Architecture of DNA elements mediating ARF transcription factor binding and auxin-responsive gene expression in Arabidopsis
| Autor: | Simon Lindhoud, Isidro Crespo, Elmar van der Wijk, Dolf Weijers, Victor G. Levitsky, Mattia Fontana, Victoria V. Mironova, Yana Sizentsova, D. Roeland Boer, Keita Tanaka, Johannes Hohlbein, Alejandra Freire-Rios |
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| Jazyk: | angličtina |
| Rok vydání: | 2020 |
| Předmět: |
Arabidopsis
Biophysics Biochemie Cooperativity Response Elements Biochemistry chemistry.chemical_compound Transcriptional regulation Gene Expression Regulation Plant Basic Helix-Loop-Helix Transcription Factors Protein–DNA interaction Auxin Gene Transcription factor ARF transcription factors Repetitive Sequences Nucleic Acid Protein-DNA interaction Plant biology Multidisciplinary Indoleacetic Acids biology Arabidopsis Proteins fungi Inverted Repeat Sequences food and beverages Promoter Laboratorium voor Celbiologie Biological Sciences biology.organism_classification Cell biology DNA-Binding Proteins Laboratory of Cell Biology Biofysica chemistry Multigene Family protein–DNA interaction EPS DNA Genome-Wide Association Study Transcription Factors |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America 117 (2020) 39 Proceedings of the National Academy of Sciences of the United States of America, 117(39), 24557-24566 Proceedings of the National Academy of Sciences of the United States of America |
| ISSN: | 0027-8424 |
| Popis: | Significance The plant hormone auxin controls many aspects of growth and development. It does so by changing the activity of AUXIN RESPONSE FACTOR (ARF) proteins that recognize specific DNA elements in plant genes and switch gene expression on or off. A major question in plant biology is how these ARF proteins bind unique DNA sequences and thus select which genes are regulated by auxin. Here, the authors systematically study the DNA architecture required for high-affinity binding of ARF proteins, and for auxin-dependent gene regulation in the plant Arabidopsis thaliana. This work shows that repeats of ARF recognition sites are critical for function, and reveals the molecular basis for the distinct activities of different repeat structures. The hormone auxin controls many aspects of the plant life cycle by regulating the expression of thousands of genes. The transcriptional output of the nuclear auxin signaling pathway is determined by the activity of AUXIN RESPONSE transcription FACTORs (ARFs), through their binding to cis-regulatory elements in auxin-responsive genes. Crystal structures, in vitro, and heterologous studies have fueled a model in which ARF dimers bind with high affinity to distinctly spaced repeats of canonical AuxRE motifs. However, the relevance of this "caliper" model, and the mechanisms underlying the binding affinities in vivo, have remained elusive. Here we biochemically and functionally interrogate modes of ARF–DNA interaction. We show that a single additional hydrogen bond in Arabidopsis ARF1 confers high-affinity binding to individual DNA sites. We demonstrate the importance of AuxRE cooperativity within repeats in the Arabidopsis TMO5 and IAA11 promoters in vivo. Meta-analysis of transcriptomes further reveals strong genome-wide association of auxin response with both inverted (IR) and direct (DR) AuxRE repeats, which we experimentally validated. The association of these elements with auxin-induced up-regulation (DR and IR) or down-regulation (IR) was correlated with differential binding affinities of A-class and B-class ARFs, respectively, suggesting a mechanistic basis for the distinct activity of these repeats. Our results support the relevance of high-affinity binding of ARF transcription factors to uniquely spaced DNA elements in vivo, and suggest that differential binding affinities of ARF subfamilies underlie diversity in cis-element function. |
| Databáze: | OpenAIRE |
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