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Title: Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an Atypical bHLH Transcription Factor, in Auxin Responses in Arabidopsis

Abstract

Auxin regulates nearly all aspects of plant growth and development including cell division, cell elongation and cell differentiation, which are achieved largely by rapid regulation of auxin response genes. However, the functions of a large number of auxin response genes remain uncharacterized. Paclobutrazol Resistance (PRE) proteins are non-DNA binding basic helix-loop-helix transcription factors that have been shown to be involved in gibberellin and brassinosteroid signaling, and light responses in Arabidopsis. Here, we provide molecular and genetic evidence that PRE6, one of the six PRE genes in Arabidopsis, is an auxin response gene, and that PRE6 is involved in the regulation of auxin signaling. By using quantitative RT-PCR, we showed that the expression level of PRE6 was increased in response to exogenously applied IAA. GUS staining results also showed that the expression of GUS reporter gene in the PRE6p:GUS transgenic seedlings was elevated in response to auxin. Phenotypic analysis showed that overexpression of PRE6 in Arabidopsis resulted in auxin-related phenotypes including elongated hypocotyl and primary roots, and reduced number of lateral roots when compared with the Col wild type seedlings, whereas opposite phenotypes were observed in the pre6 mutants. Further analysis showed that PRE6 overexpression plants were hyposensitive, whereas pre6 mutantsmore » were hypersensitive to auxin in root and hypocotyl elongation and lateral root formation assays. By using protoplasts transfection, we showed that PRE6 functions as a transcriptional repressor. Consistent with this, the expression of the auxin response reporter DR5:GUS was decreased in PRE6 overexpression lines, but increased in pre6 mutants. When co-transfected into protoplasts, ARF5 and ARF8 activated the expression of the PRE6p:GUS reporter. Chromatin immunoprecipitation assays showed that ARF5 and ARF8 can be recruited to the promoter regions of PRE6. Taken together, these results suggest that PRE6 is an auxin response gene whose expression is directly regulated by ARF5 and ARF8, and that PRE6 is a transcriptional repressor that negatively regulates auxin responses in Arabidopsis.« less

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [3];  [2]
  1. Northeast Normal Univ., Changchun (China); Chinese Academy of Sciences (CAS), Changchun (China)
  2. Northeast Normal Univ., Changchun (China)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1476426
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 8; Journal Issue: n/a; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Zheng, Kaijie, Wang, Yating, Zhang, Na, Jia, Qiming, Wang, Xutong, Hou, Chunjiang, Chen, Jin-Gui, and Wang, Shucai. Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an Atypical bHLH Transcription Factor, in Auxin Responses in Arabidopsis. United States: N. p., 2017. Web. doi:10.3389/fpls.2017.01813.
Zheng, Kaijie, Wang, Yating, Zhang, Na, Jia, Qiming, Wang, Xutong, Hou, Chunjiang, Chen, Jin-Gui, & Wang, Shucai. Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an Atypical bHLH Transcription Factor, in Auxin Responses in Arabidopsis. United States. https://doi.org/10.3389/fpls.2017.01813
Zheng, Kaijie, Wang, Yating, Zhang, Na, Jia, Qiming, Wang, Xutong, Hou, Chunjiang, Chen, Jin-Gui, and Wang, Shucai. Tue . "Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an Atypical bHLH Transcription Factor, in Auxin Responses in Arabidopsis". United States. https://doi.org/10.3389/fpls.2017.01813. https://www.osti.gov/servlets/purl/1476426.
@article{osti_1476426,
title = {Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an Atypical bHLH Transcription Factor, in Auxin Responses in Arabidopsis},
author = {Zheng, Kaijie and Wang, Yating and Zhang, Na and Jia, Qiming and Wang, Xutong and Hou, Chunjiang and Chen, Jin-Gui and Wang, Shucai},
abstractNote = {Auxin regulates nearly all aspects of plant growth and development including cell division, cell elongation and cell differentiation, which are achieved largely by rapid regulation of auxin response genes. However, the functions of a large number of auxin response genes remain uncharacterized. Paclobutrazol Resistance (PRE) proteins are non-DNA binding basic helix-loop-helix transcription factors that have been shown to be involved in gibberellin and brassinosteroid signaling, and light responses in Arabidopsis. Here, we provide molecular and genetic evidence that PRE6, one of the six PRE genes in Arabidopsis, is an auxin response gene, and that PRE6 is involved in the regulation of auxin signaling. By using quantitative RT-PCR, we showed that the expression level of PRE6 was increased in response to exogenously applied IAA. GUS staining results also showed that the expression of GUS reporter gene in the PRE6p:GUS transgenic seedlings was elevated in response to auxin. Phenotypic analysis showed that overexpression of PRE6 in Arabidopsis resulted in auxin-related phenotypes including elongated hypocotyl and primary roots, and reduced number of lateral roots when compared with the Col wild type seedlings, whereas opposite phenotypes were observed in the pre6 mutants. Further analysis showed that PRE6 overexpression plants were hyposensitive, whereas pre6 mutants were hypersensitive to auxin in root and hypocotyl elongation and lateral root formation assays. By using protoplasts transfection, we showed that PRE6 functions as a transcriptional repressor. Consistent with this, the expression of the auxin response reporter DR5:GUS was decreased in PRE6 overexpression lines, but increased in pre6 mutants. When co-transfected into protoplasts, ARF5 and ARF8 activated the expression of the PRE6p:GUS reporter. Chromatin immunoprecipitation assays showed that ARF5 and ARF8 can be recruited to the promoter regions of PRE6. Taken together, these results suggest that PRE6 is an auxin response gene whose expression is directly regulated by ARF5 and ARF8, and that PRE6 is a transcriptional repressor that negatively regulates auxin responses in Arabidopsis.},
doi = {10.3389/fpls.2017.01813},
journal = {Frontiers in Plant Science},
number = n/a,
volume = 8,
place = {United States},
year = {Tue Oct 24 00:00:00 EDT 2017},
month = {Tue Oct 24 00:00:00 EDT 2017}
}

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A competitive peptide inhibitor KIDARI negatively regulates HFR1 by forming nonfunctional heterodimers in Arabidopsis photomorphogenesis
journal, December 2012


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journal, May 2006


Plant Development Is Regulated by a Family of Auxin Receptor F Box Proteins
journal, July 2005


Auxin response factors
journal, October 2007


The Arabidopsis F-box protein TIR1 is an auxin receptor
journal, May 2005


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journal, May 2005

  • Dharmasiri, Nihal; Dharmasiri, Sunethra; Estelle, Mark
  • Nature, Vol. 435, Issue 7041
  • DOI: 10.1038/nature03543

Auxin in action: signalling, transport and the control of plant growth and development
journal, September 2006

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An ABA down-regulated bHLH transcription repressor gene, bHLH129 regulates root elongation and ABA response when overexpressed in Arabidopsis
journal, December 2015

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Ectopic expression of R3 MYB transcription factor gene OsTCL1 in Arabidopsis, but not rice, affects trichome and root hair formation
journal, January 2016

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  • DOI: 10.1038/srep19254

Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis
journal, January 2002


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journal, December 2009

  • Parry, G.; Calderon-Villalobos, L. I.; Prigge, M.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 52
  • DOI: 10.1073/pnas.0911967106

Interactions between HLH and bHLH Factors Modulate Light-Regulated Plant Development
journal, May 2012

  • Hao, Yaqi; Oh, Eunkyoo; Choi, Giltsu
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  • DOI: 10.1093/mp/sss011

Overexpression of PRE1 and its Homologous Genes Activates Gibberellin-dependent Responses in Arabidopsis thaliana
journal, May 2006

  • Lee, Sumin; Lee, Seunghee; Yang, Ki-Young
  • Plant and Cell Physiology, Vol. 47, Issue 5
  • DOI: 10.1093/pcp/pcj026

Integration of Light and Auxin Signaling
journal, November 2009

  • Halliday, K. J.; Martinez-Garcia, J. F.; Josse, E. -M.
  • Cold Spring Harbor Perspectives in Biology, Vol. 1, Issue 6
  • DOI: 10.1101/cshperspect.a001586

Aux/IAA Proteins Contain a Potent Transcriptional Repression Domain
journal, January 2004

  • Tiwari, Shiv B.; Hagen, Gretchen; Guilfoyle, Tom J.
  • The Plant Cell, Vol. 16, Issue 2
  • DOI: 10.1105/tpc.017384

Regulation of Arabidopsis Brassinosteroid Signaling by Atypical Basic Helix-Loop-Helix Proteins
journal, December 2009


A Triantagonistic Basic Helix-Loop-Helix System Regulates Cell Elongation in Arabidopsis
journal, November 2012

  • Ikeda, Miho; Fujiwara, Sumire; Mitsuda, Nobutaka
  • The Plant Cell, Vol. 24, Issue 11
  • DOI: 10.1105/tpc.112.105023

Update on the Basic Helix-Loop-Helix Transcription Factor Gene Family in Arabidopsis thaliana
journal, November 2003

  • Bailey, Paul C.; Martin, Cathie; Toledo-Ortiz, Gabriela
  • The Plant Cell, Vol. 15, Issue 11
  • DOI: 10.1105/tpc.151140

Molecular Profiles of Contrasting Shade Response Strategies in Wild Plants: Differential Control of Immunity and Shoot Elongation
journal, January 2017

  • Gommers, Charlotte M. M.; Keuskamp, Diederik H.; Buti, Sara
  • The Plant Cell, Vol. 29, Issue 2
  • DOI: 10.1105/tpc.16.00790

Composite structure of auxin response elements.
journal, October 1995


Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
journal, November 1997


The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis
journal, April 2012


Characterization of an activation-tagged mutant uncovers a role of GLABRA2 in anthocyanin biosynthesis in Arabidopsis
journal, June 2015

  • Wang, Xiaoyu; Wang, Xianling; Hu, Qingnan
  • The Plant Journal, Vol. 83, Issue 2
  • DOI: 10.1111/tpj.12887

ARF1, a Transcription Factor That Binds to Auxin Response Elements
journal, June 1997


Mechanism of Auxin-Regulated Gene Expression in Plants
journal, December 2009


Auxin Receptors and Plant Development: A New Signaling Paradigm
journal, November 2008


The IBR5 phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1-mediated repressor degradation
journal, January 2008

  • Strader, Lucia C.; Monroe-Augustus, Melanie; Bartel, Bonnie
  • BMC Plant Biology, Vol. 8, Issue 1
  • DOI: 10.1186/1471-2229-8-41

A Modular Analysis of the Auxin Signalling Network
journal, March 2015


Expression of wild-type PtrIAA14.1, a poplar Aux/IAA gene causes morphological changes in Arabidopsis
journal, June 2015


Basic helix-loop-helix transcription factors and epidermal cell fate determination in Arabidopsis
journal, December 2012

  • Zhao, Hongtao; Li, Xia; Ma, Ligeng
  • Plant Signaling & Behavior, Vol. 7, Issue 12
  • DOI: 10.4161/psb.22404

Shedding light on auxin movement: Light-regulation of polar auxin transport in the photocontrol of plant development
journal, March 2013

  • Sassi, Massimiliano; Ruberti, Ida; Vernoux, Teva
  • Plant Signaling & Behavior, Vol. 8, Issue 3
  • DOI: 10.4161/psb.23355

ATBS1 INTERACTING FACTORs negatively regulate Arabidopsis cell elongation in the triantagonistic bHLH system
journal, March 2013

  • Ikeda, Miho; Mitsuda, Nobutaka; Ohme-Takagi, Masaru
  • Plant Signaling & Behavior, Vol. 8, Issue 3
  • DOI: 10.4161/psb.23448

Works referencing / citing this record:

Plant-specific ribosome biogenesis factors in Arabidopsis thaliana with essential function in rRNA processing
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PACLOBUTRAZOL-RESISTANCE Gene Family Regulates Floral Organ Growth with Unequal Genetic Redundancy in Arabidopsis thaliana
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PACLOBUTRAZOL-RESISTANCE Gene Family Regulates Floral Organ Growth with Unequal Genetic Redundancy in Arabidopsis thaliana
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