Abstract
Aims
The effect of different MeJA doses applied prior to or simultaneously with toxic Al on biochemical and physiological properties of Vaccinium corymbosum cultivars with contrasting Al resistance was studied.
Methods
Legacy (Al-resistant) and Bluegold (Al-sensitive) plants were treated with and without toxic Al under controlled conditions: a) without Al and MeJA, b) 100 μM Al, c) 100 μM Al + 5 μM MeJA, d) 100 μM Al + 10 μM MeJA and e) 100 μM Al + 50 μM MeJA. MeJA was applied to leaves 24 h prior to or simultaneously with Al in nutrient solution. After 48 h, Al-concentration, lipid peroxidation (LP), H2O2, antioxidant activity, total phenols, total flavonoids, phenolic compounds and superoxide dismutase activity (SOD) of plant organs were analyzed.
Results
Al-concentrations increased with Al-treatment in both cultivars, being Al, LP and H2O2 concentrations reduced with low simultaneous MeJA application. Higher MeJA doses induced more oxidative damage than the lowest. Legacy increased mainly non-enzymatic compounds, whereas Bluegold increased SOD activity to counteract Al3+.
Conclusions
Low MeJA doses applied simultaneously with Al3+ increased Al-resistance in Legacy by increasing phenolic compounds, while Bluegold reduced oxidative damage through increment of SOD activity, suggesting a diminution of its Al-sensitivity. Higher MeJA doses could be potentially toxic. Studies are needed to determine the molecular mechanisms involved in the protective MeJA effect against Al-toxicity.
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References
An SH, Choi HW, Hwang IS, Hong JK, Hwang BK (2008) A novel pepper membrane-located receptor-like protein gene CaMRP1 is required for disease susceptibility, methyl jasmonate insensitivity and salt tolerance. Plant Mol Biol 67:519–533
Barceló J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot 48:75–92
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 72:248–254
Castrejón A, Eichholz I, Rohn S, Kroh LW, Huyskens-Keil S (2008) Phenolic profile and antioxidant activity of highbush blueberry (Vaccinium corymbosum L.) during fruit maturation and ripening. J Food Chem 109:564–572
Chen H, Jones AD, Howe GA (2006) Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Lett 580:2540–2546
Chen J, Yan Z, Li X (2014) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf 104:349–356
Cheng GW, Breen PJ (1991) Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J Amer Soc Hort Scl 116:865–869
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 52:4684–4689
Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: Regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci U S A 92:4114–4119
Creelman RA, Mullet JE (1997) Oligosaccharins, brassinolides, and jasmonates: nontraditional regulators of plant growth, development, and gene expression. Plant Cell 9:1211–1223
Delhaize E, Ma JF, Ryan PR (2012) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348
Du Z, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1556–1570
Ehlenfeldt MK, Prior RL (2001) Oxygen radical absorbance capacity (ORAC) and phenolic and anthocyanin concentrations in fruit and leaf tissues of highbush blueberry. J Agric Food Chem 49:2222–2227
Eraso F, Hartley RD (1990) Monomeric and dimeric constituents of plant cell walls possible factors influencing wall biodegradability. J Sci Food Agric 51:163–170
Gao XP, Wang XF, Lu YF, Zhang LY, Shen YY, Liang Z, Zhang DP (2004) Jasmonic acid is involved in the water-stress-induced betaine accumulation in pear leaves. Plant Cell Environ 27:497–507
Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol 59:309–314
Guo TR, Zhang GP, Zhang YH (2007) Physiological changes in barley plants under combined toxicity of aluminum, copper and cadmium. Colloids Surf B 57:182–188
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? Ecotoxicol Environ Saf 124:480–488
Harris CS, Burt AJ, Saleem A, Le PM, Martineau LC, Haddad PS, Bennett SAL, Arnason JT (2007) A single HPLC-PAD-APCI/MS method for the quantitative comparison of phenolic compounds found in leaf, stem, root and fruit extracts of Vaccinium angustifolium. Phytochem Anal 18:161–169
Heijari J, Nerg AM, Kainulainen P, Vuorinen M, Holopainen JK (2008) Long-term effects of exogenous methyl jasmonate application on Scots pine (Pinus sylvestris) needle chemical defense and diprionid sawfly performance. Entomol Exp Appl 128:162–171
Hu X, Li W, Chen Q, Yang Y (2009) Early signal transduction linking the synthesis of jasmonic acid in plant. Plant Signal Behav 4:696–697
Huang W, Yang X, Yao S, LwinOo T, He H, Wang A, Li C, He L (2014) Reactive oxygen species burst induced by aluminum stress triggers mitochondria-dependent programmed cell death in peanut root tip cells. Plant Physiol Biochem 82:76–84
Inostroza-Blancheteau C, Reyes-Díaz M, Aquea F, Nunes-Nesi A, Alberdi M, Arce-Johnson P (2011) Biochemical and molecular changes in response to aluminium-stress in highbush blueberry (Vaccinium corymbosum L). Plant Physiol Biochem 49:1005–1012
Inostroza-Blancheteau C, Rengel Z, Alberd M, Mora M, Aquea F, Arce-Johnson P, Reyes-Díaz M (2012) Molecular and physiological strategies to increase aluminum resistance in plants. Mol Biol Rep 39:2069–2079
Ismail A, Riemann M, Nick P (2012) The jasmonate pathway mediates salt tolerance in grapevines. J Exp Bot 63:2127–2139
Jung SJ (2004) Effect of chlorophyll reduction in Arabidopsis thaliana by methyl jasmonate or norflurazon on antioxidant systems. Plant Physiol Biochem 42:225–231
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 3:240–244
Kochian LV, Pineros MA, Liu J, Magalhaes JV (2015) Plant Adaptation to acid soils: The molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:571–598
Konan YKF, Kouassi KM, Kouakou KL, Koffi E, Kouassi KN, Sekou D, Kone M, Kouakou TH (2014) Effect of Methyl Jasmonate on Phytoalexins Biosynthesis and Induced Disease Resistance to Fusarium oxysporum f. sp. Vasinfectum in Cotton (Gossypium hirsutum L.). Intl J Agron 2014:1–11
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 54:60–63
Li Y, Nie Y, Zhang Z, Ye Z, Zou X, Zhang LH, Wang Z (2014) Comparative proteomic analysis of methyl jasmonate-induced defense responses in different rice cultivars. Proteomics 14:1088–1101
Liu J, Li Z, Wang Y, Xing D (2014) Overexpression of ALTERNATIVE OXIDASE1a alleviates mitochondria-dependent programmed cell death induced by aluminium phytotoicity in Arabidopsis. J Exp Bot 65:4465–4478
Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787
Ma B, Wan J, Shen ZG (2007) H2O2 production and antioxidant responses in seeds and early seedlings of two different rice varieties exposed to aluminum. Plant Growth Regul 52:91–100
Maksymiec W, Krupa Z (2002) Jasmonic acid and heavy metals in Arabidopsis plants- a similar physiological responses to both stressors? J Plant Physiol 159:509–515
Maksymiec W, Krupa Z (2007a) Effects of methyl jasmonate and excess copper on root and leaf growth. Biol Plant 51:322–326
Maksymiec W, Wójcik M, Krupa Z (2007b) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66:421–427
Manquián K, Zúñiga GE, Barrientos H, Escudey M, Molina M (2013) Effect of aluminum on antioxidant activity and phenolic compounds content in in vitro cultured blueberries. Bol Latinoam Caribe Plant Med Aromat 12:603–611
Mäntylä E, Blande JD, Klemola T (2014) Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature? Arthropod Plant Interact 8:143–153
Matsuo Y, Fujita Y, Ohnishi S, Tanaka T, Hirabaru H, Kai T, Sakaida H, Nishizono S, Kouno I (2010) Chemical constituents of the leaves of rabbiteye blueberry (Vaccinium ashei) and characterisation of polymeric proanthocyanidins containing phenylpropanoid units and A-type linkages. Food Chem 121:1073–1079
McDonald M, Mila I, Scalbert A (1996) Precipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitation. J Agric Food Chem 44:599–606
Menga X, Hana J, Wang Q, Tian S (2009) Changes in physiology and quality of peach fruits treated by methyl jasmonate under low temperature stress. Food Chem 114:1028–1035
Moreira X, Sampedro L, Zas R (2009) Defensive responses of Pinus pinaster seedlings to exogenous application of methyl jasmonate: Concentration effect and systemic response. Environ Exp Bot 67:94–100
Pan JW, Zhu MY, Chen H (2001) Aluminum-induced cell death in root-tip cells of barley. Environ Exp Bot 46:71–79
Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W, Inzé D, Goossens A (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci U S A 105:1380–1385
Piotrowska A, Bajguz A, Godlewska-żyłkiewicz B, Czerpak R, Kamińska M (2009) Jasmonic acid as modulator of lead toxicity in aquatic plant Wolffia arrhiza (Lemnaceae). J Exp Bot 66:507–513
Poonam S, Kaur H, Geetika S (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) Mill sp. seedlings under copper stress. Am J Plant Sci 4:817–823
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 Amer Soc Hort Sci 134:14–21
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 Amer Soc Hort Sci 135:212–222
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 (Vaccinium corymbosum L.) grown in southern Chile. J Soil Sci Plant Nutr 10:509–536
Rudell DR, Mattheis JP, Fan X, Fellman JK (2002) Methyl jasmonate enhances anthocyanin accumulation and modified production of phenolics and pigments in “Fuji” apples. J Amer Soc Hort Sci 127:435–441
Ruhland CT, Day TA (2000) Effects of ultraviolet-B radiation on leaf elongation, production and phenylpropanoid concentrations of Deschampsia antarctica and Colobanthus quitensis in Antarctica. Physiol Plant 109:244–251
Ruiz-García Y, Romero-Cascales I, Gil-Muñoz R, Fernández-Fernández JI, López-Roca JM, Gómez-Plaza E (2012) Improving grape phenolic content and wine chromatic characteristics through the use of two different elicitors: Methyl jasmonate versus benzothiadiazole. J Agric Food Chem 60:1283–1290
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. 105
Schaller A, Stintzi A (2009) Enzymes in jasmonate biosynthesis - Structure, function, regulation. Phytochemistry 70:1532–1538
Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214
Shao HB, Chu LY, Shao MA, Jaleel CA, Mi HM (2008) Higher plant antioxidants and redox signaling under environmental stresses. C R Biologies 331:433–441
Sivaguru M, Liu J, Kochian LV (2013) Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance. Plant J 76:297–307
Slinkard K, Singleton VL (1977) Total phenol analysis: automation and comparison with manual methods. Am J Enol Vitic 28:29–55
Spollansky TC, Pitta-Alvarez SI, Giulietti AM (2000) Effect of jasmonic acid and aluminum on production of tropane alkaloids in hairy root cultures of Brugmansia candida. Electron J Biotechnol 3:72–75
Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71
Wang SY (1999) Methyl jasmonate reduces water stress in strawberry. J Plant Growth Regul 18:127–134
Wang FZ, Wang QB, Kwon SY, Kwak SS, Su WA (2005) Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. J Plant Physiol 162:465–472
Wang SY, Chen C, Wang CY (2009) The influence of light and maturity on fruit quality and flavonoid content red raspberries. Food Chem 112:676–684
Wang LJ, Wu J, Wang HX, Li SS, Zheng XC, Du H, Xu YJ, Wang LS (2015) Composition of phenolic compounds and antioxidant activity in the leaves of blueberry cultivars. J Funct Foods 16:295–304
Xue YJ, Tao L, Yang ZM (2008) Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. J Agric Food Chem 56:9676–9684
Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72
Yoon JY, Hamayun M, Lee SK, Lee IJ (2010) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12:63–68
Zhang L, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092–1111
Acknowledgments
We are very grateful for FONDECYT Project N° 1120917 which supported this work and PhD fellowship N°21110919, both from the Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) of the Government of Chile, as well as the 2013 DI 13-2017 and 2015 DI 15-2015 Projects from the Dirección de Investigación at the Universidad de La Frontera, Temuco, Chile. We would like to thank Graciela Muñoz Pozo for her valuable assistance in the laboratory, and Dr. Helen Lowry for revising the language of the manuscript. Finally, we wish to thank the Doctorado en Ciencias de Recursos Naturales Program and the Laboratorio de Fisiología y Bioquímica Vegetal at the Universidad de La Frontera, Temuco, Chile.
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Ulloa-Inostroza, E.M., Alberdi, M., Meriño-Gergichevich, C. et al. Low doses of exogenous methyl jasmonate applied simultaneously with toxic aluminum improve the antioxidant performance of Vaccinium corymbosum . Plant Soil 412, 81–96 (2017). https://doi.org/10.1007/s11104-016-2985-z
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DOI: https://doi.org/10.1007/s11104-016-2985-z