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      Comparative transcriptomic and metabolic analysis reveals the effect of melatonin on delaying anthracnose incidence upon postharvest banana fruit peel

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          Abstract

          Background

          Banana anthracnose, caused by Colletotrichum musae, is one of the most severe postharvest diseases in banana. Melatonin is widely known for its role in enhancing plant stress tolerance. However, little is known about the control of melatonin on anthracnose in postharvest banana fruit.

          Results

          In this study, exogenous melatonin treatment could significantly reduce the incidence of anthracnose in ripe yellow banana fruit and delay fruit senescence. However, melatonin treatment did not affect the growth of Colletotrichum musae in vitro. Transcriptomic analysis of banana peel showed that 339 genes were up-regulated and 241 were down-regulated in the peel after melatonin treatment, compared with the control. Based on GO terms and KEGG pathway, these up-regulated genes were mainly categorized into signal transduction, cell wall formation, secondary metabolism, volatile compounds synthesis and response to stress, which might be related to the anti-anthracnose of banana fruit induced by melatonin treatment. This view was also supported by the increase of volatile compounds, cell wall components and IAA content in the melatonin-treated fruit peel via the metabolomic analysis. After melatonin treatment, auxin, ethylene and mitogen-activated protein kinase (MAPK) signaling pathways were enhanced, which might be involved in the enhanced fruit resistance by regulating physiological characteristics, disease-resistant proteins and metabolites.

          Conclusions

          Our results provide a better understanding of the molecular processes in melatonin treatment delaying banana fruit senescence and anthracnose incidence.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-019-1855-2) contains supplementary material, which is available to authorized users.

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          Most cited references43

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          Functions of melatonin in plants: a review.

          The number of studies on melatonin in plants has increased significantly in recent years. This molecule, with a large set of functions in animals, has also shown great potential in plant physiology. This review outlines the main functions of melatonin in the physiology of higher plants. Its role as antistress agent against abiotic stressors, such as drought, salinity, low and high ambient temperatures, UV radiation and toxic chemicals, is analyzed. The latest data on their role in plant-pathogen interactions are also discussed. Both abiotic and biotic stresses produce a significant increase in endogenous melatonin levels, indicating its possible role as effector in these situations. The existence of endogenous circadian rhythms in melatonin levels has been demonstrated in some species, and the data, although limited, suggest a central role of this molecule in the day/night cycles in plants. Finally, another aspect that has led to a large volume of research is the involvement of melatonin in aspects of plant development regulation. Although its role as a plant hormone is still far of from being fully established, its involvement in processes such as growth, rhizogenesis, and photosynthesis seems evident. The multiple changes in gene expression caused by melatonin point to its role as a multiregulatory molecule capable of coordinating many aspects of plant development. This last aspect, together with its role as an alleviating-stressor agent, suggests that melatonin is an excellent prospect for crop improvement.
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            Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis.

            Plant sensing of invading pathogens triggers massive metabolic reprogramming, including the induction of secondary antimicrobial compounds known as phytoalexins. We recently reported that MPK3 and MPK6, two pathogen-responsive mitogen-activated protein kinases, play essential roles in the induction of camalexin, the major phytoalexin in Arabidopsis thaliana. In search of the transcription factors downstream of MPK3/MPK6, we found that WRKY33 is required for MPK3/MPK6-induced camalexin biosynthesis. In wrky33 mutants, both gain-of-function MPK3/MPK6- and pathogen-induced camalexin production are compromised, which is associated with the loss of camalexin biosynthetic gene activation. WRKY33 is a pathogen-inducible transcription factor, whose expression is regulated by the MPK3/MPK6 cascade. Chromatin immunoprecipitation assays reveal that WRKY33 binds to its own promoter in vivo, suggesting a potential positive feedback regulatory loop. Furthermore, WRKY33 is a substrate of MPK3/MPK6. Mutation of MPK3/MPK6 phosphorylation sites in WRKY33 compromises its ability to complement the camalexin induction in the wrky33 mutant. Using a phospho-protein mobility shift assay, we demonstrate that WRKY33 is phosphorylated by MPK3/MPK6 in vivo in response to Botrytis cinerea infection. Based on these data, we conclude that WRKY33 functions downstream of MPK3/MPK6 in reprogramming the expression of camalexin biosynthetic genes, which drives the metabolic flow to camalexin production in Arabidopsis challenged by pathogens.
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              Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry.

              Melatonin, the chief hormone of the pineal gland in vertebrates, is widely distributed in the animal kingdom. Among many functions, melatonin synchronizes circadian and circannual rhythms, stimulates immune function, may increase life span, inhibits growth of cancer cells in vitro and cancer progression and promotion in vivo, and was recently shown to be a potent hydroxyl radical scavenger and antioxidant. Hydroxyl radicals are highly toxic by-products of oxygen metabolism that damage cellular DNA and other macromolecules. Herein we report that melatonin, in varying concentrations, is also found in a variety of plants. Melatonin concentrations, measured in nine different plants by radioimmunoassay, ranged from 0 to 862 pg melatonin/mg protein. The presence of melatonin was verified by gas chromatography/mass spectrometry. Our findings suggest that the consumption of plant materials that contain high levels of melatonin could alter blood melatonin levels of the indole as well as provide protection of macromolecules against oxidative damage.
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                Author and article information

                Contributors
                taotaoli@scbg.ac.cn
                wuqixian@scbg.ac.cn
                zhuhong@mail.scbg.ac.cn
                zhouyijie123@scbg.ac.cn
                ymjiang@scbg.ac.cn
                huijun_gao@aliyun.com
                +86-2037083042 , yunze@scbg.ac.cn
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                1 July 2019
                1 July 2019
                2019
                : 19
                : 289
                Affiliations
                [1 ]ISNI 0000 0001 1014 7864, GRID grid.458495.1, Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, ; Guangzhou, China
                [2 ]ISNI 0000 0001 0561 6611, GRID grid.135769.f, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, ; Guangzhou, China
                Author information
                http://orcid.org/0000-0003-3966-7657
                Article
                1855
                10.1186/s12870-019-1855-2
                6604187
                31262259
                4d679a41-4cc6-4757-92f5-9b2af91d31f9
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 21 September 2018
                : 29 May 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100009334, Pearl River S and T Nova Program of Guangzhou;
                Award ID: 201610010041
                Award Recipient :
                Funded by: National Key R&D Program of China
                Award ID: 2018YFD1000205
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31671911
                Award Recipient :
                Funded by: Excellent Young Talents Fund Program of Higher Education Institutions of Anhui Province (CN)
                Award ID: 2017QNRC001
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                anthracnose,banana fruit,cell wall,melatonin; senescence,volatile compounds
                Plant science & Botany
                anthracnose, banana fruit, cell wall, melatonin; senescence, volatile compounds

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