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 in | Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 21; pp. 7861 - 7866 |
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Main Authors | , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
National Academy of Sciences
27.05.2014
National Acad Sciences |
Subjects | |
Online Access | Get full text |
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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. |
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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 |
Author_xml | – sequence: 1 givenname: Hideki surname: Yoshida fullname: Yoshida, Hideki – sequence: 2 givenname: Ko surname: Hirano fullname: Hirano, Ko – sequence: 3 givenname: Tomomi surname: Sato fullname: Sato, Tomomi – sequence: 4 givenname: Nobutaka surname: Mitsuda fullname: Mitsuda, Nobutaka – sequence: 5 givenname: Mika surname: Nomoto fullname: Nomoto, Mika – sequence: 6 givenname: Kenichiro surname: Maeo fullname: Maeo, Kenichiro – sequence: 7 givenname: Eriko surname: Koketsu fullname: Koketsu, Eriko – sequence: 8 givenname: Rie surname: Mitani fullname: Mitani, Rie – sequence: 9 givenname: Mayuko surname: Kawamura fullname: Kawamura, Mayuko – sequence: 10 givenname: Sumie surname: Ishiguro fullname: Ishiguro, Sumie – sequence: 11 givenname: Yasuomi surname: Tada fullname: Tada, Yasuomi – sequence: 12 givenname: Masaru surname: Ohme-Takagi fullname: Ohme-Takagi, Masaru – sequence: 13 givenname: Makoto surname: Matsuoka fullname: Matsuoka, Makoto – sequence: 14 givenname: Miyako 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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Copyright | copyright © 1993–2008 National Academy of Sciences of the Uinted States of America Copyright National Academy of Sciences May 27, 2014 |
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Keywords | coactivator/corepressor exchange regulation system transcription factor gibberellin feedback regulation |
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Notes | http://dx.doi.org/10.1073/pnas.1321669111 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 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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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 |
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