Advertisement

The effect of salt stress on resveratrol and piceid accumulation in two Vitis vinifera L. cultivars

  • Imen SouidEmail author
  • Imene Toumi
  • Isidro Hermosín-Gutiérrez
  • Soumaia Nasri
  • Ahmed Mliki
  • Abdelwahed Ghorbel
Research Article
  • 43 Downloads

Abstract

Salinity is one of the most important abiotic stresses, especially in arid regions. Such devastating constraint is converted mainly to oxidative burst. Thus, plants have to develop strategies to scavenge salt-related regenerated oxidant molecules. In the present work, fully aged plants derived from two Vitis vinifera L. cultivars, the Tunisian autochthonous tolerant genotype Razegui and the salt sensitive Syrah, were analyzed regarding their short term response to 100 mM NaCl, in hydroponic cultures. The ratio [ASA/ASA + DHA] was calculated on the basis of the oxidation of ascorbic acid (ASA) into dehydroascorbic acid (DHA) in leaves. Results proved that oxidative stress was generated. This led to the accumulation of malondialdehyde which referred to a lipid peroxidation mainly in the sensitive Syrah. In order to cope with these oxidative disturbances, trans-resveratrol as well as its glucosides trans-piceid and cis-piceid have been de novo synthesized in the sensitive variety. Razegui stilbene concentrations were presented here for the first time and unexpectedly did not show a very important variation during the salt elicitation.

Keywords

Salt stress Oxidation Tolerance Antioxidant Resveratrol Piceid 

Notes

Acknowledgements

The authors would like to express their gratitude to King Khalid University, Saudi Arabia for providing administrative and technical support. The authors thank Prof. K.A Roubelakis and Dr. Panagiotis Moschou for excellent assistance.

References

  1. Agati G, Biricolti S, Guidi L, Ferrini F, Fini A, Tattini M (2011) The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J Plant Physiol 16:204–212.  https://doi.org/10.1016/j.jplph.2010.07.016 CrossRefGoogle Scholar
  2. Ali A, Strommer J (2003) A simple extraction and chromatographic system for the simultaneous analysis of anthocyanins and stilbenes of Vitis species. J Agric Food Chem 51:7246–7251.  https://doi.org/10.1021/jf030435g CrossRefGoogle Scholar
  3. Bavaresco L, Fregoni C (2001) Molecular biology and biotechnology of the grapevine. In: Roubelakis-Angelakis KA (ed) Physiological role and molecular aspects of grapevine stilbenic compounds. Kluwer Academic Publishers, Dordrecht, pp 153–182Google Scholar
  4. Borie B, Jeandet P, Parize A, Bessis R, Adrian M (2004) Resveratrol and stilbene synthase mRNA production in grapevine leaves treated with biotic and abiotic phytoalexin elicitors. Am J Enol Vitic 55:60–64Google Scholar
  5. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257.  https://doi.org/10.1093/jxb/ert430 CrossRefGoogle Scholar
  6. Boubakri H, Poutaraud A, Wahab MA, Clayeux C, Baltenweck-Guyot R, Steyer D, Marcic C, Mliki A, Soustre-Gacougnolle I (2013) Thiamine modulates metabolism of the phenylpropanoid pathway leading to enhanced resistance to Plasmopara viticola in grapevine. BMC Plant Biol 13:31–46.  https://doi.org/10.1186/1471-2229-13-31 CrossRefGoogle Scholar
  7. Caddeo C, Puccib L, Gabrieleb M, Carbonec C, Fernàndez-Busquetsd X, Valentia D, Ponsg R, Vassalloh A, Faddaa AM, Manconia M (2017) Stability, biocompatibility and antioxidant activity of PEG-modified liposomes containing resveratrol. Int J Pharm 538:40–47.  https://doi.org/10.1016/j.ijpharm.2017.12.047 CrossRefGoogle Scholar
  8. Camont L, Cottart CH, Rhayem Y, Nivet-Antoine V, Djelidi R, Collin F, Beaudeux JL, Bonnefont-Rousselot D (2009) Simple spectrophotometric assessment of the trans-/cis-resveratrol ratio in aqueous solutions. Anal Chim Acta 634:121–128.  https://doi.org/10.1016/j.aca.2008.12.003 CrossRefGoogle Scholar
  9. Carvalho LC, Vidigal P, Amâncio S (2015) Oxidative stress homeostasis in grapevine (Vitis vinifera L.). Front Environ Sci 3:20–35.  https://doi.org/10.3389/fenvs.2015.00020 CrossRefGoogle Scholar
  10. Chang X, Heene E, Qiao F, Nick P (2011) The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. PLoS ONE 6:1–12.  https://doi.org/10.1371/journal.pone.0026405 Google Scholar
  11. Chong J, Poutaraud A, Huguene P (2009) Metabolism and roles of stilbenes in plants. Plant Sci 177:143–155.  https://doi.org/10.1016/j.plantsci.2009.05.012 CrossRefGoogle Scholar
  12. Curti V, Di Lorenzo A, Dacrema M, Xiao J, Nabavi SM, Daglia M (2017) In vitro polyphenol effects on apoptosis: an update of literature data. Semin Cancer Biol 46:119–131.  https://doi.org/10.1016/j.semcancer.2017 CrossRefGoogle Scholar
  13. Daldoul S, Guillaumie S, Götz MR, Krczal G, Ghorbel A, Delrot S, Mliki A, Höfer MU (2010) Isolation and expression analysis of salt induced genes from contrasting grapevine (Vitis vinifera L.) cultivars. Plant Sci 179:489–498.  https://doi.org/10.1016/j.plantsci.2010.07.017 CrossRefGoogle Scholar
  14. Daldoul S, Hoefer M, Mliki A (2011) Osmotic stress induces the expression of VvMAP Kinase Gene in grapevine (Vitis vinifera L.). Journal of Botany 2012:1–4.  https://doi.org/10.1155/2012/737035 CrossRefGoogle Scholar
  15. Deluc LG, Decendit A, Parastamoulis Y, Mérillon JM, Cushman JC, Cramer GR (2011) Water deficit increases stilbene metabolism in Cabernet sauvignon berries. J Agric Food Chem 59:289–297.  https://doi.org/10.1021/jf1024888 CrossRefGoogle Scholar
  16. Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci 182:29–41.  https://doi.org/10.1016/j.plantsci.2011.01.018 CrossRefGoogle Scholar
  17. Duan D, Halter D, Baltenweck R, Tisch C, Tröster V, Kortekamp A, Hugueney P, Nick P (2015) Genetic diversity of stilbene metabolism in Vitis sylvestris. J Exp Bot 66:3243–3257.  https://doi.org/10.1093/jxb/erv137 CrossRefGoogle Scholar
  18. Fabris S, Momo F, Ravagnan G, Stevanato R (2008) Antioxidant properties of resveratrol and piceid on lipid peroxidation in micelles and monolamellar liposomes. Biophys Chem 135:76–83.  https://doi.org/10.1016/j.bpc.2008.03.005 CrossRefGoogle Scholar
  19. Figueiras TS, Neves-Petersen MT, Petersen SB (2011) Activation energy of light induced isomerization of resveratrol. J Fluoresc 21:1897–1906.  https://doi.org/10.1007/s10895-011-0886-3 CrossRefGoogle Scholar
  20. Flowers T, Troke PF, Yeo AR (1977) The mechanisms of salt tolerance in halophytes. Annual Review of Plant Physiology 28:89–121.  https://doi.org/10.1146/annurev.pp28.060177.000513 CrossRefGoogle Scholar
  21. Frémont L, Belguendou L, Delpal S (1999) Antioxydant activity of resveratrol and alcohol-free wine polyphenols related to LDL oxidation and polyunsaturated fatty acids. Life Sci 64:2511–2521CrossRefGoogle Scholar
  22. Gibeaut DM, Hulett J, Cramer GR, Seemann JR (1997) Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions. Plant Physiol 115:317–319.  https://doi.org/10.1104/pp.115.2.317 CrossRefGoogle Scholar
  23. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930.  https://doi.org/10.1016/j.plaphy.2010 CrossRefGoogle Scholar
  24. Goldberg DM, Ng E, Karumanchiri A, Yan J, Soleas GJ (1995) Assay of resveratrol glucosides and isomers in wine by direct-injection high-performance liquid chromatography. J Chromatogr A 708:89–98.  https://doi.org/10.1016/0021-9673(95)00368-W CrossRefGoogle Scholar
  25. Griesser M, Weingart G, Schoedl-Hummel K, Neumann N, Becker M, Varmuza K, Liebner K, Schuhmacher R, Forneck A (2015) Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. Pinot noir). Plant Physiol Biochem 88:17–26.  https://doi.org/10.1016/j.plaphy.2015.01.004 CrossRefGoogle Scholar
  26. 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. Innovative Food Science and Emerging Technologies 11:231–238.  https://doi.org/10.1016/j.ifset.2009.10.005 CrossRefGoogle Scholar
  27. Hanana M, Deluc L, Fouquet R, Daldoul S, Léon C, Barrieu F, Ghorbel A, Mliki A, Hamdi S (2008) Identification and characterization of ‘rd22’ dehydration responsive gene in grapevine (Vitis vinifera L.). CR Biol 331:569–578.  https://doi.org/10.1016/j.crvi.2008.05.002 CrossRefGoogle Scholar
  28. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198.  https://doi.org/10.1016/0003-9861(68)90654-1 CrossRefGoogle Scholar
  29. Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. CAB Technical Communication. No. 22 (2nd edn), pp. 297–315Google Scholar
  30. Hossain MA, Fujita M (2010) Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. Physiol Mol Biol Plants 16:19–29CrossRefGoogle Scholar
  31. Ismail A, Riemann M, Nick P (2012) Jasmonate pathway mediates salt tolerance in grapevines. J Exp Bot 63:2127–2139.  https://doi.org/10.1093/jxb/err426 CrossRefGoogle Scholar
  32. Ismail A, Seo M, Takebayashi Y, Kamiya Y, Eiche E, Nick P (2014a) Salt adaptation requires efficient fine-tuning of jasmonate signalling. Protoplasma 251:881–898.  https://doi.org/10.1007/s00709-013-0591-y CrossRefGoogle Scholar
  33. Ismail A, Takeda S, Nick P (2014b) Life and death under salt stress: same players, different timing? J Exp Bot 65:2963–2979.  https://doi.org/10.1093/jxb/eru159 CrossRefGoogle Scholar
  34. Ismail A, Seo M, Takebayashi Y, Kamiya Y, Nick P (2015) A balanced JA/ABA status may correlate with adaptation to osmotic stress in Vitis cells. J Plant Physiol 185:57–64.  https://doi.org/10.1016/j.jplph.2015.06.014 CrossRefGoogle Scholar
  35. Jeandet P, Breuil AC, Adrian M, Weston LA, Debord S, Meunier P, Maume G, Bessis R (1997) HPLC analysis of grapevine phytoalexins coupling array detection and fluorometry. Anal Chem 69:5172–5177.  https://doi.org/10.1021/ac970582b CrossRefGoogle Scholar
  36. Jeandet P, Clément C, Cordelier S (2019) Regulation of resveratrol biosynthesis in grapevine: new approaches for disease resistance? J Exp Bot 70:375–378.  https://doi.org/10.1093/jxb/ery446 CrossRefGoogle Scholar
  37. Jellouli N, Ben Jouira H, Skouri H, Ghorbel A, Gourgouri A, Mliki A (2008) Proteomic analysis of Tunisian grapevine cultivar Razegui under salt stress. J Plant Physiol 165:471–481.  https://doi.org/10.1016/j.jplph.2007.02.009 CrossRefGoogle Scholar
  38. Jiang J, Xi H, Dai Z, Lecourieux F, Yuan L, Liu X, Patra B, Wei Y, Li S, Wang L (2019) VvWRKY8 represses stilbene synthase genes through direct interaction with VvMYB14 to control resveratrol biosynthesis in grapevine. J Exp Bot 70:715–729.  https://doi.org/10.1093/jxb/ery401 CrossRefGoogle Scholar
  39. Kao CH (2017) Mechanisms of salt tolerance in rice plants: reactive oxygen species scavenging-systems. J Taiwan Agric Res 66:1–8.  https://doi.org/10.6156/JTAR/2017.06601.01 Google Scholar
  40. Kostopoulou Z, Therios I, Molassiotis A (2014) Resveratrol and its combination with α-tocopherol mediate salt adaptation in citrus seedlings. Plant Physiol Biochem 78:1–9.  https://doi.org/10.1016/j.plaphy.2014.02.011 CrossRefGoogle Scholar
  41. Lachman J, Kotíkovál Z, Hejtmánková A, Pivec V, Pšeničnaja O, Šulc M, Střalková R, Dědina M (2016) Resveratrol and piceid isomers concentrations in grapevine shoots, leaves, and tendrils. Hort Sci 43:25–32.  https://doi.org/10.17221/258/2014-hortsci Google Scholar
  42. Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism. Biochem Biophys Res Commun 495:286–291.  https://doi.org/10.1016/j.bbrc.2017.11.043 CrossRefGoogle Scholar
  43. Maurer LH, Bersch AM, Santos RO, Trindade SC, Costa EL, Peres MM, Malmann CA, Schneider M, Bochi VC, Sautter CK, Emanuelli T (2017) Postharvest UV-C irradiation stimulates the non-enzymatic and enzymatic antioxidant system of ‘Isabel’ hybrid grapes (Vitis labrusca × Vitis vinifera L.). Food Res Int 102:738–747.  https://doi.org/10.1016/j.foodres.2017.09.053 CrossRefGoogle Scholar
  44. Mikulski D, Molski M (2010) Quantitative structure–antioxidant activity relationship of trans-resveratrol oligomers, trans-4,4′-dihydroxystilbene dimer, trans-resveratrol-3-O-glucuronide, glucosides: trans-piceid, cis-piceid, trans-astringin and trans-resveratrol-4′-O-β-D-glucopyranoside. Eur J Med Chem 45:2366–2380.  https://doi.org/10.1016/j.ejmech.2010.02.016 CrossRefGoogle Scholar
  45. Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:1–16.  https://doi.org/10.3389/fpls.2015.00069 CrossRefGoogle Scholar
  46. Pezet R, Perret C, Jean-Denis JB, Tabacchi R, Gindro K, Viret O (2003) δ-vinifrein a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves. J Agric Food Chem 51:5488–5492.  https://doi.org/10.1021/jf030227o CrossRefGoogle Scholar
  47. Pugajera I, Perkons I, Górnaś P (2018) Identification and determination of stilbenes by Q-TOF in grape skins, seeds, juice and stems. J Food Compos Anal 74:44–52.  https://doi.org/10.1016/j.jfca.2018.09.007 CrossRefGoogle Scholar
  48. Qiao F, Chang XL, Nick P (2010) The cytoskeleton enhances gene expression in the response to the Harpin elicitor in grapevine. J Exp Bot 61:4021–4031.  https://doi.org/10.1093/jxb/erq221 CrossRefGoogle Scholar
  49. Regev-Shoshani G, Shoseyov O, Bilkis I, Kerem Z (2003) Glycosylation of resveratrol protects it from enzymic oxidation. Biochem J 374:157–163.  https://doi.org/10.1042/BJ20030141 CrossRefGoogle Scholar
  50. Rhoades JD, Loveday J (1990) Salinity in irrigated agriculture. In: Steward BA, Nielsen DR (eds) Irrigation of agricultural crops. Agronomists, monograph, vol 1. American Society of Civil Engineers, Reston, pp 1089–1142Google Scholar
  51. Romero-Pérez AI, Ibern-Gómez M, Lamuela-Raventós RM, de La Torre-Boronat MC (1999) Piceid, the major resveratrol derivative in grape juices. J Agric Food Chem 47:1533–1536.  https://doi.org/10.1021/jf981024g CrossRefGoogle Scholar
  52. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421.  https://doi.org/10.1007/1-4020-4225-6 Google Scholar
  53. Sato M, Suzuki Y, Okuda T, Yokotsuka K (1997) Contents of resveratrol, piceid, and their isomers in commercially available wines made from grapes cultivated in Japan. Biosci Biotechnol Biochem 61:1800–1805CrossRefGoogle Scholar
  54. Sgarbi E, Fornasiero RB, Lins AP, Bonatti PM (2003) Phenol metabolism is differentially affected by ozone in two cell lines from grape (Vitis vinifera L.) leaf. Plant Sci 165:951–957.  https://doi.org/10.1016/S0168-9452(03)00219-X CrossRefGoogle Scholar
  55. Souid I, Hassene Z, Sánchez-Palomo E, Pérez-Coello MS, Ghorbel A (2008) Aroma potential of three autochthonous grapevine varieties from Tunisia. J Int Sci Vigne Vin 42: 231-239.  https://doi.org/10.20870/oeno-one.2008.42.4.813
  56. Su D, Cheng Y, Liu M, Liu D, Cui H, Zhang B, Zhou S, Yang T, Mei Q (2013) Comparision of piceid and resveratrol in antioxidation and antiproliferation activities In Vitro. PLoS ONE 8:1–13.  https://doi.org/10.1371/journal.pone.0054505 Google Scholar
  57. Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545.  https://doi.org/10.1104/pp.103.032250 CrossRefGoogle Scholar
  58. Sun B, Ribes AM, Leandro MC, Belchior AP, Spranger MI (2006) Stilbenes: quantitative extraction from grape skins, contribution of grape solids to wine and variation during wine maturation. Anal Chim Acta 563:382–390.  https://doi.org/10.1016/j.aca.2005.12.002 CrossRefGoogle Scholar
  59. Toumi I, Gargouri M, Nouairi I, Moschou PN, Ben Salem-Fnayou A, Mliki A, Zarrouk M, Ghorbel A (2008) Water stress induced changes in the leaf lipid composition of four grapevine genotypes with different drought tolerance. Biol Plant 52:161–164CrossRefGoogle Scholar
  60. Villangó SZ, Szekeres A, Bencsik O, Láposi R, Pálfi Z, Zsófi ZS (2016) The effect of postveraison water deficit on the phenolic composition and concentration of the Kékfrankos (Vitis vinifera L.) berry. Sci Hortic 209:113–116.  https://doi.org/10.1016/j.scienta.2016.06.010 CrossRefGoogle Scholar
  61. Vitrac X, Monti JP, Vercauteren J, Deffieux G, Mérillon JM (2002) Direct liquid chromatographic analysis of resveratrol derivatives and flavononols in wines with absorbance and fluorescence detection. Anal Chim Acta 485:103–110.  https://doi.org/10.1016/S0003-2670(01)01498-2 CrossRefGoogle Scholar
  62. Wang SY, Jiao HJ, Faust M (1991) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiol Plant 82:231–236.  https://doi.org/10.1111/j.1399-3054.1991.tb00086.x CrossRefGoogle Scholar
  63. Wani AS, Ahmad A, Hayat C, Fariduddin Q (2013) Salt-induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. Saudi J Biol Sci 20:183–193CrossRefGoogle Scholar
  64. Xi HF, Ma L, Wang LN, Li SH, Wang LJ (2015) Differential response of the biosynthesis of resveratrols and flavonoids to UV-C irradiation in grape leaves. N Z J Crop Hortic Sci 43:1–10.  https://doi.org/10.1080/01140671.2014.989862 CrossRefGoogle Scholar
  65. Xiong L, Zhu J (2002) Salt tolerance. Arabidopsis Book 1:e0048.  https://doi.org/10.1199/tab.0048 CrossRefGoogle Scholar
  66. Xu A, Cheng Zhan JI, 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.  https://doi.org/10.1007/s11240-015-0761-z CrossRefGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2019

Authors and Affiliations

  1. 1.Campus for Girls Study, Pre-Medical Department, Sciences FacultyKing Khaled UniversityAbhaSaudi Arabia
  2. 2.Central Analytical Laboratory of Animal FeedsSoukraTunisia
  3. 3.Department of BiologyUniversity of CreteHeraklionGreece
  4. 4.Escuela Universitaría de Ingeniería Técnica AgrícolaCiudad RealSpain
  5. 5.Laboratory of Grapevine Molecular PhysiologyUniversity of Tunis IITunisTunisia

Personalised recommendations