Multiple MONOPTEROS-Dependent Pathways Are Involved in Leaf Initiation1[C][W][OA]

Initiation of leaves at the flanks of the shoot apical meristem occurs at sites of auxin accumulation and pronounced expression of auxin-inducible PIN-FORMED1 (PIN) genes, suggesting a feedback loop to progressively focus auxin in concrete spots. Because PIN expression is regulated by auxin response factor activity, including MONOPTEROS (MP), it appeared possible that MP affects leaf formation as a positive regulator of PIN genes and auxin transport. Here, we analyze a novel, completely leafless phenotype arising from simultaneous interference with both auxin signaling and auxin transport. We show that mp pin1 double mutants, as well as mp mutants treated with auxin-efflux inhibitors, display synergistic abnormalities not seen in wild type regardless of how strongly auxin transport was reduced. The synergism of abnormalities indicates that the role of MP in shoot meristem organization is not limited to auxin transport regulation. In the mp mutant background, auxin transport inhibition completely abolishes leaf formation. Instead of forming leaves, the abnormal shoot meristems dramatically increase in size, harboring correspondingly enlarged expression domains of CLAVATA3 and SHOOTMERISTEMLESS, molecular markers for the central stem cell zone and the complete meristem, respectively. The observed synergism under conditions of auxin efflux inhibition was further supported by an unrestricted PIN1 expression in mp meristems, as compared to a partial restriction in wild-type meristems. Auxin transport-inhibited mp meristems also lacked detectable auxin maxima. We conclude that MP promotes the focusing of auxin and leaf initiation in part through pathways not affected by auxin efflux inhibitors.

• Publication year

  2008

• Venue

  Plant Physiology

• Publication date

  2008-08-08

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1104/pp.108.119396PMID 18685044PMCID PMC2556819
• 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.

• Connecting the paths in plant stem cell regulation.

  2007cited by this paper
• Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana.

  2007cited by this paper
• Mutations in the TORNADO2 gene affect cellular decisions in the peripheral zone of the shoot apical meristem of Arabidopsisthaliana

  2007cited by this paper
• Molecular and cellular aspects of auxin-transport-mediated development.

  2007cited by this paper
• Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity.

  2006cited by this paper
• A plausible model of phyllotaxis

  2006cited by this paper
• An auxin-driven polarized transport model for phyllotaxis

  2006cited by this paper
• PIN Proteins Perform a Rate-Limiting Function in Cellular Auxin Efflux

  2006cited by this paper
• PINOID Positively Regulates Auxin Efflux in Arabidopsis Root Hair Cells and Tobacco Cells[W]

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

  2006cited by this paper
• The role of hormones in shoot apical meristem function.

  2006cited by this paper
• Dynamic integration of auxin transport and signalling.

  2006influential reference
• Cell Differentiation and Organ Initiation at the Shoot Apical Meristem

  2006cited by this paper
• TCP Transcription Factors Control the Morphology of Shoot Lateral Organs via Negative Regulation of the Expression of Boundary-Specific Genes in Arabidopsis[W][OA]

  2006cited by this paper
• Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem

  2005influential reference
• CORONA, a Member of the Class III Homeodomain Leucine Zipper Gene Family in Arabidopsis, Regulates Stem Cell Specification and Organogenesisw⃞

  2005cited by this paper
• Stem cell regulation in the Arabidopsis shoot apical meristem.

  2005cited by this paper
• Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression

  2005cited by this paper
• Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization

  2004cited by this paper
• PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis

  2004cited by this paper
• A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux

  2004influential reference
• Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana

  2004cited by this paper
• Enlarged meristems and delayed growth in plp mutants result from lack of CaaX prenyltransferases.

  2004cited by this paper
• Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4

  2004cited by this paper
• Regulation of phyllotaxis by polar auxin transport

  2003influential reference
• Auxin Signaling in Arabidopsis Leaf Vascular Development1

  2003cited by this paper
• Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1

  2003cited by this paper
• CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation.

  2003cited by this paper
• The DORNROSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem ccll fate and lateral organ development.

  2003influential reference
• The CUP-SHAPED COTYLEDON3 Gene Is Required for Boundary and Shoot Meristem Formation in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012203.

  2003cited by this paper
• Local, efflux-dependent auxin gradients as a common module for plant organ formation.

  2003influential reference
• YABBY Polarity Genes Mediate the Repression of KNOX Homeobox Genes in Arabidopsis

  2002cited by this paper
• The role of regulated protein degradation in auxin response

  2002cited by this paper
• ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis.

  2002cited by this paper
• Genetics of Aux/IAA and ARF action in plant growth and development

  2002cited by this paper
• The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport.

  2001cited by this paper
• Polar auxin transport: controlling where and how much.

  2001cited by this paper
• Cell signalling at the shoot meristem

  2001cited by this paper
• PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem.

  2000cited by this paper
• In situ analysis of RNA and protein expression in whole mounts facilitates detection of floral gene expression dynamics.

  2000influential reference
• Initiation of axillary and floral meristems in Arabidopsis.

  2000cited by this paper
• Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs

  2000cited by this paper
• Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis

  2000influential reference
• Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis.

  2000cited by this paper
• Mechanisms that control knox gene expression in the Arabidopsis shoot.

  2000cited by this paper
• Regulation of auxin response by the protein kinase PINOID.

  2000cited by this paper
• The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes.

  2000cited by this paper
• Plant Microtechnique and Microscopy

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

  1999cited by this paper
• Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes.

  1999cited by this paper
• Dimerization and DNA binding of auxin response factors.

  1999cited by this paper
• Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems.

  1999cited by this paper
• A molecular basis for auxin action.

  1999cited by this paper
• The ARF family of transcription factors and their role in plant hormone-responsive transcription

  1998cited by this paper
• The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development

  1998cited by this paper
• The development of apical embryonic pattern in Arabidopsis.

  1998cited by this paper
• Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.

  1998cited by this paper
• Protein-protein interactions among the Aux/IAA proteins.

  1997cited by this paper
• Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.

  1997cited by this paper
• Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.

  1997influential reference
• A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis

  1996cited by this paper
• KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis.

  1996cited by this paper
• AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth.

  1996cited by this paper
• CLAVATA3 IS A SPECIFIC REGULATOR OF SHOOT AND FLORAL MERISTEM DEVELOPMENT AFFECTING THE SAME PROCESSES AS CLAVATA1

  1995cited by this paper
• Morphogenesis in pinoid mutants of Arabidopsis thaliana

  1995cited by this paper
• CLAVATA1, a regulator of meristem and flower development in Arabidopsis.

  1993cited by this paper
• amp1 ‐ a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering

  1993cited by this paper
• The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo

  1993cited by this paper
• Normal and Abnormal Development in the Arabidopsis Vegetative Shoot Apex.

  1992cited by this paper
• Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation.

  1991influential reference
• Growth and development of the axr1 mutants of Arabidopsis.

  1990cited by this paper
• CHANGES IN EPILOBIUM PHYLLOTAXY INDUCED BY N‐1‐NAPHTHYLPHTHALAMIC ACID AND α‐4‐CHLOROPHENOXYISOBUTYRIC ACID

  1981cited by this paper
• Patterns in plant development: Subject index

  1972cited by this paper
• On the mechanism of electrocrystallization

  1972cited by this paper
• Literature cited

  1924cited by this paper

• TMO5 regulates PIN1 polarity convergence and organogenesis downstream of MONOPTEROS in the Arabidopsis shoot

  2025cites this paper
• The homeodomain of the Raphanus sativus WOX4 binds to the promoter of the LOG3 cytokinin biosynthesis gene

  2024cites this paper
• The vascular development-related transcription factor BoSCR participates in leaf development by regulating BoPIN1 expression in ornamental kale

  2024cites this paper
• Characterization of the Arabidopsis mutant oligocellula6-D reveals the importance of leaf initiation in determining final leaf size.

  2024cites this paper
• Functional Modules in the Meristems: “Tinkering” in Action

  2023cites this paper
• Nitric Oxide Alters the Pattern of Auxin Maxima and PIN-FORMED1 During Shoot Development

  2021cites this paper
• OsARF11 Promotes Growth, Meristem, Seed, and Vein Formation during Rice Plant Development

  2021cites this paper
• Integration of Core Mechanisms Underlying Plant Aerial Architecture

  2021cites this paper
• The role of auxin and sugar signaling in dominance inhibition of inflorescence growth by fruit load

  2021cites this paper
• Identification of Auxin Response Factor-Encoding Genes Expressed in Distinct Phases of Leaf Vein Development and with Overlapping Functions in Leaf Formation

  2019cites this paper
• Functional Coordination of the Chromatin-Remodeling Factor AtINO80 and the Histone Chaperones NRP1/2 in Inflorescence Meristem and Root Apical Meristem

  2019cites this paper
• The Diverse Roles of Auxin in Regulating Leaf Development

  2019cites this paper
• Coordination of tissue cell polarity by auxin transport and signaling

  2019cites this paper
• Auxin and above-ground meristems

  2018cites this paper
• Identification des modules de la signalisation auxinique impliqués dans la morphogenèse foliaire

  2017influential citation
• Regulation of shoot apical meristem activity

  2017influential citation
• Cis-regulatory Elements Controlling Expression of the Auxin Response Factor MONOPTEROS and its Irrepressible Variant MP∆

  2017influential citation
• Transcriptional Responses to the Auxin Hormone.

  2016cites this paper
• Molecular Mechanisms of Floral Boundary Formation in Arabidopsis

  2016cites this paper
• Genetic analysis of the role of the OsARF11 gene in rice development

  2016influential citation
• Beyond the Divide: Boundaries for Patterning and Stem Cell Regulation in Plants

  2015cites this paper
• Organogenesis in plants: initiation and elaboration of leaves.

  2015cites this paper
• Overcoming recalcitrance - Auxin response factor functions in plant regeneration

  2015cites this paper
• Cell walls as a stage for intercellular communication regulating shoot meristem development

  2015cites this paper
• Translational Control of Arabidopsis Meristem Stability and Organogenesis by the Eukaryotic Translation Factor eIF3h

  2014cites this paper
• MONOPTEROS directly activates the auxin-inducible promoter of the Dof5.8 transcription factor gene in Arabidopsis thaliana leaf provascular cells

  2014cites this paper
• LEAFY and Polar Auxin Transport Coordinately Regulate Arabidopsis Flower Development

  2014cites this paper
• Regulation of plant translation by upstream open reading frames.

  2014cites this paper
• incurvata 13 , a Novel Allele of AUXIN RESISTANT 6 , Reveals a Speci fi c Role for Auxin and the SCF Complex in Arabidopsis Embryogenesis , Vascular Speci fi cation , and Leaf Flatness 1

  2013cites this paper
• The plant vascular system: evolution, development and functions.

  2013cites this paper
• ERECTA Family Genes Regulate Auxin Transport in the Shoot Apical Meristem and Forming Leaf Primordia1[C][W][OPEN]

  2013cites this paper
• Hormone interactions in xylem development: a matter of signals

  2013cites this paper
• incurvata13, a Novel Allele of AUXIN RESISTANT6, Reveals a Specific Role for Auxin and the SCF Complex in Arabidopsis Embryogenesis, Vascular Specification, and Leaf Flatness1[W][OA]

  2013cites this paper
• Unifoliata-Afila interactions in pea leaf morphogenesis.

  2013cites this paper
• Organogenesis in Vitro under Altered Auxin Signaling Conditions

  2013influential citation
• Regulation of Auxin Transport in Arabidopsis Leaf Vascular Development

  2012influential citation
• The roles of SHORT INTERNODES/STYLISH genes, regulators of auxin homeostasis, during leaf vein development in Arabidopsis thaliana

  2012cites this paper
• A novel, semi-dominant allele of MONOPTEROS provides insight into leaf initiation and vein pattern formation

  2012cites this paper
• Patterning the embryo in higher plants: Emerging pathways and challenges

  2011cites this paper
• Organogenesis from stem cells in planta: multiple feedback loops integrating molecular and mechanical signals

  2011cites this paper
• Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo.

  2010cites this paper
• Expression of a gymnosperm PIN homologous gene correlates with auxin immunolocalization pattern at cotyledon formation and in demarcation of the procambium during Picea abies somatic embryo development and in seedling tissues.

  2010cites this paper
• Translation reinitiation and development are compromised in similar ways by mutations in translation initiation factor eIF3h and the ribosomal protein RPL24

  2010cites this paper
• Vascular pattern formation in plants.

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

  2010cites this paper
• The roles of auxin signaling and transport in leaf initiation and vascular pattern formation in arabidopsis thaliana

  2009influential citation
• A gain-of-function mutation in IAA18 alters Arabidopsis embryonic apical patterning

  2009cites this paper
• Meristematic sculpting in fruit development.

  2009cites this paper
• Microdissection of Shoot Meristem Functional Domains

  2009cites this paper
• Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves

  2009cites this paper
• Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology?

  2009cites this paper