Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module.

The role of auxin as main regulator of vascular differentiation is well established, and a direct correlation between the rate of xylem differentiation and the amount of auxin reaching the (pro)cambial cells has been proposed. It has been suggested that thermospermine produced by ACAULIS5 (ACL5) and bushy and dwarf2 (BUD2) is one of the factors downstream to auxin contributing to the regulation of this process in Arabidopsis. Here, we provide an in-depth characterization of the mechanism through which ACL5 modulates xylem differentiation. We show that an increased level of ACL5 slows down xylem differentiation by negatively affecting the expression of homeodomain-leucine zipper (HD-ZIP) III and key auxin signaling genes. This mechanism involves the positive regulation of thermospermine biosynthesis by the HD-ZIP III protein Arabidopsis thaliana homeobox8 tightly controlling the expression of ACL5 and BUD2. In addition, we show that the HD-ZIP III protein REVOLUTA contributes to the increased leaf vascularization and long hypocotyl phenotype of acl5 likely by a direct regulation of auxin signaling genes such as like auxin resistant2 (LAX2) and LAX3. We propose that proper formation and differentiation of xylem depend on a balance between positive and negative feedback loops operating through HD-ZIP III genes.

• Publication year

  2014

• Venue

  Molecular Plant

• Publication date

  2014-06-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1093/mp/ssu051PMID 24777988
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Arabidopsis KANADI1 Acts as a Transcriptional Repressor by Interacting with a Specific cis-Element and Regulates Auxin Biosynthesis, Transport, and Signaling in Opposition to HD-ZIPIII Factors[W]

  2014cited by this paper
• The Arabidopsis leaf provascular cell transcriptome is enriched in genes with roles in vein patterning.

  2013cited by this paper
• Patterning of Leaf Vein Networks by Convergent Auxin Transport Pathways

  2013cited by this paper
• Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem.

  2013cited by this paper
• A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis.

  2013cited by this paper
• Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses.

  2012cited by this paper
• Thermospermine is not a minor polyamine in the plant kingdom.

  2012cited by this paper
• AUX/LAX Genes Encode a Family of Auxin Influx Transporters That Perform Distinct Functions during Arabidopsis Development[C][W]

  2012cited by this paper
• Linking photoreceptor excitation to changes in plant architecture.

  2012cited by this paper
• A chemical biology approach reveals an opposite action between thermospermine and auxin in xylem development in Arabidopsis thaliana.

  2012cited by this paper
• PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature

  2011cited by this paper
• Arabidopsis as a model for wood formation.

  2011cited by this paper
• Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation

  2010cited by this paper
• Hormonal control of the shoot stem-cell niche

  2010cited by this paper
• Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate

  2010cited by this paper
• The BUD2 mutation affects plant architecture through altering cytokinin and auxin responses in Arabidopsis

  2010cited by this paper
• Control of leaf and vein development by auxin.

  2010cited by this paper
• Norspermine substitutes for thermospermine in the control of stem elongation in Arabidopsis thaliana

  2010cited by this paper
• Regulatory mechanisms for specification and patterning of plant vascular tissues.

  2010cited by this paper
• Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves

  2009cited by this paper
• Identifying New Components Participating in the Secondary Cell Wall Formation of Vessel Elements in Zinnia and Arabidopsis[W]

  2009cited by this paper
• Stem cell function during plant vascular development

  2009cited by this paper
• Standardization of real-time PCR gene expression data from independent biological replicates.

  2008cited by this paper
• ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death

  2008cited by this paper
• Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system

  2008cited by this paper
• Thermospermine is required for stem elongation in Arabidopsis thaliana.

  2008cited by this paper
• TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.

  2008cited by this paper
• Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana.

  2007cited by this paper
• Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine

  2007cited by this paper
• Regulation of HD-ZIP III Genes by MicroRNA 165

  2007cited by this paper
• Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis.

  2007cited by this paper
• Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY

  2007cited by this paper
• oneChannelGUI: a graphical interface to Bioconductor tools, designed for life scientists who are not familiar with R language

  2007cited by this paper
• Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity.

  2007cited by this paper
• BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development

  2006cited by this paper
• Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis.

  2006cited by this paper
• Control of leaf vascular patterning by polar auxin transport.

  2006cited by this paper
• Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity.

  2006cited by this paper
• The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene

  2006cited by this paper
• Arabidopsis thickvein Mutation Affects Vein Thickness and Organ Vascularization, and Resides in a Provascular Cell-Specific Spermine Synthase Involved in Vein Definition and in Polar Auxin Transport1

  2005cited by this paper
• The PIN auxin efflux facilitators: evolutionary and functional perspectives.

  2005cited by this paper
• Auxin inhibits endocytosis and promotes its own efflux from cells

  2005cited by this paper
• Class III homeodomain leucine-zipper proteins regulate xylem cell differentiation.

  2005cited by this paper
• Transcription switches for protoxylem and metaxylem vessel formation.

  2005cited by this paper
• Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency.

  2005cited by this paper
• Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation

  2004cited by this paper
• GO: : TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes

  2004cited by this paper
• BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis

  2004cited by this paper
• PIN and AUX/LAX proteins: their role in auxin accumulation.

  2004cited by this paper
• Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments

  2004cited by this paper
• HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation.

  2003cited by this paper
• Auxin Signaling in Arabidopsis Leaf Vascular Development1

  2003cited by this paper
• Arabidopsis : a laboratory manual

  2002cited by this paper
• VH1, a Provascular Cell–Specific Receptor Kinase That Influences Leaf Cell Patterns in Arabidopsis

  2002cited by this paper
• The arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems.

  2001cited by this paper
• Alteration of auxin polar transport in the Arabidopsis ifl1 mutants.

  2001cited by this paper
• Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.

  2001cited by this paper
• Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases.

  2000cited by this paper
• ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase

  2000cited by this paper
• Auxin is required for leaf vein pattern in Arabidopsis.

  1999cited by this paper
• IFL1, a Gene Regulating Interfascicular Fiber Differentiation in Arabidopsis, Encodes a Homeodomain-Leucine Zipper Protein

  1999cited by this paper
• Responses of plant vascular systems to auxin transport inhibition.

  1999cited by this paper
• The Arabidopsis Athb-8, -9 and genes are members of a small gene family coding for highly related HD-ZIP proteins

  1998cited by this paper
• Long-distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants

  1998cited by this paper
• ACL5: an Arabidopsis gene required for internodal elongation after flowering.

  1997cited by this paper
• The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana.

  1995cited by this paper
• Polyamine content and translocation in soybean plants

  1993cited by this paper
• The Athb‐1 and −2 HD‐Zip domains homodimerize forming complexes of different DNA binding specificities.

  1993cited by this paper
• GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants.

  1987cited by this paper
• The control of vessel size and density along the plant axis: a new hypothesis

  1983cited by this paper
• The Control of the Patterned Differentiation of Vascular Tissues

  1981cited by this paper

• Recruitment of bifunctional regulator thermospermine to methylated ribosomes directs xylem fate.

  2026cites this paper
• Rewiring vascular patterning through translational control in Arabidopsis

  2026cites this paper
• Regulatory Mechanisms Underlying Stem Strength and Toughness in Dicotyledonous Plants: Implications for Soybean Breeding.

  2026cites this paper
• Gene regulation of structural support in plants: impacts of downregulation on growth and resilience

  2026cites this paper
• Molecular Insights into DNA Recognition by HD-Zip Transcription Factors.

  2025cites this paper
• Identification of crucial genes sustaining the curled leaf phenotype in perennial transgenic poplar via advanced proteomic and phosphoproteomic analyses.

  2025cites this paper
• Coordination and regulation of vascular development in roots.

  2025cites this paper
• Duckweed genomes and epigenomes underlie triploid hybridization and clonal reproduction.

  2025cites this paper
• The response to thermospermine is fine-tuned by the balance between SAC51 and LHW family proteins in Arabidopsis thaliana

  2025cites this paper
• Divergent evolution of a thermospermine-dependent regulatory pathway in land plants.

  2024cites this paper
• Quantification of Xylem-Specific Thermospermine-Dependent Translation of SACL Transcripts with Dual Luciferase Reporter System.

  2024cites this paper
• TARGET OF MONOPTEROS (TMO)：A key type of Transcription Factors Orchestrating Plant Development and Environmental Response.

  2024cites this paper
• A Solanum lycopersicum polyamine oxidase contributes to the control of plant growth, xylem differentiation, and drought stress tolerance.

  2024cites this paper
• ACL5 acquired strict thermospermine synthesis activity during the emergence of vascular plants

  2024cites this paper
• GhHB14_D10 and GhREV_D5, two HD-ZIP III transcription factors, play a regulatory role in cotton fiber secondary cell wall biosynthesis

  2024cites this paper
• The Ins and Outs of Homeodomain-Leucine Zipper/Hormone Networks in the Regulation of Plant Development

  2024cites this paper
• Hormonal control of the molecular networks guiding vascular tissue development in the primary root meristem of Arabidopsis thaliana.

  2023cites this paper
• The microRNA7833-AUX6 module plays a critical role in wood development by modulating cellular auxin influx in Populus tomentosa.

  2023cites this paper
• Suppression of the dwarf phenotype of an Arabidopsis mutant defective in thermospermine biosynthesis by a synonymous codon change in the SAC51 uORF

  2023cites this paper
• The genomes and epigenomes of aquatic plants (Lemnaceae) promote triploid hybridization and clonal reproduction

  2023cites this paper
• HD-ZIP III-dependent local promotion of brassinosteroid synthesis suppresses vascular cell division in Arabidopsis root apical meristem

  2023cites this paper
• Genome-Wide Identification of the HD-ZIP III Subfamily in Upland Cotton Reveals the Involvement of GhHB8-5D in the Biosynthesis of Secondary Wall in Fiber and Drought Resistance

  2022cites this paper
• CkREV regulates xylem vessel development in Caragana korshinskii in response to drought

  2022cites this paper
• Loss of function of an Arabidopsis homologue of JMJD6 suppresses the dwarf phenotype of acl5, a mutant defective in thermospermine biosynthesis

  2022cites this paper
• The HD-Zip transcription factor SlHB15A regulates abscission by modulating jasmonoyl-isoleucine biosynthesis.

  2022cites this paper
• CkREV Enhances the Drought Resistance of Caragana korshinskii through Regulating the Expression of Auxin Synthetase Gene CkYUC5

  2022cites this paper
• Current status and perspectives on the role of polyamines in plant immunity

  2021cites this paper
• Hydro-Electro Hybrid Priming Promotes Carrot (Daucus carota L.) Seed Germination by Activating Lipid Utilization and Respiratory Metabolism

  2021cites this paper
• Plant Copper Amine Oxidases: Key Players in Hormone Signaling Leading to Stress-Induced Phenotypic Plasticity

  2021cites this paper
• Overexpression of PtoCYCD3;3 Promotes Growth and Causes Leaf Wrinkle and Branch Appearance in Populus

  2021cites this paper
• Multi-level analysis of the interactions between REVOLUTA and MORE AXILLARY BRANCHES 2 in controlling plant development reveals parallel, independent and antagonistic functions

  2020cites this paper
• Plant vascular development: mechanisms and environmental regulation

  2020cites this paper
• HD-ZIPs govern vascular cell fate: An HD view on patterning and

  2020cites this paper
• ACAULIS5 Is Required for Cytokinin Accumulation and Function During Secondary Growth of Populus Trees

  2020cites this paper
• Control of vein-forming, striped gene expression by auxin signaling

  2020cites this paper
• Putrescine metabolism modulates the biphasic effects of brassinosteroids on canola and Arabidopsis salt tolerance.

  2020cites this paper
• Light affects tissue patterning of the hypocotyl in the shade-avoidance response

  2020cites this paper
• Leaf-Wounding Long-Distance Signaling Targets AtCuAOβ Leading to Root Phenotypic Plasticity

  2020cites this paper
• Identification of Conserved Gene-Regulatory Networks that Integrate Environmental Sensing and Growth in the Root Cambium.

  2020cites this paper
• Local and Systemic Effects of Brassinosteroid Perception in Developing Phloem.

  2020cites this paper
• Effect of Thermospermine on the Growth and Expression of Polyamine-Related Genes in Rice Seedlings

  2019cites this paper
• Auxin-mediated Aux/IAA-ARF-HB signaling cascade regulates secondary xylem development in Populus.

  2019cites this paper
• How plants grow up.

  2019cites this paper
• Integrated analysis of high-throughput sequencing data shows abscisic acid-responsive genes and miRNAs in strawberry receptacle fruit ripening

  2019cites this paper
• A transcriptional analysis reveals an extensive range of genes responsible for increasing the tolerance of Carrizo citrange to oxygen deficiency

  2019cites this paper
• How to organize bidirectional tissue production?

  2019cites this paper
• Polyamines as Quality Control Metabolites Operating at the Post-Transcriptional Level

  2019cites this paper
• Transcriptome dynamics of cork oak (Quercus suber) somatic embryogenesis reveals active gene players in transcription regulation and phytohormone homeostasis of embryo development

  2019cites this paper
• Conservation of Thermospermine Synthase Activity in Vascular and Non-vascular Plants

  2019cites this paper
• A positive feedback loop comprising LHW-TMO5 and local auxin biosynthesis regulates initial vascular development in Arabidopsis roots.

  2019cites this paper
• Cell wall composition and transcriptomics in stem tissues of stinging nettle (Urtica dioica L.): Spotlight on a neglected fibre crop

  2019cites this paper
• Thermospermine Synthase (ACL5) and Diamine Oxidase (DAO) Expression Is Needed for Zygotic Embryogenesis and Vascular Development in Scots Pine

  2019cites this paper
• A PXY-Mediated Transcriptional Network Integrates Signaling Mechanisms to Control Vascular Development in Arabidopsis[OPEN]

  2019cites this paper
• North, East, South, West: mapping vascular tissues onto the Arabidopsis root.

  2018cites this paper
• Multiple Pathways in the Control of the Shade Avoidance Response

  2018cites this paper
• Multiple Links between HD-Zip Proteins and Hormone Networks

  2018cites this paper
• Molecules for Sensing Polyamines and Transducing Their Action in Plants.

  2018cites this paper
• A galling insect activates plant reproductive programs during gall development

  2018cites this paper
• Secondary development in the stem: when Arabidopsis and trees are closer than it seems.

  2017cites this paper
• Class III HD-ZIPs govern vascular cell fate: an HD view on patterning and differentiation.

  2017influential citation
• Secondary growth as a determinant of plant shape and form.

  2017cites this paper
• The shady side of leaf development: the role of the REVOLUTA/KANADI1 module in leaf patterning and auxin-mediated growth promotion.

  2017cites this paper
• Genetic Networks in Plant Vascular Development.

  2017cites this paper
• Regulation of vascular cell division.

  2017cites this paper
• Altered expression of polyamine transporters reveals a role for spermidine in the timing of flowering and other developmental response pathways.

  2017cites this paper
• Spatial specificity of auxin responses coordinates wood formation

  2017cites this paper
• A role for LAX2 in regulating xylem development and lateral-vein symmetry in the leaf

  2017cites this paper
• The Arabidopsis polyamine oxidase/dehydrogenase 5 interferes with cytokinin and auxin signaling pathways to control xylem differentiation

  2017cites this paper
• Polyamine metabolism and activation of lipid signalling pathways in Arabidopsis thaliana

  2017cites this paper
• Realizing pipe dreams – a detailed picture of vascular development

  2016cites this paper
• Transcriptional Regulation of Gene Expression at Early Stages of Arabidopsis Vein Development

  2016cites this paper
• A Predictive Coexpression Network Identifies Novel Genes Controlling the Seed-to-Seedling Phase Transition in Arabidopsis thaliana1[OPEN]

  2016cites this paper
• The SAC51 Family Plays a Central Role in Thermospermine Responses in Arabidopsis.

  2016influential citation
• Chemical control of xylem differentiation by thermospermine, xylemin, and auxin

  2016cites this paper
• Comparative Analysis of miRNAs and Their Target Transcripts between a Spontaneous Late-Ripening Sweet Orange Mutant and Its Wild-Type Using Small RNA and Degradome Sequencing

  2016cites this paper
• 1,3-di(benzo[d]oxazol-5-yl)urea acts as either adventitious rooting adjuvant or xylogenesis enhancer in carob and pine microcuttings depending on the presence/absence of exogenous indole-3-butyric acid

  2016influential citation
• Moderate stress responses and specific changes in polyamine metabolism characterize Scots pine somatic embryogenesis.

  2016cites this paper
• Genetic and hormonal control of vascular tissue proliferation.

  2016cites this paper
• Functional mechanism of bHLH complexes during early vascular development.

  2016cites this paper
• SCUOLA DOTTORALE IN BIOLOGIA XXVIII Ciclo Sezione “Scienze Biomolecolari e Cellulari” Molecular and physiological aspects regarding the Arabidopsis polyamine oxidase gene family

  2016influential citation
• Arabidopsis SHR and SCR transcription factors and AUX1 auxin influx carrier control the switch between adventitious rooting and xylogenesis in planta and in in vitro cultured thin cell layers

  2015cites this paper
• Control of vein network topology by auxin transport

  2015cites this paper
• Meta-Analysis of Arabidopsis KANADI1 Direct Target Genes Identifies a Basic Growth-Promoting Module Acting Upstream of Hormonal Signaling Pathways1[OPEN]

  2015cites this paper
• Mutations in Ribosomal Proteins, RPL4 and RACK1, Suppress the Phenotype of a Thermospermine-Deficient Mutant of Arabidopsis thaliana

  2015cites this paper
• Interplay of HD-Zip II and III transcription factors in auxin-regulated plant development.

  2015cites this paper
• Cell Wall Amine Oxidases: New Players in Root Xylem Differentiation under Stress Conditions

  2015cites this paper
• A Negative Feedback Loop Controlling bHLH Complexes Is Involved in Vascular Cell Division and Differentiation in the Root Apical Meristem.

  2015cites this paper
• PHABULOSA Mediates an Auxin Signaling Loop to Regulate Vascular Patterning in Arabidopsis1[OPEN]

  2015influential citation
• Xylem development - from the cradle to the grave.

  2015cites this paper
• A bHLH-Based Feedback Loop Restricts Vascular Cell Proliferation in Plants.

  2015cites this paper
• (Pro)cambium formation and proliferation: two sides of the same coin?

  2014cites this paper