title: Repression of Lateral Organ Boundary Genes by PENNYWISE and POUND-FOOLISH Is Essential for Meristem Maintenance and Flowering in Arabidopsis.
abstract: In the model plant Arabidopsis (Arabidopsis thaliana), endogenous and environmental signals acting on the shoot apical meristem cause acquisition of inflorescence meristem fate. This results in changed patterns of aerial development seen as the transition from making leaves to the production of flowers separated by elongated internodes. Two related BEL1-like homeobox genes, PENNYWISE (PNY) and POUND-FOOLISH (PNF), fulfill this transition. Loss of function of these genes impairs stem cell maintenance and blocks internode elongation and flowering. We show here that pny pnf apices misexpress lateral organ boundary genes BLADE-ON-PETIOLE1/2 (BOP1/2) and KNOTTED-LIKE FROM ARABIDOPSIS THALIANA6 (KNAT6) together with ARABIDOPSIS THALIANA HOMEOBOX GENE1 (ATH1). Inactivation of genes in this module fully rescues pny pnf defects. We further show that BOP1 directly activates ATH1, whereas activation of KNAT6 is indirect. The pny pnf restoration correlates with renewed accumulation of transcripts conferring floral meristem identity, including FD, SQUAMOSA PROMOTER-BINDING PROTEIN LIKE genes, LEAFY, and APETALA1. To gain insight into how this module blocks flowering, we analyzed the transcriptome of BOP1-overexpressing plants. Our data suggest a central role for the microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE-microRNA172 module in integrating stress signals conferred in part by promotion of jasmonic acid biosynthesis. These data reveal a potential mechanism by which repression of lateral organ boundary genes by PNY-PNF is essential for flowering.
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Madiha
authors.initials: M
authors.lastname: Khan
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Laura
authors.initials: L
authors.lastname: Ragni
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Paul
authors.initials: P
authors.lastname: Tabb
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Brenda C
authors.identifier: http://orcid.org/0000-0002-0050-4001
authors.initials: BC
authors.lastname: Salasini
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Steven
authors.initials: S
authors.lastname: Chatfield
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Raju
authors.initials: R
authors.lastname: Datla
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: John
authors.identifier: http://orcid.org/0000-0002-3526-7982
authors.initials: J
authors.lastname: Lock
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Xiahezi
authors.initials: X
authors.lastname: Kuai
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Charles
authors.initials: C
authors.lastname: Després
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Marcel
authors.identifier: http://orcid.org/0000-0001-7896-6049
authors.initials: M
authors.lastname: Proveniers
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Cao
authors.initials: C
authors.lastname: Yongguo
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Daoquan
authors.identifier: http://orcid.org/0000-0001-7144-1274
authors.initials: D
authors.lastname: Xiang
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Halima
authors.initials: H
authors.lastname: Morin
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Jean-Pierre
authors.initials: JP
authors.lastname: Rullière
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.).
authors.forename: Sylvie
authors.identifier: http://orcid.org/0000-0001-5026-095X
authors.initials: S
authors.lastname: Citerne
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.) shelley_hepworth@carleton.ca pautot@versailles.inra.fr.
authors.forename: Shelley R
authors.identifier: http://orcid.org/0000-0002-6496-3792
authors.initials: SR
authors.lastname: Hepworth
authors.affiliation: Department of Biology, Carleton University, Ottawa, Ontario, Canada K1S 5B6 (M.K., P.T., B.C.S., S.Ch., J.L., S.R.H.);Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique-AgroParisTech, Bâtiment 2, Institut National de la Recherche Agronomique Centre de Versailles-Grignon, 78026 Versailles cedex, France (L.R., H.M., J.-P.R., S.Ci., V.P.); Plant Biotechnology Institute,National Research Council Canada, Saskatoon, Saskatchewan, Canada S7N 0W9 (R.D., C.Y., D.X.);Department of Biological Sciences, Brock University, St. Catharines, Ontario, Canada L2S 3A1 (X.K, C.D.); andMolecular Plant Physiology, Department of Biology, Faculty of Sciences, Utrecht University, CH-3584 Utrecht, The Netherlands (M.P.) shelley_hepworth@carleton.ca pautot@versailles.inra.fr.
authors.forename: Véronique
authors.identifier: http://orcid.org/0000-0003-1808-5172
authors.initials: V
authors.lastname: Pautot
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development / Q000502:physiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D003517:Cyclopentanes / Q000378:metabolism; D035264:Flowers / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D018506:Gene Expression Regulation, Plant; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism*; D018519:Meristem / Q000235:genetics / Q000254:growth & development / Q000502:physiology; D035683:MicroRNAs / Q000235:genetics; D009154:Mutation; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D054883:Oxylipins / Q000378:metabolism; D010937:Plant Growth Regulators / Q000378:metabolism; D012097:Repressor Proteins / Q000235:genetics / Q000378:metabolism*; D012098:Reproduction; D015398:Signal Transduction
chemical_list: D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D018398:Homeodomain Proteins; D035683:MicroRNAs; D009687:Nuclear Proteins; D054883:Oxylipins; D010937:Plant Growth Regulators; D012097:Repressor Proteins; C487569:RPL protein, Arabidopsis; C496963:BOP1 protein, Arabidopsis; C506721:BOP2 protein, Arabidopsis; C559759:Mirn156 microRNA, Arabidopsis; C543702:Mirn172 microRNA, Arabidopsis; C561284:PNF protein, Arabidopsis; C416221:SPL protein, Arabidopsis; C011006:jasmonic acid