The lipid code-dependent phosphoswitch PDK1-D6PK activates PIN-mediated auxin efflux in Arabidopsis
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
PubMed
32393881
DOI
10.1038/s41477-020-0648-9
PII: 10.1038/s41477-020-0648-9
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis metabolismus MeSH
- buněčná membrána metabolismus MeSH
- fosfolipidy metabolismus MeSH
- kyseliny indoloctové metabolismus MeSH
- membránové transportní proteiny metabolismus fyziologie MeSH
- proteinkinasy PDK fyziologie MeSH
- proteiny huseníčku fyziologie MeSH
- regulátory růstu rostlin metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- fosfolipidy MeSH
- kyseliny indoloctové MeSH
- membránové transportní proteiny MeSH
- proteinkinasy PDK MeSH
- proteiny huseníčku MeSH
- regulátory růstu rostlin MeSH
Directional intercellular transport of the phytohormone auxin mediated by PIN-FORMED (PIN) efflux carriers has essential roles in both coordinating patterning processes and integrating multiple external cues by rapidly redirecting auxin fluxes. PIN activity is therefore regulated by multiple internal and external cues, for which the underlying molecular mechanisms are not fully elucidated. Here, we demonstrate that 3'-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASE1 (PDK1), which is conserved in plants and mammals, functions as a molecular hub that perceives upstream lipid signalling and modulates downstream substrate activity through phosphorylation. Using genetic analysis, we show that the loss-of-function Arabidopsis pdk1.1 pdk1.2 mutant exhibits a plethora of abnormalities in organogenesis and growth due to defective polar auxin transport. Further cellular and biochemical analyses reveal that PDK1 phosphorylates D6 protein kinase, a well-known upstream activator of PIN proteins. We uncover a lipid-dependent phosphorylation cascade that connects membrane-composition-based cellular signalling with plant growth and patterning by regulating morphogenetic auxin fluxes.
Institute of Experimental Botany The Czech Academy of Sciences Prague Czech Republic
Institute of Science and Technology Austria Klosterneuburg Austria
Zobrazit více v PubMed
Swarup, K. et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946–954 (2008). PubMed DOI
Petrášek, J. et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918 (2006). PubMed DOI
Adamowski, M. & Friml, J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27, 20–32 (2015). PubMed DOI PMC
Geisler, M. et al. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44, 179–194 (2005). PubMed DOI
Armengot, L., Marquès-Bueno, M. M. & Jaillais, Y. Regulation of polar auxin transport by protein and lipid kinases. J. Exp. Bot. 67, 4015–4037 (2016). PubMed DOI
Friml, J. et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862–865 (2004). PubMed DOI
Dhonukshe, P. et al. Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137, 3245–3255 (2010). PubMed DOI
Grones, P. et al. PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism. Sci. Rep. 8, 10279 (2018). PubMed DOI PMC
Zourelidou, M. et al. The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136, 627–636 (2009). PubMed DOI
Zourelidou, M. et al. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3, e02860 (2014). DOI PMC
Marhava, P. et al. A molecular rheostat adjusts auxin flux to promote root protophloem differentiation. Nature 558, 297–300 (2018). PubMed DOI
Jia, W. et al. Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating PIN1 in Arabidopsis. PLoS Biol. 14, e1002550 (2016). PubMed DOI PMC
Dory, M. et al. Coevolving MAPK and PID phosphosites indicate an ancient environmental control of PIN auxin transporters in land plants. FEBS Lett. 592, 89–102 (2018). PubMed DOI
Rigó, G. et al. Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25, 1592–1608 (2013). PubMed DOI PMC
Michniewicz, M. et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044–1056 (2007). PubMed DOI
Dai, M. et al. A PP6-type phosphatase holoenzyme directly regulates PIN phosphorylation and auxin efflux in Arabidopsis. Plant Cell 24, 2497–2514 (2012). PubMed DOI PMC
Guo, X. et al. TYPE-ONE PROTEIN PHOSPHATASE4 regulates pavement cell interdigitation by modulating PIN-FORMED1 polarity and trafficking in Arabidopsis. Plant Physiol. 167, 1058–1075 (2015). PubMed DOI 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. USA 114, E887–E896 (2017). PubMed DOI PMC
Laetitia, M. et al. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nat. Plants 2, 16089 (2016). DOI
Wang, P. et al. Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED 2 auxin efflux transporter in response to salt stress. Plant Cell 31, 250–271 (2019). PubMed DOI
Barbosa, I. C. R. et al. Phospholipid composition and a polybasic motif determine D6 PROTEIN KINASE polar association with the plasma membrane and tropic responses. Development 143, 4687–4700 (2016). PubMed
Pearce, L. R., Komander, D. & Alessi, D. R. The nuts and bolts of AGC protein kinases. Nat. Rev. Mol. Cell Biol. 11, 9–22 (2010). PubMed DOI
Rintelen, F., Stocker, H., Thomas, G. & Hafen, E. PDK1 regulates growth through Akt and S6K in Drosophila. Proc. Natl. Acad. Sci. USA 98, 15020–15025 (2001). PubMed DOI PMC
Lawlor, M. A. et al. Essential role of PDK1 in regulating cell size and development in mice. EMBO J. 21, 3728–3738 (2002). PubMed DOI PMC
Deak, M., Casamayor, A., Currie, R. A., Peter Downes, C. & Alessi, D. R. Characterisation of a plant 3-phosphoinositide-dependent protein kinase-1 homologue which contains a pleckstrin homology domain. FEBS Lett. 451, 220–226 (1999). PubMed DOI
Rentel, M. C. et al. OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858–861 (2004). PubMed DOI
Anthony, R. G., Khan, S., Costa, J., Pais, M. S. & Bögre, L. The Arabidopsis protein kinase PTI1-2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J. Biol. Chem. 281, 37536–37546 (2006). PubMed DOI
Camehl, I. et al. The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathog. 7, e1002051 (2011). PubMed DOI PMC
Anthony, R. G. et al. A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J. 23, 572–581 (2004). PubMed DOI PMC
Rademacher, E. H. & Offringa, R. Evolutionary adaptations of plant AGC kinases: from light signaling to cell polarity regulation. Front. Plant Sci. 3, 250 (2012). PubMed DOI PMC
Zegzouti, H. et al. Structural and functional insights into the regulation of Arabidopsis AGC VIIIa kinases. J. Biol. Chem. 281, 35520–35530 (2006). PubMed DOI
Scholz, S. et al. The AGC protein kinase UNICORN controls planar growth by attenuating PDK1 in Arabidopsis thaliana. PLoS Genet. 15, e1007927 (2019). PubMed DOI PMC
Xiao, Y. & Offringa, R. PDK1 regulates auxin transport and Arabidopsis vascular development through AGC1 kinase PAX. Nat. Plants https://doi.org/10.1038/s41477-020-0650-2 (2020).
Friml, J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661–673 (2002). PubMed DOI
Band, L. R. et al. Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc. Natl Acad. Sci. USA 109, 4668–4673 (2012). PubMed DOI PMC
Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999). PubMed DOI
Friml, J. et al. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426, 147–153 (2003). PubMed DOI
Prát, T. et al. WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genet. 14, e1007177 (2018). PubMed DOI PMC
Zadnikova, P. et al. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137, 607–617 (2010). PubMed DOI
Stepanova, A. N. et al. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177–191 (2008). PubMed DOI
Friml, J., Wiśniewska, J., Benková, E., Mendgen, K. & Palme, K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002). PubMed DOI
Gray, W. M., Ostin, A., Sandberg, G., Romano, C. P. & Estelle, M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7197–7202 (2002). DOI
Franklin, K. A. et al. PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl Acad. Sci. USA 108, 20231–20235 (2011). PubMed DOI PMC
Parry, G. & Estelle, M. Auxin receptors: a new role for F-box proteins. Curr. Opin. Cell Biol. 18, 152–156 (2006). PubMed DOI
Brumos, J. et al. Local auxin biosynthesis is a key regulator of plant development. Dev. Cell 47, 306–318 (2018). PubMed DOI
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. 12, 2175–2187 (1998). PubMed DOI PMC
Swarup, R. et al. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057–1065 (2005). PubMed DOI
Zegzouti, H., Anthony, R. G., Jahchan, N., Bogre, L. & Christensen, S. K. Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc. Natl Acad. Sci. USA 103, 6404–6409 (2006). PubMed DOI PMC
Zhang, J., Nodzynski, T., Pencik, A., Rolcik, J. & Friml, J. PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc. Natl Acad. Sci. USA 107, 918–922 (2010). PubMed DOI
Van Leeuwen, W., Ökrész, L., Bögre, L. & Munnik, T. Learning the lipid language of plant signalling. Trends Plant Sci. 9, 378–384 (2004). PubMed DOI
Geldner, N. et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230 (2003). PubMed DOI
Noack, L. C. & Jaillais, Y. Precision targeting by phosphoinositides: how PIs direct endomembrane trafficking in plants. Curr. Opin. Plant Biol. 40, 22–33 (2017). PubMed DOI
Platre, M. P. et al. Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine. Science 364, 57–62 (2019). PubMed DOI
Mei, Y., Jia, W., Chu, Y. & Xue, H. Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins. Cell Res. 22, 581–597 (2011). PubMed DOI PMC
Stenzel, I. et al. Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis. Plant Cell 25, 4894–4911 (2013). PubMed PMC
Tejos, R. et al. Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 26, 2114–2128 (2014). PubMed DOI PMC
Gao, H. B., Chu, Y. J. & Xue, H. W. Phosphatidic acid (PA) binds PP2AA1 to regulate PP2A activity and PIN1 polar localization. Mol. Plant 6, 1692–1702 (2013). PubMed DOI
Zhang, J. et al. Inositol trisphosphate-induced Ca PubMed DOI
Xu, J. et al. A molecular framework for plant regeneration. Science 311, 385–388 (2006). PubMed DOI
Benková, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003). PubMed DOI
Xu, J. & Scheres, B. Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17, 525–536 (2005). PubMed DOI PMC
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998). PubMed DOI
Liu, W., Xu, Z. H., Luo, D. & Xue, H. W. Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J. 36, 189–202 (2003). PubMed DOI
Rook, F. et al. Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J. 15, 253–263 (1998). PubMed DOI
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). PubMed DOI
Baster, P. et al. SCFTIR1/AFB-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 32, 260–274 (2013). PubMed DOI
Abas, L. et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8, 249–256 (2006). PubMed DOI
Lewis, D. R. & Muday, G. K. Measurement of auxin transport in Arabidopsis thaliana. Nat. Protoc. 4, 437–451 (2009). PubMed DOI
Tan, S. et al. Salicylic acid targets protein phosphatase 2A to attenuate growth in plants. Curr. Biol. 30, 381–395 (2020). PubMed DOI PMC
Exploring lipid-protein interactions in plant membranes
Phosphatidic Acid in Plant Hormonal Signaling: From Target Proteins to Membrane Conformations
AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells
Dissecting Hierarchies between Light, Sugar and Auxin Action Underpinning Root and Root Hair Growth