Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism

The activity of bHLH transcription factor MYC2, a key regulator in jasmonate signaling and plant specialized metabolism, is sensitive to repression by JASMONATE-ZIM-domain (JAZ) proteins and co-activation by the mediator subunit MED25. The substitution of a conserved aspartic acid (D) to asparagine...

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Main Authors: Hou, Xin, Singh, Sanjay Kumar, Werkman, Joshua R., Liu, Yongliang, Yuan, Qinghua, Wu, Xia, Patra, Barunava, Sui, Xueyi, Lyu, Ruiqing, Wang, Bingwu, Liu, Xiaoyu, Li, Yongqing, Ma, Wei, Pattanaik, Sitakanta, Yuan, Ling
Other Authors: School of Biological Sciences
Format: Journal Article
Language:English
Published: 2023
Subjects:
Online Access:https://hdl.handle.net/10356/170131
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author Hou, Xin
Singh, Sanjay Kumar
Werkman, Joshua R.
Liu, Yongliang
Yuan, Qinghua
Wu, Xia
Patra, Barunava
Sui, Xueyi
Lyu, Ruiqing
Wang, Bingwu
Liu, Xiaoyu
Li, Yongqing
Ma, Wei
Pattanaik, Sitakanta
Yuan, Ling
author2 School of Biological Sciences
author_facet School of Biological Sciences
Hou, Xin
Singh, Sanjay Kumar
Werkman, Joshua R.
Liu, Yongliang
Yuan, Qinghua
Wu, Xia
Patra, Barunava
Sui, Xueyi
Lyu, Ruiqing
Wang, Bingwu
Liu, Xiaoyu
Li, Yongqing
Ma, Wei
Pattanaik, Sitakanta
Yuan, Ling
author_sort Hou, Xin
collection NTU
description The activity of bHLH transcription factor MYC2, a key regulator in jasmonate signaling and plant specialized metabolism, is sensitive to repression by JASMONATE-ZIM-domain (JAZ) proteins and co-activation by the mediator subunit MED25. The substitution of a conserved aspartic acid (D) to asparagine (N) in the JAZ-interacting domain (JID) of Arabidopsis MYC2 affects interaction with JAZ, although the mechanism remained unclear. The effects of the conserved residue MYC2D128 on interaction with MED25 have not been investigated. Using tobacco as a model, we generated all possible substitutions of aspartic acid 128 (D128) in NtMYC2a. NtMYC2aD128N partially desensitized the repression by JAZ proteins, while strongly interacting with MED25, resulting in increased expression of nicotine pathway genes and nicotine accumulation in tobacco hairy roots overexpressing NtMYC2aD128N compared to those overexpressing NtMYC2a. The proline substitution, NtMYC2aD128P, negatively affected transactivation and abolished the interaction with JAZ proteins and MED25. Structural modeling and simulation suggest that the overall stability of the JID binding pocket is a predominant cause for the observed effects of substitutions at D128. The D128N substitution has an overall stabilizing effect on the binding pocket, which is destabilized by D128P. Our study offers an innovative tool to increase the production of plant natural products.
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spelling ntu-10356/1701312023-09-04T15:32:05Z Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism Hou, Xin Singh, Sanjay Kumar Werkman, Joshua R. Liu, Yongliang Yuan, Qinghua Wu, Xia Patra, Barunava Sui, Xueyi Lyu, Ruiqing Wang, Bingwu Liu, Xiaoyu Li, Yongqing Ma, Wei Pattanaik, Sitakanta Yuan, Ling School of Biological Sciences Science::Biological sciences Transcriptional Regulation Protein-Protein Interaction The activity of bHLH transcription factor MYC2, a key regulator in jasmonate signaling and plant specialized metabolism, is sensitive to repression by JASMONATE-ZIM-domain (JAZ) proteins and co-activation by the mediator subunit MED25. The substitution of a conserved aspartic acid (D) to asparagine (N) in the JAZ-interacting domain (JID) of Arabidopsis MYC2 affects interaction with JAZ, although the mechanism remained unclear. The effects of the conserved residue MYC2D128 on interaction with MED25 have not been investigated. Using tobacco as a model, we generated all possible substitutions of aspartic acid 128 (D128) in NtMYC2a. NtMYC2aD128N partially desensitized the repression by JAZ proteins, while strongly interacting with MED25, resulting in increased expression of nicotine pathway genes and nicotine accumulation in tobacco hairy roots overexpressing NtMYC2aD128N compared to those overexpressing NtMYC2a. The proline substitution, NtMYC2aD128P, negatively affected transactivation and abolished the interaction with JAZ proteins and MED25. Structural modeling and simulation suggest that the overall stability of the JID binding pocket is a predominant cause for the observed effects of substitutions at D128. The D128N substitution has an overall stabilizing effect on the binding pocket, which is destabilized by D128P. Our study offers an innovative tool to increase the production of plant natural products. Published version This work is supported partially by the Harold R. Burton Endowed Professorship to L.Y., and by the grants 2018530000241001 and 2022530000241012 from the Yunnan Tobacco Company, the National Key Research and Development Program of China (2019YFC1711100), the Kentucky Tobacco Research and Development Center (KTRDC), The Shandong Province Modern Agricultural Technology System (SDAIT-25- 02), The China Tobacco Shandong Industrial Corporation Major Project (202102004), The Shandong Tobacco Company Science and Technology Project (KN294, KN291, KN293, KN287), The Shandong Weifang Tobacco Company Science and Technology Project (2021-57), and The Shandong Rizhao Tobacco Company Science and Technology Project (2022-003). 2023-08-30T04:21:28Z 2023-08-30T04:21:28Z 2023 Journal Article Hou, X., Singh, S. K., Werkman, J. R., Liu, Y., Yuan, Q., Wu, X., Patra, B., Sui, X., Lyu, R., Wang, B., Liu, X., Li, Y., Ma, W., Pattanaik, S. & Yuan, L. (2023). Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism. International Journal of Biological Macromolecules, 252, 126472-. https://dx.doi.org/10.1016/j.ijbiomac.2023.126472 0141-8130 https://hdl.handle.net/10356/170131 10.1016/j.ijbiomac.2023.126472 37625752 252 126472 en International Journal of Biological Macromolecules © 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). application/pdf
spellingShingle Science::Biological sciences
Transcriptional Regulation
Protein-Protein Interaction
Hou, Xin
Singh, Sanjay Kumar
Werkman, Joshua R.
Liu, Yongliang
Yuan, Qinghua
Wu, Xia
Patra, Barunava
Sui, Xueyi
Lyu, Ruiqing
Wang, Bingwu
Liu, Xiaoyu
Li, Yongqing
Ma, Wei
Pattanaik, Sitakanta
Yuan, Ling
Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
title Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
title_full Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
title_fullStr Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
title_full_unstemmed Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
title_short Partial desensitization of MYC2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
title_sort partial desensitization of myc2 transcription factor alters the interaction with jasmonate signaling components and affects specialized metabolism
topic Science::Biological sciences
Transcriptional Regulation
Protein-Protein Interaction
url https://hdl.handle.net/10356/170131
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