Abstract
Master transcription factors reprogram cell fate in multicellular eukaryotes. Pioneer transcription factors have prominent roles in this process because of their ability to contact their cognate binding motifs in closed chromatin. Reprogramming is pervasive in plants, whose development is plastic and tuned by the environment, yet little is known about pioneer transcription factors in this kingdom. Here, we show that the master transcription factor LEAFY (LFY), which promotes floral fate through upregulation of the floral commitment factor APETALA1 (AP1), is a pioneer transcription factor. In vitro, LFY binds to the endogenous AP1 target locus DNA assembled into a nucleosome. In vivo, LFY associates with nucleosome occupied binding sites at the majority of its target loci, including AP1. Upon binding, LFY ‘unlocks’ chromatin locally by displacing the H1 linker histone and by recruiting SWI/SNF chromatin remodelers, but broad changes in chromatin accessibility occur later. Our study provides a mechanistic framework for patterning of inflorescence architecture and uncovers striking similarities between LFY and animal pioneer transcription factor.
Highlights
Master transcription factors reprogram cell fate in multicellular eukaryotes
Using recombinant, purified, full-length LFY protein (Supplementary Fig. 1a) we tested LFY binding to this naked AP1 regulatory DNA fragment by electrophoretic mobility shift assays (EMSAs)
Based on the apparent dissociation constants (5–10 nM), the affinity of LFY for the endogenous sequencebased nucleosomal template is high (Fig. 1c), albeit slightly lower than those described for mammalian pioneer transcription factors (1-2 nM or 2–6 nM)[14,15]
Summary
Master transcription factors reprogram cell fate in multicellular eukaryotes. Pioneer transcription factors have prominent roles in this process because of their ability to contact their cognate binding motifs in closed chromatin. While it is easy to imagine how master transcription factors bind to active genes in open chromatin to trigger silencing, it is difficult to envision how these sequence-specific binding proteins can access their cognate motifs in silent chromatin to activate gene expression This is because nucleosomes are refractory for most transcription factor binding[7,8,9,10,11]. Defining criteria for pioneer transcription factors are (1) ability to bind cis motifs in the context of a nucleosome both in vitro and in vivo, (2) facilitating access of additional, non-pioneer, transcription factors to target loci via local chromatin opening and (3) cell fate reprograming[13,14,15,23,24]
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