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Title: Defining a Two-pronged Structural Model for PB1 (Phox/Bem1p) Domain Interaction in Plant Auxin Responses

Abstract

Phox/Bem1p (PB1) domains are universal structural modules that use surfaces of different charge for protein-protein association. In plants, PB1-mediated interactions of auxin response factors (ARF) and auxin/indole 3-acetic acid inducible proteins regulate transcriptional events modulated by the phytohormone auxin. Here we investigate the thermodynamic and structural basis for Arabidopsis thaliana ARF7 PB1 domain self-interaction. Isothermal titration calorimetry and NMR experiments indicate that key residues on both the basic and acidic faces of the PB1 domain contribute to and organize coordinately to stabilize protein-protein interactions. Calorimetric analysis of ARF7PB1 site-directed mutants defines a two-pronged electrostatic interaction. Furthermore, the canonical PB1 interaction between a lysine and a cluster of acidic residues provides one prong with an arginine and a second cluster of acidic residues defining the other prong. Evolutionary conservation of this core recognition feature and other co-varying interface sequences allows for versatile PB1-mediated interactions in auxin signaling.

Authors:
 [1];  [2];  [3];  [3];  [1];  [1];  [4];  [4];  [2];  [1];  [1]
+ Show Author Affiliations
  1. Washington Univ., St. Louis, MO (United States)
  2. Washington Univ. School of Medicine, St. Louis, MO (United States)
  3. Univ. of Wisconsin, Madison, WI (United States)
  4. Iowa State Univ., Ames, IA (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institutes of Health (NIH); National Science Foundation (NSF); USDA, National Institute of Food and Agriculture (NIFA)
OSTI Identifier:
1351393
Grant/Contract Number:  
P41GM103399; P41RR002301; S10RR02781; S10RR08438; S10RR023438; S10RR025062; S10RR029220; DMB-8415048; OIA-9977486; BIR-9214394; R00 GM089987-03; MOW-2010-05240; MOW-2014-01877; MCB-1157771
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 290; Journal Issue: 20; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; nuclear magnetic resonance (NMR); plant biochemistry; plant hormone; protein structure; protein-protein interaction

Citation Formats

Korasick, David A., Chatterjee, Srirupa, Tonelli, Marco, Dashti, Hesam, Lee, Soon Goo, Westfall, Corey S., Fulton, D. Bruce, Andreotti, Amy H., Amarasinghe, Gaya K., Strader, Lucia C., and Jez, Joseph M. Defining a Two-pronged Structural Model for PB1 (Phox/Bem1p) Domain Interaction in Plant Auxin Responses. United States: N. p., 2015. Web. doi:10.1074/jbc.M115.648253.
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Korasick, David A., Chatterjee, Srirupa, Tonelli, Marco, Dashti, Hesam, Lee, Soon Goo, Westfall, Corey S., Fulton, D. Bruce, Andreotti, Amy H., Amarasinghe, Gaya K., Strader, Lucia C., & Jez, Joseph M. Defining a Two-pronged Structural Model for PB1 (Phox/Bem1p) Domain Interaction in Plant Auxin Responses. United States. https://doi.org/10.1074/jbc.M115.648253
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Korasick, David A., Chatterjee, Srirupa, Tonelli, Marco, Dashti, Hesam, Lee, Soon Goo, Westfall, Corey S., Fulton, D. Bruce, Andreotti, Amy H., Amarasinghe, Gaya K., Strader, Lucia C., and Jez, Joseph M. Fri . "Defining a Two-pronged Structural Model for PB1 (Phox/Bem1p) Domain Interaction in Plant Auxin Responses". United States. https://doi.org/10.1074/jbc.M115.648253. https://www.osti.gov/servlets/purl/1351393.
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@article{osti_1351393,
title = {Defining a Two-pronged Structural Model for PB1 (Phox/Bem1p) Domain Interaction in Plant Auxin Responses},
author = {Korasick, David A. and Chatterjee, Srirupa and Tonelli, Marco and Dashti, Hesam and Lee, Soon Goo and Westfall, Corey S. and Fulton, D. Bruce and Andreotti, Amy H. and Amarasinghe, Gaya K. and Strader, Lucia C. and Jez, Joseph M.},
abstractNote = {Phox/Bem1p (PB1) domains are universal structural modules that use surfaces of different charge for protein-protein association. In plants, PB1-mediated interactions of auxin response factors (ARF) and auxin/indole 3-acetic acid inducible proteins regulate transcriptional events modulated by the phytohormone auxin. Here we investigate the thermodynamic and structural basis for Arabidopsis thaliana ARF7 PB1 domain self-interaction. Isothermal titration calorimetry and NMR experiments indicate that key residues on both the basic and acidic faces of the PB1 domain contribute to and organize coordinately to stabilize protein-protein interactions. Calorimetric analysis of ARF7PB1 site-directed mutants defines a two-pronged electrostatic interaction. Furthermore, the canonical PB1 interaction between a lysine and a cluster of acidic residues provides one prong with an arginine and a second cluster of acidic residues defining the other prong. Evolutionary conservation of this core recognition feature and other co-varying interface sequences allows for versatile PB1-mediated interactions in auxin signaling.},
doi = {10.1074/jbc.M115.648253},
journal = {Journal of Biological Chemistry},
number = 20,
volume = 290,
place = {United States},
year = {Fri Apr 03 00:00:00 EDT 2015},
month = {Fri Apr 03 00:00:00 EDT 2015}
}
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https://doi.org/10.1074/jbc.M115.648253
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    Works referencing / citing this record:

    Regulation of auxin transcriptional responses
    journal, April 2020

    • Powers, Samantha K.; Strader, Lucia C.
    • Developmental Dynamics, Vol. 249, Issue 4
    • DOI: 10.1002/dvdy.139

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    • Wang, Zan; Wang, Xuemin; Zhang, Han
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    • Chandler, John William
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    A Review of Auxin Response Factors (ARFs) in Plants
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    Aux/IAA Gene Family in Plants: Molecular Structure, Regulation, and Function
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    • Luo, Jie; Zhou, Jing-Jing; Zhang, Jin-Zhi
    • International Journal of Molecular Sciences, Vol. 19, Issue 1
    • DOI: 10.3390/ijms19010259
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