Disruption of gene silencing by Polycomb protein complexes leads to homeotic transformations and altered developmental-phase identity in plants. Here we define short genomic fragments, known as Polycomb response elements (PREs), that direct Polycomb repressive complex 2 (PRC2) placement at developmental genes regulated by silencing in Arabidopsis thaliana. We identify transcription factor families that bind to these PREs, colocalize with PRC2 on chromatin, physically interact with and recruit PRC2, and are required for PRC2-mediated gene silencing in vivo. Two of the cis sequence motifs enriched in the PREs are cognate binding sites for the identified transcription factors and are necessary and sufficient for PRE activity. Thus PRC2 recruitment in Arabidopsis relies in large part on binding of trans-acting factors to cis-localized DNA sequence motifs.
Plants monitor seasonal cues to optimize reproductive success by tuning onset of reproduction and inflorescence architecture. TERMINAL FLOWER 1 (TFL1) and FLOWERING LOCUS T (FT) and their orthologs antagonistically regulate these life history traits, yet their mechanism of action, antagonism and targets remain poorly understood. Here, we show that TFL1 is recruited to thousands of loci by the bZIP transcription factor FD. We identify the master regulator of floral fate, LEAFY (LFY) as a target under dual opposite regulation by TFL1 and FT and uncover a pivotal role of FT in promoting flower fate via LFY upregulation. We provide evidence that the antagonism between FT and TFL1 relies on competition for chromatin-bound FD at shared target loci. Direct TFL1-FD regulated target genes identify this complex as a hub for repressing both master regulators of reproductive development and endogenous signalling pathways. Our data provide mechanistic insight into how TFL1-FD sculpt inflorescence architecture, a trait important for reproductive success, plant architecture and yield.
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.
17Plants monitor seasonal cues, such as day-length, to optimize life history traits including 18 onset of reproduction and inflorescence architecture 1-3 . Florigen family transcriptional 19 co-regulators TERMINAL FLOWER 1 (TFL1) and FLOWERING LOCUS T (FT) 20 antagonistically regulate these vital processes 4-6 yet how TFL1 and FT execute their 21 roles and what the mechanism is for their antagonism remains poorly understood. We 22 Main 35Plant development occurs after embryogenesis and is plastic, this allows modulation of 36 the final body plan in response to environmental cues to enhance growth and 37 reproductive success 7,8 . Of particular importance for species survival is the timing of the 38 formation of flowers that give rise to seeds which occurs in response to the seasonal 39 cues photoperiod and temperature 1,3,9 . For example, in plants that flower only once, like 40Arabidopsis and most crops, an early switch to flower formation allows rapid completion 41 of the life-cycle in a short growing season, but reduces total seed set or yield 10-12 . By 42 contrast, delaying flower formation supports formation of more seeds, but extends the 43 time to seed set. In many plant species, these alternative developmental trajectories are 44 tuned in response to daylength in antagonistic fashion by two members of the florigen 45 family of proteins 12,13 . FT promotes onset of the reproductive phase and flower 46 formation (determinacy), while TFL1 promotes vegetative development and branch fate 47 (indeterminacy) 4-6,13 . In Arabidopsis, which flowers in the spring, FT accumulates only 48 when the daylength exceeds a critical threshold, while TFL1 is present in both short-day 49 and long-day conditions 1,3,14 . A key unanswered question is how FT and TFL1 50 modulate plant form -what are the downstream processes they set in motion and what 51 is molecular basis for their antagonism? 52 53Accumulating evidence points to roles of FT and TFL1, which lack ability to bind DNA, 54 in transcriptional activation and repression, respectively, by forming complexes with a 55 bZIP transcription factor, FLOWERING LOCUS D (FD) 12,15-19 , although non-nuclear 56 functions for both proteins have also been described 20,21 . Mechanistic insight into 57 florigen activity has been hampered by their low protein abundance. To overcome this 58 limitation and to test the role of TFL1 in the nucleus, we conducted TFL1 chromatin 59 immunoprecipitation followed by sequencing (ChIP-seq). Towards this end, we first 60 generated a biologically active, genomic GFP-tagged version of TFL1 (gTFL1-GFP tfl1-61 1) (Supplementary Fig. 1a, b). Next, we enriched for TFL1 expressing cells by isolating 62 shoot apices from 42-day-old short-day-grown inflorescences just prior to onset of 63 flower formation (Fig. 1a). Finally, we optimized low abundance ChIP by combining 64 eight individual ChIP reactions per ChIP-seq replicate. We conducted FD ChIP-seq in 65 4 analogous fashion using a published 22 , biologically active ( Supplementary Fig. 1c), 66 genomic...
This year marks the 100th anniversary of the experiments by Garner and Allard that showed that plants measure the duration of the night and day (the photoperiod) to time flowering. This discovery led to the identification of Flowering Locus T (FT) in Arabidopsis and Heading Date 3a (Hd3a) in rice as a mobile signal that promotes flowering in tissues distal to the site of cue perception. FT/Hd3a belong to the family of phosphatidylethanolamine-binding proteins (PEBPs). Collectively, these proteins control plant developmental transitions and plant architecture. Several excellent recent reviews have focused on the roles of PEBPs in diverse plant species; here we will primarily highlight recent advances that enhance our understanding of the mechanism of action of PEBPs and discuss critical open questions.
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