Mechanistic framework for cell-intrinsic re-establishment of PIN2 polarity after cell division

. 2018 Dec ; 4 (12) : 1082-1088. [epub] 20181203

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30518833
Odkazy

PubMed 30518833
PubMed Central PMC6394824
DOI 10.1038/s41477-018-0318-3
PII: 10.1038/s41477-018-0318-3
Knihovny.cz E-zdroje

Cell polarity, manifested by the localization of proteins to distinct polar plasma membrane domains, is a key prerequisite of multicellular life. In plants, PIN auxin transporters are prominent polarity markers crucial for a plethora of developmental processes. Cell polarity mechanisms in plants are distinct from other eukaryotes and still largely elusive. In particular, how the cell polarities are propagated and maintained following cell division remains unknown. Plant cytokinesis is orchestrated by the cell plate-a transient centrifugally growing endomembrane compartment ultimately forming the cross wall1. Trafficking of polar membrane proteins is typically redirected to the cell plate, and these will consequently have opposite polarity in at least one of the daughter cells2-5. Here, we provide mechanistic insights into post-cytokinetic re-establishment of cell polarity as manifested by the apical, polar localization of PIN2. We show that the apical domain is defined in a cell-intrinsic manner and that re-establishment of PIN2 localization to this domain requires de novo protein secretion and endocytosis, but not basal-to-apical transcytosis. Furthermore, we identify a PINOID-related kinase WAG1, which phosphorylates PIN2 in vitro6 and is transcriptionally upregulated specifically in dividing cells, as a crucial regulator of post-cytokinetic PIN2 polarity re-establishment.

Zobrazit více v PubMed

Smertenko A, et al. Plant Cytokinesis: Terminology for Structures and Processes. Trends Cell Biol. 2017;27:885–894. PubMed

Geldner N, et al. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature. 2001;413:425–428. PubMed

Mravec J, et al. Cell Plate Restricted Association of DRP1A and PIN Proteins Is Required for Cell Polarity Establishment in Arabidopsis. Curr Biol. 2011;21:1055–1060. PubMed

Men S, et al. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol. 2008;10:237–244. PubMed

Yoshinari A, et al. DRP1-Dependent Endocytosis is Essential for Polar Localization and Boron-Induced Degradation of the Borate Transporter BOR1 in Arabidopsis thaliana. Plant Cell Physiol. 2016;57:1985–2000. PubMed

Dhonukshe P, et al. Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development. 2010;137:3245–55. PubMed

Kania U, et al. Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol. 2014;4 140017. PubMed PMC

Abas L, et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol. 2006;8:249–56. PubMed

Baster P, et al. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 2013;32:260–74. PubMed PMC

Dhonukshe P, et al. Endocytosis of Cell Surface Material Mediates Cell Plate Formation during Plant Cytokinesis. Dev Cell. 2006;10:137–150. PubMed

Gurskaya NG, et al. Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat Biotechnol. 2006;24:461–465. PubMed

Richter S, et al. Delivery of endocytosed proteins to the cell-division plane requires change of pathway from recycling to secretion. Elife. 2014;2014:1–16. PubMed PMC

Lauber MH, et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol. 1997;139:1485–93. PubMed PMC

Sparks E, et al. Spatiotemporal signalling in plant development. Nat Rev Genet. 2013;14:631–44. PubMed PMC

Mazur E, et al. Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis. Sci Rep. 2016;6 33754. PubMed PMC

Prát T, et al. WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLOS Genet. 2018;14:e1007177. PubMed PMC

Simon S, et al. Defining the selectivity of processes along the auxin response chain: a study using auxin analogues. New Phytol. 2013;200:1034–1048. PubMed

Sena G, et al. Organ regeneration does not require a functional stem cell niche in plants. Nature. 2009;457:1150–1153. PubMed PMC

Kleine-Vehn J, et al. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol Plant. 2008;1:1056–66. PubMed

Kleine-Vehn J, et al. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol. 2011;7:540. PubMed PMC

Feraru E, et al. PIN Polarity Maintenance by the Cell Wall in Arabidopsis. Curr Biol. 2011;21:338–343. PubMed

Martinière A, et al. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci U S A. 2012;109:12805–10. PubMed PMC

Kitakura S, et al. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell. 2011;23:1920–31. PubMed PMC

Adamowski M, et al. A Functional Study of AUXILIN-LIKE1 and 2, Two Putative Clathrin Uncoating Factors in Arabidopsis. Plant Cell. 2018;30:700–716. PubMed PMC

Friml J, et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science. 2004;306:862–865. PubMed

Michniewicz M, et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell. 2007;130:1044–56. PubMed

Kleine-Vehn J, et al. PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell. 2009;21:3839–49. PubMed PMC

Zhang J, et al. PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci U S A. 2010;107:918–22. PubMed PMC

Huang F, et al. Phosphorylation of Conserved PIN Motifs Directs Arabidopsis PIN1 Polarity and Auxin Transport. Plant Cell. 2010;22:1129–1142. PubMed PMC

Weller B, et al. Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth. Proc Natl Acad Sci U S A. 2017;114:E887–E896. PubMed PMC

Furutani M, et al. Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development. 2011;138:2069–78. PubMed

Salanenka Y, et al. Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. Proc Natl Acad Sci. 2018;115:3716–3721. PubMed PMC

Clough SJ, Bent AF. Floral dip: a simplified method forAgrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. PubMed

Luschnig C, et al. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998;12:2175–87. PubMed PMC

von Wangenheim D, et al. Live tracking of moving samples in confocal microscopy for vertically grown roots. Elife. 2017;6:e26792. PubMed PMC

Jásik J, et al. PIN2 Turnover in Arabidopsis Root Epidermal Cells Explored by the Photoconvertible Protein Dendra2. PLoS One. 2013;8:e61403. PubMed PMC

Schindelin J, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682. PubMed PMC

Grabov a, et al. Morphometric analysis of root shape. New Phytol. 2005;165:641–651. PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...