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Title: Structural insights into alternative splicing-mediated desensitization of jasmonate signaling

Jasmonate ZIM-domain (JAZ) transcriptional repressors play a key role in regulating jasmonate (JA) signaling in plants. Below a threshold concentration of jasmonoyl isoleucine (JA-Ile), the active form of JA, the C-terminal Jas motif of JAZ proteins binds MYC transcription factors to repress JA signaling. With increasing JA-Ile concentration, the Jas motif binds to JA-Ile and the COI1 subunit of the SCF COI1 E3 ligase, which mediates ubiquitination and proteasomal degradation of JAZ repressors, resulting in derepression of MYC transcription factors. JA signaling subsequently becomes desensitized, in part by feedback induction of JAZ splice variants that lack the C-terminal Jas motif but include an N-terminal cryptic MYC-interaction domain (CMID). The CMID sequence is dissimilar to the Jas motif and is incapable of recruiting SCF COI1, allowing CMID-containing JAZ splice variants to accumulate in the presence of JA and to re-repress MYC transcription factors as an integral part of reestablishing signal homeostasis. The mechanism by which the CMID represses MYC transcription factors remains elusive. Here we describe the crystal structure of the MYC3–CMID JAZ10 complex. In contrast to the Jas motif, which forms a single continuous helix when bound to MYC3, the CMID adopts a loop–helix–loop–helix architecture with modular interactions with bothmore » the Jas-binding groove and the backside of the Jas-interaction domain of MYC3. In conclusion, this clamp-like interaction allows the CMID to bind MYC3 tightly and block access of MED25 (a subunit of the Mediator coactivator complex) to the MYC3 transcriptional activation domain, shedding light on the enigmatic mechanism by which JAZ splice variants desensitize JA signaling.« less
Authors:
 [1] ;  [2] ;  [3] ;  [4] ;  [4] ;  [5] ;  [6] ;  [7] ;  [8] ; ORCiD logo [9]
  1. Nanjing Agricultural Univ., Nanjing (China). College of Plant Protection; Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab.; Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Sciences; Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry; Wuhan Univ. (China). College of Life Sciences, State Key Lab. of Hybrid Rice
  2. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Sciences; Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry
  3. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology
  4. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab.
  5. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology; Michigan State Univ., East Lansing, MI (United States). Plant Resilience Inst.
  6. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Sciences; Chinese Academy of Sciences (CAS), Shanghai (China). Key Lab. of Receptor Research, VARI-SIMM Center, Center for Structure and Function of Drug Targets, Shanghai Inst. of Materia Medica, Shanghai Inst. for Biological Sciences
  7. Nanjing Agricultural Univ., Nanjing (China). College of Plant Protection
  8. Michigan State Univ., East Lansing, MI (United States). Dept. of Energy Plant Research Lab.; Michigan State Univ., East Lansing, MI (United States). Dept. of Plant Biology; Michigan State Univ., East Lansing, MI (United States). Plant Resilience Inst.; Michigan State Univ., East Lansing, MI (United States). Howard Hughes Medical Inst.
  9. Van Andel Research Inst. (VARI), Grand Rapids, MI (United States). Lab. of Structural Biology and Biochemistry
Publication Date:
Grant/Contract Number:
AC02-06CH11357; FG02-91ER20021
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 7; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Michigan State Univ., East Lansing, MI (United States)
Sponsoring Org:
USDOE Office of Science (SC)
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; signaling; plant hormone; plant defense; plant pathogen; plant insect
OSTI Identifier:
1341769
Alternate Identifier(s):
OSTI ID: 1356423

Zhang, Feng, Ke, Jiyuan, Zhang, Li, Chen, Rongzhi, Sugimoto, Koichi, Howe, Gregg A., Xu, H. Eric, Zhou, Mingguo, He, Sheng Yang, and Melcher, Karsten. Structural insights into alternative splicing-mediated desensitization of jasmonate signaling. United States: N. p., Web. doi:10.1073/pnas.1616938114.
Zhang, Feng, Ke, Jiyuan, Zhang, Li, Chen, Rongzhi, Sugimoto, Koichi, Howe, Gregg A., Xu, H. Eric, Zhou, Mingguo, He, Sheng Yang, & Melcher, Karsten. Structural insights into alternative splicing-mediated desensitization of jasmonate signaling. United States. doi:10.1073/pnas.1616938114.
Zhang, Feng, Ke, Jiyuan, Zhang, Li, Chen, Rongzhi, Sugimoto, Koichi, Howe, Gregg A., Xu, H. Eric, Zhou, Mingguo, He, Sheng Yang, and Melcher, Karsten. 2017. "Structural insights into alternative splicing-mediated desensitization of jasmonate signaling". United States. doi:10.1073/pnas.1616938114.
@article{osti_1341769,
title = {Structural insights into alternative splicing-mediated desensitization of jasmonate signaling},
author = {Zhang, Feng and Ke, Jiyuan and Zhang, Li and Chen, Rongzhi and Sugimoto, Koichi and Howe, Gregg A. and Xu, H. Eric and Zhou, Mingguo and He, Sheng Yang and Melcher, Karsten},
abstractNote = {Jasmonate ZIM-domain (JAZ) transcriptional repressors play a key role in regulating jasmonate (JA) signaling in plants. Below a threshold concentration of jasmonoyl isoleucine (JA-Ile), the active form of JA, the C-terminal Jas motif of JAZ proteins binds MYC transcription factors to repress JA signaling. With increasing JA-Ile concentration, the Jas motif binds to JA-Ile and the COI1 subunit of the SCFCOI1 E3 ligase, which mediates ubiquitination and proteasomal degradation of JAZ repressors, resulting in derepression of MYC transcription factors. JA signaling subsequently becomes desensitized, in part by feedback induction of JAZ splice variants that lack the C-terminal Jas motif but include an N-terminal cryptic MYC-interaction domain (CMID). The CMID sequence is dissimilar to the Jas motif and is incapable of recruiting SCFCOI1, allowing CMID-containing JAZ splice variants to accumulate in the presence of JA and to re-repress MYC transcription factors as an integral part of reestablishing signal homeostasis. The mechanism by which the CMID represses MYC transcription factors remains elusive. Here we describe the crystal structure of the MYC3–CMIDJAZ10 complex. In contrast to the Jas motif, which forms a single continuous helix when bound to MYC3, the CMID adopts a loop–helix–loop–helix architecture with modular interactions with both the Jas-binding groove and the backside of the Jas-interaction domain of MYC3. In conclusion, this clamp-like interaction allows the CMID to bind MYC3 tightly and block access of MED25 (a subunit of the Mediator coactivator complex) to the MYC3 transcriptional activation domain, shedding light on the enigmatic mechanism by which JAZ splice variants desensitize JA signaling.},
doi = {10.1073/pnas.1616938114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 7,
volume = 114,
place = {United States},
year = {2017},
month = {1}
}

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