Abstract

Transcription factors activate or repress target gene expression or switch between activation and repression. In animals and yeast, Groucho/Tup1 corepressor proteins are recruited by diverse transcription factors to induce context-specific transcriptional repression. Two groups of Groucho/Tup1-like corepressors have been described in plants. LEUNIG and LEUNIG_HOMOLOG constitute one group and TOPLESS (TPL) and the four TPL-related (TPR) corepressors form the other. To discover the processes in which TPL and the TPR corepressors operate, high-throughput yeast two-hybrid approaches were used to identify interacting proteins. We found that TPL/TPR corepressors predominantly interact directly with specific transcription factors, many of which were previously implicated in transcriptional repression. The interacting transcription factors reveal that the TPL/TPR family has been coopted multiple times to modulate gene expression in diverse processes, including hormone signaling, stress responses, and the control of flowering time, for which we also show biological validation. The interaction data suggest novel mechanisms for the involvement of TPL/TPR corepressors in auxin and jasmonic acid signaling. A number of short repression domain (RD) sequences have previously been identified in Arabidopsis (Arabidopsis thaliana) transcription factors. All known RD sequences were enriched among the TPL/TPR interactors, and novel TPL-RD interactions were identified. We show that the presence of RD sequences is essential for TPL/TPR recruitment. These data provide a framework for TPL/TPR-dependent transcriptional repression. They allow for predictions about new repressive transcription factors, corepressor interactions, and repression mechanisms and identify a wide range of plant processes that utilize TPL/TPR-mediated gene repression.

Highlights

  • Transcription factors activate or repress target gene expression or switch between activation and repression

  • We show that all known plant repression domain (RD) sequences are enriched among the TPL/TPR interactome and that these domains are necessary for TPL/ TPR recruitment

  • Since the majority of all TPL/TPR interactions were with transcription factors, we attempted to determine the range of transcription factor interactions by screening an arrayed yeast two-hybrid library of 1,296 Arabidopsis transcription factors (Paz-Ares and The REGIA Consortium, 2002; Castrillo et al, 2011) with each TPL/TPR protein, making a total of 6,480 individual interaction tests

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Summary

Introduction

Transcription factors activate or repress target gene expression or switch between activation and repression. These data provide a framework for TPL/TPR-dependent transcriptional repression They allow for predictions about new repressive transcription factors, corepressor interactions, and repression mechanisms and identify a wide range of plant processes that utilize TPL/ TPR-mediated gene repression. As well as directly interacting with YABBY transcription factors (Stahle et al, 2009), LUG/LUH corepressors indirectly interact with transcription factors via the SEUSS adaptor protein or related SEUSS-LIKE proteins (Franks et al, 2002; Sridhar et al, 2004) Another Gro/Tup corepressor family, TOPLESS (TPL; including TPL and TPL-related [TPR]), has recently been described in plants that interacts both directly and indirectly with. It has been shown that in maize (Zea mays), the zinc (Zn)-finger transcription factor RAMOSA1 interacts with the TPL/TPR factor REL2 to repress indeterminate meristem fate (Gallavotti et al, 2010), demonstrating another involvement of TPL/TPR corepressors in meristem maintenance, acting with a different transcription factor and with an opposite developmental outcome

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