DELLA protein functions as a transcriptional activator through the DNA binding of the INDETERMINATE DOMAIN family proteins

DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has been proposed to function as a transcriptional activator. However, because DELLA lacks a DNA-binding domain, intermediate protein(s) mediating t...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 111; no. 21; pp. 7861 - 7866
Main Authors Yoshida, Hideki, Hirano, Ko, Sato, Tomomi, Mitsuda, Nobutaka, Nomoto, Mika, Maeo, Kenichiro, Koketsu, Eriko, Mitani, Rie, Kawamura, Mayuko, Ishiguro, Sumie, Tada, Yasuomi, Ohme-Takagi, Masaru, Matsuoka, Makoto, Ueguchi-Tanaka, Miyako
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 27.05.2014
National Acad Sciences
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Abstract DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has been proposed to function as a transcriptional activator. However, because DELLA lacks a DNA-binding domain, intermediate protein(s) mediating the DELLA/DNA interaction are believed to be necessary for activating DELLA target genes. Here, using yeast hybrid screenings, we identified five members of INDETERMINATE DOMAIN (IDD) protein family which bind physically to both DELLA and the promoter sequence of the GA-positive regulator SCARECROW-LIKE 3 (SCL3), which previously was characterized as a DELLA direct target gene. Transient assays using Arabidopsis protoplasts demonstrated that a luciferase reporter controlled by the SCL3 promoter was additively transactivated by REPRESSOR of ga1-3 (RGA) and IDDs. Phenotypic analysis of transgenic plants expressing AtIDD3 (one of the 16 IDDs in the Arabidopsis genome) fused with the plant-specific repression domain (SRDX) supported the possibility that AtIDD3 is positively involved in GA signaling. In addition, we found that SCL3 protein also interacts with IDDs, resulting in the suppression of its target gene expression. In this context, DELLA and SCL3 interact competitively with IDD proteins to regulate downstream gene expression. These results suggest that the coregulators DELLA and SCL3, using IDDs as transcriptional scaffolds for DNA binding, antagonistically regulate the expression of their downstream targets to control the GA signaling pathway.
AbstractList Gibberellin (GA)-dependent degradation of DELLA protein, a key negative regulator, is essential for GA action. However, it is unclear how DELLA regulates downstream gene expression. Although possessing strong transactivation activity, DELLA lacks a DNA-binding domain. Therefore, a model has been proposed in which DELLA acts as a transcriptional coactivator with another transcription factor or factors containing a DNA-binding domain. Here, we show that some members of the INDETERMINATE DOMAIN (IDD) protein family are such intermediate proteins. The DELLA/IDD complex up-regulates the expression of the GA-positive regulator SCARECROW-LIKE 3 ( SCL3 ). Meanwhile, SCL3 protein also interacts with IDD proteins to suppress its own expression. We propose that a coregulator exchange system between DELLA (as coactivator) and SCL3 (as corepressor) regulates the expression of SCL3 . DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has been proposed to function as a transcriptional activator. However, because DELLA lacks a DNA-binding domain, intermediate protein(s) mediating the DELLA/DNA interaction are believed to be necessary for activating DELLA target genes. Here, using yeast hybrid screenings, we identified five members of INDETERMINATE DOMAIN (IDD) protein family which bind physically to both DELLA and the promoter sequence of the GA-positive regulator SCARECROW-LIKE 3 ( SCL3 ), which previously was characterized as a DELLA direct target gene. Transient assays using Arabidopsis protoplasts demonstrated that a luciferase reporter controlled by the SCL3 promoter was additively transactivated by REPRESSOR of ga1-3 (RGA) and IDDs. Phenotypic analysis of transgenic plants expressing AtIDD3 (one of the 16 IDDs in the Arabidopsis genome) fused with the plant-specific repression domain (SRDX) supported the possibility that AtIDD3 is positively involved in GA signaling. In addition, we found that SCL3 protein also interacts with IDDs, resulting in the suppression of its target gene expression. In this context, DELLA and SCL3 interact competitively with IDD proteins to regulate downstream gene expression. These results suggest that the coregulators DELLA and SCL3, using IDDs as transcriptional scaffolds for DNA binding, antagonistically regulate the expression of their downstream targets to control the GA signaling pathway.
DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has been proposed to function as a transcriptional activator. However, because DELLA lacks a DNA-binding domain, intermediate protein(s) mediating the DELLA/DNA interaction are believed to be necessary for activating DELLA target genes. Here, using yeast hybrid screenings, we identified five members of INDETERMINATE DOMAIN (IDD) protein family which bind physically to both DELLA and the promoter sequence of the GA-positive regulator SCARECROW-LIKE 3 (SCL3), which previously was characterized as a DELLA direct target gene. Transient assays using Arabidopsis protoplasts demonstrated that a luciferase reporter controlled by the SCL3 promoter was additively transactivated by REPRESSOR of ga1-3 (RGA) and IDDs. Phenotypic analysis of transgenic plants expressing AtIDD3 (one of the 16 IDDs in the Arabidopsis genome) fused with the plant-specific repression domain (SRDX) supported the possibility that AtIDD3 is positively involved in GA signaling. In addition, we found that SCL3 protein also interacts with IDDs, resulting in the suppression of its target gene expression. In this context, DELLA and SCL3 interact competitively with IDD proteins to regulate downstream gene expression. These results suggest that the coregulators DELLA and SCL3, using IDDs as transcriptional scaffolds for DNA binding, antagonistically regulate the expression of their downstream targets to control the GA signaling pathway.
DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has been proposed to function as a transcriptional activator. However, because DELLA lacks a DNA-binding domain, intermediate protein(s) mediating the DELLA/DNA interaction are believed to be necessary for activating DELLA target genes. Here, using yeast hybrid screenings, we identified five members of indeterminate domain (IDD) protein family which bind physically to both DELLA and the promoter sequence of the GA-positive regulator SCARECROW-LIKE 3 (SCL3), which previously was characterized as a DELLA direct target gene. Transient assays using Arabidopsis protoplasts demonstrated that a luciferase reporter controlled by the SCL3 promoter was additively transactivated by REPRESSOR of ga1-3 (RGA) and IDDs. Phenotypic analysis of transgenic plants expressing AtIDD3 (one of the 16 IDDs in the Arabidopsis genome) fused with the plant-specific repression domain (SRDX) supported the possibility that AtIDD3 is positively involved in GA signaling. In addition, we found that SCL3 protein also interacts with IDDs, resulting in the suppression of its target gene expression. In this context, DELLA and SCL3 interact competitively with IDD proteins to regulate downstream gene expression. These results suggest that the coregulators DELLA and SCL3, using IDDs as transcriptional scaffolds for DNA binding, antagonistically regulate the expression of their downstream targets to control the GA signaling pathway.DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has been proposed to function as a transcriptional activator. However, because DELLA lacks a DNA-binding domain, intermediate protein(s) mediating the DELLA/DNA interaction are believed to be necessary for activating DELLA target genes. Here, using yeast hybrid screenings, we identified five members of indeterminate domain (IDD) protein family which bind physically to both DELLA and the promoter sequence of the GA-positive regulator SCARECROW-LIKE 3 (SCL3), which previously was characterized as a DELLA direct target gene. Transient assays using Arabidopsis protoplasts demonstrated that a luciferase reporter controlled by the SCL3 promoter was additively transactivated by REPRESSOR of ga1-3 (RGA) and IDDs. Phenotypic analysis of transgenic plants expressing AtIDD3 (one of the 16 IDDs in the Arabidopsis genome) fused with the plant-specific repression domain (SRDX) supported the possibility that AtIDD3 is positively involved in GA signaling. In addition, we found that SCL3 protein also interacts with IDDs, resulting in the suppression of its target gene expression. In this context, DELLA and SCL3 interact competitively with IDD proteins to regulate downstream gene expression. These results suggest that the coregulators DELLA and SCL3, using IDDs as transcriptional scaffolds for DNA binding, antagonistically regulate the expression of their downstream targets to control the GA signaling pathway.
Author Sato, Tomomi
Mitsuda, Nobutaka
Maeo, Kenichiro
Mitani, Rie
Kawamura, Mayuko
Hirano, Ko
Matsuoka, Makoto
Ishiguro, Sumie
Ueguchi-Tanaka, Miyako
Ohme-Takagi, Masaru
Koketsu, Eriko
Nomoto, Mika
Yoshida, Hideki
Tada, Yasuomi
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  surname: Ueguchi-Tanaka
  fullname: Ueguchi-Tanaka, Miyako
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24821766$$D View this record in MEDLINE/PubMed
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DocumentTitleAlternate DELLA acts as a coactivator using IDD proteins
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Keywords coactivator/corepressor exchange regulation system
transcription factor
gibberellin feedback regulation
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Author contributions: H.Y., K.H., M.M., and M.U.-T. designed research; H.Y., K.H., T.S., N.M., M.N., K.M., E.K., R.M., and M.K. performed research; N.M., M.N., K.M., S.I., Y.T., and M.O.-T. contributed new reagents/analytic tools; H.Y., K.H., T.S., N.M., and M.U.-T. analyzed data; and H.Y., T.S., M.M., and M.U.-T. wrote the paper.
Edited by Mark Estelle, University of California, San Diego, La Jolla, CA, and approved April 17, 2014 (received for review November 20, 2013)
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Snippet DELLA protein is a key negative regulator of gibberellin (GA) signaling. Although how DELLA regulates downstream gene expression remains unclear, DELLA has...
Gibberellin (GA)-dependent degradation of DELLA protein, a key negative regulator, is essential for GA action. However, it is unclear how DELLA regulates...
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StartPage 7861
SubjectTerms Arabidopsis
Arabidopsis - metabolism
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis Proteins - physiology
Biological Sciences
Co-Repressor Proteins - genetics
Co-Repressor Proteins - metabolism
Deoxyribonucleic acid
DNA
DNA Primers
DNA-binding domains
DNA-Binding Proteins - genetics
Gene expression
Gene expression regulation
Gene Expression Regulation, Plant - genetics
Gene Expression Regulation, Plant - physiology
Genes
Genotype & phenotype
Gibberellins
hybrids
luciferase
Phenotypes
Plant Proteins - metabolism
Plants
Promoter regions
Proteins
Protoplasts
signal transduction
transactivators
transcription (genetics)
Transcription factors
Transcription Factors - metabolism
Transcriptional Activation - genetics
Transgenic plants
Two-Hybrid System Techniques
Yeasts
Title DELLA protein functions as a transcriptional activator through the DNA binding of the INDETERMINATE DOMAIN family proteins
URI https://www.jstor.org/stable/23774689
http://www.pnas.org/content/111/21/7861.abstract
https://www.ncbi.nlm.nih.gov/pubmed/24821766
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