonse Lavallée, Dan Ben-Hanna, Dabuki, Early Superior, Flame seedless, Kishmish, Muscat Hamburg, Perlette, Spring Blush, Superior, Thompson seedless, Zeiny, Gamay, Gamaret, Pinot, Shasla | Irradiation of grape berries with UV-C or inoculation of grape berries with Rhizopus stolonifer | Stilbenes (resveratrol and pterostilbene) | Increased stilbene accumulation, greater with UV-C compared to fungal inoculum | [183] |
| V. vinifera cv. Napoleon | Irradiation of grape berries with UV-C or UV-B | Stilbenes (resveratrol and piceid); anthocyanins; flavonoids; hydroxycinnamic acids (caffeoyltartaric acid and chlorogenic acid) | Increased stilbene accumulation, greater with UV-C compared to UV-B (3 and 2-fold, respectively) | [184] |
| V. vinifera cv. Corvina | Irradiation of grape berries with UV-B and wilting at different temperatures | Stilbenes (trans and cis-resveratrol, trans and cis-piceid); total polyphenols, flavonoids, anthocyanins, catechins, and proanthocyanidins | Enhanced stilbene accumulation and STS gene expression | [185] |
| V. vinifera cvs. Black Corinth and Flame seedless | Irradiation of grape berries with UV-C | Resveratrol; total anthocyanins | Greater resveratrol increase (4-fold) in cv. Flame Seedless. Lower increase in cv. Black Corinth. Negative relationship between resveratrol synthesis and anthocyanin concentration | [186] |
| V. vinifera cv. Flame seedless, Red Globe, Crimson seedless, Napoleon, Superior seedless, Moscatel Italica, Dominga | Irradiation of grape berries with UV-C | Trans- and cis-resveratrol, trans-piceatannol, trans-piceid, trans-astringin, α-viniferin, ε-viniferin | Increased stilbene concentration, with higher accumulation of trans-resveratrol, trans-piceatannol, and viniferins | [187] |
| V. vinifera cv. Monastrell | Irradiation of grape berries with UV-C, followed by traditional maceration | Stilbenes (trans-resveratrol, trans-piceatannol); anthocyanins; flavonols; flavanols (total catechins); hydroxycinnamic acids (p-coumaroyltartaric acid) | Increased in trans-piceatannol and trans-resveratrol content (1.5 and 2-fold, respectively) in wines without impacting standard oenological parameters | [188] |
| V. vinifera cvs. Tempranillo, Cabernet-Sauvignon, Merlot, Syrah, Monastrell, Garnacha, Cariñena | Irradiation of grape berries with UV-C | Trans-resveratrol, trans-piceatannol, α-viniferin, ε-viniferin | Increased concentrations of trans-resveratrol, trans-piceatannol, and viniferins in grape skins of all varieties, except Monastrell, in which only trans-piceatannol concentration increased | [189] |
| V. vinifera cv. Superior | Irradiation of grape berries with UV-C | Trans-resveratrol, trans-piceid, trans-piceatannol, viniferins (resveratrol dehydrodimers and dehydrotrimers) | Increased trans-resveratrol accumulation (10-fold); induction of trans-piceid, trans-piceatannol, and viniferins (not detected in control grapes) | [190] |
| V. vinifera cv. Superior | Comparison of UV-C and ozone (O3) treatments on grape berries | Trans-resveratrol, piceatannol, and viniferins (resveratrol dehydrodimers and dehydrotrimers) | Increased accumulation of stilbenes after both UV-C and O3 treatments. O3 more effective than UV-C in inducing the accumulation of viniferins | [191] |
| V. vinifera cv. Superior | Irradiation of grape berries with UV-C, followed by maceration with Na2S2O5 and enzymes | Stilbenes (trans-resveratrol; trans-piceid; trans-piceatannol, viniferins); hydroxycinnamic acids; flavonols; flavanols (catechins and procyanidins) | Increased stilbene concentration (35-fold) in grape juice under optimum conditions (maceration for 2 h at 45 °C with 0.2% Na2S2O5 using UV-C-treated grape berries) | [192] |
| V. vinifera cv. Red Globe | Irradiation of grape berries with UV-B nanosecond laser pulses | Trans-resveratrol | Increased trans-resveratrol accumulation (6-fold) in grape berries subjected to a resonant wavelength of the compound (302.1 nm) | [193] |
| V. vinifera sylvestris var. V9. V15, V16; V. vinifera sativa var. Merlot, Syrah, Graciano, Tempranillo, Palomino fino, Palomino negro, Tintilla de Rota; V. vinifera sativa hybrid Orion, Regent | Irradiation of grape berries with UV-C | Trans-resveratrol, piceatannol, ε-viniferin, δ-viniferin | Increased stilbene concentration, with differences depending on variety and campaign, but not on subspecies | [194] |
| V. vinifera × V. labrusca cv. Kyoho | Irradiation of grape berries with UV-C and storage at different temperatures (0 °C or 20 °C) | Resveratrol | Increased resveratrol concentration, especially in UV-treated grapes stored at high temperature | [195] |
| V. vinifera cv. Redglobe | Irradiation of grape berries with UV-C and storage at different temperatures (25 °C or 4 °C) | Stilbenes (trans-resveratrol, cis- and trans-piceid); flavonols; anthocyanins; flavanols (catechins) | Increased concentration of cis- and trans-piceid after UV-C treatment and cold storage | [196] |
| V. vinifera cv. Crimson | Treatment of grape berries with UV-C and chitosan, followed by storage at different temperatures | Trans-resveratrol | Increased resveratrol content in grapes and lower susceptibility to fungal decay after UV-C treatment combined with chitosan coating followed by storage at 20 °C for 24 h before refrigerated storage | [197] |
| V. amurensis cv. Tonghua-3 | Treatment of grape berries with UV-C | Trans- and cis-resveratrol | Increased accumulation of stilbene compounds, up-regulation of multiple STS genes, down-regulation of CHS genes | [198] |
| V. vinifera × V. labrusca cv. Summer Black | Treatment of grape berries with UV-B or UV-C | Stilbenes (trans-resveratrol, trans-piceid); gallic acid; hydroxycinnamic acids (caffeic acid, trans-ferulic acid); flavanols [(+)-catechin, (−)-epicatechin, epicatechin gallate] | Increased accumulation of phenolic compounds and STS gene expression, more induced by UV-C than UV-B | [199] |
| V. vinifera cv. Kyoho | Irradiation of grape berries with UV-B | Trans-resveratrol, trans-scirpusin A, trans-ε-viniferin, trans-δ-viniferin, trans-pterostilbene | Increased production of the analyzed stilbenes, up-regulation of stilbene biosynthetic genes | [200] |
| Arachis hypogaea cv. Georgia green | Treatment of peanuts with UV-C or ultrasonication | Trans-resveratrol, trans-piceid | Increased resveratrol, piceid, and total stilbene concentration, more induced by ultrasound than UV-C | [201] |
| A. hypogaea var. Jinpoong | Leaves subjected to UV-C, wounding, paraquat, H2O2, salicylic acid, jasmonic acid ethephon, abscisic acid | Resveratrol | Maximum resveratrol increases in response to UV (over 200-fold), followed by paraquat (20-fold) and wounding, H2O2, salicylic acid, jasmonic acid, and ethephon (between 2- and 9-fold) | [202] |
| A. hypogaea Georgia green | Treatment of peanuts with UV-C | Trans-resveratrol | Increased trans-resveratrol accumulation (10-fold) | [203] |
| Gnetum parvifolium | Treatment of 1-year-old seedlings with high temperature (40 °C) and UV-C treatments | Resveratrol and piceatannol | Both high temperature and UV-C strongly induce the expression of PAL, C4H-, 4CL-, and STS-like genes, but only UV-C enhance stilbene accumulation | [204] |
| Gnetum parvifolium | Treatment of 1-year-old seedlings with high temperature (40 °C) and UV-C treatments | Resveratrol and piceatannol | Both high temperature and UV-C strongly induce the expression of PAL, C4H, 4CL, STS, and CYP genes. High temperatures do not affect stilbene accumulation in stems but decrease stilbene concentration in roots at 3 h. UV-C irradiation induces total stilbene accumulation in stems but not in roots. | [205] |
| Pinus sylvestris | Treatment of needles from 5-years-old plantlets with UV-C | Pinosylvin and pinosylvin monomethylether | Induction of PMT2 expression | [134] |
| V. vinifera cv. Sangiovese | Potted vines grown in air-conditioned greenhouses under high temperature or low temperature regimes (26 and 21 °C as average and 42 and 35 °C as maximum air daily temperature, respectively) | Stilbenes | Increased expression of STS and PAL genes under low temperatures | [206] |
| V. vinifera cv. Cabernet Sauvignon | Treatment of cell suspension cultures with high temperature (38 °C) or low temperature (16 °C) and CuSO4 | Stilbenes | Downregulation of STS expression under both low and high temperature and upregulation of STS expression in response to CuSO4 | [207] |
| V. vinifera cv. Cardinal | Treatment of grape berries with low temperature (0 °C) and high CO2 levels (20%) | Trans-resveratrol; total anthocyanins | Low temperature reduces trans-resveratrol content in both treated and non-treated grapes, although the decrease is higher in CO2-treated grapes | [208] |
| V. vinifera cvs. Dominga, Superior seedless, Autumn Royal, Red Globe | Treatment of grape berries with low temperature (0 °C) and high CO2 levels (3 days) | Resveratrol, resveratrol-glucoside, trans-piceatannol, z-miyabenol, pallidol | Stilbene accumulation in response to low temperature and CO2 is cultivar dependent. High CO2 levels activate stilbene pathways in cv. Dominga. Low temperature increase stilbenes biosynthesis in cv. Red Globe. Stilbene accumulation is independent of the atmosphere storage in cvs. Superior Seedless and Autumn Royal | [209] |
| V. vinifera cv. Shiraz | Treatment of grape berries with high light (2500 μmol m−2 s−1), high temperature (40 °C), oxidative stress (120 μM menadione), 3.026 mM abscisic acid, and 200 μM jasmonic acid (JA) | Resveratrol, piceid, and viniferin | At the pre-veraison stage, an increase in anthocyanins levels is accompanied by a declining stilbene accumulation in response to JA, menadione, and high light. At the veraison stage, mild change in anthocyanin levels in response to all the treatments is accompanied by stilbene accumulation | [210] |
| V. vinifera cv. Barbera | Treatment of cell suspensions with red LED light (1.34 μE m−2 s−1, 625 ± 10 nm) and 10 μM methyl-jasmonate (MeJa) | Stilbenes (cis- and trans-piceid, cis- and trans-resveratrol, cis- and trans-resveratroloside); catechins; anthocyanins | Strong increase in total stilbenes induced by MeJa, whose effect is enhanced by a red light. Increase in total anthocyanins in response to MeJa, used alone or in combination with a red light. Decrease in catechins under red light; increase in response to MeJa alone or in combination with red light | [211] |
| V. labruscana cvs. Campbell Early and Kyoho | Treatment of grape berries and leaves with fluorescent white light and purple, blue, and red LED lights | Cis- and trans-resveratrol, cis- and trans-piceid, cis- and trans-piceatannol | Increased accumulation of stilbenes (mainly trans- and cis-piceid) and induction of stilbene biosynthetic genes in response to red and blue LED light | [212,213] |
| V. vinifera cv. Negramaro | Light-exposed and dark-maintained cell cultures | Trans-resveratrol, trans-piceid, cis-ε-viniferin, trans-ε-viniferin, trans-δ-viniferin | Higher levels of trans-resveratrol and viniferins under darkness; higher levels of trans-piceid under light | [214] |
| V. vinifera cv. Shahani | High-level white light irradiation (10,000 lux) and MeJa (25, 50, 100 and 200 μM) | Stilbenes (trans-resveratrol, trans-piceid); total phenols; total flavonoids | Inhibitory effect of high light on stilbene biosynthesis; 50 μM MeJa is optimal for efficient production of total phenols, flavonoids, and stilbenes | [215] |
| V. vinifera cv. Malvasia; V. rupestris Du Lut | Light-exposed and dark-maintained cell cultures | Trans-resveratrol, trans-piceid, trans-ε-viniferin, trans-δ-viniferin | Increase in stilbene content under light conditions | [40] |
| Arachis hypogaea | White LED light and UV-C radiation during peanut germination | Stilbenes (resveratrol, piceid, piceatannol); total phenols; total flavonoids | White light significantly induces stilbene accumulation by upregulating the expression of genes and enzymes involved in the stilbene biosynthetic pathway. UV-C is more effective than white light in promoting stilbene accumulation | [216] |
| V. vinifera cvs. Cabernet Franc, Chardonnay, Chenin, Malbec (Côt), Gamay, Grolleau, Pinot Noir, Sauvignon Blanc | Wounding (stem pruning) | Trans-resveratrol, trans-piceatannol, trans-ε-viniferin, ampelopsin A, trans-miyabenol C, cis- and trans-vitisin B, hopeaphenol, isohopeaphenol | Induction of trans-resveratrol and trans-piceatannol during the first 6 weeks of storage at 20 °C | [217] |
| V. vinifera cv. Pinot Noir | Wounding (leaf discs) | Stilbenes | Increase in transcription levels of several STS genes | [60] |
| V. vinifera cv. Pinot Noir | Wounding (leaf discs) | Stilbenes | Increased transcript level of VviSTS29, -41, and -48, coupled with the induction of WRKY and R2R3-MYB transcription factors | [218] |
| V. vinifera cv. Alphonse Lavallée | Mechanical stress (low-energy ultrasound) alone or in combination with MeJa on cell suspension cultures | Trans-resveratrol, trans-piceid, trans-ε-viniferin, trans-δ-viniferin | Increase in trans-ε-viniferin production in response to ultrasounds. Increase in trans-δ-viniferin in response to ultrasound and MeJa co-treatment | [219] |
| V. quinquangularis | Wounding, exogenous stress-associated hormones, and biotic stress in leaves of transgenic tobacco transformed with VqSTS36 promoter fused to the GUS reporter gene | Stilbenes | Induction of VqSTS36 promoter activity in response to wounding, salicylic acid, and inoculation with the phytopathogenic fungus Erysiphe cichoracearum | [220] |
| Pinus sylvestris | Wounding of stem-phloem alone or in combination with fungal infection | Stilbenes | Transient increase in STS and PMT expression in response to wounding, more pronounced with wounding in combination with fungal inoculation | [221] |
| P. sylvestris | Wounding of seedlings | Pinosylvin and pinosylvin monomethyl ether | Upregulation of stilbene biosynthetic genes including PMT2 during heartwood formation and in response to stress | [222] |
| P. sylvestris | Wounding and infection of seedlings with Heterobasidion parviporum or H. annosum | Pinosylvin and pinosylvin monomethylether | Significantly higher amounts of stilbenes 10 days after treatment. Greater increase in infected than in just wounded samples | [223] |
| P. sylvestris | Wounding 5-years-old seedlings | Pinosylvin and pinosylvin monomethylether | Induction of PMT2 | [134] |
| V. vinifera cv. Pinot Noir | Mechanical wounding on freshly pruned canes | Trans-resveratrol and trans-piceatannol | Transient expression of PAL and STS genes, followed by a rapid accumulation of stilbenes | [224] |
| Arachis hypogaea | Wounding stress (cotyledons) | Resveratrol, arachidin-3, arachidin-4 | Induction of all analyzed stilbenes | [225] |
| A. hypogaea | Wounding stress (size reduction, grinding, chopping, slicing, ultrasound) | Trans-resveratrol | Slicing produces the highest increase of trans-resveratrol accumulation | [203] |
| Pinus sylvestris | Ozone fumigation (saplings grown in phytotron) | Stilbenes | Enhanced STS and PMT transcript levels in needles but not in healthy phloem | [221] |
| V. quinquangularis (accession Shang-24; powdery mildew (PM) resistant); V. pseudoreticulata (accession Hunan-1; PM susceptible) | Infection by Uncinula necator (sin. Erysiphe necator) | Stilbenes | VqSTS36 transcript levels increase substantially following PM infection | [220] |
| V. vinifera cv. Barbera | Elicitation of cell suspension cultures with salicylic acid, Na-orthovanadate, jasmonates, chitosan, D-glucosamine, N-acetyl-D-glucosamine, ampicillin, rifampicin | Trans- and cis-resveratrol | Induction of ex-novo synthesis of stilbenes stilbene synthase protein by MeJa and chitosan | [226] |
| V. vinifera cv. Gamay Fréaux var. Teinturier | Elicitation of cell suspension cultures with MeJa in combination with sucrose | Stilbenes (trans-resveratrol and piceids); total anthocyanins | Induction of PAL, CHS, STS, UDP-glucose: flavonoid-O-glucosyltransferase, proteinase inhibitor and chitinase gene expression. Enhanced accumulation of piceids and anthocyanins in cells, and trans-resveratrol and piceids in culture medium | [227] |
| V. vinifera cv. Monastrell albino | Elicitation of cell suspension cultures with MeJa and cyclodextrin (CDs) used independently or in combination | Trans-resveratrol | Induction of stilbene biosynthetic gene expression by MeJa and CDs when used independently. Enhanced trans-resveratrol production in CDs-treated cells but not in MeJa-treated cells | [228] |
| V. vinifera cv. Barbera | Elicitation of cell suspension cultures with chitosan | Trans- and cis-resveratrol | Induction of trans-resveratrol production and STS gene expression | [229] |
| V. vinifera cvs. Red Globe and Michele Palieri | Elicitation of calli with MeJa | Trans-piceid, resveratrol glucoside, cis-piceid, resveratrol diglucoside, resveratrol dimer monoglucosides, resveratrol dimer diglucosides, resveratrol dimer triglucosides, resveratrol dimer tetraglucosides, picetannol monoglycosylated, picetannol diglycosylated | Enhanced production of stilbenes, mainly trans-piceid and ε-viniferin | [230] |
| V. vinifera cv. Isabelle | Elicitation of calli with biotic (fungal extract of Fusarium oxysporum) and abiotic (mannitol, abscisic acid, jasmonic acid) elicitors | Trans-resveratrol | Optimum accumulation of trans-resveratrol with a combined treatment of mannitol (2 mM) and jasmonic acid (40 µM) | [231] |
| V. vinifera cv. Barbera | Elicitation of cell suspension cultures with chitosan | Mono-glucosylated derivatives resveratrol (trans- and cis-piceid and trans- and cis-resveratroloside) | Increased in trans-resveratrol endogenous accumulation and decreased release into the culture medium. De-novo synthesis and/or accumulation of STS proteins. No influence on cis-resveratrol and on resveratrol mono-glucosides | [232] |
| V. vinifera cv. Italia | Elicitation of calli and cell suspension cultures with MeJa, jasmonic acid or chitosan | Trans-resveratrol, piceid trans-δ-viniferin, trans-ε-viniferin | Induction of trans-resveratrol, piceid, and viniferins by jasmonates. Jasmonic acid enhances simultaneously δ- and ε-viniferin biosynthesis, whereas MeJa stimulates preferentially δ-viniferin production. | [233] |
| V. vinifera cv. Monastrell | Elicitation of cell suspension cultures with MeJa, cyclodextrins, and UV-C used independently or in combination | Trans-resveratrol | Highest increase in trans-reveratrol production was obtained with the combined use of MeJa, cyclodextrins, and an optimal sucrose concentration. Greatest release of trans-resveratrol into the culture medium is achieved with the combined use of MeJa, cyclodextrin, and UV-C | [234] |
| V. vinifera cv. Gamay Fréaux | Elicitation of cell suspension cultures with indanoyl-isoleucine (In-Ile), N-linolenoyl-l-glutamine (Lin-Gln), and insect saliva (from Manduca sexta larvae) | 3-O-Glucosyl-resveratrol; 4-(3,5-dihydroxy-phenyl)-phenol; total anthocyanins | Increased accumulation of phenolic acids, particularly 3-O-glucosyl-resveratrol, in response to In-Ile, Lin-Gln, and saliva | [235] |
| V. vinifera cv. Hongbaladuo; V. vinifera × V. amurensis cv. Beihong | Treatment of leaves and berries with CaCl2 and UV-C used alone or in combination | Cis- and trans-resveratrol | Increased resveratrol content with single treatments, greater increase with combined treatment | [236] |
| V. vinifera cv. Gamay Fréaux | Elicitation of cell suspension cultures with jasmonic acid, salicylic acid, β-glucan, and chitosan | Stilbenes (trans-resveratrol and trans-piceid); total anthocyanins | Increased resveratrol production with co-treatment with jasmonic acid and β-glucan | [237] |
| V. vinifera cv. Negramaro | Elicitation of cell cultures with chitosan, MeJa, jasmonic acid, coronatine, and 12-oxo-phytodienoic acid | Trans-resveratrol, trans-piceid, cis-ε-viniferin, trans-ε-viniferin, trans-δ-viniferin | MeJa is the most effective in inducing trans-resveratrol the biosynthesis, while 12-oxo-phytodienoic acid, jasmonic acid, and coronatine are the most effective in inducing the biosynthesis of viniferins | [214] |
| V. vinifera cv. Monastrell | Elicitation cell suspension cultures with cyclodextrins and coronatine | Trans-resveratrol | Induction of stilbene biosynthetic genes by cyclodextrins and/or coronatine. Maximum level of trans-resveratrol production and secretion into the culture medium with co-treatment with 50 mM cyclodextrins and 1 μM coronatine | [238] |
| V. vinifera cv. Tempranillo | Foliar application of MeJa, chitosan, and yeast extract | Stilbenes (trans- and cis-piceid and trans- and cis-resveratrol); flavonols; anthocyanins; hydroxybenzoic acids; hydroxycinnamic acids | MeJa and yeast extract improve both grape and wine anthocyanin content. Stilbene content is clearly improved by yeast extract | [239] |
| Vitis vinifera L. cv. Kalecik Karası | Elicitation of grape berries with ultrasound | Trans-resveratrol | About 20-fold increase in trans-resveratrol content in grape skin | [240] |
| Arachis hypogaea cv. Tainan No. 14 | Elicitation of calli with bacteria and fungi (both viable and autoclaved) or with chitin | Trans-resveratrol and trans-piceatannol | Induction of stilbene biosynthesis by fungi (both viable and autoclaved) and chitin | [241] |
| A. hypogaea cv. Hull line 3 | Elicitation of hairy root cultures with MeJa and methyl-β-cyclodextrin | Trans-resveratrol, trans-piceatannol, trans-arachidin-1 and trans-arachidin-3 | Co-treatment with MeJa and cyclodextrin led to high levels of stilbenes in the culture medium | [242] |
| Arachis hypogaea cv. Georgia green | Treatment of peanuts with ultrasonication or UV-C | Trans-resveratrol, trans-piceid | Increased resveratrol, piceid, and total stilbene concentration, more induced by ultrasound than UV-C | [201] |