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      Endoplasmic reticulum–localized UBC34 interaction with lignin repressors MYB221 and MYB156 regulates the transactivity of the transcription factors in Populus tomentosa

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          Abstract

          Background

          Regulation of lignin biosynthesis is known to occur at the level of transcription factors (TFs), of which R2R3-MYB family members have been proposed to play a central role via the AC cis-elements. Despite the important roles of TFs in lignin biosynthesis, the post-translational regulation of these TFs, particularly their ubiquitination regulation, has not been thoroughly explored.

          Results

          We describe the discovery of a Populus tomentosa E2 ubiquitin-conjugating enzyme 34 (PtoUBC34), which is involved in the post-translational regulation of transactivation activity of lignin-associated transcriptional repressors PtoMYB221 and PtoMYB156. PtoUBC34 is localized at the endoplasmic reticulum (ER) membrane where it interacts with transcriptional repressors PtoMYB221 and PtoMYB156. This specific interaction allows for the translocation of TFs PtoMYB221 and PtoMYB156 to the ER and reduces their repression activity in a PtoUBC34 abundance-dependent manner. By taking a molecular biology approach with quantitative real-time polymerase chain reaction (qRT-PCR) analysis, we found that PtoUBC34 is expressed in all aboveground tissues of trees in P. tomentosa, and in particular, it is ubiquitous in all distinct differentiation stages across wood formation, including phloem differentiation, cambium maintaining, early and developing xylem differentiation, secondary cell wall thickening, and programmed cell death. Additionally, we discovered that PtoUBC34 is induced by treatment with sodium chloride and heat shock.

          Conclusions

          Our data suggest a possible mechanism by which lignin biosynthesis is regulated by ER-localized PtoUBC34 in poplar, probably through the ER-associated degradation (ERAD) of lignin-associated repressors PtoMYB221 and PtoMYB156.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-019-1697-y) contains supplementary material, which is available to authorized users.

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          Most cited references69

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          The ubiquitin-26S proteasome system at the nexus of plant biology.

          Plants, like other eukaryotes, rely on proteolysis to control the abundance of key regulatory proteins and enzymes. Strikingly, genome-wide studies have revealed that the ubiquitin-26S proteasome system (UPS) in particular is an exceedingly large and complex route for protein removal, occupying nearly 6% of the Arabidopsis thaliana proteome. But why is the UPS so pervasive in plants? Data accumulated over the past few years now show that it targets numerous intracellular regulators that have central roles in hormone signalling, the regulation of chromatin structure and transcription, tailoring morphogenesis, responses to environmental challenges, self recognition and battling pathogens.
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            A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis.

            SECONDARY WALL-ASSOCIATED NAC DOMAIN PROTEIN1 (SND1) is a master transcriptional switch activating the developmental program of secondary wall biosynthesis. Here, we demonstrate that a battery of SND1-regulated transcription factors is required for normal secondary wall biosynthesis in Arabidopsis thaliana. The expression of 11 SND1-regulated transcription factors, namely, SND2, SND3, MYB103, MYB85, MYB52, MYB54, MYB69, MYB42, MYB43, MYB20, and KNAT7 (a Knotted1-like homeodomain protein), was developmentally associated with cells undergoing secondary wall thickening. Of these, dominant repression of SND2, SND3, MYB103, MYB85, MYB52, MYB54, and KNAT7 significantly reduced secondary wall thickening in fiber cells. Overexpression of SND2, SND3, and MYB103 increased secondary wall thickening in fibers, and overexpression of MYB85 led to ectopic deposition of lignin in epidermal and cortical cells in stems. Furthermore, SND2, SND3, MYB103, MYB85, MYB52, and MYB54 were able to induce secondary wall biosynthetic genes. Direct target analysis using the estrogen-inducible system revealed that MYB46, SND3, MYB103, and KNAT7 were direct targets of SND1 and also of its close homologs, NST1, NST2, and vessel-specific VND6 and VND7. Together, these results demonstrate that a transcriptional network consisting of SND1 and its downstream targets is involved in regulating secondary wall biosynthesis in fibers and that NST1, NST2, VND6, and VND7 are functional homologs of SND1 that regulate the same downstream targets in different cell types.
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              The ubiquitin 26S proteasome proteolytic pathway.

              Much of plant physiology, growth, and development is controlled by the selective removal of short-lived regulatory proteins. One important proteolytic pathway involves the small protein ubiquitin (Ub) and the 26S proteasome, a 2-MDa protease complex. In this pathway, Ub is attached to proteins destined for degradation; the resulting Ub-protein conjugates are then recognized and catabolized by the 26S proteasome. This review describes our current understanding of the pathway in plants at the biochemical, genomic, and genetic levels, using Arabidopsis thaliana as the model. Collectively, these analyses show that the Ub/26S proteasome pathway is one of the most elaborate regulatory mechanisms in plants. The genome of Arabidopsis encodes more than 1400 (or >5% of the proteome) pathway components that can be connected to almost all aspects of its biology. Most pathway components participate in the Ub-ligation reactions that choose with exquisite specificity which proteins should be ubiquitinated. What remains to be determined is the identity of the targets, which may number in the thousands in plants.
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                Author and article information

                Contributors
                yqin1986@foxmail.com
                cyjnn@126.com
                572444385@qq.com
                1335159897@qq.com
                dingluo2011@126.com
                +86 10 51503833 , weijianhua@baafs.net.cn
                +86 10 51503833 , wanghongzhi@baafs.net.cn
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                12 March 2019
                12 March 2019
                2019
                : 19
                : 97
                Affiliations
                [1 ]ISNI 0000 0004 0646 9053, GRID grid.418260.9, Beijing Agro-Biotechnology Research Center, , Beijing Academy of Agricultural and Forestry Sciences, ; No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097 People’s Republic of China
                [2 ]ISNI 0000 0004 0646 9053, GRID grid.418260.9, Beijing Key Laboratory of Agricultural Genetic Resources and Biotechnology, , Beijing Academy of Agricultural and Forestry Sciences, ; No. 9, Shuguang Huayuan Middle Road, Haidian District, Beijing, 100097 People’s Republic of China
                Author information
                http://orcid.org/0000-0001-9052-9319
                Article
                1697
                10.1186/s12870-019-1697-y
                6416899
                30866808
                99b9dd87-d781-480a-8024-21e51ca9744d
                © 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
                : 9 October 2018
                : 27 February 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31770708
                Award ID: 31270593
                Award Recipient :
                Funded by: National Key R&D Program of China
                Award ID: 2016YFD0600104
                Award Recipient :
                Funded by: Science Foundation of the Beijing Academy of Agriculture and Forestry Sciences
                Award ID: KJCX20170203
                Award Recipient :
                Funded by: National Key Program on Transgenic Research of China
                Award ID: 2018ZX0802002
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                lignin biosynthesis,ptoubc34,transcriptional repressor,ptomyb221,ptomyb156,er-associated degradation

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