AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
714055
European Research Council - International
I 3630
Austrian Science Fund FWF - Austria
PubMed
33705718
PubMed Central
PMC8112251
DOI
10.1016/j.cub.2021.02.028
PII: S0960-9822(21)00269-4
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, cell polarity, lateral diffusion, plant development, polar auxin transport, positive feedback, protein phosphorylation,
- MeSH
- Arabidopsis * genetika metabolismus MeSH
- biologický transport MeSH
- kořeny rostlin metabolismus MeSH
- kyseliny indoloctové MeSH
- membránové transportní proteiny genetika MeSH
- polarita buněk MeSH
- proteiny huseníčku * genetika metabolismus MeSH
- regulace genové exprese u rostlin MeSH
- rostlinné buňky metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- kyseliny indoloctové MeSH
- membránové transportní proteiny MeSH
- proteiny huseníčku * MeSH
Polar subcellular localization of the PIN exporters of the phytohormone auxin is a key determinant of directional, intercellular auxin transport and thus a central topic of both plant cell and developmental biology. Arabidopsis mutants lacking PID, a kinase that phosphorylates PINs, or the MAB4/MEL proteins of unknown molecular function display PIN polarity defects and phenocopy pin mutants, but mechanistic insights into how these factors convey PIN polarity are missing. Here, by combining protein biochemistry with quantitative live-cell imaging, we demonstrate that PINs, MAB4/MELs, and AGC kinases interact in the same complex at the plasma membrane. MAB4/MELs are recruited to the plasma membrane by the PINs and in concert with the AGC kinases maintain PIN polarity through limiting lateral diffusion-based escape of PINs from the polar domain. The PIN-MAB4/MEL-PID protein complex has self-reinforcing properties thanks to positive feedback between AGC kinase-mediated PIN phosphorylation and MAB4/MEL recruitment. We thus uncover the molecular mechanism by which AGC kinases and MAB4/MEL proteins regulate PIN localization and plant development.
Institute of Science and Technology Austria 1190 Vienna Austria
Institute of Science and Technology Austria 3400 Klosterneuburg Austria
Zobrazit více v PubMed
Gälweiler L., Guan C., Müller A., Wisman E., Mendgen K., Yephremov A., Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 1998;282:2226–2230. PubMed
Wisniewska J., Xu J., Seifertová D., Brewer P.B., Růžička K., Blilou I. Polar PIN localization directs auxin flow in plants. Science. 2006;312:883. PubMed
Adamowski M., Friml J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell. 2015;27:20–32. PubMed PMC
Petrášek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertová D. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006;312:914–918. PubMed
Luschnig C., Gaxiola R.A., Grisafi P., Fink G.R. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998;12:2175–2187. PubMed PMC
Smetana O., Mäkilä R., Lyu M., Amiryousefi A., Sánchez Rodríguez F., Wu M.-F., Solé-Gil A., Leal Gavarrón M., Siligato R., Miyashima S. High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature. 2019;565:485–489. PubMed
Ding Z., Friml J. Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl. Acad. Sci. USA. 2010;107:12046–12051. PubMed PMC
Ding Z., Galván-Ampudia C.S., Demarsy E., Łangowski Ł., Kleine-Vehn J., Fan Y., Morita M.T., Tasaka M., Fankhauser C., Offringa R., Friml J. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat. Cell Biol. 2011;13:447–452. PubMed
Rakusová H., Abbas M., Han H., Song S., Robert H.S., Friml J. Termination of shoot gravitropic responses by auxin feedback on PIN3 polarity. Curr. Biol. 2016;26:3026–3032. PubMed
Grones P., Abas M., Hajný J., Jones A., Waidmann S., Kleine-Vehn J., Friml J. PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism. Sci. Rep. 2018;8:10279. PubMed PMC
Mazur E., Gallei M., Adamowski M., Han H., Robert H.S., Friml J. Clathrin-mediated trafficking and PIN trafficking are required for auxin canalization and vascular tissue formation in Arabidopsis. Plant Sci. 2020;293:110414. PubMed
Hajný J., Prát T., Rydza N., Rodriguez L., Tan S., Verstraeten I., Domjan D., Mazur E., Smakowska-Luzan E., Smet W. Receptor kinase module targets PIN-dependent auxin transport during canalization. Science. 2020;370:550–557. PubMed PMC
Kozubowski L., Saito K., Johnson J.M., Howell A.S., Zyla T.R., Lew D.J. Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr. Biol. 2008;18:1719–1726. PubMed PMC
Johnson J.M., Jin M., Lew D.J. Symmetry breaking and the establishment of cell polarity in budding yeast. Curr. Opin. Genet. Dev. 2011;21:740–746. PubMed PMC
Feraru E., Feraru M.I., Kleine-Vehn J., Martinière A., Mouille G., Vanneste S., Vernhettes S., Runions J., Friml J. PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol. 2011;21:338–343. PubMed
Kleine-Vehn J., Wabnik K., Martinière A., Łangowski Ł., Willig K., Naramoto S., Leitner J., Tanaka H., Jakobs S., Robert S. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 2011;7:540. PubMed PMC
Friml J., Yang X., Michniewicz M., Weijers D., Quint A., Tietz O., Benjamins R., Ouwerkerk P.B.F., Ljung K., Sandberg G. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science. 2004;306:862–865. PubMed
Michniewicz M., Zago M.K., Abas L., Weijers D., Schweighofer A., Meskiene I., Heisler M.G., Ohno C., Zhang J., Huang F. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell. 2007;130:1044–1056. PubMed
Benjamins R., Quint A., Weijers D., Hooykaas P., Offringa R. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development. 2001;128:4057–4067. PubMed
Huang F., Zago M.K., Abas L., van Marion A., Galván-Ampudia C.S., Offringa R. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell. 2010;22:1129–1142. PubMed PMC
Zhang J., Nodzynski 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
Dhonukshe P., Huang F., Galvan-Ampudia C.S., Mähönen A.P., Kleine-Vehn J., Xu J., Quint A., Prasad K., Friml J., Scheres B., Offringa R. 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
Treml B.S., Winderl S., Radykewicz R., Herz M., Schweizer G., Hutzler P., Glawischnig E., Ruiz R.A.T. The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo. Development. 2005;132:4063–4074. PubMed
Furutani M., Kajiwara T., Kato T., Treml B.S., Stockum C., Torres-Ruiz R.A., Tasaka M. The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development. 2007;134:3849–3859. PubMed
Cheng Y., Qin G., Dai X., Zhao Y. NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2008;105:21017–21022. PubMed PMC
Furutani M., Sakamoto N., Yoshida S., Kajiwara T., Robert H.S., Friml J., Tasaka M. Polar-localized NPH3-like proteins regulate polarity and endocytosis of PIN-FORMED auxin efflux carriers. Development. 2011;138:2069–2078. PubMed
Furutani M., Nakano Y., Tasaka M. MAB4-induced auxin sink generates local auxin gradients in Arabidopsis organ formation. Proc. Natl. Acad. Sci. USA. 2014;111:1198–1203. PubMed PMC
Bennett S.R.M., Alvarez J., Bossinger G., Smyth D.R. Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 1995;8:505–520.
Robert H.S., Quint A., Brand D., Vivian-Smith A., Offringa R. BTB and TAZ domain scaffold proteins perform a crucial function in Arabidopsis development. Plant J. 2009;58:109–121. PubMed
Preuten T., Hohm T., Bergmann S., Fankhauser C. Defining the site of light perception and initiation of phototropism in Arabidopsis. Curr. Biol. 2013;23:1934–1938. PubMed
Liscum E., Nittler P., Koskie K. The continuing arc toward phototropic enlightenment. J. Exp. Bot. 2020;71:1652–1658. PubMed PMC
Tan S., Luschnig C., Friml J. Pho-view of auxin: reversible protein phosphorylation in auxin biosynthesis, transport and signaling. Mol. Plant. 2021;14:151–165. PubMed
Barbosa I.C.R., Hammes U.Z., Schwechheimer C. Activation and polarity control of PIN-FORMED auxin transporters by phosphorylation. Trends Plant Sci. 2018;23:523–538. PubMed
Vieten A., Vanneste S., Wisniewska J., Benková E., Benjamins R., Beeckman T., Luschnig C., Friml J. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development. 2005;132:4521–4531. PubMed
Weller B., Zourelidou M., Frank L., Barbosa I.C.R., Fastner A., Richter S., Jürgens G., Hammes U.Z., Schwechheimer C. Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux-dependent growth. Proc. Natl. Acad. Sci. USA. 2017;114:E887–E896. PubMed PMC
Zourelidou M., Absmanner B., Weller B., Barbosa I.C., Willige B.C., Fastner A., Streit V., Port S.A., Colcombet J., de la Fuente van Bentem S. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife. 2014;3:e02860. PubMed PMC
Kleine-Vehn J., Huang F., Naramoto S., Zhang J., Michniewicz M., Offringa R., Friml J. 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
Barbosa I.C.R., Zourelidou M., Willige B.C., Weller B., Schwechheimer C. D6 PROTEIN KINASE activates auxin transport-dependent growth and PIN-FORMED phosphorylation at the plasma membrane. Dev. Cell. 2014;29:674–685. PubMed
Kleine-Vehn J., Łangowski Ł., Wisniewska J., Dhonukshe P., Brewer P.B., Friml J. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol. Plant. 2008;1:1056–1066. PubMed
Simon M.L.A., Platre M.P., Marquès-Bueno M.M., Armengot L., Stanislas T., Bayle V., Caillaud M.-C., Jaillais Y. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nat. Plants. 2016;2:16089. PubMed PMC
Zegzouti H., Li W., Lorenz T.C., Xie M., Payne C.T., Smith K., Glenny S., Payne G.S., Christensen S.K. Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. J. Biol. Chem. 2006;281:35520–35530. PubMed
Tan S., Zhang X., Kong W., Yang X.-L., Molnár G., Vondráková Z., Filepová R., Petrášek J., Friml J., Xue H.-W. The lipid code-dependent phosphoswitch PDK1-D6PK activates PIN-mediated auxin efflux in Arabidopsis. Nat. Plants. 2020;6:556–569. PubMed
Dejonghe W., Kuenen S., Mylle E., Vasileva M., Keech O., Viotti C., Swerts J., Fendrych M., Ortiz-Morea F.A., Mishev K. Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification. Nat. Commun. 2016;7:11710. PubMed PMC
Kitakura S., Vanneste S., Robert S., Löfke C., Teichmann T., Tanaka H., Friml J. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell. 2011;23:1920–1931. PubMed PMC
Dhonukshe P., Aniento F., Hwang I., Robinson D.G., Mravec J., Stierhof Y.-D.D., Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 2007;17:520–527. PubMed
Adamowski M., Narasimhan M., Kania U., Glanc M., De Jaeger G., Friml J. A functional study of AUXILIN-LIKE1 and 2, two putative clathrin uncoating factors in Arabidopsis. Plant Cell. 2018;30:700–716. PubMed PMC
Glanc M., Fendrych M., Friml J. Mechanistic framework for cell-intrinsic re-establishment of PIN2 polarity after cell division. Nat. Plants. 2018;4:1082–1088. PubMed PMC
Łangowski Ł., Wabnik K., Li H., Vanneste S., Naramoto S., Tanaka H., Friml J. Cellular mechanisms for cargo delivery and polarity maintenance at different polar domains in plant cells. Cell Discov. 2016;2:16018. PubMed PMC
Ke M., Ma Z., Wang D., Sun Y., Wen C., Huang D., Chen Z., Yang L., Tan S., Li R. Salicylic acid regulates PIN2 auxin transporter hyperclustering and root gravitropic growth via Remorin-dependent lipid nanodomain organisation in Arabidopsis thaliana. New Phytol. 2020;229:963–978. PubMed PMC
Martinière A., Lavagi I., Nageswaran G., Rolfe D.J., Maneta-Peyret L., Luu D.-T., Botchway S.W., Webb S.E.D., Mongrand S., Maurel C. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc. Natl. Acad. Sci. USA. 2012;109:12805–12810. PubMed PMC
Men S., Boutté Y., Ikeda Y., Li X., Palme K., Stierhof Y.-D., Hartmann M.-A., Moritz T., Grebe M. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 2008;10:237–244. PubMed
Sabatini S., Beis D., Wolkenfelt H., Murfett J., Guilfoyle T., Malamy J., Benfey P., Leyser O., Bechtold N., Weisbeek P., Scheres B. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell. 1999;99:463–472. PubMed
Teale W.D., Pasternak T., Dal Bosco C., Dovzhenko A., Kratzat K., Bildl W., Schwörer M., Falk T., Ruperti B., Schaefer J.V. Flavonol-mediated stabilization of PIN efflux complexes regulates polar auxin transport. EMBO J. 2021;40:e104416. PubMed PMC
Li H., von Wangenheim D., Zhang X., Tan S., Darwish-Miranda N., Naramoto S., Wabnik K., De Rycke R., Kaufmann W.A., Gütl D. Cellular requirements for PIN polar cargo clustering in Arabidopsis thaliana. New Phytol. 2021;229:351–369. PubMed PMC
Yoshida S., van der Schuren A., van Dop M., van Galen L., Saiga S., Adibi M., Möller B., Ten Hove C.A., Marhavy P., Smith R. A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis. Nat. Plants. 2019;5:160–166. PubMed PMC
van Dop M., Fiedler M., Mutte S., de Keijzer J., Olijslager L., Albrecht C., Liao C.-Y., Janson M.E., Bienz M., Weijers D. DIX domain polymerization drives assembly of plant cell polarity complexes. Cell. 2020;180:427–439.e12. PubMed PMC
Marhavá P., Bassukas A.E.L., Zourelidou M., Kolb M., Moret B., Fastner A. A molecular rheostat adjusts auxin flux to promote root protophloem differentiation. Nature. 2018;558:297–300. PubMed
Zourelidou M., Müller I., Willige B.C., Nill C., Jikumaru Y., Li H., Schwechheimer C. The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development. 2009;136:627–636. PubMed
Wells C.D., Fawcett J.P., Traweger A., Yamanaka Y., Goudreault M., Elder K., Kulkarni S., Gish G., Virag C., Lim C. A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell. 2006;125:535–548. PubMed
Winckler B., Forscher P., Mellman I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature. 1999;397:698–701. 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
Kubátová Z., Pejchar P., Potocký M., Sekereš J., Žárský V., Kulich I. Arabidopsis trichome contains two plasma membrane domains with different lipid compositions which attract distinct EXO70 subunits. Int. J. Mol. Sci. 2019;20:3803. PubMed PMC
Kania U., Fendrych M., Friml J. Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol. 2014;4:140017. PubMed PMC
Marhavá P., Aliaga Fandino A.C., Koh S.W.H., Jelínková A., Kolb M., Janacek D.P. Plasma membrane domain patterning and self-reinforcing polarity in Arabidopsis. Dev. Cell. 2020;52:223–235.e5. PubMed
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
Mao H., Nakamura M., Viotti C., Grebe M. A framework for lateral membrane trafficking and polar tethering of the PEN3 ATP-binding cassette transporter. Plant Physiol. 2016;172:2245–2260. PubMed PMC
Chiou J.G., Balasubramanian M.K., Lew D.J. Cell polarity in yeast. Annu. Rev. Cell Dev. Biol. 2017;33:77–101. PubMed PMC
Baster P., Robert S., Kleine-Vehn J., Vanneste S., Kania U., Grunewald W., De Rybel B., Beeckman T., Friml J. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 2013;32:260–274. PubMed PMC
Abas L., Benjamins R., Malenica N., Paciorek T., Wiśniewska J., Moulinier-Anzola J.C., Sieberer T., Friml J., Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 2006;8:249–256. PubMed
Friml J., Benková E., Blilou I., Wisniewska J., Hamann T., Ljung K., Woody S., Sandberg G., Scheres B., Jürgens G., Palme K. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell. 2002;108:661–673. 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
Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. PubMed PMC
de Chaumont F., Dallongeville S., Chenouard N., Hervé N., Pop S., Provoost T., Meas-Yedid V., Pankajakshan P., Lecomte T., Le Montagner Y. Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods. 2012;9:690–696. PubMed
R Core Team . R Foundation for Statistical Computing; 2017. R: a language and environment for statistical computing.https://www.R-project.org/
RStudio Team . RStudio; 2020. RStudio: integrated development for R.https://www.rstudio.com/
Wickham H. Springer-Verlag; 2009. ggplot2: Elegant Graphics for Data Analysis.http://ggplot2.org
Clough S.J., Bent A.F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. PubMed
Salanenka Y., Verstraeten I., Löfke C., Tabata K., Naramoto S., Glanc M., Friml J. Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. Proc. Natl. Acad. Sci. USA. 2018;115:3716–3721. PubMed PMC
Yu H., Zhang Y., Moss B.L., Bargmann B.O.R., Wang R., Prigge M., Nemhauser J.L., Estelle M. Untethering the TIR1 auxin receptor from the SCF complex increases its stability and inhibits auxin response. Nat. Plants. 2015;1:14030. PubMed PMC
Curtis M.D., Grossniklaus U. A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 2003;133:462–469. PubMed PMC
Gleave A.P. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 1992;20:1203–1207. PubMed
Sawano A., Miyawaki A. Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res. 2000;28:e78. PubMed PMC
Schirawski J., Planchais S., Haenni A.L. An improved protocol for the preparation of protoplasts from an established Arabidopsis thaliana cell suspension culture and infection with RNA of turnip yellow mosaic tymovirus: a simple and reliable method. J. Virol. Methods. 2000;86:85–94. PubMed
Meskiene I., Baudouin E., Schweighofer A., Liwosz A., Jonak C., Rodriguez P.L., Jelinek H., Hirt H. Stress-induced protein phosphatase 2C is a negative regulator of a mitogen-activated protein kinase. J. Biol. Chem. 2003;278:18945–18952. PubMed
Fülöp K., Pettkó-Szandtner A., Magyar Z., Miskolczi P., Kondorosi E., Dudits D., Bakó L. The Medicago CDKC;1-CYCLINT;1 kinase complex phosphorylates the carboxy-terminal domain of RNA polymerase II and promotes transcription. Plant J. 2005;42:810–820. PubMed
Sauer M., Paciorek T., Benková E., Friml J. Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat. Protoc. 2006;1:98–103. PubMed