Effect of phenolic acids on the antioxidant system of tomato plants (Solanum lycopersicum Mill.)
DOI:
https://doi.org/10.15517/am.v32i3.45101Keywords:
enzymatic antioxidants, no-enzymatic antioxidants, antioxidant capacityAbstract
Introduction. Phenolic acids belong to the group of phenolic compounds, their synthesis and concentration in plants increases when they are under biotic or abiotic stress conditions. Objective. To evaluate the effect of phenolic acids on the enzymatic and non-enzymatic antioxidant defense system in tomato plants subjected to biotic stress. Materials and methods. The experiment was carried out from March to December 2016, in Saltillo, Mexico. A tomate crop Saladette type of the Rio Fuego variety (Solanum lycopersicum Mill.) was stablished. Tomato plants inoculated with Clavibacter michiganensis subsp. michiganensis (1X105 CFU ml-1) were foliar sprayed with phenolic acids at a dose of 1 kg ha-1 with the Defens Gr® product (IA: phenolic acids 10 000 ppm). Leaves were sampled at 15, 31, and 92 days after the transplantation (ddt) and fruits at 90 ddt. Six treatments were used: 1) absolute control (T0), 2) application of phenolic acids before the inoculation with Clavibacter (AFA), 3) application of phenolic acids after inoculation with Clavibacter (AFD), 4) application of phenolic acids before and after inoculation with Clavibacter (AFAD), 5) only application of phenolic acids (AF), and 6) only inoculation with Clavibacter (Cmm). Results. The application of phenolic acids intervened in the activity of enzymatic and non-enzymatic antioxidants. A higher antioxidant capacity was found in leaf than in fruit, which was determined by ABTS (2,2’-azino-bis (3-ethylbenzothiazolin-6-sulfonic acid)) and DPPH (1,1-diphenyl-2-picrilhydrazil). The inoculation of tomato plants increased the activity of catalase and phenylalanine ammonium lyase enzymes in leaf; in addition, there was reduction of superoxide dismutase enzyme activity and total phenol content. Conclusion. Phenolic acids intervened in the enzymatic defense mechanisms of the plant and reduced the stress levels caused by inoculation.
Downloads
References
Apolonio-Rodríguez, I., Franco-Mora, O., Salgado-Siclán, M. L., & Aquino-Martínez, J. G. (2017). Inhibición in vitro de Botrytis cinerea con extractos de hojas de vid silvestre (Vitis spp.). Revista Mexicana de Fitopatología, 35(2), 170–185. http://doi.org/10.18781/R.MEX.FIT.1611-1
Appel, K., & Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Arvouet-Grand, A., Vennat, B., Pourrat, A., & Lergret, P. (1994). Standardisation dun extrait de propolis et identification des principaux constituants. Journal de Pharmacie de Belgique, 49(6), 462–468.
Asada, K. (1999). The water cycle in chloroplast: scavenging of active oxygen and dissipation of excess photons. Annual Reviews Plant Physiology and Plant Molecular Biology, 50, 601–639. https://doi.org/10.1146/annurev.arplant.50.1.601
Asada, K. (2000). The water-water cycle as alternative photon and electron sinks. Philosophical Transactions Royal Society London B Biological Science, 355(1402), 1419–1431. https://doi.org/10.1098/rstb.2000.0703
Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology, 141, 391–396. https://doi.org/10.1104/pp.106.082040
Balasundram, N., Sundram, K., & Samman, S. (2006). Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chemistry, 99(1), 191–203. https://doi.org/10.1016/j.foodchem.2005.07.042
Baraldi, R., Bertazza, G., Fontana, A. R., Murcia, G., Pontin, M. A., & Piccoli, P. N. (2017). ABA and GA3 regulate the synthesis of primary and secondary metabolites related to alleviation from biotic and abiotic stresses in grapevine. Phytochemistry, 135, 34–52. https://doi.org/10.1016/j.phytochem.2016.12.007
Bellaloui, N. (2012). Soybean seed phenol, lignin, and isoflavones partitioning as affected by seed node position and genotype differences. Food and Nutrition Sciences, 3(4), 447–454. https://doi.org/10.4236/fns.2012.34064
Blanke, M. M., & Lenz, E. (1989). Fruit photosynthesis. Plant Cell Environment, 12(1), 31–46. https://doi.org/10.1111/j.1365-3040.1989.tb01914.x
Borboa, F. J., Rueda, P. E. O., Acedo, F. E., Ponce, J. F., Cruz, M., Grimaldo, J. O., & García, O. A. M. (2009). Detección de Clavibacter michiganensis subespecie michiganensis en el tomate del estado de Sonora, México. Revista Fitotecnia Mexicana, 32(4), 319–326. http://doi.org/10.35196/rfm.2009.4.319-326
Cansev, A., Gulen, H., & Eris, A. (2011). The activities of catalase and ascorbate peroxidase in olive (Olea europaea L. Cv. Gemlik) under low temperature stress. Horticulture, Environment and Biotechnology, 52(2), 113–120. https://doi.org/10.1007/s13580-011-0126-4
CAYMAN CHEMICAL. (2017). Superoxide dismutase assay kit item № 706002. https://www.caymanchem.com/pdfs/706002.pdf
Cervilla, L. M., Blasco, B., Rios, J. J., Rosales, M. A., Sanchez-Rodriguez, E., Rubio-Wilhelmi, M. M., Romero, L., & Ruiz, J. M. (2012). Parameters symptomatic for boron toxicity in leaves of tomato plants. Journal of Botany, 2012, Article 726206. https://doi.org/10.1155/2012/726206
Daferera, D. J., Ziogas, B. N., & Polissiou, M. G. (2003). The effectiveness of plant essential oils in the growth of Botrytis cinerea, Fusarium sp. and Clavibacter michiganensis subsp. michiganensis. Crop Protection, 22(1), 39–44. https://doi.org/10.1016/S0261(02)00095-9
Diao, Y., Xu. H., Li, G., Yu, A., Yu, X., W. Hu., Zheng, X., Li, S., Wang, Y., & Hu, Z. (2014). Cloning a glutathione peroxidase gene from Nelumbo nucifera and enhanced salt tolerance by overexpressing in rice. Molecular Biology Reports, 41, 4919–4927. https://doi.org/10.1007/s11033-014-3358-4
Di-Rienzo, J. A., Casanoves, F., Balzarini, M. G., González, L., Tablada, M., & Robledo, C. W. (2008). InfoStat versión 2008. Universidad Nacional de Córdoba. https://www.infostat.com.ar/
Dubreuil-Maurizi, C., & Poinssot, B. (2012). Role of glutathione in plant signaling under biotic stress. Plant Signaling & Behavior, 7(2), 210–212. https://doi.org/10.4161/psb.18831
Edet, E. E., Ofem, J. E., Igile, G. O., Ofem, O. E., Zainab, D. B., & Akwaowo, G. (2015). Antioxidant capacity of different African seeds and vegetables and correlation with the contents of ascorbic acid, phenolics and flavonoids. Journal of Medicinal Plants Research, 9(13), 454–461. https://doi.org/10.5897/JMPR2014.5660
Feng, X., Lai, Z., Lin, Y., Lai, G., & Lian, C. (2015). Genome-wide identification and characterization of the superoxide dismutase gene family in Musa acuminata cv. Tianbaojiao (AAA group). BMC Genomics, 16(823), 2–16. https://doi.org/10.1186/s12864-015-2046-7
Flohé, L., & Günzler, W. A. (1984). Assays of glutathione peroxidase. Methods in Enzymology, 105, 114–120. https://doi.org/10.1016/s0076-6879(84)05015-1
Flores-Torres, L. M., Flores-Olivas, A., Ochoa-Fuentes, Y. M., López -Arroyo, J. I., Olalde-Portugal, V., Benavides-Mendoza, A., González-Morales, S., & Zamora-Villa, V. M. (2017). Comparison of enzymes and phenolic compounds in three citrus species infected with Candidatus Liberibacter asiaticus. Revista Mexicana de Fitopatología, 35(2), 314–325. https://doi.org/10.18781/R.MEX.FIT.1608-2
Foyer, C. H., & Noctor, G. (2005). Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell and Environment, 29, 1056–107. https://doi.org/10.1111/j.1365-3040.2005.01327.x
Gartemann, K. H., Kirchner O., Engemann, J., Gräfen, I., Eichenlaub, R., & Burger, A. (2003). Clavibacter michiganensis subsp. michiganensis: First steps in the understanding of virulence of a Gram-positive phytopathogenic bacterium. Journal of Biotechnology, 106(2–3), 179–191. https://doi.org/10.1016/j.jbiotec.2003.07.011
Gaviria, M. C., Hernández, A. J., Lobo, A. M., Medina, C. C., & Rojano, B. (2012). Cambios en la actividad antioxidante en frutos de mortiño (Vaccinium meridionale Sw.) durante su desarrollo y maduración. Revista Facultad Nacional de Agronomía Medellín, 65(1), 6487–6495. http://www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0304-28472012000100019.
Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is fundamental theme of aerobic life. Plant Physiology, 141, 312–322. https://doi.org/10.1104/pp.106.077073
Herbette, S., Labrouhe, D. T., Drevet, J. R., & Roeckel-Drevet, P. (2011). Transgenic tomatoes showing higher glutathione peroxydase antioxidant activity are more resistant to an abiotic stress but more susceptible to biotic stresses. Plant Science, 180(3), 548–553. https://doi.org/10.1016/j.plantsci.2010.12.002
Jones, J. D., & Dangl, J. L. (2006). The plant immune system. Nature, 444(7117), 323–329. https://doi.org/10.1038/nature05286
Lu, L., Wang, J., Zhu, R., Lu, H., Zheng, X., & Yu, T. (2015). Transcript profiling analysis of Rhodosporidium paludigenum mediated signaling pathways and defense responses in mandarin orange. Food Chemistry, 172, 603–612. https://doi.org/10.1016/j.foodchem.2014.09.097
Maddox, C. E., Laur, L. M., & Tian, L. (2010). Antibacterial activity of phenolic compounds against the phytopathogen Xylella fastidiosa. Current Microbiology, 60(1), 53–58. https://doi.org/10.1007/s00284-009-9501-0
Maham, S., Muhammad, K., & Muhammad, S. (2018). Differential responses of plants to biotic stress and the role of metabolites. In P. Ahmad, M. Abass, V. Pratap, D. Kumar, P Alam, & M. Nasser (Eds.), Plant metabolites and regulation under environmental stress (pp. 69–87). Academic Press. https://doi.org/10.1016/B978-0-12-812689-9.00004-2
Marquéz-García, B., Fernández, M. Á., & Córdoba, F. (2009). Phenolics composition in Erica sp. differentially exposed to metal pollution in the Iberian Southwestern Pyritic Belt. Bioresource Technology, 100(1), 446–451. https://doi.org/10.1016/j.biortech.2008.04.070
Mendoza, L., K. Yánez, K., Vivanco, M., Melo, R., & Cotoras, M. (2013). Characterization of extracts from winery by-products with antifungal activity against Botrytis cinerea. Industrial Crops and Products, 43, 360–364. https://doi.org/10.1016/j.indcrop.2012.07.048
Michalak, A. (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies, 15(4), 523–530.
Miller, N. J., Rice-Evans, C., Davies, M. J., Gopinathan, V., & Milner, A. (1993). A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clinical Science, 84, 407–412. https://doi.org/10.1042/cs0840407
Mittler, R., Vanderauwera, S., Gollery, M., & Breusegem, F. V. (2004). Reactive oxygen gene network of plants. Trends in Plant Science, 9(10), 490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Nakano, Y., & Asada, K. (1987). Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation inascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant and Cell Physiology, 28(1), 131–140. https://doi.org/10.1093/oxfordjournals.pcp.a077268.
Navrot, N., Roubier, N., Gelbaye, E., & Jacquot. J. P. (2007). Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiologia Plantarum, 129, 185–195. https://doi.org/10.1111/j.1399-3054.2006.00777.x
Ozyigit, I. I., Filiz, E., Vatansever, R., Kurtoglu, K. Y., Koc, I., Öztürk, M. X., & Anjum, N. A. (2016). Identification and comparative analysis of H2O2-scavenging enzymes (ascorbate peroxidase and glutathione peroxidase) in selected plants employing bioinformatics approaches. Frontiers in Plant Science, 7, Article 301. https://doi.org/10.3389/fpls.2016.00301
Pérez, E., de-la-Noval, B. M., Martínez, B., Torres, W., Medina, A., Hernández, A., & León, O. (2015). Inducción de mecanismos de defensa en plantas de tomate (Solanum lycopersicon L.) micorrizadas frente al ataque de Oidiopsis taurica (Lev.) Salm. Cultivos Tropicales, 36(1), 98–106. http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S0258-59362015000100013
Pignocchi, C., Fletcher, J. M., Wilkinson, J. E., Barnes, J. D., & Foyer, C. H. (2003). The function of ascorbate oxidase in tobacco. Plant Physiology, 132(3), 1631–1641. https://doi.org/10.1104/pp.103.022798
Ramos, S. J., Faquin, V., Guilherme, L. R. G., Castro, E. M., Ávila, F. W., Carvalho, G. S., Bastos, C. E. A., & Oliveira, C. (2010). Selenium biofortification and antioxidant activity in lettuce plants fed with selenate and selenite. Plant Soil and Environment, 56(12), 584–588. https://doi.org/10.17221/113/2010-PSE
Rueda-Barrientos, M. C., Martínez-Fernández, E., Villegas-Torres, O. G., Sainz-Aispuro, M. J., Peña-Chora, G., Hernández-Velazquez, V. M., & Hernández-Romano, J. (2017). Sensibilidad de la prueba de InmunoStrips® en la detección de Clavibacter michiganensis subsp. michiganensis en tomate. Acta Agrícola y Pecuaria, 3(2), 50–57. https://doi.org/10.30973/aap/2017.3.2/4
Servicio de Información Agroalimentaria y Pesquera. (2017). Atlas Agroalimentario 2017. http://nube.siap.gob.mx/gobmx_publicaciones_siap/pag/2017/Atlas-Agroalimentario-2017
Shi, J. X., Cui, M. H., Yang, L., Kim, Y. J., & Zhang, D. B. (2015). Genetic and biochemical mechanisms of pollen wall development. Trends in Plant Science, 20(11), 741–753. https://doi.org/10.1016/j.tplants.2015.07.010
Singleton, V. L., Orthofer, R., & Lamuela-Raventos, R. M. (1999). Analisys of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteau reagent. Methods in Enzymology, 299, 152–178. https://doi.org/10.1016/S0076-6879(99)99017-1
Steiner, A. (1961). A universal method for preparing nutrient solutions of a certain desired composition. Plant and Soil, 15(2), 134–154. https://doi.org/10.1007/BF01347224
Sykłowska-Baranek, K., Pietrosiuk, A., & Naliwajski, M. R. (2012). Effect of l-phenylalanine on PAL activity and production of naphthoquinone pigments in suspension cultures of Arnebia euchroma (Royle) Johnst. In Vitro Cellular & Developmental Biology – Plant, 48(5), 555–564. https://doi.org/10.1007/s11627-012-9443-2
Treutter, D. (2008). Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biology, 7(6), 581–591. https://doi.org/10.1055/s-2005-873009
Vandenabeele, S., Vanderauwera, S., Vuylsteke, M., Rombauts, S., Langebartels, C., Seidilitz, H. K., Zabeau, M., Van-Montagu, M., Inze, D., & Van-Breusegem, F. (2004). Catalase deficiency drastically affects gene expression induced by high light in Arabiodpsis thaliana. The Plant Journal, 39(1), 45–58. https://doi.org/10.1111/j.1365-313X.2004.02105.x
van-Loon, L. C., Rep, M., & C. M. J. (2006). Significance of inducible defense related proteins in infected plants. Annual Review of Phytopathology, 44, 135–162. https://doi.org/10.1146/annurev.phyto.44.070505.143425
Xu, G., Ye, X., Liu, D., Ma, Y., & Chen, J. (2008). Composition and distribution of phenolic acids in Ponkan (Citrus poonensis Hort. ex Tanaka) and Huyou (Citrus paradisi Macf. Changshanhuyou) during maturity. Journal of Food Composition and Analysis, 21(5), 382–389. https://doi.org/10.1016/j.jfca.2008.03.003
Xue, T., Hartikainen, H., & Piironen, V. (2001). Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant and Soil, 237(1), 55–61. https://doi.org/10.1023/A:1013369804867.
Wang, B., Lüttge, U., & Ratajczak, R. (2004). Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3, halophyte Suaeda salsa L. Journal of Plant Physiology, 161(3), 285–293. https://doi.org/10.1078/0176-1617-01123
Wang, X., Fang, G., & Yang, J. (2017). A thioredoxin-dependent glutathione peroxidase (OsGPX5) is required for rice normal development and salt stress Tolerance. Plant Molecular Biology Reporter, 35, 333–342. https://doi.org/10.1007/s11105-017-1026-2
Zárate-Martínez, W., González-Morales, S., Ramírez-Godina, F., Robledo-Olivo, A., & Juárez-Maldonado, A. (2018). Efecto de los ácidos fenólicos en plantas de tomate (Lycopersicon esculentum Mill.) inoculadas con Clavibacter michiganensis. Revista Mexicana de Ciencias Agrícolas, Esp.(20), 4367–4379. https://doi.org/10.29312/remexca.v0i20.1005
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
1. Proposed policy for open access journals
Authors who publish in this journal accept the following conditions:
a. Authors retain the copyright and assign to the journal the right to the first publication, with the work registered under the attribution, non-commercial and no-derivative license from Creative Commons, which allows third parties to use what has been published as long as they mention the authorship of the work and upon first publication in this journal, the work may not be used for commercial purposes and the publications may not be used to remix, transform or create another work.
b. Authors may enter into additional independent contractual arrangements for the non-exclusive distribution of the version of the article published in this journal (e.g., including it in an institutional repository or publishing it in a book) provided that they clearly indicate that the work was first published in this journal.
c. Authors are permitted and encouraged to publish their work on the Internet (e.g. on institutional or personal pages) before and during the review and publication process, as it may lead to productive exchanges and faster and wider dissemination of published work (see The Effect of Open Access).
