Protective Effect of Methyl Jasmonate on Photosynthetic Performance and Its Association with Antioxidants in Contrasting Aluminum-Resistant Blueberry Cultivars Exposed to Aluminum

  • Elizabeth M. Ulloa-Inostroza
  • M. Alberdi
  • A. G. Ivanov
  • M. Reyes-DíazEmail author
Research Article


Methyl jasmonate (MeJA) protective effect on photosynthetic performance and its association with antioxidants in two highbush blueberry (Vaccinium corymbosum L.) cultivars with contrasting aluminum (Al) resistance under Al toxicity was determined. Legacy (Al-resistant) and Bluegold (Al-sensitive) cultivars were subjected to control, MeJA, Al, and their combination (Al+MeJA) for 0, 24, and 48 h under greenhouse conditions. Al concentration, oxidative damage (malondialdehyde (MDA) and H2O2 concentrations), antioxidant activity (AA), superoxide dismutase (SOD) and catalase (CAT) activities, total polyphenols (TPP), chlorogenic acid, and in vivo photosynthetic performance were determined. The exposure to Al toxicity increased the Al concentration (up to 15-fold) and oxidative damage (up to 5.5-fold) compared to the control at 48 h, despite the antioxidant responses (SOD and CAT activities) were increased (up to 4-fold), mainly in the Al-sensitive cultivar at 48 h. Concomitantly, the photosynthetic performance was strongly reduced in the Al-sensitive cultivar (1.6-fold), while the Al-resistant cultivar was more stable during the experiment. However, when cultivars were exposed to Al+MeJA, the Al accumulation and oxidative damage strongly decreased (7-fold and 1.6-fold, respectively), increasing AA, SOD and CAT activities, and TPP in both cultivars during the first hours of Al exposure. The MeJA application decreased Al uptake and stimulated antioxidant pathways, which may counteract the toxic Al effects, protecting the photosynthetic apparatus in both cultivars, being more evident in the Al-sensitive cultivar.


Chlorophyll fluorescence Methyl jasmonate Photosynthesis Pigments Oxidative stress 



We are very grateful for FONDECYT Project no. 1171286 which supported this work and PhD fellowship no. 21110919, both from the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) of the Government of Chile, as well as the DI 13-2017, DI 15-2015, and DI 16-2011 Projects from the Dirección de Investigación at the Universidad de La Frontera, Temuco, Chile. Finally, we wish to thank Mariela Mora for her valuable assistance in the laboratory.


  1. Ali S, Zeng F, Qiu L, Zhang G (2011) The effect of chromium and aluminum on growth, root morphology, photosynthetic parameters and transpiration of the two barley cultivars. Biol Plant 55:291–296CrossRefGoogle Scholar
  2. Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153CrossRefGoogle Scholar
  3. Banhos OFAA, Carvalho BM dO, da Veiga EB, Bressan ACG, Tanaka FAO, Habermann G (2016) Aluminum-induced decrease in CO2 assimilation in ‘Rangpur’ lime is associated with low stomatal conductance rather than low photochemical performances. Scientia Hort 205:133–140CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Briat JF, Dubos C, Gaymard F (2015) Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20:33–40CrossRefGoogle Scholar
  6. Chen L-S, Qi Y-P, Liu X-H (2005a) Effects of aluminum on light energy utilization and photoprotective systems in citrus leaves. Ann Bot 96:35–41CrossRefGoogle Scholar
  7. Chen L-S, Qi Y-P, Smith BR, Liu XH (2005b) Aluminum-induced decrease in CO2 assimilation in citrus seedlings is unaccompanied by decreased activities of key enzymes involved in CO2 assimilation. Tree Physiol 25:317–324CrossRefGoogle Scholar
  8. Chen J, Yan Z, Li X (2014) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotox Environ Saf 104:349–356CrossRefGoogle Scholar
  9. Chinnici F, Bendini A, Gaiani A, Riponi C (2004) Radical scavenging activities of peels and pulps from cv. Golden delicious apples as related to their phenolic composition. J Agr Food Chem 52:4684–4689CrossRefGoogle Scholar
  10. Demmig-Adams B, Adams IIIWW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21CrossRefGoogle Scholar
  11. Du Z, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1556–1570CrossRefGoogle Scholar
  12. Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J 2015:1–18CrossRefGoogle Scholar
  13. Farooq MA, Gill RA, Islam F, Ali B, Liu H, Xu J, He S, Zhou W (2016) Methyl jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L. Front Plant Sci 11:468Google Scholar
  14. Fleming J, Joshi JG (1987) Ferritin: isolation of aluminum–ferritin complex from brain. Proc Natl Acad Sci U S A 84:7866–7870CrossRefGoogle Scholar
  15. Garcia-Plazaola JI, Becerril JM (1999) A rapid HPLC method to measure liphophilic antioxidant in stressed plants: simultaneous determination of carotenoids and tocopherols. Phytochem Anal 10:307–313CrossRefGoogle Scholar
  16. Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  17. Hanaka A, Wójcik M, Dresler S, Mroczek-Zdyrska M, Maksymiec W (2016) Does methyl jasmonate modify the oxidative stress response in Phaseolus coccineus treated with Cu? Ecotox Environ Saf 124:480–488Google Scholar
  18. Hasni I, Yaakoubi H, Hamdani S, Tajmir-Riahi H-A, Carpentier R (2015a) Mechanism of interaction of Al3+ with the proteins composition of photosystem II. PLoS One 10:e0120876CrossRefGoogle Scholar
  19. Hasni I, Msilini N, Hamdani S, Tajmir-Riahi H-A, Carpentier R (2015b) Characterization of the structural changes and photochemical activity of photosystem I under Al3+ effect. J Photochem Photobiol B Biol 149:292–299CrossRefGoogle Scholar
  20. Hoagland DR, Arnon DI (1959) The water culture method for growing plants without soil. California Agr Expt Sta 347:1–32Google Scholar
  21. Inostroza-Blancheteau C, Soto B, Ulloa P, Aquea F, Reyes-Díaz M (2008) Resistance mechanisms of aluminum (Al3+) phytotoxicity in cereals: physiological, genetic and molecular bases. J Soil Sci Plant Nutr 8:57–71Google Scholar
  22. Ismail A, Riemann M, Nick P (2012) The jasmonate pathway mediates salt tolerance in grapevines. J Exp Bot 63:2127–2139CrossRefGoogle Scholar
  23. Ivanov AG, Sane PV, Hurry V, Öquist G, Hüner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574CrossRefGoogle Scholar
  24. Jiang HX, Chen LS, Zheng J-G, Han S, Tang N, Smith BR (2008) Aluminum-induced effects on photosystem II photochemistry in Citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863–1871CrossRefGoogle Scholar
  25. Keramat B, Kalantari KM, Arvin MJ (2009) Effects of methyl jasmonate in regulating cadmium induced oxidative stress in soybean plant (Glycine max L.). Afr J Microbiol Res 3:240–244Google Scholar
  26. Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598CrossRefGoogle Scholar
  27. Kulbat K (2016) The role of phenolic compounds in plant resistance. Biotechnol Food Sci 80:97–108Google Scholar
  28. Larronde F, Gaudillière JP, Krisa S, Decendit A, Deffieux G, Mérillon JM (2003) Airborne methyl jasmonate induces stilbene accumulation in leaves and berries of grapevine plants. Am J Enol Vitic 54:60–63Google Scholar
  29. Li Z, Xing D (2011) Mechanistic study of mitochondria dependent programmed cell death induced by aluminum phytotoxicity using fluorescence techniques. J Exp Bot 62:331–343CrossRefGoogle Scholar
  30. Li Z, Xing F, Xing D (2012) Characterization of target site of aluminum phytotoxicity in photosynthetic electron transport by fluorescence techniques in tobacco leaves. Plant Cell Physiol 53:1295–1309CrossRefGoogle Scholar
  31. Lidon FC, Barreiro MG, Ramalho JDC, Lauriano JA (1999) Effects of aluminum toxicity on nutrient accumulation in maize shoots: implications on photosynthesis. J Plant Nutr 22:397–416CrossRefGoogle Scholar
  32. Locke AM, Ort DR (2014) Leaf hydraulic conductance declines in coordination with photosynthesis, transpiration and leaf water status as soybean leaves age regardless of soil moisture. J Exp Bot 65:6617–6627CrossRefGoogle Scholar
  33. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  34. McAinsh MR, Clayton H, Mansfield TA, Alistair M (1996) Hetherington changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042CrossRefGoogle Scholar
  35. Meriño-Gergichevich C, Alberdi M, Ivanov AG, Reyes-Díaz M (2010) Al3+-Ca2+ interaction in plants growing in acid soils: Al-phytotoxicity response tocalcareous amendments. J Soil Sci Plant Nutr 10:217–243Google Scholar
  36. Meriño-Gergichevich C, Ondrasek G, Zovko M, Šamec D, Alberdi M, Reyes-Díaz M (2015) Comparative study of methodologies to determine the antioxidant capacity of Al-toxified blueberry amended with calcium sulfate. J Soil Sci Plant Nutr 15:965–978Google Scholar
  37. Moustaka J, Ouzounidou G, Bayçu G, Moustakas M (2016) Aluminum resistance in wheat involves maintenance of leaf Ca(2+) and Mg(2+) content, decreased lipid peroxidation and Al accumulation, and low photosystem II excitation pressure. Biometals 29:611–623CrossRefGoogle Scholar
  38. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749CrossRefGoogle Scholar
  39. Pinhero RG, Rao MV, Paliyath G, Murr DP, Fletcher RA (1997) Changes in activities of antioxidant enzymes and their relationship to genetic and paclobutrazol-induced chilling tolerance of maize seedlings. Plant Physiol 114:695–704CrossRefGoogle Scholar
  40. Piotrowska A, Bajguz A, Godlewska-żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffiaarrhiza (Lemnaceae). J Exp Bot 66:507–513CrossRefGoogle Scholar
  41. Quinteiro Ribeiro MA, Furtado de Almeida A-A, Schramm Mielke M, Pinto Gomes F, Pires M, Baligar VC (2013) Aluminum effects on growth, photosynthesis, and mineral nutrition of cacao genotypes. J Plant Nutr 36:1161–1179CrossRefGoogle Scholar
  42. Reyes-Díaz M, Alberdi M, Mora ML (2009) Short-term aluminum stress differentially affects the photochemical efficiency of photosystem II in highbush blueberry genotypes. J Am Soc Hort Sci 134:14–21Google Scholar
  43. Reyes-Díaz M, Inostroza-Blancheteau C, Millaleo R, Cruces E, Wulff-Zottele C, Alberdi M, Mora ML (2010) Long-term aluminum exposure effects on physiological and biochemical features of highbush blueberry cultivars. J Am Soc Hort Sci 135:212–222Google Scholar
  44. Reyes-Díaz M, Meriño-Gergichevich C, Alarcón E, Alberdi M, Horst WJ (2011) Calcium sulfate ameliorates the effect of aluminum toxicity differentially in genotypes of highbush blueberry (Vacciniumcorymbosum L.). J Soil Sci Plant Nutr 11:59–78CrossRefGoogle Scholar
  45. Ribera AE, Reyes-Díaz M, Alberdi M, Zuniga GE, Mora ML (2010) Antioxidant compounds in skin and pulp of fruits change among genotypes and maturity stages in highbush blueberry (VacciniumcorymbosumL.) grown in southern Chile. J Soil Sci Plant Nutr 10:509–536CrossRefGoogle Scholar
  46. Roselló M, Poschenrieder C, Gunsé B, Barceló J, Llugany M (2015) Differential activation of genes related to aluminium tolerance in two contrasting rice cultivars. J Inorg Biochem 152:160–166CrossRefGoogle Scholar
  47. Ryan PR, Delhaize E (2010) The convergent evolution of aluminium resistance in plants exploits a convenient currency. Funct Plant Biol 37:275–284CrossRefGoogle Scholar
  48. Sadzawka AM, Grez R, Carrasco MA, Mora ML (2004) Métodos de análisis de tejidos vegetales. Comisión de normalización y acreditación, sociedad chilena de la ciencia del suelo, In: Editorial salesianos impresores, Santiago, Chile, p.105Google Scholar
  49. Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214CrossRefGoogle Scholar
  50. Silva S, Pinto G, Dias MC, Correia CM, Moutinho-Pereira J, Pinto-Carnide O, Santos C (2012) Aluminium long-term stress differently affects photosynthesis in rye genotypes. Plant Physiol Biochem 54:105–112CrossRefGoogle Scholar
  51. Sirhindi G, Mir MA, Abd-Allah EF, Ahmad P, Gucel S (2016) Jasmonic acid modulates the physio-biochemical attributes, antioxidant enzyme activity, and gene expression in glycine max under nickel toxicity. Front Plant Sci 7:591CrossRefGoogle Scholar
  52. Slinkard K, Singleton VL (1977) Total phenol analysis: automation and comparison with manual methods. Am J Enol Vitic 28:29–55Google Scholar
  53. Tighe-Neira R, Díaz-Harris R, Leonelli-Cantergiani G, Mejías-Lagos P, Iglesias-González C, Inostroza-Blancheteau C (2018) Effect of Ulex europaeus L. extracts on polyphenol concentration in Capsicum annuum L. and Lactuca sativa L. J Soil Sci Plant Nutr 18:893–903Google Scholar
  54. Ulloa-Inostroza EM, Alberdi M, Meriño-Gergichevich C, Reyes-Díaz M (2017) Low doses of exogenous methyl jasmonate applied simultaneously with toxic aluminum improves the antioxidant performance of Vaccinium corymbosum. Plant Soil 412:81–96CrossRefGoogle Scholar
  55. Xue YJ, Ling T, Yang ZM (2008) Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. J Agric Food Chem 56:9676–9684CrossRefGoogle Scholar
  56. Yan Z, Chen J, Li X (2013) Methyl jasmonate as modulator of Cd toxicity in Capsicum frutescens var. fasciculatum seedlings. Ecotox Environ Saf 98:203–209Google Scholar
  57. Yang M, Tan L, Xu Y, Zhao Y, Cheng F, Ye S, Jiang W (2015) Effect of low pH and aluminum toxicity on the photosynthetic characteristics of different fast-growing eucalyptus vegetatively propagated clones. PLoS One 10:e0130963CrossRefGoogle Scholar
  58. Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448CrossRefGoogle Scholar
  59. Zhang XB, Liu P, Yang YS, Xu GD (2007) Effect of Al in soil on photosynthesis and related morphological and physiological characteristics of two soybean genotypes. Bot Stud 48:435–444Google Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  • Elizabeth M. Ulloa-Inostroza
    • 1
    • 2
    • 3
  • M. Alberdi
    • 3
    • 4
  • A. G. Ivanov
    • 5
    • 6
  • M. Reyes-Díaz
    • 3
    • 4
    Email author
  1. 1.Programa de Doctorado en Ciencias de Recursos NaturalesUniversidad de La FronteraTemucoChile
  2. 2.Laboratorio de Fisiología Vegetal AplicadaUniversidad de AysénCoyhaiqueChile
  3. 3.Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Technological Bioresource Nucleus (BIOREN-UFRO)Universidad de La FronteraTemucoChile
  4. 4.Departamento de Ciencias Químicas y Recursos NaturalesUniversidad de La FronteraTemucoChile
  5. 5.Department of Biology and the BiotronUniversity of Western OntarioLondonCanada
  6. 6.Institute of Biophysics and Biomedical EngineeringBulgarian Academy of SciencesSofiaBulgaria

Personalised recommendations