Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling
Abstract
Jasmonates (JAs) are plant hormones with crucial roles in development and stress resilience. They activate MYC transcription factors by mediating the proteolysis of MYC inhibitors called JAZ proteins. In the absence of JA, JAZ proteins bind and inhibit MYC through the assembly of MYC–JAZ–Novel Interactor of JAZ (NINJA)–TPL repressor complexes. However, JAZ and NINJA are predicted to be largely intrinsically unstructured, which has precluded their experimental structure determination. Through a combination of biochemical, mutational, and biophysical analyses and AlphaFold-derived ColabFold modeling, we characterized JAZ–JAZ and JAZ–NINJA interactions and generated models with detailed, high-confidence domain interfaces. We demonstrate that JAZ, NINJA, and MYC interface domains are dynamic in isolation and become stabilized in a stepwise order upon complex assembly. By contrast, most JAZ and NINJA regions outside of the interfaces remain highly dynamic and cannot be modeled in a single conformation. Our data indicate that the small JAZ Zinc finger expressed in Inflorescence Meristem (ZIM) motif mediates JAZ–JAZ and JAZ–NINJA interactions through separate surfaces, and our data further suggest that NINJA modulates JAZ dimerization. This study advances our understanding of JA signaling by providing insights into the dynamics, interactions, and structure of the JAZ–NINJA core of the JA repressor complex.
- Authors:
-
- Van Andel Institute, Grand Rapids, MI (United States)
- Nanjing Agricultural University (China)
- Michigan State University, East Lansing, MI (United States)
- UF Scripps Biomedical Research, Jupiter, FL (United States)
- Van Andel Institute, Grand Rapids, MI (United States); Nanjing Agricultural University (China); Jiangsu Province and Chinese Academy of Sciences, Nanjing (China)
- Michigan State University, East Lansing, MI (United States); University of Tsukuba (Japan)
- Van Andel Institute, Grand Rapids, MI (United States); Nanjing Agricultural University (China)
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
- OSTI Identifier:
- 2229523
- Grant/Contract Number:
- FG02-91ER20021
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant Communications
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 6; Journal ID: ISSN 2590-3462
- Publisher:
- Cell Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; JAZ protein; NINJA; AlphaFold; ColabFold; MYC; hydrogen-deuterium exchange
Citation Formats
Zhou, X. Edward, Zhang, Yaguang, Yao, Jian, Zheng, Jie, Zhou, Yuxin, He, Qing, Moreno, Javier, Lam, Vinh Q., Cao, Xiaoman, Sugimoto, Koichi, Vanegas-Cano, Leidy, Kariapper, Leena, Suino-Powell, Kelly, Zhu, Yuanye, Novick, Scott, Griffin, Patrick R., Zhang, Feng, Howe, Gregg A., and Melcher, Karsten. Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling. United States: N. p., 2023.
Web. doi:10.1016/j.xplc.2023.100639.
Zhou, X. Edward, Zhang, Yaguang, Yao, Jian, Zheng, Jie, Zhou, Yuxin, He, Qing, Moreno, Javier, Lam, Vinh Q., Cao, Xiaoman, Sugimoto, Koichi, Vanegas-Cano, Leidy, Kariapper, Leena, Suino-Powell, Kelly, Zhu, Yuanye, Novick, Scott, Griffin, Patrick R., Zhang, Feng, Howe, Gregg A., & Melcher, Karsten. Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling. United States. https://doi.org/10.1016/j.xplc.2023.100639
Zhou, X. Edward, Zhang, Yaguang, Yao, Jian, Zheng, Jie, Zhou, Yuxin, He, Qing, Moreno, Javier, Lam, Vinh Q., Cao, Xiaoman, Sugimoto, Koichi, Vanegas-Cano, Leidy, Kariapper, Leena, Suino-Powell, Kelly, Zhu, Yuanye, Novick, Scott, Griffin, Patrick R., Zhang, Feng, Howe, Gregg A., and Melcher, Karsten. Wed .
"Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling". United States. https://doi.org/10.1016/j.xplc.2023.100639. https://www.osti.gov/servlets/purl/2229523.
@article{osti_2229523,
title = {Assembly of JAZ–JAZ and JAZ–NINJA complexes in jasmonate signaling},
author = {Zhou, X. Edward and Zhang, Yaguang and Yao, Jian and Zheng, Jie and Zhou, Yuxin and He, Qing and Moreno, Javier and Lam, Vinh Q. and Cao, Xiaoman and Sugimoto, Koichi and Vanegas-Cano, Leidy and Kariapper, Leena and Suino-Powell, Kelly and Zhu, Yuanye and Novick, Scott and Griffin, Patrick R. and Zhang, Feng and Howe, Gregg A. and Melcher, Karsten},
abstractNote = {Jasmonates (JAs) are plant hormones with crucial roles in development and stress resilience. They activate MYC transcription factors by mediating the proteolysis of MYC inhibitors called JAZ proteins. In the absence of JA, JAZ proteins bind and inhibit MYC through the assembly of MYC–JAZ–Novel Interactor of JAZ (NINJA)–TPL repressor complexes. However, JAZ and NINJA are predicted to be largely intrinsically unstructured, which has precluded their experimental structure determination. Through a combination of biochemical, mutational, and biophysical analyses and AlphaFold-derived ColabFold modeling, we characterized JAZ–JAZ and JAZ–NINJA interactions and generated models with detailed, high-confidence domain interfaces. We demonstrate that JAZ, NINJA, and MYC interface domains are dynamic in isolation and become stabilized in a stepwise order upon complex assembly. By contrast, most JAZ and NINJA regions outside of the interfaces remain highly dynamic and cannot be modeled in a single conformation. Our data indicate that the small JAZ Zinc finger expressed in Inflorescence Meristem (ZIM) motif mediates JAZ–JAZ and JAZ–NINJA interactions through separate surfaces, and our data further suggest that NINJA modulates JAZ dimerization. This study advances our understanding of JA signaling by providing insights into the dynamics, interactions, and structure of the JAZ–NINJA core of the JA repressor complex.},
doi = {10.1016/j.xplc.2023.100639},
journal = {Plant Communications},
number = 6,
volume = 4,
place = {United States},
year = {Wed Jun 14 00:00:00 EDT 2023},
month = {Wed Jun 14 00:00:00 EDT 2023}
}
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