Tolerance to Stress Combination in Tomato Plants: New Insights in the Protective Role of Melatonin
Abstract
:1. Introduction
2. Results
2.1. Melatonin Effect on Tomato Plant Growth
2.2. Melatonin Effect on Photosynthetic-Related Parameters
2.3. Melatonin Effect on Oxidative Stress
3. Discussion
3.1. Melatonin Promotes Growth under Abiotic Stress Combination by Improving Photosynthesis and the Protection of the Photosynthetic Machinery
3.2. Melatonin Protects Plants from Massive ROS Production under Abiotic Stress Combination by Reducing ROS Production and by Modulating the Expression of some Oxidative-Metabolism Related Genes
4. Materials and Methods
4.1. Plant Material and Growth Conditions
4.2. Melatonin and Melatonin-Derivatives Quantification
4.3. Leaf Gas Exchange and Chlorophyll Fluorescence Parameters
4.4. Photosynthetic Pigments Concentration
4.5. H2O2 Quantification
4.6. Lipid Peroxidation
4.7. Protein Oxidation
4.8. Antioxidant Capacity
4.9. Antioxidant Enzymes Quantification
4.10. RNA Extraction and qRT-PCR Experiments
4.11. Statistical Analysis
5. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Intergovernmental Panel on Climate Change (IPCC). Climate Change 2014: Impact Adaptation and Vulnerability; IPCC: Geneva, Switzerland, 2014; p. 151. [Google Scholar]
- Rizhsky, L.; Liang, H.; Shuman, J.; Shulaev, V.; Davletova, S.; Mittler, R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004, 134, 1683–1696. [Google Scholar] [CrossRef] [PubMed]
- Mittler, R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006, 11, 15–19. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, N.; Rivero, R.M.; Shulaev, V.; Blumwald, E.; Mittler, R. Abiotic and biotic stress combinations. New Phytol. 2014, 203, 32–43. [Google Scholar] [CrossRef] [PubMed]
- Rivero, R.M.; Mestre, T.C.; Mittler, R.; Rubio, F.; Garcia-Sanchez, F.; Martinez, V. The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants. Plant Cell Environ. 2014, 37, 1059–1073. [Google Scholar] [CrossRef] [PubMed]
- Martinez, V.; Mestre, T.C.; Rubio, F.; Girones-Vilaplana, A.; Moreno, D.A.; Mittler, R.; Rivero, R.M. Accumulation of flavonols over hydroxycinnamic acids favors oxidative damage protection under abiotic stress. Front. Plant Sci. 2016, 7, 838. [Google Scholar] [CrossRef] [PubMed]
- Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive oxygen species, abiotic stress and stress combination. Plant J. 2017, 90, 856–867. [Google Scholar] [CrossRef] [PubMed]
- Rasmussen, S.; Barah, P.; Suarez-Rodriguez, M.C.; Bressendorff, S.; Friis, P.; Costantino, P.; Bones, A.M.; Nielsen, H.B.; Mundy, J. Transcriptome responses to combinations of stresses in Arabidopsis thaliana. Plant Physiol. 2013, 161, 1783–1794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamaguchi, T.; Blumwald, E. Developing salt-tolerant crop plants: Challenges and opportunities. Trends Plant Sci. 2005, 10, 615–620. [Google Scholar] [CrossRef] [PubMed]
- Foyer, C.H.; Allen, J.F. Lessons from redox signaling in plants. Antioxid. Redox Signal. 2003, 5, 3–5. [Google Scholar] [CrossRef] [PubMed]
- Foyer, C.H.; Noctor, G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 2005, 17, 1866–1875. [Google Scholar] [CrossRef] [PubMed]
- Shi, H.; Jiang, C.; Ye, T.; Tan, D.-X.; Reiter, R.J.; Zhang, H.; Liu, R.; Chan, Z. Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in Bermudagrass [Cynodon dactylon (l). Pers.] by exogenous melatonin. J. Exp. Bot. 2015, 66, 681–694. [Google Scholar] [CrossRef] [PubMed]
- Prasad, T.K.; Anderson, M.D.; Martin, B.A.; Stewart, C.R. Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 1994, 6, 65–74. [Google Scholar] [CrossRef] [PubMed]
- Bose, J.; Rodrigo-Moreno, A.; Shabala, S. ROS homeostasis in halophytes in the context of salinity stress tolerance. J. Exp. Bot. 2014, 65, 1241–1257. [Google Scholar] [CrossRef] [PubMed]
- Arnao, M.B.; Hernandez-Ruiz, J. Melatonin: Plant growth regulator and/or biostimulator during stress? Trends Plant Sci. 2014, 19, 789–797. [Google Scholar] [CrossRef] [PubMed]
- Dubbels, R.; Reiter, R.J.; Klenke, E.; Goebel, A.; Schnakenberg, E.; Ehlers, C.; Schiwara, H.W.; Schloot, W. Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J. Pineal Res. 1995, 18, 28–31. [Google Scholar] [CrossRef] [PubMed]
- Zhang, N.; Sun, Q.; Zhang, H.; Cao, Y.; Weeda, S.; Ren, S.; Guo, Y.D. Roles of melatonin in abiotic stress resistance in plants. J. Exp. Bot. 2015, 66, 647–656. [Google Scholar] [CrossRef] [PubMed]
- Tan, D.X.; Hardeland, R.; Manchester, L.C.; Rosales-Corral, S.; Coto-Montes, A.; Boga, J.A.; Reiter, R.J. Emergence of naturally occurring melatonin isomers and their proposed nomenclature. J. Pineal Res. 2012, 53, 113–121. [Google Scholar] [CrossRef] [PubMed]
- Hattori, A.; Migitaka, H.; Iigo, M.; Itoh, M.; Yamamoto, K.; Ohtani-Kaneko, R.; Hara, M.; Suzuki, T.; Reiter, R.J. Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem. Mol. Biol. Int. 1995, 35, 627–634. [Google Scholar] [PubMed]
- Wei, W.; Li, Q.T.; Chu, Y.N.; Reiter, R.J.; Yu, X.M.; Zhu, D.H.; Zhang, W.K.; Ma, B.; Lin, Q.; Zhang, J.S.; et al. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J. Exp. Bot. 2015, 66, 695–707. [Google Scholar] [CrossRef] [PubMed]
- Tan, D.X.; Manchester, L.C.; Reiter, R.J.; Plummer, B.F.; Limson, J.; Weintraub, S.T.; Qi, W. Melatonin directly scavenges hydrogen peroxide: A potentially new metabolic pathway of melatonin biotransformation. Free Radic. Biol. Med. 2000, 29, 1177–1185. [Google Scholar] [CrossRef]
- Allegra, M.; Reiter, R.J.; Tan, D.X.; Gentile, C.; Tesoriere, L.; Livrea, M.A. The chemistry of melatonin’s interaction with reactive species. J. Pineal Res. 2003, 34, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Zhang, N.; Sun, Q.; Li, H.; Li, X.; Cao, Y.; Zhang, H.; Li, S.; Zhang, L.; Qi, Y.; Ren, S.; et al. Melatonin improved anthocyanin accumulation by regulating gene expressions and resulted in high reactive oxygen species scavenging capacity in cabbage. Front. Plant Sci. 2016, 7, 197. [Google Scholar] [CrossRef] [PubMed]
- Galano, A.; Tan, D.X.; Reiter, R.J. On the free radical scavenging activities of melatonin´s metabolites, AFMK and AMK. J. Pineal Res. 2013, 54, 254–257. [Google Scholar] [CrossRef] [PubMed]
- Tan, D.X.; Manchester, L.C.; Esteban-Zubero, E.; Zhou, Z.; Reiter, R.J. Melatonin as a potent and inducible endogenous antioxidant: Synthesis and metabolism. Molecules 2015, 20, 18886–18906. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.-J.; Zhang, N.; Yang, R.-C.; Wang, L.; Sun, Q.-Q.; Li, D.-B.; Cao, Y.-Y.; Weeda, S.; Zhao, B.; Ren, S.; et al. Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J. Pineal Res. 2014, 57, 269–279. [Google Scholar] [CrossRef] [PubMed]
- Arnao, M.B.; Hernández-Ruiz, J. Growth conditions determine different melatonin levels in Lupinus albus L. J. Pineal Res. 2013, 55, 149–155. [Google Scholar] [CrossRef] [PubMed]
- Riga, P.; Medina, S.; García-Flores, L.A.; Gil-Izquierdo, Á. Melatonin content of pepper and tomato fruits: Effects of cultivar and solar radiation. Food Chem. 2014, 156, 347–352. [Google Scholar] [CrossRef] [PubMed]
- Koyama, F.C.; Carvalho, T.L.G.; Alves, E.; da Silva, H.B.; de Azevedo, M.F.; Hemerly, A.S.; Garcia, C.R.S. The structurally related auxin and melatonin tryptophan-derivatives and their roles in Arabidopsis thaliana and in the human malaria parasite Plasmodium falciparum. J. Eukar. Microbiol. 2013, 60, 646–651. [Google Scholar] [CrossRef] [PubMed]
- Weeda, S.; Zhang, N.; Zhao, X.; Ndip, G.; Guo, Y.; Buck, G.A.; Fu, C.; Ren, S. Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS ONE 2014, 9, e93462. [Google Scholar] [CrossRef] [PubMed]
- Zhang, N.; Zhao, B.; Zhang, H.-J.; Weeda, S.; Yang, C.; Yang, Z.-C.; Ren, S.; Guo, Y.-D. Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J. Pineal Res. 2013, 54, 15–23. [Google Scholar] [CrossRef] [PubMed]
- Okazaki, M.; Ezura, H. Profiling of melatonin in the model tomato (Solanum lycopersicum L.) cultivar micro-tom. J. Pineal Res. 2009, 46, 338–343. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Chang, J.; Chen, H.; Wang, Z.; Gu, X.; Wei, C.; Zhang, Y.; Ma, J.; Yang, J.; Zhang, X. Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Front. Plant Sci. 2017, 8, 295. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.Y.; Liu, J.L.; Wang, W.X.; Sun, Y. Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 2016, 54, 19–27. [Google Scholar] [CrossRef]
- Dawood, M.G.; El-Awadi, M.E. Alleviation of salinity stress on Vicia faba L. plants via seed priming with melatonin. Acta Biol. Colomb. 2015, 20, 223–235. [Google Scholar] [CrossRef]
- Xu, X.D.; Sun, Y.; Guo, X.Q.; Sun, B.; Zhang, J. Effects of exogenous melatonin on ascorbate metabolism system in cucumber seedlings under high temperature stress. J. App. Ecol. 2010, 21, 2580–2586. [Google Scholar]
- Kocal, N.; Sonnewald, U.; Sonnewald, S. Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv Vesicatoria. Plant Physiol. 2008, 148, 1523–1536. [Google Scholar] [CrossRef] [PubMed]
- Tomaz, T.; Bagard, M.; Pracharoenwattana, I.; Linden, P.; Lee, C.; Lindén, P.; Carroll, A.; Ströher, E.; Smith, S.; Gardeström, P.; et al. Mitochondrial malate dehydrogenase lowers leaf respiration and alters photorespiration and plant growth in Arabidopsis. Plant Physiol. 2010, 154, 1143–1157. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Shi, Y.; Zhang, X.; Du, H.; Xu, B.; Huang, B. Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). Environ. Exp. Bot. 2017, 138, 36–45. [Google Scholar] [CrossRef]
- Chaves, M.M.; Flexas, J.; Pinheiro, C. Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Annals Bot. 2009, 103, 551–560. [Google Scholar] [CrossRef] [PubMed]
- Byeon, Y.; Back, K. Melatonin synthesis in rice seedlings in vivo is enhanced at high temperatures and under dark conditions due to increased serotonin N-acetyltransferase and N-acetylserotonin methyltransferase activities. J. Pineal Res. 2014, 56, 189–195. [Google Scholar] [CrossRef] [PubMed]
- Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop Plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef] [PubMed]
- Suzuki, N.; Mittler, R. Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiol. Plant. 2006, 126, 45–51. [Google Scholar] [CrossRef]
- Storozhenko, S.; De Pauw, P.; Van Montague, M.; Inze, D.; Kushnir, S. The heat-shock element is a functional component of the Arabidopsis APX1 gene promotor. Plant Physiol. 1998, 118, 1005–1014. [Google Scholar] [CrossRef] [PubMed]
- You, J.; Chan, Z. ROS regulation during abiotic stress responses in crop plants. Front. Plant Sci. 2015, 6, 1092. [Google Scholar]
- Srivastava, A.K.; Srivastava, S.; Lokhande, V.H.; D’Souza, S.F.; Suprasanna, P. Salt stress reveals differential antioxidant and energetics responses in glycophyte (Brassica juncea L.) and halophyte (Sesuvium portulacastrum L.). Front. Environ. Sci. 2015, 3, 19. [Google Scholar] [CrossRef]
- Mittler, R.; Blumwald, E. Genetic engineering for modern agriculture: Challenges and perspectives. Annu. Rev. Plant Biol. 2010, 61, 443–462. [Google Scholar] [CrossRef] [PubMed]
- Afreen, F.; Zobayed, S.M.; Kozai, T. Melatonin in Glycyrrhiza uralensis: Response of plant roots to spectral quality of light and UV-B radiation. J. Pineal Res. 2006, 41, 108–115. [Google Scholar] [CrossRef] [PubMed]
- Apel, K.; Hirt, H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004, 55, 373–399. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.L.; Xu, H.; Li, D.; Gao, X.; Li, T.L.; Wang, R. Effect of melatonin priming on photosynthetic capacity of tomato leaves under low-temperature stress. Photosynthetica 2018, 56, 1–9. [Google Scholar] [CrossRef]
- Giovannucci, E. Tomatoes, tomato-based products, lycopene, and cancer: Review of the epidemiologic literature. J. Natl. Cancer Inst. 1999, 91, 317–331. [Google Scholar] [CrossRef] [PubMed]
- Whatley, F.W.; Arnon, D.I. Photosynthesis phosphorylation in plants. Methods Enzymol. 1963, 6, 308–313. [Google Scholar]
- McNevin, W.M.; Uron, P.F. Separation of hydrogen peroxide from organic hydroperoxides. Anal Chem. 1953, 25, 1760–1761. [Google Scholar] [CrossRef]
- Brennan, T.; Frenkel, C. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol. 1977, 59, 411–416. [Google Scholar] [CrossRef] [PubMed]
- Rivero, R.M.; Kojima, M.; Gepstein, A.; Sakakibara, H.; Mittler, R.; Gepstein, S.; Blumwald, E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA 2007, 104, 19631–19636. [Google Scholar] [CrossRef] [PubMed]
- Fu, J.M.; Huang, B.R. Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Env. Exp. Bot. 2001, 45, 105–114. [Google Scholar] [CrossRef]
- Mestre, T.C.; Garcia-Sanchez, F.; Rubio, F.; Martinez, V.; Rivero, R.M. Glutathione homeostasis as an important and novel factor controlling blossom-end rot development in calcium-deficient tomato fruits. J. Plant Physiol. 2012, 169, 1719–1727. [Google Scholar] [CrossRef] [PubMed]
- Reznick, A.Z.; Packer, L. Oxidative damage to proteins: Spectrophotometric method for carbonyl assay. Oxygen Rad. Biol. Syst. 1994, 233, 357–363. [Google Scholar]
- Distefano, S.; Palma, J.M.; Gomez, M.; del Rio, L.A. Characterization of endoproteases from plant peroxisomes. Biochem. J. 1997, 327, 399–405. [Google Scholar] [CrossRef] [PubMed]
- Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Chance, B.; Maehly, A.C. Assay of catalases and peroxidases. Methods Enzymol. 1955, 2, 764–775. [Google Scholar]
- Aebi, H. Catalase in vitro. Methods Enzymol. 1984, 105, 121–126. [Google Scholar] [PubMed]
- McCord, J.M.; Fridovich, I. The utility of superoxide dismutase in studying free radical reactions: I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J. Biol. Chem. 1969, 244, 6056–6063. [Google Scholar] [PubMed]
- Spitz, D.R.; Oberley, L.W. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal. Biochem. 1989, 179, 8–18. [Google Scholar] [CrossRef]
- Miyake, C.; Asada, K. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol. 1992, 33, 541–553. [Google Scholar]
- Nakano, Y.; Asada, K. Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol. 1987, 28, 131–140. [Google Scholar]
- Halliwell, B.; Foyer, C.H. Ascorbic acid, metal ions and the superoxide radical. Biochem. J. 1976, 155, 697–700. [Google Scholar] [CrossRef] [PubMed]
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Martinez, V.; Nieves-Cordones, M.; Lopez-Delacalle, M.; Rodenas, R.; Mestre, T.C.; Garcia-Sanchez, F.; Rubio, F.; Nortes, P.A.; Mittler, R.; Rivero, R.M. Tolerance to Stress Combination in Tomato Plants: New Insights in the Protective Role of Melatonin. Molecules 2018, 23, 535. https://doi.org/10.3390/molecules23030535
Martinez V, Nieves-Cordones M, Lopez-Delacalle M, Rodenas R, Mestre TC, Garcia-Sanchez F, Rubio F, Nortes PA, Mittler R, Rivero RM. Tolerance to Stress Combination in Tomato Plants: New Insights in the Protective Role of Melatonin. Molecules. 2018; 23(3):535. https://doi.org/10.3390/molecules23030535
Chicago/Turabian StyleMartinez, Vicente, Manuel Nieves-Cordones, Maria Lopez-Delacalle, Reyes Rodenas, Teresa C. Mestre, Francisco Garcia-Sanchez, Francisco Rubio, Pedro A. Nortes, Ron Mittler, and Rosa M. Rivero. 2018. "Tolerance to Stress Combination in Tomato Plants: New Insights in the Protective Role of Melatonin" Molecules 23, no. 3: 535. https://doi.org/10.3390/molecules23030535