title: Spatio-temporal sequence of cross-regulatory events in root meristem growth.
abstract: A central question in developmental biology is how multicellular organisms coordinate cell division and differentiation to determine organ size. In Arabidopsis roots, this balance is controlled by cytokinin-induced expression of SHORT HYPOCOTYL 2 (SHY2) in the so-called transition zone of the meristem, where SHY2 negatively regulates auxin response factors (ARFs) by protein-protein interaction. The resulting down-regulation of PIN-FORMED (PIN) auxin efflux carriers is considered the key event in promoting differentiation of meristematic cells. Here we show that this regulation involves additional, intermediary factors and is spatio-temporally constrained. We found that the described cytokinin-auxin crosstalk antagonizes BREVIS RADIX (BRX) activity in the developing protophloem. BRX is an auxin-responsive target of the prototypical ARF MONOPTEROS (MP), a key promoter of vascular development, and transiently enhances PIN3 expression to promote meristem growth in young roots. At later stages, cytokinin induction of SHY2 in the vascular transition zone restricts BRX expression to down-regulate PIN3 and thus limit meristem growth. Interestingly, proper SHY2 expression requires BRX, which could reflect feedback on the auxin responsiveness of SHY2 because BRX protein can directly interact with MP, likely acting as a cofactor. Thus, cross-regulatory antagonism between BRX and SHY2 could determine ARF activity in the protophloem. Our data suggest a model in which the regulatory interactions favor BRX expression in the early proximal meristem and SHY2 prevails because of supplementary cytokinin induction in the later distal meristem. The complex equilibrium of this regulatory module might represent a universal switch in the transition toward differentiation in various developmental contexts.
authors.affiliation: Department of Plant Molecular Biology, University of Lausanne, CH-1015 Lausanne, Switzerland.
authors.forename: Emanuele
authors.initials: E
authors.lastname: Scacchi
authors.forename: Paula
authors.initials: P
authors.lastname: Salinas
authors.forename: Bojan
authors.initials: B
authors.lastname: Gujas
authors.forename: Luca
authors.initials: L
authors.lastname: Santuari
authors.forename: Naden
authors.initials: N
authors.lastname: Krogan
authors.forename: Laura
authors.initials: L
authors.lastname: Ragni
authors.forename: Thomas
authors.initials: T
authors.lastname: Berleth
authors.forename: Christian S
authors.initials: CS
authors.lastname: Hardtke
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D015153:Blotting, Western; D003583:Cytokinins / Q000494:pharmacology; D004268:DNA-Binding Proteins / Q000235:genetics / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental / Q000187:drug effects; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D005966:Glucuronidase / Q000235:genetics / Q000378:metabolism; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D007210:Indoleacetic Acids / Q000494:pharmacology; D018519:Meristem / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D018613:Microscopy, Confocal; D009154:Mutation; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D010937:Plant Growth Regulators / Q000494:pharmacology; D018517:Plant Roots / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D030821:Plants, Genetically Modified; D020133:Reverse Transcriptase Polymerase Chain Reaction; D013997:Time Factors; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; C483078:BREVIS RADIX protein, Arabidopsis; D003583:Cytokinins; D004268:DNA-Binding Proteins; D007210:Indoleacetic Acids; C111371:MONOPTEROS protein, Arabidopsis; D009687:Nuclear Proteins; C449300:PIN3 protein, Arabidopsis; D010937:Plant Growth Regulators; C117994:SHY2 protein, Arabidopsis; D014157:Transcription Factors; D049452:Green Fluorescent Proteins; D005966:Glucuronidase