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      Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [ Cynodon dactylon (L). Pers.] by exogenous melatonin

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          Summary

          Exogenous melatonin application confers abiotic stress resistance in bermudagrass through modulation of antioxidants and metabolic homeostasis, and extensive transcriptional reprogramming such as the reorientation of photorespiratory, carbohydrate, and nitrogen metabolism.

          Abstract

          Melatonin ( N-acetyl-5-methoxytryptamine), a well-known animal hormone, is also involved in plant development and abiotic stress responses. In this study, it is shown that exogenous application of melatonin conferred improved salt, drought, and cold stress resistances in bermudagrass. Moreover, exogenous melatonin treatment alleviated reactive oxygen species (ROS) burst and cell damage induced by abiotic stress; this involved activation of several antioxidants. Additionally, melatonin-pre-treated plants exhibited higher concentrations of 54 metabolites, including amino acids, organic acids, sugars, and sugar alcohols, than non-treated plants under abiotic stress conditions. Genome-wide transcriptomic profiling identified 3933 transcripts (2361 up-regulated and 1572 down-regulated) that were differentially expressed in melatonin-treated plants versus controls. Pathway and gene ontology (GO) term enrichment analyses revealed that genes involved in nitrogen metabolism, major carbohydrate metabolism, tricarboxylic acid (TCA)/org transformation, transport, hormone metabolism, metal handling, redox, and secondary metabolism were over-represented after melatonin pre-treatment. Taken together, this study provides the first evidence of the protective roles of exogenous melatonin in the bermudagrass response to abiotic stresses, partially via activation of antioxidants and modulation of metabolic homeostasis. Notably, metabolic and transcriptomic analyses showed that the underlying mechanisms of melatonin could involve major reorientation of photorespiratory and carbohydrate and nitrogen metabolism.

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          Most cited references73

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          Melatonin as a natural ally against oxidative stress: a physicochemical examination.

          Oxidative stress has been proven to be related to the onset of a large number of health disorders. This chemical stress is triggered by an excess of free radicals, which are generated in cells because of a wide variety of exogenous and endogenous processes. Therefore, finding strategies for efficiently detoxifying free radicals has become a subject of a great interest, from both an academic and practical points of view. Melatonin is a ubiquitous and versatile molecule that exhibits most of the desirable characteristics of a good antioxidant. The amount of data gathered so far regarding the protective action of melatonin against oxidative stress is overwhelming. However, rather little is known concerning the chemical mechanisms involved in this activity. This review summarizes the current progress in understanding the physicochemical insights related to the free radical-scavenging activity of melatonin. Thus far, there is a general agreement that electron transfer and hydrogen transfer are the main mechanisms involved in the reactions of melatonin with free radicals. However, the relative importance of other mechanisms is also analyzed. The chemical nature of the reacting free radical also has an influence on the relative importance of the different mechanisms of these reactions. Therefore, this point has also been discussed in detail in the current review. Based on the available data, it is concluded that melatonin efficiently protects against oxidative stress by a variety of mechanisms. Moreover, it is proposed that even though it has been referred to as the chemical expression of darkness, perhaps it could also be referred to as the chemical light of health. © 2011 John Wiley & Sons A/S.
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            Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates.

            Twenty-four edible plants were investigated for the presence of melatonin, heretofore considered to be a molecule found only in the animal kingdom. The amount of melatonin in different plants varied greatly with highest melatonin being present in plants of the rice family. Melatonin was identified by radioimmunoassay and verified by high performance liquid chromatography with fluorescence detection. Feeding a diet containing plant products rich in melatonin to chicks increased radioimmunoassayable levels of melatonin in their blood. Likewise, melatonin extracted from plants inhibited binding of [125I]iodomelatonin to rabbit brain. Thus, melatonin ingested in foodstuffs enters the blood and is capable of binding to melatonin binding sites in the brain of mammals.
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              Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.).

              A comprehensive investigation was carried out to determine the changes that occurred in water-stressed cucumber (Cucumis sativus L.) in response to melatonin treatment. We examined the potential roles of melatonin during seed germination and root generation and measured its effect on reactive oxygen species (ROS) levels, antioxidant enzyme activities, and photosynthesis. Melatonin alleviated polyethylene glycol induced inhibition of seed germination, with 100 μm melatonin-treated seeds showing the greatest germination rate. Melatonin stimulated root generation and vitality and increased the root:shoot ratio; therefore, melatonin may have an effect on strengthening cucumber roots. Melatonin treatment significantly reduced chlorophyll degradation. Seedlings treated with 100 μm melatonin clearly showed a higher photosynthetic rate, thus reversing the effect of water stress. Furthermore, the ultrastructure of chloroplasts in water-stressed cucumber leaves was maintained after melatonin treatment. The antioxidant levels and activities of the ROS scavenging enzymes, i.e., superoxide dismutase, peroxidase, and catalase, were also increased by melatonin. These results suggest that the adverse effects of water stress can be minimized by the application of melatonin. © 2012 John Wiley & Sons A/S.
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                Author and article information

                Journal
                J Exp Bot
                J. Exp. Bot
                jexbot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                February 2015
                15 September 2014
                15 September 2014
                : 66
                : 3
                : 681-694
                Affiliations
                1Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences , Wuhan, 430074, China
                2Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences , Shanghai, 201602, China
                3University of Chinese Academy of Sciences , Beijing, 100039, China
                4Department of Cellular and Structural Biology, The University of Texas Health Science Center , San Antonio, TX, USA
                Author notes
                * These authors contributed equally to this work.
                To whom correspondence should be addressed. E-mail: zhulongch@ 123456wbgcas.cn or ryliu@ 123456sibs.ac.cn or hengzhang@ 123456gmail.com
                Article
                10.1093/jxb/eru373
                4321537
                25225478
                9bcc6767-d6e7-40f8-81a0-ca20db422377
                © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Pages: 14
                Categories
                Research Paper

                Plant science & Botany
                abiotic stress,antioxidant,bermudagrass,melatonin,metabolites,reactive oxygen species,transcriptomic.

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