LEAFY is a pioneer transcription factor and licenses cell reprogramming to floral fate

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.

LEAFY, a Pioneer Transcription Factor in Plants: A Mini-Review

“…Further analysis is required to understand the precise function of the plant MADS domain in the context of chromatin. LFY was the most well-characterized pioneer factor of all the master regulators ( Jin et al, 2021 ; Lai et al, 2021 ). LFY is only found in plants ( Maizel et al, 2005 ).…”

“…The first property is direct binding to a target DNA sequence inside a nucleosome ( Figure 1 ). This feature is often examined through electrophoretic mobility shift assays (EMSAs; Fernandez et al, 2019 ; Jin et al, 2021 ; Lai et al, 2021 ) and sequential TF and core histone chromatin immunoprecipitation (ChIP; Desvoyes et al, 2018 ; Jin et al, 2021 ) to provide evidence that putative pioneer factors have specific chromatin-binding properties suitable for such activities. To exclude the possible contribution to other factors, in vitro and in vivo experiments are required.…”

“…Consistent with the role of TFL1 in repressing LFY expression, tfl1 mutant, and TFL1 overexpressor plants showed LFY overexpressor and lfy mutant phenotypes, respectively, in terms of secondary inflorescence number: The knockout mutation of TFL1 decreased the number of secondary inflorescences, while the constitutive overexpression of TFL1 increased the number of secondary inflorescences ( Ratcliffe et al, 1998 ). TFL1 is a member of the phosphatidylethanolamine-binding protein (PEBP) family ( Jin et al, 2021 ) and is thought to act as a transcriptional cofactor in a floral repression complex that includes the basic leucine zipper (bZIP) transcription factor FD ( Honma and Goto, 2001 ; Abe et al, 2005 ; Ho and Weigel, 2014 ; Collani et al, 2019 ; Goretti et al, 2020 ; Zhu et al, 2020 ). FD recruits TFL1 to the second exon of LFY ( Figure 2C ; Zhu et al, 2020 ).…”

“…Besides cis -elements in the DNA targets themselves, in vivo modifications in the context of chromatin are important for the DNA-binding activity of LFY. EMSA data indicate that LFY associates with the nucleosomal regulatory region of AP1 in vitro ( Jin et al, 2021 ; Lai et al, 2021 ; first property). When the cis -element was mutated, LFY did not bind to the nucleosomal substrate, suggesting that LFY binds to nucleosomal DNA via its cis -element in vitro ( Jin et al, 2021 ).…”

“…Molecular genetic, biochemical, and crystal structural analyses have revealed common features of pioneer factors in animals. A pioneer factor in plants was recently identified by two independent groups ( Jin et al, 2021 ; Lai et al, 2021 ). In this mini-review, the author describes the latest advances in our understanding of this pioneer factor, LEAFY (LFY).…”