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2.
Plant Cell Rep ; 33(1): 1-21, 2014 Jan.
Article in English | MEDLINE | ID: mdl-23903948

ABSTRACT

Microtubules are subcellular nanotubes composed of α- and ß-tubulin that arise from microtubule nucleation sites, mainly composed of γ-tubulin complexes [corrected]. Cell wall encased plant cells have evolved four distinct microtubule arrays that regulate cell division and expansion. Microtubule-associated proteins, the so called MAPs, construct, destruct and reorganize microtubule arrays thus regulating their spatiotemporal transitions during the cell cycle. By physically binding to microtubules and/or modulating their functions, MAPs control microtubule dynamic instability and/or interfilament cross talk. We survey the recent analyses of Arabidopsis MAPs such as MAP65, MOR1, CLASP, katanin, TON1, FASS, TRM, TAN1 and kinesins in terms of their effects on microtubule array organizations and plant development.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Microtubule-Associated Proteins/metabolism , Microtubules/metabolism , Protein Binding
3.
Plant Physiol ; 162(1): 304-18, 2013 May.
Article in English | MEDLINE | ID: mdl-23542149

ABSTRACT

Plant roots are colonized by an immense number of microbes, referred to as the root microbiome. Selected strains of beneficial soil-borne bacteria can protect against abiotic stress and prime the plant immune system against a broad range of pathogens. Pseudomonas spp. rhizobacteria represent one of the most abundant genera of the root microbiome. Here, by employing a germ-free experimental system, we demonstrate the ability of selected Pseudomonas spp. strains to promote plant growth and drive developmental plasticity in the roots of Arabidopsis (Arabidopsis thaliana) by inhibiting primary root elongation and promoting lateral root and root hair formation. By studying cell type-specific developmental markers and employing genetic and pharmacological approaches, we demonstrate the crucial role of auxin signaling and transport in rhizobacteria-stimulated changes in the root system architecture of Arabidopsis. We further show that Pseudomonas spp.-elicited alterations in root morphology and rhizobacteria-mediated systemic immunity are mediated by distinct signaling pathways. This study sheds new light on the ability of soil-borne beneficial bacteria to interfere with postembryonic root developmental programs.


Subject(s)
Arabidopsis/microbiology , Gene Expression Regulation, Plant , Indoleacetic Acids/metabolism , Plant Roots/microbiology , Pseudomonas/physiology , Signal Transduction , Arabidopsis/cytology , Arabidopsis/genetics , Arabidopsis/growth & development , Biological Transport , Gene Expression Regulation, Developmental , Indoleacetic Acids/analysis , Mutation , Phenotype , Plant Roots/cytology , Plant Roots/genetics , Plant Roots/growth & development , Seedlings/cytology , Seedlings/genetics , Seedlings/growth & development , Seedlings/microbiology , Species Specificity
4.
Nature ; 495(7442): 529-33, 2013 Mar 28.
Article in English | MEDLINE | ID: mdl-23515161

ABSTRACT

Recent evidence indicates a correlation between orientation of the plant cortical microtubule cytoskeleton and localization of polar cargoes. However, the molecules and mechanisms that create this correlation have remained unknown. Here we show that, in Arabidopsis thaliana, the microtubule orientation regulators CLASP and MAP65 (refs 3, 4) control the abundance of polarity regulator PINOID kinase at the plasma membrane. By localized upregulation of clathrin-dependent endocytosis at cortical microtubule- and clathrin-rich domains orthogonal to the axis of polarity, PINOID accelerates the removal of auxin transporter PIN proteins from those sites. This mechanism links directional microtubule organization to the polar localization of auxin transporter PIN proteins, and clarifies how microtubule-enriched cell sides are kept distinct from polar delivery domains. Our results identify the molecular machinery that connects microtubule organization to the regulation of the axis of PIN polarization.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Arabidopsis/metabolism , Cell Polarity/physiology , Microtubule-Associated Proteins/metabolism , Microtubules/metabolism , Protein Serine-Threonine Kinases/metabolism , Arabidopsis Proteins/genetics , Cell Membrane/metabolism , Cell Polarity/genetics , Clathrin/metabolism , Endocytosis , Indoleacetic Acids/metabolism , Membrane Transport Proteins/metabolism , Microtubule-Associated Proteins/genetics , Mutant Proteins/genetics , Mutant Proteins/metabolism , Protein Transport
5.
Plant Cell Physiol ; 54(3): 333-42, 2013 Mar.
Article in English | MEDLINE | ID: mdl-23248201

ABSTRACT

Formative cell divisions utilizing precise rotations of cell division planes generate and spatially place asymmetric daughters to produce different cell layers. Therefore, by shaping tissues and organs, formative cell divisions dictate multicellular morphogenesis. In animal formative cell divisions, the orientation of the mitotic spindle and cell division planes relies on intrinsic and extrinsic cortical polarity cues. Plants lack known key players from animals, and cell division planes are determined prior to the mitotic spindle stage. Therefore, it appears that plants have evolved specialized mechanisms to execute formative cell divisions. Despite their profound influence on plant architecture, molecular players and cellular mechanisms regulating formative divisions in plants are not well understood. This is because formative cell divisions in plants have been difficult to track owing to their submerged positions and imprecise timings of occurrence. However, by identifying a spatiotemporally inducible cell division plane switch system applicable for advanced microscopy techniques, recent studies have begun to uncover molecular modules and mechanisms for formative cell divisions. The identified molecular modules comprise developmentally triggered transcriptional cascades feeding onto microtubule regulators that now allow dissection of the hierarchy of the events at better spatiotemporal resolutions. Here, we survey the current advances in understanding of formative cell divisions in plants in the context of embryogenesis, stem cell functionality and post-embryonic organ formation.


Subject(s)
Cell Division , Indoleacetic Acids/metabolism , Plant Development , Plant Growth Regulators/metabolism , Plants/embryology , Arabidopsis/cytology , Arabidopsis/embryology , Arabidopsis/genetics , Arabidopsis/growth & development , Meristem/cytology , Meristem/embryology , Meristem/genetics , Meristem/growth & development , Mutation , Phenotype , Plant Cells , Plant Proteins/genetics , Plant Proteins/metabolism , Plant Roots/cytology , Plant Roots/embryology , Plant Roots/genetics , Plant Roots/growth & development , Plants/genetics , Spindle Apparatus
6.
Cell ; 150(5): 1002-15, 2012 Aug 31.
Article in English | MEDLINE | ID: mdl-22921914

ABSTRACT

In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a "flip flop" that constrains asymmetric cell division to the stem cell region.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Arabidopsis/metabolism , Plant Roots/cytology , Amino Acid Sequence , Asymmetric Cell Division , Cyclin D/metabolism , Cyclin-Dependent Kinases/metabolism , Indoleacetic Acids/metabolism , Mesophyll Cells/metabolism , Molecular Sequence Data , Phosphorylation , Plant Roots/metabolism , Sequence Alignment
7.
Development ; 139(18): 3402-12, 2012 Sep.
Article in English | MEDLINE | ID: mdl-22912415

ABSTRACT

When a plant germinates in the soil, elongation of stem-like organs is enhanced whereas leaf and root growth is inhibited. How these differential growth responses are orchestrated by light and integrated at the organismal level to shape the plant remains to be elucidated. Here, we show that light signals through the master photomorphogenesis repressor COP1 to coordinate root and shoot growth in Arabidopsis. In the shoot, COP1 regulates shoot-to-root auxin transport by controlling the transcription of the auxin efflux carrier gene PIN-FORMED1 (PIN1), thus appropriately tuning shoot-derived auxin levels in the root. This in turn directly influences root elongation and adapts auxin transport and cell proliferation in the root apical meristem by modulating PIN1 and PIN2 intracellular distribution in the root in a COP1-dependent fashion, thus permitting a rapid and precise tuning of root growth to the light environment. Our data identify auxin as a long-distance signal in developmental adaptation to light and illustrate how spatially separated control mechanisms can converge on the same signaling system to coordinate development at the whole plant level.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Indoleacetic Acids/metabolism , Light , Membrane Transport Proteins/metabolism , Plant Roots/metabolism , Plant Shoots/metabolism , Arabidopsis/genetics , Arabidopsis/radiation effects , Arabidopsis Proteins/genetics , Biological Transport/genetics , Biological Transport/radiation effects , Gene Expression Regulation, Plant/genetics , Gene Expression Regulation, Plant/radiation effects , Membrane Transport Proteins/genetics , Plant Roots/genetics , Plant Roots/radiation effects , Plant Shoots/genetics , Plant Shoots/radiation effects , Ubiquitin-Protein Ligases
8.
Curr Biol ; 22(14): 1319-25, 2012 Jul 24.
Article in English | MEDLINE | ID: mdl-22683260

ABSTRACT

PIN-FORMED (PIN) protein-mediated auxin polar transport is critically important for development, pattern formation, and morphogenesis in plants. Auxin has been implicated in the regulation of polar auxin transport by inhibiting PIN endocytosis, but how auxin regulates this process is poorly understood. Our genetic screen identified the Arabidopsis SPIKE1 (SPK1) gene whose loss-of-function mutations increased lateral root density and retarded gravitropic responses, as do pin2 knockout mutations. SPK1 belongs to the conserved DHR2-Dock family of Rho guanine nucleotide exchange factors. The spk1 mutations induced PIN2 internalization that was not suppressed by auxin, as did the loss-of-function mutations for Rho-like GTPase from Plants 6 (ROP6)-GTPase or its effector RIC1. Furthermore, SPK1 was required for auxin induction of ROP6 activation. Our results have established a Rho GTPase-based auxin signaling pathway that maintains PIN2 polar distribution to the plasma membrane via inhibition of its internalization in Arabidopsis roots. Our findings provide new insights into signaling mechanisms that underlie the regulation of the dynamic trafficking of PINs required for long-distance auxin transport and that link auxin signaling to PIN-mediated pattern formation and morphogenesis.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , GTP-Binding Proteins/metabolism , Microtubule-Associated Proteins/metabolism , Monomeric GTP-Binding Proteins/metabolism , Arabidopsis/genetics , Arabidopsis/growth & development , Indoleacetic Acids/metabolism , Morphogenesis , Plant Roots/genetics , Plant Roots/growth & development , Plant Roots/metabolism , Signal Transduction
9.
ScientificWorldJournal ; 2012: 981658, 2012.
Article in English | MEDLINE | ID: mdl-22645499

ABSTRACT

Cell polarity establishment, maintenance, and alteration are central to the developmental and response programs of nearly all organisms and are often implicated in abnormalities ranging from patterning defects to cancer. By residing at the distinct plasma membrane domains polar cargoes mark the identities of those domains, and execute localized functions. Polar cargoes are recruited to the specialized membrane domains by directional secretion and/or directional endocytic recycling. In plants, auxin efflux carrier PIN proteins display polar localizations in various cell types and play major roles in directional cell-to-cell transport of signaling molecule auxin that is vital for plant patterning and response programs. Recent advanced microscopy studies applied to single cells in intact plants reveal subcellular PIN dynamics. They uncover the PIN polarity generation mechanism and identified important roles of AGC kinases for polar PIN localization. AGC kinase family members PINOID, WAG1, and WAG2, belonging to the AGC-3 subclass predominantly influence the polar localization of PINs. The emerging mechanism for AGC-3 kinases action suggests that kinases phosphorylate PINs mainly at the plasma membrane after initial symmetric PIN secretion for eventual PIN internalization and PIN sorting into distinct ARF-GEF-regulated polar recycling pathways. Thus phosphorylation status directs PIN translocation to different cell sides. Based on these findings a mechanistic framework evolves that suggests existence of cell side-specific recycling pathways in plants and implicates AGC3 kinases for differential PIN recruitment among them for eventual PIN polarity establishment, maintenance, and alteration.


Subject(s)
Cell Polarity/physiology , Indoleacetic Acids/metabolism , Arabidopsis Proteins/metabolism , Endocytosis , Fluorescent Dyes/pharmacology , Gene Expression Regulation, Plant , Microscopy/methods , Models, Biological , Phosphorylation , Plant Physiological Phenomena , Plant Roots/metabolism , Protein Transport , Signal Transduction
10.
Cell ; 149(2): 383-96, 2012 Apr 13.
Article in English | MEDLINE | ID: mdl-22500804

ABSTRACT

Despite their pivotal role in plant development, control mechanisms for oriented cell divisions have remained elusive. Here, we describe how a precisely regulated cell division orientation switch in an Arabidopsis stem cell is controlled by upstream patterning factors. We show that the stem cell regulatory PLETHORA transcription factors induce division plane reorientation by local activation of auxin signaling, culminating in enhanced expression of the microtubule-associated MAP65 proteins. MAP65 upregulation is sufficient to reorient the cortical microtubular array through a CLASP microtubule-cell cortex interaction mediator-dependent mechanism. CLASP differentially localizes to cell faces in a microtubule- and MAP65-dependent manner. Computational simulations clarify how precise 90° switches in cell division planes can follow self-organizing properties of the microtubule array in combination with biases in CLASP localization. Our work demonstrates how transcription factor-mediated processes regulate the cellular machinery to control orientation of formative cell divisions in plants.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Arabidopsis/metabolism , Microtubule-Associated Proteins/metabolism , Plant Cells/metabolism , Cell Division , Indoleacetic Acids/metabolism , Meristem/cytology , Meristem/metabolism , Plant Epidermis/cytology , Plant Epidermis/metabolism , Plant Roots/cytology , Plant Roots/metabolism , Transcription Factors/metabolism
11.
PLoS Biol ; 10(4): e1001299, 2012.
Article in English | MEDLINE | ID: mdl-22509133

ABSTRACT

Cell polarization via asymmetrical distribution of structures or molecules is essential for diverse cellular functions and development of organisms, but how polarity is developmentally controlled has been poorly understood. In plants, the asymmetrical distribution of the PIN-FORMED (PIN) proteins involved in the cellular efflux of the quintessential phytohormone auxin plays a central role in developmental patterning, morphogenesis, and differential growth. Recently we showed that auxin promotes cell interdigitation by activating the Rho family ROP GTPases in leaf epidermal pavement cells. Here we found that auxin activation of the ROP2 signaling pathway regulates the asymmetric distribution of PIN1 by inhibiting its endocytosis. ROP2 inhibits PIN1 endocytosis via the accumulation of cortical actin microfilaments induced by the ROP2 effector protein RIC4. Our findings suggest a link between the developmental auxin signal and polar PIN1 distribution via Rho-dependent cytoskeletal reorganization and reveal the conservation of a design principle for cell polarization that is based on Rho GTPase-mediated inhibition of endocytosis.


Subject(s)
Actin Cytoskeleton/metabolism , Arabidopsis Proteins/metabolism , Cell Polarity , Clathrin/metabolism , Endocytosis , GTP-Binding Proteins/metabolism , Membrane Transport Proteins/metabolism , Arabidopsis/cytology , Arabidopsis/growth & development , Arabidopsis/metabolism , Carrier Proteins/metabolism , Indoleacetic Acids/metabolism , Morphogenesis , Plant Epidermis/cytology , Plant Epidermis/growth & development , Plant Epidermis/metabolism , Plant Leaves/cytology , Recombinant Proteins/metabolism , Signal Transduction , Nicotiana/cytology , Nicotiana/growth & development , Nicotiana/metabolism
12.
Plant Signal Behav ; 6(9): 1333-7, 2011 Sep.
Article in English | MEDLINE | ID: mdl-21852755

ABSTRACT

The analysis of cell polarity in plants is fueled by the discovery and analysis of auxin efflux carrier PIN proteins that show polar localizations in various plant cell types in line with their roles in directional cell to cell auxin transport. As this asymmetry in cellular PIN localization drives directional auxin fluxes, abnormalities in PIN localizations modify auxin transport culminating into range of auxin distribution defective phenotypes. Because of this influence of PIN localization on plant development via changes in auxin distribution, mechanisms establishing, maintaining and altering PIN polarity are of intense interest in the plant field during the recent years. Recent findings suggest that two categories of molecules, namely AGC-3 kinase family members PINOID, WAG1, WAG2 and ARF-GEF family member GNOM predominantly influence the polar localization of PINs. The emerging mechanism for AGC-3 kinases and ARF-GEF action suggest that AGC-3 kinases predominantly phosphorylate PINs at the plasma membrane for eventual PIN internalization and PIN sorting into ARF-GEF GNOM independent polar recycling pathways. In case of mutant for AGC-3 kinases or mutations in AGC-3 kinase-targeted PIN residues, much less phosphorylated PINs are recruited into ARFGEF GNOM-dependent polar recycling pathway. When ARF-GEF GNOM is inactive, the bias is shifted for rerouting less efficiently phosphorylated PINs into GNOM-independent polar recycling pathways that generally prefer efficiently phosphorylated PINs. Thus, balance shifts between the extent of AGC-3 kinase mediated PIN phosphorylation and the functioning of ARFGEF instruct PIN polarity establishment and/or PIN polarity alterations. Recent studies report utilization of this AGC-3 kinase and ARF-GEF PIN polarity regulation module during diverse developmental and response programs including shoot patterning, root growth, phototropism, gravitropism, organogenesis, leaf epidermal cell indentations and fruit valve margin formation. Based on these findings the same theme of phosphorylated PIN sorting into differential polar recycling pathways for PIN polarity establishment and alteration seems to be employed in a context-dependent manner.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Cell Polarity/genetics , Cell Polarity/physiology , Gene Expression Regulation, Plant/genetics , Gene Expression Regulation, Plant/physiology , Phosphorylation , Protein Serine-Threonine Kinases/genetics , Protein Serine-Threonine Kinases/metabolism
13.
Curr Biol ; 21(13): 1123-8, 2011 Jul 12.
Article in English | MEDLINE | ID: mdl-21700457

ABSTRACT

The pattern of plant organ initiation at the shoot apical meristem (SAM), termed phyllotaxis, displays regularities that have long intrigued botanists and mathematicians alike. In the SAM, the central zone (CZ) contains a population of stem cells that replenish the surrounding peripheral zone (PZ), where organs are generated in regular patterns. These patterns differ between species and may change in response to developmental or environmental cues [1]. Expression analysis of auxin efflux facilitators of the PIN-FORMED (PIN) family combined with modeling of auxin transport has indicated that organ initiation is associated with intracellular polarization of PIN proteins and auxin accumulation [2-10]. However, regulators that modulate PIN activity to determine phyllotactic patterns have hitherto been unknown. Here we reveal that three redundantly acting PLETHORA (PLT)-like AP2 domain transcription factors control shoot organ positioning in the model plant Arabidopsis thaliana. Loss of PLT3, PLT5, and PLT7 function leads to nonrandom, metastable changes in phyllotaxis. Phyllotactic changes in plt3plt5plt7 mutants are largely attributable to misregulation of PIN1 and can be recapitulated by reducing PIN1 dosage, revealing that PLT proteins are key regulators of PIN1 activity in control of phyllotaxis.


Subject(s)
Arabidopsis Proteins/physiology , Arabidopsis/growth & development , Transcription Factors/physiology , Arabidopsis/genetics , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Biological Transport , Gene Expression Regulation, Plant , Membrane Transport Proteins/genetics , Membrane Transport Proteins/metabolism , Membrane Transport Proteins/physiology , Meristem/genetics , Meristem/growth & development , Meristem/metabolism , Plant Leaves/genetics , Plant Leaves/growth & development , Plant Leaves/metabolism , Transcription Factors/genetics , Transcription Factors/metabolism
14.
Curr Biol ; 21(12): 1055-60, 2011 Jun 21.
Article in English | MEDLINE | ID: mdl-21658946

ABSTRACT

The polarized transport of the phytohormone auxin [1], which is crucial for the regulation of different stages of plant development [2, 3], depends on the asymmetric plasma membrane distribution of the PIN-FORMED (PIN) auxin efflux carriers [4, 5]. The PIN polar localization results from clathrin-mediated endocytosis (CME) from the plasma membrane and subsequent polar recycling [6]. The Arabidopsis genome encodes two groups of dynamin-related proteins (DRPs) that show homology to mammalian dynamin-a protein required for fission of endocytic vesicles during CME [7, 8]. Here we show by coimmunoprecipitation (coIP), bimolecular fluorescence complementation (BiFC), and Förster resonance energy transfer (FRET) that members of the DRP1 group closely associate with PIN proteins at the cell plate. Localization and phenotypic analysis of novel drp1 mutants revealed a requirement for DRP1 function in correct PIN distribution and in auxin-mediated development. We propose that rapid and specific internalization of PIN proteins mediated by the DRP1 proteins and the associated CME machinery from the cell plate membranes during cytokinesis is an important mechanism for proper polar PIN positioning in interphase cells.


Subject(s)
Arabidopsis Proteins/physiology , Arabidopsis/cytology , Cell Polarity , Dynamins/physiology , Membrane Transport Proteins/physiology , Amino Acid Sequence , Arabidopsis/genetics , Arabidopsis Proteins/chemistry , Arabidopsis Proteins/genetics , Dynamins/chemistry , Dynamins/genetics , Genome, Plant , Green Fluorescent Proteins/genetics , Immunoprecipitation , Membrane Transport Proteins/chemistry , Membrane Transport Proteins/genetics , Molecular Sequence Data , Spectrometry, Fluorescence
15.
Cell Res ; 21(6): 970-8, 2011 Jun.
Article in English | MEDLINE | ID: mdl-21423279

ABSTRACT

Within a multicellular tissue cells may coordinately form a singular or multiple polar axes, but it is unclear whether a common mechanism governs different types of polar axis formation. The phosphorylation status of PIN proteins, which is directly affected by the PINOID (PID) protein kinase and the PP2A protein phosphatase, is known to regulate the apical-basal polarity of PIN localization in bipolar cells of roots and shoot apices. Here, we provide evidence that the phosphorylation status-mediated PIN polarity switch is widely used to modulate cellular processes in Arabidopsis including multipolar pavement cells (PC) with interdigitated lobes and indentations. The degree of PC interdigitation was greatly reduced either when the FYPP1 gene, which encodes a PP2A called phytochrome-associated serine/threonine protein phosphatase, was knocked out or when the PID gene was overexpressed (35S::PID). These genetic modifications caused PIN1 localization to switch from lobe to indentation regions. The PP2A and PID mediated switching of PIN1 localization is strikingly similar to their regulation of the apical-basal polarity switch of PIN proteins in other cells. Our findings suggest a common mechanism for the regulation of PIN1 polarity formation, a fundamental cellular process that is crucial for pattern formation both at the tissue/organ and cellular levels.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Cell Shape/genetics , Membrane Transport Proteins/metabolism , Plant Epidermis/cytology , Plant Leaves/cytology , Arabidopsis/physiology , Arabidopsis Proteins/genetics , Gene Knockout Techniques , Indoleacetic Acids/pharmacology , Membrane Transport Proteins/genetics , Phenotype , Phosphoprotein Phosphatases/genetics , Phosphoprotein Phosphatases/metabolism , Phosphorylation , Plant Epidermis/physiology , Plant Leaves/physiology , Protein Phosphatase 2/genetics , Protein Phosphatase 2/metabolism , Protein Serine-Threonine Kinases/genetics , Protein Serine-Threonine Kinases/metabolism , Protein Transport
16.
Cell ; 143(1): 111-21, 2010 Oct 01.
Article in English | MEDLINE | ID: mdl-20887896

ABSTRACT

Spatial distribution of the plant hormone auxin regulates multiple aspects of plant development. These self-regulating auxin gradients are established by the action of PIN auxin transporters, whose activity is regulated by their constitutive cycling between the plasma membrane and endosomes. Here, we show that auxin signaling by the auxin receptor AUXIN-BINDING PROTEIN 1 (ABP1) inhibits the clathrin-mediated internalization of PIN proteins. ABP1 acts as a positive factor in clathrin recruitment to the plasma membrane, thereby promoting endocytosis. Auxin binding to ABP1 interferes with this action and leads to the inhibition of clathrin-mediated endocytosis. Our study demonstrates that ABP1 mediates a nontranscriptional auxin signaling that regulates the evolutionarily conserved process of clathrin-mediated endocytosis and suggests that this signaling may be essential for the developmentally important feedback of auxin on its own transport.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/cytology , Arabidopsis/metabolism , Clathrin/metabolism , Endocytosis , Indoleacetic Acids/metabolism , Plant Proteins/metabolism , Receptors, Cell Surface/metabolism , Cell Membrane/metabolism , Membrane Transport Proteins/metabolism
17.
Development ; 137(19): 3245-55, 2010 Oct.
Article in English | MEDLINE | ID: mdl-20823065

ABSTRACT

Polar membrane cargo delivery is crucial for establishing cell polarity and for directional transport processes. In plants, polar trafficking mediates the dynamic asymmetric distribution of PIN FORMED (PIN) carriers, which drive polar cell-to-cell transport of the hormone auxin, thereby generating auxin maxima and minima that control development. The Arabidopsis PINOID (PID) protein kinase instructs apical PIN localization by phosphorylating PINs. Here, we identified the PID homologs WAG1 and WAG2 as new PIN polarity regulators. We show that the AGC3 kinases PID, WAG1 and WAG2, and not other plant AGC kinases, instruct recruitment of PINs into the apical recycling pathway by phosphorylating the middle serine in three conserved TPRXS(N/S) motifs within the PIN central hydrophilic loop. Our results put forward a model by which apolarly localized PID, WAG1 and WAG2 phosphorylate PINs at the plasma membrane after default non-polar PIN secretion, and trigger endocytosis-dependent apical PIN recycling. This phosphorylation-triggered apical PIN recycling competes with ARF-GEF GNOM-dependent basal recycling to promote apical PIN localization. In planta, expression domains of PID, WAG1 and WAG2 correlate with apical localization of PINs in those cell types, indicating the importance of these kinases for apical PIN localization. Our data show that by directing polar PIN localization and PIN-mediated polar auxin transport, the three AGC3 kinases redundantly regulate cotyledon development, root meristem size and gravitropic response, indicating their involvement in both programmed and adaptive plant development.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Cell Membrane/metabolism , Membrane Transport Proteins/metabolism , Protein Serine-Threonine Kinases/metabolism , Amino Acid Motifs , Amino Acid Sequence , Arabidopsis/genetics , Arabidopsis/growth & development , Arabidopsis Proteins/chemistry , Arabidopsis Proteins/genetics , Endocytosis , Membrane Transport Proteins/genetics , Microscopy, Electron, Scanning , Molecular Sequence Data , Phosphorylation , Plant Roots/growth & development , Plant Roots/metabolism , Plants, Genetically Modified , Protein Binding , Protein Serine-Threonine Kinases/genetics , Protein Transport , Signal Transduction
18.
Commun Integr Biol ; 2(2): 184-90, 2009 Mar.
Article in English | MEDLINE | ID: mdl-20835291

ABSTRACT

Auxin efflux carrier PIN proteins have been intensively investigated as they are the first polar cargos to be identified in plants with a direct relevance for plant patterning. Based on their polar localization; PIN proteins direct the intercellular flow of signaling molecule auxin and thus bear a rate limiting effect on the formation of auxin activity gradients. With this influence on directionality and extent of auxin transport PINs play crucial roles in plant body organization. Many factors such as vesicle trafficking regulator ARF-GEF GNOM, a kinase PINOID, a retromer complex and membrane sterol composition influence polar PIN localization. Recent work uncovers the mechanism that generates default PIN polarity. Real time PIN tracking reveals that PIN polarity is generated from initially non-polar secretion via endocytosis and subsequent polar recycling. In addition, the Rab5 endocytic pathway emerges to be important for polar PIN localization as Rab5 interference causes non-polar distribution of PINs. This non-polar distribution of PINs during embryogenesis transiently alters auxin activity gradients and changes organ identity by transforming embryonic leaf cells to root fates. These findings for the first time link PIN polarity-based auxin activity gradient to cell fate decisions and thus demonstrate morphogen (a substance influencing cell fates on its concentration gradient) characters of auxin. They also suggest an auxin activity distribution-dependent sensing module that executes differential apical and basal developmental program during plant embryogenesis.

19.
Nature ; 456(7224): 962-6, 2008 Dec 18.
Article in English | MEDLINE | ID: mdl-18953331

ABSTRACT

Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication-a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.


Subject(s)
Arabidopsis/cytology , Arabidopsis/metabolism , Cell Lineage , Cell Polarity , Endocytosis , Indoleacetic Acids/metabolism , Arabidopsis/embryology , Arabidopsis/enzymology , Arabidopsis Proteins/metabolism , Embryonic Development , Membrane Transport Proteins/metabolism , Plant Leaves/embryology , Plant Leaves/metabolism , Plant Roots/embryology , Plant Roots/metabolism , Protein Transport , Seeds/cytology , Seeds/embryology , Seeds/enzymology , Seeds/metabolism , rab5 GTP-Binding Proteins/metabolism
20.
Curr Biol ; 18(7): 526-31, 2008 Apr 08.
Article in English | MEDLINE | ID: mdl-18394892

ABSTRACT

Cell polarity manifested by the polar cargo delivery to different plasma-membrane domains is a fundamental feature of multicellular organisms. Pathways for polar delivery have been identified in animals; prominent among them is transcytosis, which involves cargo movement between different sides of the cell [1]. PIN transporters are prominent polar cargoes in plants, whose polar subcellular localization determines the directional flow of the signaling molecule auxin [2, 3]. In this study, we address the cellular mechanisms of PIN polar targeting and dynamic polarity changes. We show that apical and basal PIN targeting pathways are interconnected but molecularly distinct by means of ARF GEF vesicle-trafficking regulators. Pharmacological or genetic interference with the Arabidopsis ARF GEF GNOM leads specifically to apicalization of basal cargoes such as PIN1. We visualize the translocation of PIN proteins between the opposite sides of polarized cells in vivo and show that this PIN transcytosis occurs by endocytic recycling and alternative recruitment of the same cargo molecules by apical and basal targeting machineries. Our data suggest that an ARF GEF-dependent transcytosis-like mechanism is operational in plants and provides a plausible mechanism to trigger changes in PIN polarity and hence auxin fluxes during embryogenesis and organogenesis.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Cell Polarity/physiology , Guanine Nucleotide Exchange Factors/metabolism , Membrane Transport Proteins/metabolism , Transport Vesicles/physiology , Arabidopsis/embryology , Arabidopsis/physiology , Brefeldin A , Indoleacetic Acids/metabolism , Morphogenesis/physiology
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