Skip to main content
Log in

Foliar application of the triterpene derivative 24-methylen-elemo-lanosta-8,24-dien-3-one alleviates salt toxicity in grapevine

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

This work focused on the effect triterpene derivative 24-methylen-elemo-lanosta-8,24-dien-3-one (F3) on the induction of salt stress tolerance of the Moroccan grapevine cv. “Doukkali”. Hardwood cuttings of the grapevine from a homogeneous plant material collected in the field were grown in hydroponic medium under different salt concentrations and treated with 50 or 100 µg ml−1 of F3. Salt stress affected several physiological and biochemical parameters including relative water content, chlorophyll a and b content, peroxidase, and polyphenol oxidase activities, which decreased along with time. Meanwhile, proline, proteins, soluble sugars, H2O2, and carotenoid content, as well as phenolic compound content increased, suggesting an evidence of tolerance of this local variety to salinity. An exogenous supply of the triterpenic product increased all these parameters under normal conditions. In addition, F3 at low dose was found to be successful in lowering Na+ content and alleviating the inhibitory effects of salt stress on relative water content as well as on chlorophyll a and b.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbas S, Latif HH, Elsherbiny EA (2013) Effect of 24-epibrassinolide on the physiological and genetic changes on two varieties of pepper under salt stress conditions. Pak J Bot 45:1273–1284

    Google Scholar 

  • Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18. https://doi.org/10.3390/agronomy7010018

    Article  Google Scholar 

  • Agami RA (2013) Alleviating the adverse effects of NaCl stress in maize seedlings by pretreating seeds with salicylic acid and 24-epibrassinolide. South Afr J Bot 88:171–177

    Article  CAS  Google Scholar 

  • Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877

    Article  CAS  PubMed  Google Scholar 

  • Al Hassan M, Morosan M, Lpoez-Gresa MdP, Vicente O, Boscaiu M (2016) Salinity-induced variation in biochemical markers provides insight into the mechanisms of salt tolerance in common (Phaseolus vulgaris) and runner (P. coccineus) beans. Int J Mol Sci 17:1582. https://doi.org/10.3390/ijms17091582

    Article  PubMed Central  Google Scholar 

  • Ali B, Hayat S, Fariduddin Q, Ahmad A (2008) 24-Epibrassinolide protects against the stress generated by salinity and nickel in Brassica juncea. Chemosphere 72:1387–1392

    Article  CAS  PubMed  Google Scholar 

  • Avalbaev AM, Yuldashev RA, Fatkhutdinova RA, Urusov FA, Safutdinova YV, Shakirova FM (2010) The influence of 24-epibrassinolide on the hormonal status of wheat plants under sodium chloride. Appl Biochem Microbiol 46:99–102

    Article  CAS  Google Scholar 

  • Bajguz A (2000) Effect of brassinosteroids on nucleic acid and protein content in cultured cell of Chlorella vulgaris. Plant Physiol Biochem 38:209–215

    Article  CAS  Google Scholar 

  • Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027–1046

    Article  CAS  PubMed  Google Scholar 

  • Basel S (2012) Salt stress alters physiological indicators in cotton (Gossypium hirsutum L.). Soil Environ 31:113–118

    Google Scholar 

  • Bates LS, Waldren RD, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Ben Abdallah S, Aung B, Aymot L, Lachaal M, Karray-Bouraoui N, Hannoufi A (2016) Salt stress (NaCl) affects plant growth and branch pathways of carotenoids and flavonoids biosynthesis in Solanum nigrum. Acta Physiol Plant 38:72–84

    Article  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of protein utilizing the principe of protein—dye briding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Coleman WK (2008) Evaluation of wild solanum species for drought resistance: 1. Solanum gandarillasii Cardenas. Environ Exp Bot 62:221–230

    Article  Google Scholar 

  • Cui D, Wu D, Liu J, Li D, Xu C, Li S, Li P, Zhang H, Liu X, Jiang C, Wang L, Chen T, Chen H, Zhao L (2015) Proteomic analysis of seedling roots of two maize inbred lines that differ significantly in the salt stress response. PLoS One 10:e0116697. https://doi.org/10.1371/journal.pone.0116697

    Article  PubMed  PubMed Central  Google Scholar 

  • Darne G, Madero-Tamargo J (1979) Description of method for extracting total soluble lipids, total soluble glucides and total soluble phenols of vine organs. Vitis 18:221–228

    CAS  Google Scholar 

  • Dash M, Panda K (2001) Salt stress induced changes in growth and enzyme activities. Biol Plant 44:587–589

    Article  CAS  Google Scholar 

  • De Costa F, Yendo AC, Fleck JD, Gosmann G, Fett-Neto AG (2013) Accumulation of bioactive triterpene saponin fraction of Quillaja brasiliensis leaves is associated with abiotic and biotic stresses. Plant Physiol Biochem 66:56–62

    Article  PubMed  Google Scholar 

  • De Pascal S, Maggio A, Fogliano V, Ambrosino P, Ritieni A (2001) Irrigation with saline water improves carotenoids content and antioxidant activity of tomato. J Hortic Sci Biotechnol 76:447–453

    Article  Google Scholar 

  • Djanaguiraman M, Ramadass R (2004) Effect of salinity on chlorophyll content of rice genotypes. Agric Sci Digest 24:178–181

    Google Scholar 

  • Downton WJS, Loveys BR, Grant WJR (1990) Salinity effects on the stomatal behavior of grapevine. New Phytol 116:499–503

    Article  CAS  Google Scholar 

  • Du Bois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  Google Scholar 

  • Fozouni M, Abbaspour N, Doulati Baneh H (2012) Short term response of grapevine grown hydroponically to salinity: mineral composition and growth parameters. Vitis 51:95–101

    CAS  Google Scholar 

  • Garcia M, Charbaji T (1993) Effect of sodium chloride salinity on cation equilibria in grapevine. J Plant Nutr 16:2225–2237

    Article  CAS  Google Scholar 

  • Hansen TH, Laursen KH, Persson DP, Pedas P, Husted S, Schjoerring JK (2009) Micro-scaled high-throughput digestion of plant tissue samples for multi-elemental analysis. Plant Methods 5:12. https://doi.org/10.1186/1746-4811-5-12

    Article  PubMed  PubMed Central  Google Scholar 

  • Haubrick LL, Assman SM (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Zhao L, Chen D, Liang M, Liu Z, Shao H, Long X (2013) Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem Artichoke plantlets. PLoS One 8:e62085. https://doi.org/10.1371/journal.pone.0062085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethyl formamide and 80% acetone. Plant Physiol 77:483–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlidag H, Yilidirim E, Turam M (2011) Role of 24-epibrassinolide in mitigating the adverse effects of salt stress on stomatal conductance, membrane permeability and leaf water content, ionic composition in salt stressed strawberry (Fragaria × ananassa). Sci Hortic 130:133–140

    Article  CAS  Google Scholar 

  • Kim HJ, Chen F, Wang X, Choi JH (2006) Effect of methyl jasmonate on phenolics, isothiocyanate, and metabolic enzymes in radish sprout (Raphanus sativus L.). J Agric Food Chem 54:7263–7269

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Masia A, Ventura M, Gemma H, Sansavini S (1998) Effect of some plant growth regulator treatments on apple fruit ripening. Plant Growth Regul 25:127–134

    Article  CAS  Google Scholar 

  • Misra N, Gupta AK (2005) Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Sci 169:331–339

    Article  CAS  Google Scholar 

  • Moerschbacher B, Heck B, Kogel KH, Obs O, Reisener H (1986) An elicitor of the hypersensitive lignification response in wheat leaves isolated from the rust fungus Puccinia graminis f. sp. tritici. II. Induction of enzymes correlated with the biosynthesis of lignin. Z Naturforsch 41:839–844

    CAS  Google Scholar 

  • Mohammdkhani N, Heidari R, Abbaspour N (2013) Effects of salinity on antioxidant system in four grape (Vitis vinifera L.). Vitis 52:105–110

    Google Scholar 

  • Mordue AJ, Blackwell A (1993) Azadirachtin: an update. J Insect Physiol 39:303–324

    Article  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  CAS  PubMed  Google Scholar 

  • Patakas A, Noitsakis B (1999) Mechanisms involved in diurnal changes of osmotic potential in grapevines under drought conditions. J Plant Physiol 154:767–774

    Article  CAS  Google Scholar 

  • Peng Z, He P, Sun J, Pan Z, Gong W, Lu Y, Du X (2016) Na+ compartmentalization related to salinity stress seedlings. Sci Rep 6:34848. https://doi.org/10.1038/srep34548

    Article  Google Scholar 

  • Pereira PS, Ticli FK, França SC, de Souza Breves CM, Lourenco MV (2007) Enhanced triterpene production in Tabernaemontana catharinensis cell suspension cultures in response to biotic elicitors. Quim Nova 30:1349–1852

    Google Scholar 

  • Plengmuankhae W, Tantitadapitak C (2015) Low temperature and water dehydration increase the levels of asiaticoside and madecassoside in Centella asiatica (L.) urban. South Afr J Bot 97:196–203

    Article  CAS  Google Scholar 

  • Rady MM (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Sci Hortic 129:232–237

    Article  CAS  Google Scholar 

  • Sasse JM (2003) Physiological actions of brassinosteroids: an update. Plant Growth Regul 22:276–288

    Article  CAS  Google Scholar 

  • Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570. https://doi.org/10.3389/fpls.2016.00570

    Article  PubMed  PubMed Central  Google Scholar 

  • Shahbaz M, Ashraf M (2007) Influence of exogenous application of brassinosteroids on growth and mineral nutrients of wheat (Triticum aestivum L.) under saline conditions. Pak J Bot 39:513–522

    Google Scholar 

  • Shahid MA, Pervez MA, Balal RM, Mattson NS, Rashid A, Ahmad R et al (2011) Brassinosteroid (24-epibrassinolide) enhances growth and alleviates the deleterious effects induced by salt stress in pea (Pisum sativum L.). Aust J Crop Sci 5:500–510

    CAS  Google Scholar 

  • Shang Q, Song S, Zhang Z, Guo S (2006) Exogenous brassinosteroid induced salt resistance of cucumber (Cucumis sativus L.) seedlings. Sci Agric Sin 39:1872–1877

    CAS  Google Scholar 

  • Sharma I, Ching E, Saini S, Bhardwaj R, Pati PK (2013) Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety pusa basmati-1. Plant Physiol Biochem 69:17–26

    Article  CAS  PubMed  Google Scholar 

  • Sharma I, Bhardwaj R, Pati PK (2015) Exogenous application of 28-homobrassinolide modulates the dynamics of salt and pesticides induced stress responses in an elite rice variety pusa basmati-1. J Plant Growth Regul 34:509–518

    Article  CAS  Google Scholar 

  • Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131

    Article  CAS  PubMed  Google Scholar 

  • Sirhindi G, Kumar S, Bharadwaj R, Kumar R (2009) Effects of 24-epibrassinolide and 28-homobrassinolide on the growth and antioxidant enzyme activities in the seedlings of Brassica juncea L. Physiol Mol Plant Pathol 15:335–341

    CAS  Google Scholar 

  • Smaili A, Mazoir N, Rifai LA, Koussa T, Makroum K, Benharref A, Faize L, Alburquerque N, Burgos L, Belfaiza M, Faize M (2017a) Antimicrobial activity of two semisynthetic triterpene derivatives from Euphorbia officinarum latex against fungal and bacterial phytopathogens. Nat Prod Commun 12:331–336

    Google Scholar 

  • Smaili A, Mazoir N, Rifai LA, Koussa T, Makroum K, Kabil EM, Benharref A, Faize M (2017b) Triterpene derivatives from Euphorbia enhance resistance against Verticillium wilt of tomato. Phytochemistry 135:169–180

    Article  CAS  PubMed  Google Scholar 

  • Stobart A, Griffiths WT, Ameen-Bukhari I, Sherwood RP (1985) The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiol Plant 6:293–298

    Article  Google Scholar 

  • Taffouo VD, Wamba OF, Yombi E, Nono GV, Akoa A (2010) Growth, yield, water status and ionic distribution response of three bambara groundnut (Vigna subterranean (L.) verdc.) landraces grown under saline conditions. Int J Bot 6:53–58

    Article  CAS  Google Scholar 

  • Taibi K, Taibi T, Ait Abderrahim L, Ennajah A, Belkhodja M, Mulet JM (2016) Effect of salt stress on growth, chlorophyll content, lipid peroxidation and antioxidant defence systems in Phaseolus vulgaris L. South Afr J Bot 105:306–312

    Article  CAS  Google Scholar 

  • Taranto F, Pasqualone A, Mangini G, Tripodi P, Miazzi MM, Pavan S, Montemurro C (2017) Polyphenol oxidases in crops: biochemical, physiological and genetic aspects. Int J Mol Sci 18:377. https://doi.org/10.3390/ijms18020377

    Article  PubMed Central  Google Scholar 

  • Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A (2014) Triterpene biosynthesis in plants. Annu Rev Plant Biol 65:225–257

    Article  CAS  PubMed  Google Scholar 

  • Vardhini BV, Anjum NA (2015) Brassinosteroids make plant life easier under abiotic stresses mainly by modulating major components of antioxidant defense system. Front Environ Sci 2:1–15. https://doi.org/10.3389/fenvs2014.00067

    Article  Google Scholar 

  • Vardhini BV, Sujatha E, Rao SSR (2012) Influence of brassinosteroids on metabolites of Raphanus sativus L. J Phytol 4:45–47

    Google Scholar 

  • Wahid A, Ghazanfar A (2006) Possible involvement of some secondary metabolites in salt tolerance of sugarcane. J Plant Physiol 163:723–730

    Article  CAS  PubMed  Google Scholar 

  • Walker PR, Blackmore DH, Clingeleffer PR (2010) Impact of rootstock on yield and ion concentrations in petioles, juice and wine of Shiraz and Chardonnay in different viticultural environments with different irrigation water salinity. Aust J Grape Wine Res 16:243–257

    Article  CAS  Google Scholar 

  • Wang CM, Zhang JL, Liu S, Li Z, Wu GQ, Cai JY, Flowers TJ, Wang SM (2009) Puccinellia tenuiflora maintains a low Na+ level under salinity by limiting unidirectional Na+ influx resulting in a high selectivity for K+ over Na+. Plant Cell Environ 32:486–496

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Zhang P, Meng J, Xi Z (2015) Effect of exogenous 24-epibrassinolide on chlorophyll fluorescence, leaf surface and cellular ultrastructure of grape seedlings (Vitis vinifera L.) under water stress. Acta Physiol Plant 37:1729–1740

    Article  CAS  Google Scholar 

  • Wu JY, Wong K, Ho KP, Zhou LG (2005) Enhancement of saponin production in Panax ginseng cell culture by osmotic stress and nutrient feeding. Enzyme Microb Technol 36:133–138

    Article  CAS  Google Scholar 

  • Yu IQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogues S (2004) A role of brassinosteroids in the regulation of photosynthesis in Cucumis sativas. J Exp Bot 55:1135–1143

    Article  CAS  PubMed  Google Scholar 

  • Zine H, Rifai LA, Koussa T, Bentiss F, Guesmi S, Laachir A, Makroum K, Belfaiza M, Faize M (2017) Themononuclear nickel(II) complex bis(azido-κN)bis[2,5-bis(pyridin-2-yl)-1, 3,4-thiadiazole-κ2N2, N3]nickel(II) protects tomato from Verticillium dahliae by inhibiting fungal growth and activating plant defences. Pest Manag Sci 73:188–197

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. N. Alburquerque from CEBAS-CSIC (Murcia, Spain) for carrying out the mineral analyses of the samples.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohamed Faize.

Additional information

Communicated by L. Bavaresco.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rifai, L.A., Mazoir, N., Koussa, T. et al. Foliar application of the triterpene derivative 24-methylen-elemo-lanosta-8,24-dien-3-one alleviates salt toxicity in grapevine. Acta Physiol Plant 40, 57 (2018). https://doi.org/10.1007/s11738-018-2636-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2636-5

Keywords

Navigation