Cellular mechanisms for cargo delivery and polarity maintenance at different polar domains in plant cells
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27462465
PubMed Central
PMC4950145
DOI
10.1038/celldisc.2016.18
PII: celldisc201618
Knihovny.cz E-zdroje
- Klíčová slova
- lateral diffusion, polar recycling, polar secretion, protein clustering, protein dynamics modeling, protein trafficking,
- Publikační typ
- časopisecké články MeSH
The asymmetric localization of proteins in the plasma membrane domains of eukaryotic cells is a fundamental manifestation of cell polarity that is central to multicellular organization and developmental patterning. In plants, the mechanisms underlying the polar localization of cargo proteins are still largely unknown and appear to be fundamentally distinct from those operating in mammals. Here, we present a systematic, quantitative comparative analysis of the polar delivery and subcellular localization of proteins that characterize distinct polar plasma membrane domains in plant cells. The combination of microscopic analyses and computational modeling revealed a mechanistic framework common to diverse polar cargos and underlying the establishment and maintenance of apical, basal, and lateral polar domains in plant cells. This mechanism depends on the polar secretion, constitutive endocytic recycling, and restricted lateral diffusion of cargos within the plasma membrane. Moreover, our observations suggest that polar cargo distribution involves the individual protein potential to form clusters within the plasma membrane and interact with the extracellular matrix. Our observations provide insights into the shared cellular mechanisms of polar cargo delivery and polarity maintenance in plant cells.
Department of Biological Science Graduate School of Science University of Osaka Osaka Japan
Institute of Science and Technology Austria Klosterneuburg Austria
Institute of Science and Technology Austria Masaryk University Brno Czech Republic
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Yang Z. Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 2008; 24: 551–575. PubMed PMC
Grebe M. Cell polarity: lateral perspectives. Curr Biol 2010; 20: R446–R448. PubMed
Nakamura M, Kiefer CS, Grebe M. Planar polarity, tissue polarity and planar morphogenesis in plants. Curr Opin Plant Biol 2012; 15: 593–600. PubMed
Dettmer J, Friml J. Cell polarity in plants: when two do the same, it is not the same. Curr Opin Cell Biol 2011; 23: 686–696. PubMed
Geldner N. Cell polarity in plants - a PARspective on PINs. Curr Opin Plant Biol 2009; 12: 42–48. PubMed
Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci USA 2012; 109: 10101–10106. PubMed PMC
Roppolo D, De Rybel B, Tendon VD et al. A novel protein family mediates Casparian strip formation in the endodermis. Nature 2011; 473: 380–383. PubMed
Alassimone J, Naseer S, Geldner N. A developmental framework for endodermal differentiation and polarity. Proc Natl Acad Sci USA 2010; 107: 5214–5219. PubMed PMC
Prodon F, Chenevert J, Sardet C. Establishment of animal-vegetal polarity during maturation in ascidian oocytes. Dev Biol 2006; 290: 297–311. PubMed
Rose L, Gonczy P. Polarity establishment, asymmetric division and segregation of fate determinants in early C. elegans embryos. WormBook 2014, 30: 1–43. PubMed
Woods B, Kuo CC, Wu CF, Zyla TR, Lew DJ. Polarity establishment requires localized activation of Cdc42. J Cell Biol 2015; 211: 19–26. PubMed PMC
Petrasek J, Mravec J, Bouchard R et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 2006; 312: 914–918. PubMed
Grunewald W, Friml J. The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 2010; 29: 2700–2714. PubMed PMC
Kleine-Vehn J, Friml J. Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol 2008; 24: 447–473. PubMed
Vanneste S, Friml J. Auxin: a trigger for change in plant development. Cell 2009; 136: 1005–1016. PubMed
Dhonukshe P, Aniento F, Hwang I et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 2007; 17: 520–527. PubMed
Geldner N, Friml J, Stierhof Y-D, Jürgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 2001; 413: 425–428. PubMed
Kleine-Vehn J, Wabnik K, Martinière A et al. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 2011; 7: 540. PubMed PMC
Kitakura S, Vanneste S, Robert S et al. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant cell 2011; 23: 1920–1931. PubMed PMC
Men S, Boutté Y, Ikeda Y et al. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 2008; 10: 237–244. PubMed
Geldner N, Anders N, Wolters H et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 2003; 112: 219–230. PubMed
Kleine-Vehn J, Huang F, Naramoto S et al. PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 2009; 21: 3839–3849. PubMed PMC
Tanaka H, Kitakura S, De Rycke R, De Groodt R, Friml J. Fluorescence imaging-based screen identifies ARF GEF component of early endosomal trafficking. Curr Biol 2009; 19: 391–397. PubMed
Tanaka H, Kitakura S, Rakusová H et al. Cell polarity and patterning by PIN1 trafficking through early endosomal compartments in Arabidopsis thaliana. PLoS Genet 2013; 9: e1003540. PubMed PMC
Teh O-k, Moore I. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 2007; 448: 493–496. PubMed
Richter S, Kientz M, Brumm S et al. Delivery of endocytosed proteins to the cell-division plane requires change of pathway from recycling to secretion. eLife 2014; 3: e02131. PubMed PMC
Naramoto S, Kleine-Vehn J, Robert S et al. ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci USA 2010; 107: 21890–21895. PubMed PMC
Naramoto S, Otegui MS, Kutsuna N et al. Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis. Plant Cell 2014; 26: 3062–3076. PubMed PMC
Feraru E, Feraru MI, Kleine-Vehn J et al. PIN polarity maintenance by the cell wall in Arabidopsis. Curr Biol 2011; 21: 338–343. PubMed
Martinière A, Lavagi I, Nageswaran G et al. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci USA 2012; 109: 12805–12810. PubMed PMC
Heisler MG, Hamant O, Krupinski P et al. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol 2010; 8: e1000516. PubMed PMC
Hamant O, Meyerowitz EM, Traas J. Is cell polarity under mechanical control in plants? Plant Signal Behav 2011; 6: 137–139. PubMed PMC
Wiśniewska J, Xu J, Seifertová D et al. Polar PIN localization directs auxin flow in plants. Science 2006; 312: 883. PubMed
Dai M, Zhang C, Kania U et al. A PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in Arabidopsis. Plant Cell 2012; 24: 2497–2514. PubMed PMC
Friml J, Yang X, Michniewicz M et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 2004; 306: 862–865. PubMed
Huang F, Zago MK, Abas L, van Marion A, Galván-Ampudia CS, Offringa R. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 2010; 22: 1129–1142. PubMed PMC
Michniewicz M, Zago MK, Abas L et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 2007; 130: 1044–1056. PubMed
Zhang J, Nodzyński T, Pěnčík A, Rolčík J, Friml J. PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA 2010; 107: 918–922. PubMed PMC
Łangowski Ł, Růžička K, Naramoto S, Kleine-Vehn J, Friml J. Trafficking to the outer polar domain defines the root-soil interface. Curr Biol 2010; 20: 904–908. PubMed
Takano J, Miwa K, Yuan L, von Wirén N, Fujiwara T. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 2005; 102: 12276–12281. PubMed PMC
Takano J, Tanaka M, Toyoda A et al. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci USA 2010; 107: 5220–5225. PubMed PMC
Benková E, Michniewicz M, Sauer M et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 2003; 115: 591–602. PubMed
Abas L, Benjamins R, Malenica N et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 2006; 8: 249–256. PubMed
Růžička K, Strader LC, Bailly A et al. Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proc Natl Acad Sci USA 2010; 107: 10749–10753. PubMed PMC
Stein M, Dittgen J, Sánchez-Rodríguez C et al. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 2006; 18: 731–746. PubMed PMC
Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 2000; 97: 3718–3723. PubMed PMC
Friedrichsen DM, Joazeiro CAP, Li J, Hunter T, Chory J. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol 2000; 123: 1247–1255. PubMed PMC
Geldner N, Dénervaud-Tendon V, Hyman DL, Mayer U, Stierhof Y-D, Chory J. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 2009; 59: 169–178. PubMed PMC
Chen Y, Lagerholm BC, Yang B, Jacobson K. Methods to measure the lateral diffusion of membrane lipids and proteins. Methods 2006; 39: 147–153. PubMed
Kleine-Vehn J, Wabnik K, Martiniere A et al. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 2011; 7: 540. PubMed PMC
Boutté Y, Frescatada-Rosa M, Men SZ et al. Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J 2010; 29: 546–558. PubMed PMC
Goehring NW, Chowdhury D, Hyman AA, Grill SW. FRAP analysis of membrane-associated proteins: lateral diffusion and membrane-cytoplasmic exchange. Biophys J 2010; 99: 2443–2452. PubMed PMC
Hosy E, Martiniere A, Choquet D, Maurel C, Luu DT. Super-resolved and dynamic imaging of membrane proteins in plant cells reveal contrasting kinetic profiles and multiple confinement mechanisms. Mol Plant 2015; 8: 339–342. PubMed
Sauer M, Paciorek T, Benkova E, Friml J. Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat Protoc 2006; 1: 98–103. PubMed
Wabnik K, Kleine-Vehn J, Govaerts W, Friml J. Prototype cell-to-cell auxin transport mechanism by intracellular auxin compartmentalization. Trends Plant Sci 2011; 16: 468–475. PubMed
Dhonukshe P, Huang F, Galvan-Ampudia CS et al. Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 2010; 137: 3245–3255. PubMed
Lyczak R, Gomes J-E, Bowerman B. Heads or tails: cell polarity and axis formation in the early Caenorhabditis elegans embryo. Dev Cell 2002; 3: 157–166. PubMed
Mostov K, Su T, ter Beest M. Polarized epithelial membrane traffic: conservation and plasticity. Nat Cell Biol 2003; 5: 287–293. PubMed
St Johnston D, Ahringer J. Cell polarity in eggs and epithelia: parallels and diversity. Cell 2010; 141: 757–774. PubMed
Kleine-Vehn J, Dhonukshe P, Sauer M et al. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 2008; 18: 526–531. PubMed
Feraru E, Feraru MI, Asaoka R et al. BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis. Plant Cell 2012; 24: 3074–3086. PubMed PMC
Reichardt I, Slane D, El Kasmi F et al. Mechanisms of functional specificity among plasma-membrane syntaxins in Arabidopsis. Traffic 2011; 12: 1269–1280. PubMed
Campanoni P, Blatt MR. Membrane trafficking and polar growth in root hairs and pollen tubes. J Exp Bot 2007; 58: 65–74. PubMed
Pumplin N, Zhang X, Noar RD, Harrison MJ. Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proc Natl Acad Sci USA 2012; 109: E665–E672. PubMed PMC
Dhonukshe P, Tanaka H, Goh T et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 2008; 456: 962–966. PubMed PMC
Gadeyne A, Sanchez-Rodriguez C, Vanneste S et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 2014; 156: 691–704. PubMed
Wabnik K, Kleine-Vehn J, Balla J et al. Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 2010; 6: 447. PubMed PMC
Furutani M, Sakamoto N, Yoshida S et al. Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development 2011; 138: 2069–2078. PubMed
Friml J, Vieten A, Sauer M et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 2003; 426: 147–153. PubMed
Reinhardt D, Pesce E-R, Stieger P et al. Regulation of phyllotaxis by polar auxin transport. Nature 2003; 426: 255–260. PubMed
Scarpella E, Marcos D, Friml J, Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev 2006; 20: 1015–1027. PubMed PMC
Sauer M, Balla J, Luschnig C et al. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 2006; 20: 2902–2911. PubMed PMC
Sorefan K, Girin T, Liljegren SJ et al. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 2009; 459: 583–586. PubMed
Ding Z, Galván-Ampudia CS, Demarsy E et al. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 2011; 13: 447–452. PubMed
Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 2002; 415: 806–809. PubMed
Rakusová H, Gallego-Bartolomé J, Vanstraelen M et al. Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. Plant J 2011; 67: 817–826. PubMed
Ge L, Peer W, Robert S et al. Arabidopsis ROOT UVB SENSITIVE2/WEAK AUXIN RESPONSE1 is required for polar auxin transport. Plant Cell 2010; 22: 1749–1761. PubMed PMC
Löfke C, Zwiewka M, Heilmann I, Van Montagu MCE, Teichmann T, Friml J. Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc Natl Acad Sci USA 2013; 110: 3627–3632. PubMed PMC
Marhavý P, Vanstraelen M, De Rybel B et al. Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 2013; 32: 149–158. PubMed PMC
Whitford R, Fernandez A, Tejos R et al. GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev Cell 2012; 22: 678–685. PubMed
Xu J, Scheres B. Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 2005; 17: 525–536. PubMed PMC
Boutté Y, Ikeda Y, Grebe M. Mechanisms of auxin-dependent cell and tissue polarity. Curr Opin Plant Biol 2007; 10: 616–623. PubMed
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AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells
The Nuts and Bolts of PIN Auxin Efflux Carriers
A Functional Study of AUXILIN-LIKE1 and 2, Two Putative Clathrin Uncoating Factors in Arabidopsis