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Florigen Family Chromatin Recruitment, Competition and Target Genes bioRxiv preprint doi: https://doi.org/10.1101/2020.02.04.934026; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Florigen family chromatin recruitment, competition and target genes 2 Yang Zhu1, Samantha Klasfeld1, Cheol Woong Jeong1,3†, Run Jin1, Koji Goto4, 3 Nobutoshi Yamaguchi1,2† and Doris Wagner1* 4 1 Department of Biology, University of Pennsylvania, 415 S. University Ave, 5 Philadelphia, PA 19104, USA 6 2 Current address: Science and Technology, Nara Institute of Science and Technology, 7 8916-5 Takayama-cho, Ikoma-shi, Nara 630-0192, Japan 8 3 Current address: LG Economic Research Institute, LG Twin tower, Seoul 07336, 9 Korea 10 4 Research Institute for Biological Sciences, Okayama Prefecture, 7549-1, Kibichuoh- 11 cho, Kaga-gun, Okayama, 716-1241, Japan 12 *Correspondence: [email protected] 13 † equal contribution 14 15 16 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.04.934026; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 17 Abstract 18 Plants monitor seasonal cues, such as day-length, to optimize life history traits including 19 onset of reproduction and inflorescence architecture 1-3. Florigen family transcriptional 20 co-regulators TERMINAL FLOWER 1 (TFL1) and FLOWERING LOCUS T (FT) 21 antagonistically regulate these vital processes 4-6 yet how TFL1 and FT execute their 22 roles and what the mechanism is for their antagonism remains poorly understood. We 23 show genome-wide, that TFL1 is recruited to the chromatin by the bZIP transcription 24 factor FLOWERING LOCUS D (FD) in Arabidopsis. We find that seasonal cue-mediated 25 upregulation of FT competes TFL1 from chromatin-bound FD at key target loci. We 26 identify the master regulator of floral fate, LEAFY (LFY) as a target under dual opposite 27 regulation by TFL1 and FT. Exonic bZIP motifs in LFY are critical for repression by 28 TFL1, upregulation by FT and adoption of floral fate. Transcriptomic identification of 29 target genes directly repressed by the TFL1-FD complex not only identifies key 30 regulators of onset of reproduction and floral fate, but reveals that TFL1-FD repress 31 sugar and hormone signalling pathways and chromatin regulators. Our data provide 32 mechanistic insight into how florigen family member sculpt inflorescence architecture, a 33 trait important for reproductive success and yield. 34 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.04.934026; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 35 Main 36 Plant development occurs after embryogenesis and is plastic, this allows modulation of 37 the final body plan in response to environmental cues to enhance growth and 38 reproductive success 7,8. Of particular importance for species survival is the timing of the 39 formation of flowers that give rise to seeds which occurs in response to the seasonal 40 cues photoperiod and temperature 1,3,9. For example, in plants that flower only once, like 41 Arabidopsis and most crops, an early switch to flower formation allows rapid completion 42 of the life-cycle in a short growing season, but reduces total seed set or yield 10-12. By 43 contrast, delaying flower formation supports formation of more seeds, but extends the 44 time to seed set. In many plant species, these alternative developmental trajectories are 45 tuned in response to daylength in antagonistic fashion by two members of the florigen 46 family of proteins 12,13. FT promotes onset of the reproductive phase and flower 47 formation (determinacy), while TFL1 promotes vegetative development and branch fate 48 (indeterminacy) 4-6,13. In Arabidopsis, which flowers in the spring, FT accumulates only 49 when the daylength exceeds a critical threshold, while TFL1 is present in both short-day 50 and long-day conditions 1,3,14. A key unanswered question is how FT and TFL1 51 modulate plant form – what are the downstream processes they set in motion and what 52 is molecular basis for their antagonism? 53 54 Accumulating evidence points to roles of FT and TFL1, which lack ability to bind DNA, 55 in transcriptional activation and repression, respectively, by forming complexes with a 56 bZIP transcription factor, FLOWERING LOCUS D (FD) 12,15-19, although non-nuclear 57 functions for both proteins have also been described 20,21. Mechanistic insight into 58 florigen activity has been hampered by their low protein abundance. To overcome this 59 limitation and to test the role of TFL1 in the nucleus, we conducted TFL1 chromatin 60 immunoprecipitation followed by sequencing (ChIP-seq). Towards this end, we first 61 generated a biologically active, genomic GFP-tagged version of TFL1 (gTFL1-GFP tfl1- 62 1) (Supplementary Fig. 1a, b). Next, we enriched for TFL1 expressing cells by isolating 63 shoot apices from 42-day-old short-day-grown inflorescences just prior to onset of 64 flower formation (Fig. 1a). Finally, we optimized low abundance ChIP by combining 65 eight individual ChIP reactions per ChIP-seq replicate. We conducted FD ChIP-seq in 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.04.934026; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 66 analogous fashion using a published 22, biologically active (Supplementary Fig. 1c), 67 genomic fusion protein (gFD-GUS fd-1). Our ChIP-seq uncovered 3,308 and 4,422 68 significant TFL1 and FD peaks (MACS2 summit qval≤10-10), respectively (Fig. 1b). The 69 TFL1 peaks significantly overlapped with the FD peaks (72% overlap, pval<10-300, 70 hypergeometric test; Fig. 1b, c). We performed de novo motif analysis and identified the 71 bZIP G-box cis motif, a known FD binding site 23, as most significantly enriched 72 (pval<10-470) and frequently present (> 84%) under TFL1 and TFL1/FD co-bound peaks 73 (Fig. 1d and Supplementary Figs. 2, 3). To test whether TFL1 occupancy depends on 74 presence of functional FD, we next performed TFL1 ChIP-seq in the fd-1 null mutant. 75 TFL1 chromatin occupancy was strongly reduced in fd-1 (Fig. 1c, e). Our data suggest 76 a prominent role of TFL1 in the nucleus and indicate that FD recruits TFL1 to the 77 chromatin of target loci. 78 79 Annotating FD and TFL1 peaks to genes identified 2,699 joint TFL1 and FD targets. 80 Gene Ontology (GO) term enrichment analysis implicates these targets in abiotic and 81 endogenous stimulus response and reproductive development (Supplementary Table 82 1). Joint TFL1 and FD peaks were present at loci that promote onset of the reproductive 83 phase in response to inductive photoperiod 1,3,24 like GIGANTEA (GI), CONSTANS (CO), 84 and SUPPRESSOR OF CONSTANS1 (SOC1) and of flower fate 24,25 such as LFY, 85 APETALA1 (AP1), and FRUITFULL (FUL) (Fig. 1f). Identification of these TFL1 and FD 86 bound targets fits well with TFL1’s known biological role (suppression of onset of 87 reproduction and flower formation) and proposed molecular function (opposition of gene 88 activation) 4-6,15. We selected the LFY gene, which encodes a master regulator of flower 89 fate (Supplementary Fig. 4a - f) 6,26-28, to further probe the molecular mechanism of 90 action of TFL1. To test whether LFY expression is directly repressed by the TFL1-FD 91 complex, we generated transgenic plants expressing a steroid inducible version of TFL1 92 (TFL1ER; Supplementary Fig. 5). A single steroid treatment reduced LFY levels by 50% 93 after 4 hours (Supplementary Fig. 4g), suggesting that the TFL1-FD complex 94 represses LFY. 95 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.04.934026; this version posted February 4, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 96 To better understand TFL1 recruitment to the LFY locus, we identified the genomic 97 region sufficient and the cis motifs necessary for TFL1 association with LFY. TFL1 and 98 FD peak summits were located in the second exon of LFY (Fig.1f and Supplementary 99 Fig. 4h, i) and LFY reporters that lack the second exon were not repressed in response 100 to TFL1 overexpression (Supplementary Fig. 6a, b). Exonic transcription factor binding 101 sites, although rare, are found in both animals and plants, and frequently link to 102 developmental regulation 29,30. We identified three putative bZIP binding sites in LFY 103 exon two: an evolutionarily conserved G-box and two partially conserved C-boxes (Fig. 104 2a). LFY exon two alone – when randomly integrated into the genome- was sufficient to 105 recruit TFL1 (Fig. 2b). The recruitment was abolished when the three bZIP binding 106 motifs were mutated (Fig.
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