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      Transcriptome analysis provides new insights into the transcriptional regulation of methyl jasmonate-induced flavonoid biosynthesis in pear calli

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          Abstract

          Background

          Flavonoid biosynthesis is strongly influenced by phytohormones. For example, methyl jasmonate (MeJA) enhances the flavonoid accumulation in pear. However, the molecular mechanism underlying the MeJA-induced flavonoid biosynthesis in pear is largely uncharacterized. Therefore, the transcriptome of pear calli treated with MeJA was analyzed to elucidate the mechanism regulating MeJA-mediated flavonoid biosynthesis.

          Results

          The application of exogenous MeJA significantly enhanced flavonoid accumulation, especially anthocyanin, in pear calli. A weighted gene co-expression network analysis identified the differentially expressed genes associated with MeJA-induced flavonoid biosynthesis. The MeJA treatment upregulated the expression of the flavonoid biosynthesis pathway structural genes ( PcCHS, PcCHI, PcF3H, PcDFR, PcANS, PcANR2a, and PcLAR1). The MYB family members were the main transcription factors regulating the MeJA-induced flavonoid biosynthesis, but the bHLH, AP2-EREBP, NAC, WRKY, and TIFY families were also involved. In addition to PcMYB10, which is a known positive regulator of anthocyanin biosynthesis in pear, several novel MYB candidates that may regulate flavonol and proanthocyanidin biosynthesis were revealed. Yeast two-hybrid and bimolecular fluorescence complementation assays demonstrated that PcMYB10 and PcMYC2 can directly interact with each other and bind to JAZ repressors (PcJAZ1 and PcJAZ2).

          Conclusions

          The PcMYB10–PcMYC2 molecular complex is likely involved in the regulation of jasmonate-mediated flavonoid biosynthesis at the transcript level. The data generated in this study may clarify the transcriptional regulatory network associated with the MeJA-induced flavonoid accumulation in pear calli and provide a solid foundation for future studies.

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          Most cited references38

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          JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.

          Jasmonate and related signalling compounds have a crucial role in both host immunity and development in plants, but the molecular details of the signalling mechanism are poorly understood. Here we identify members of the jasmonate ZIM-domain (JAZ) protein family as key regulators of jasmonate signalling. JAZ1 protein acts to repress transcription of jasmonate-responsive genes. Jasmonate treatment causes JAZ1 degradation and this degradation is dependent on activities of the SCF(COI1) ubiquitin ligase and the 26S proteasome. Furthermore, the jasmonoyl-isoleucine (JA-Ile) conjugate, but not other jasmonate-derivatives such as jasmonate, 12-oxo-phytodienoic acid, or methyl-jasmonate, promotes physical interaction between COI1 and JAZ1 proteins in the absence of other plant proteins. Our results suggest a model in which jasmonate ligands promote the binding of the SCF(COI1) ubiquitin ligase to and subsequent degradation of the JAZ1 repressor protein, and implicate the SCF(COI1)-JAZ1 protein complex as a site of perception of the plant hormone JA-Ile.
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            The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses.

            Jasmonates (JAs) trigger an important transcriptional reprogramming of plant cells to modulate both basal development and stress responses. In spite of the importance of transcriptional regulation, only one transcription factor (TF), the Arabidopsis thaliana basic helix-loop-helix MYC2, has been described so far as a direct target of JAZ repressors. By means of yeast two-hybrid screening and tandem affinity purification strategies, we identified two previously unknown targets of JAZ repressors, the TFs MYC3 and MYC4, phylogenetically closely related to MYC2. We show that MYC3 and MYC4 interact in vitro and in vivo with JAZ repressors and also form homo- and heterodimers with MYC2 and among themselves. They both are nuclear proteins that bind DNA with sequence specificity similar to that of MYC2. Loss-of-function mutations in any of these two TFs impair full responsiveness to JA and enhance the JA insensitivity of myc2 mutants. Moreover, the triple mutant myc2 myc3 myc4 is as impaired as coi1-1 in the activation of several, but not all, JA-mediated responses such as the defense against bacterial pathogens and insect herbivory. Our results show that MYC3 and MYC4 are activators of JA-regulated programs that act additively with MYC2 to regulate specifically different subsets of the JA-dependent transcriptional response.
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              COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.

              The coi1 mutation defines an Arabidopsis gene required for response to jasmonates, which regulate defense against insects and pathogens, wound healing, and pollen fertility. The wild-type allele, COI1, was mapped to a 90-kilobase genomic fragment and located by complementation of coi1-1 mutants. The predicted amino acid sequence of the COI1 protein contains 16 leucine-rich repeats and an F-box motif. It has similarity to the F-box proteins Arabidopsis TIR1, human Skp2, and yeast Grr1, which appear to function by targeting repressor proteins for removal by ubiquitination.
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                Author and article information

                Contributors
                apekshika@zju.edu.cn
                nijunbei@zju.edu.cn
                yuanyinxiao123@126.com
                songlingbai@zju.edu.cn
                ywteng@zju.edu.cn
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                25 August 2020
                25 August 2020
                2020
                : 20
                : 388
                Affiliations
                [1 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, College of Agriculture and Biotechnology, Zhejiang University, ; Hangzhou, 310058 Zhejiang Province China
                [2 ]The Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, the Ministry of Agriculture of China, Hangzhou, 310058 Zhejiang Province China
                [3 ]Zhejiang Provincial Key Laboratory of Integrative Biology of Horticultural Plants, Hangzhou, 310058 Zhejiang Province China
                [4 ]GRID grid.449910.1, ISNI 0000 0004 4677 4319, Department of Export Agriculture, , Uva Wellassa University, ; Badulla, 90000 Sri Lanka
                Author information
                http://orcid.org/0000-0001-8656-9035
                Article
                2606
                10.1186/s12870-020-02606-x
                7446162
                32842960
                d0f04bd8-c92e-40d8-a6cb-95c7a1e356a1
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 20 May 2020
                : 16 August 2020
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Plant science & Botany
                methyl jasmonate,flavonoid,transcriptome,wgcna,pcmyb10,pcmyc2
                Plant science & Botany
                methyl jasmonate, flavonoid, transcriptome, wgcna, pcmyb10, pcmyc2

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