Effects of FLOWERING LOCUS T on FD during the transition to flowering at the shoot apical meristem of Arabidopsis thaliana

The transition to flowering is a crucial step in the plant life cycle that is controlled by multiple endogenous and environmental cues, including hormones, sugars, temperature, and photoperiod. Permissive photoperiod induces FLOWERING LOCUS T (FT) in the phloem companion cells of leaves. The FT protein then acts as a florigen that is transported to the shoot apical meristem (SAM) where it physically interacts with the bZIP transcription factor FD and 14-3-3 proteins. However, despite the importance of FD for promoting flowering, its direct transcriptional targets are largely unknown. Here we combined ChIP-seq and RNA-seq to identify targets of FD at the genome-wide scale and assess the contribution of FT to binding DNA. We further investigated the ability of FD to form protein complexes with FT and TFL1 through the interaction with 14-3-3 proteins. Importantly, we observe direct binding of FD to targets involved in several aspects of the plant development not directly related to the regulation of flowering time. Our results confirm FD as central regulator of the floral transition at the shoot meristem and provides evidence for crosstalk between the regulation of flowering and other signaling pathways. Material Distribution The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.cell.com/molecular-plant/authors): Markus Schmid (markus.schmid@umu.se). Contact Information Umeå Plant Science Centre (UPSC), Dept. of Plant Physiology Umeå University, SE-901 87 Umeå, SWEDEN

[1]  S. Mirarab,et al.  Sequence Analysis , 2020, Encyclopedia of Bioinformatics and Computational Biology.

[2]  K. Shimamoto,et al.  TFL1-Like Proteins in Rice Antagonize Rice FT-Like Protein in Inflorescence Development by Competition for Complex Formation with 14-3-3 and FD , 2018, Plant & cell physiology.

[3]  Diqiu Yu,et al.  The bHLH Transcription Factors MYC2, MYC3, and MYC4 Are Required for Jasmonate-Mediated Inhibition of Flowering in Arabidopsis. , 2017, Molecular plant.

[4]  G. Howe,et al.  Regulation of growth–defense balance by the JASMONATE ZIM‐DOMAIN (JAZ)‐MYC transcriptional module , 2017, The New phytologist.

[5]  G. Theißen,et al.  MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution , 2016, Development.

[6]  Li Xu,et al.  Transcriptional Mechanism of Jasmonate Receptor COI1-Mediated Delay of Flowering Time in Arabidopsis[OPEN] , 2015, Plant Cell.

[7]  Young Hun Song,et al.  Photoperiodic flowering: time measurement mechanisms in leaves. , 2015, Annual review of plant biology.

[8]  Y. Machida,et al.  Calcium-dependent protein kinases responsible for the phosphorylation of a bZIP transcription factor FD crucial for the florigen complex formation , 2015, Scientific Reports.

[9]  Maida Romera-Branchat,et al.  Flowering responses to seasonal cues: what's new? , 2014, Current opinion in plant biology.

[10]  Paul Theodor Pyl,et al.  HTSeq—a Python framework to work with high-throughput sequencing data , 2014, bioRxiv.

[11]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[12]  Jae-Hoon Jung,et al.  The Arabidopsis floral repressor BFT delays flowering by competing with FT for FD binding under high salinity. , 2014, Molecular Plant.

[13]  D. Weigel,et al.  Structural Features Determining Flower-Promoting Activity of Arabidopsis FLOWERING LOCUS T[W][OPEN] , 2014, Plant Cell.

[14]  Xiaofeng Gu,et al.  Photoperiodic Regulation of Flowering Time through Periodic Histone Deacetylation of the Florigen Gene FT , 2013, PLoS biology.

[15]  Hélène Touzet,et al.  SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data , 2012, Bioinform..

[16]  Jychian Chen,et al.  Arabidopsis thaliana CENTRORADIALIS homologue (ATC) acts systemically to inhibit floral initiation in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[17]  J. Ahn,et al.  Role of SEPALLATA3 (SEP3) as a downstream gene of miR156-SPL3-FT circuitry in ambient temperature-responsive flowering , 2012, Plant signaling & behavior.

[18]  Jae-Hyung Lee,et al.  The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[19]  I. Ellis,et al.  Differential oestrogen receptor binding is associated with clinical outcome in breast cancer , 2011, Nature.

[20]  B. Causier,et al.  The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[21]  F. Parcy,et al.  Integrating long-day flowering signals: a LEAFY binding site is essential for proper photoperiodic activation of APETALA1. , 2011, The Plant journal : for cell and molecular biology.

[22]  K. Goto,et al.  Arabidopsis TERMINAL FLOWER1 Is Involved in the Regulation of Flowering Time and Inflorescence Development through Transcriptional Repression[C][W][OA] , 2011, Plant Cell.

[23]  Shojiro Tamaki,et al.  14-3-3 proteins act as intracellular receptors for rice Hd3a florigen , 2011, Nature.

[24]  Philip Machanick,et al.  MEME-ChIP: motif analysis of large DNA datasets , 2011, Bioinform..

[25]  M. Schmid,et al.  Regulation of flowering time: all roads lead to Rome , 2011, Cellular and Molecular Life Sciences.

[26]  S. Chattopadhyay,et al.  MYC2, a bHLH transcription factor, modulates the adult phenotype of SPA1 , 2010, Plant signaling & behavior.

[27]  Ilha Lee,et al.  Regulation and function of SOC1, a flowering pathway integrator. , 2010, Journal of experimental botany.

[28]  L. Farinelli,et al.  Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP) , 2010, Nature Protocols.

[29]  D. Inzé,et al.  NINJA connects the co-repressor TOPLESS to jasmonate signalling , 2010, Nature.

[30]  Richard Durbin,et al.  Fast and accurate long-read alignment with Burrows–Wheeler transform , 2010, Bioinform..

[31]  Detlef Weigel,et al.  miR156-Regulated SPL Transcription Factors Define an Endogenous Flowering Pathway in Arabidopsis thaliana , 2009, Cell.

[32]  Clifford A. Meyer,et al.  Model-based Analysis of ChIP-Seq (MACS) , 2008, Genome Biology.

[33]  Rainer Hedrich,et al.  Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. , 2008, The Plant journal : for cell and molecular biology.

[34]  J. Mathieu,et al.  Export of FT Protein from Phloem Companion Cells Is Sufficient for Floral Induction in Arabidopsis , 2007, Current Biology.

[35]  Fabio Fornara,et al.  FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis , 2007, Science.

[36]  Stefan R. Henz,et al.  A divergent external loop confers antagonistic activity on floral regulators FT and TFL1 , 2006, The EMBO journal.

[37]  Joonki Kim,et al.  CONSTANS Activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to Promote Flowering in Arabidopsis1[w] , 2005, Plant Physiology.

[38]  A. Samach,et al.  The Flowering Integrator FT Regulates SEPALLATA3 and FRUITFULL Accumulation in Arabidopsis Leavesw⃞ , 2005, The Plant Cell Online.

[39]  K. Goto,et al.  FD, a bZIP Protein Mediating Signals from the Floral Pathway Integrator FT at the Shoot Apex , 2005, Science.

[40]  Wolfgang Busch,et al.  Integration of Spatial and Temporal Information During Floral Induction in Arabidopsis , 2005, Science.

[41]  K. Goto,et al.  TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. , 2005, Plant & cell physiology.

[42]  Tracy Money,et al.  A single amino acid converts a repressor to an activator of flowering. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[44]  Minsoo Kim,et al.  Analysis of flowering pathway integrators in Arabidopsis. , 2005, Plant & cell physiology.

[45]  Shelley Hepworth,et al.  CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis , 2004, Development.

[46]  Ilha Lee,et al.  The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[47]  E. Grotewold,et al.  MYB transcription factors in Arabidopsis. , 2002, Trends in plant science.

[48]  M. Koornneef,et al.  A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana , 1991, Molecular and General Genetics MGG.

[49]  R. Weiss Regulation of Growth , 1965, Nature.

[50]  Rory Stark,et al.  DiBind : Dierential binding analysis of ChIP-Seq peak data , 2016 .

[51]  R. Stark,et al.  DiffBind : Differential binding analysis of ChIP-Seq peak data , 2012 .

[52]  Young Hun Song,et al.  CONSTANS and ASYMMETRIC LEAVES 1 complex is involved in the induction of FLOWERING LOCUS T in photoperiodic flowering in Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[53]  Claude-Alain H. Roten,et al.  Theoretical and practical advances in genome halving , 2004 .

[54]  J. Riechmann bZIP transcription factors in Arabidopsis , 2002 .