A nanodomain-anchored scaffolding complex is required for the function and localization of phosphatidylinositol 4-kinase alpha in plants

. 2022 Jan 20 ; 34 (1) : 302-332.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34010411

Phosphoinositides are low-abundant lipids that participate in the acquisition of membrane identity through their spatiotemporal enrichment in specific compartments. Phosphatidylinositol 4-phosphate (PI4P) accumulates at the plant plasma membrane driving its high electrostatic potential, and thereby facilitating interactions with polybasic regions of proteins. PI4Kα1 has been suggested to produce PI4P at the plasma membrane, but how it is recruited to this compartment is unknown. Here, we pin-point the mechanism that tethers Arabidopsis thaliana phosphatidylinositol 4-kinase alpha1 (PI4Kα1) to the plasma membrane via a nanodomain-anchored scaffolding complex. We established that PI4Kα1 is part of a complex composed of proteins from the NO-POLLEN-GERMINATION, EFR3-OF-PLANTS, and HYCCIN-CONTAINING families. Comprehensive knockout and knockdown strategies revealed that subunits of the PI4Kα1 complex are essential for pollen, embryonic, and post-embryonic development. We further found that the PI4Kα1 complex is immobilized in plasma membrane nanodomains. Using synthetic mis-targeting strategies, we demonstrate that a combination of lipid anchoring and scaffolding localizes PI4Kα1 to the plasma membrane, which is essential for its function. Together, this work opens perspectives on the mechanisms and function of plasma membrane nanopatterning by lipid kinases.

Komentář v

PubMed

Zobrazit více v PubMed

Antignani V, Klocko AL, Bak G, Chandrasekaran SD, Dunivin T, Nielsen E (2015) Recruitment of PLANT U-BOX13 and the PI4Kβ1/β2 phosphatidylinositol-4 kinases by the small GTPase RabA4B plays important roles during salicylic acid-mediated plant defense signaling in Arabidopsis. Plant Cell  27: 243–261 PubMed PMC

Ashkenazy H, Abadi S, Martz E, Chay O, Mayrose I, Pupko T, Ben-Tal N (2016) ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res  44: W344–350 PubMed PMC

Audhya A, Emr SD (2002) Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev Cell  2: 593–605 PubMed

Audhya A, Foti M, Emr SD (2000) Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol Biol Cell  11: 2673–2689 PubMed PMC

Baird D, Stefan C, Audhya A, Weys S, Emr SD (2008) Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3. J Cell Biol  183: 1061–1074 PubMed PMC

Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA  98: 10037–10041 PubMed PMC

Balla A, Tuymetova G, Barshishat M, Geiszt M, Balla T (2002) Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J Biol Chem  277: 20041–20050 PubMed

Balla A, Tuymetova G, Tsiomenko A, Várnai P, Balla T (2005) A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. MBoC  16: 1282–1295 PubMed PMC

Barbosa ICR, Shikata H, Zourelidou M, Heilmann M, Heilmann I, Schwechheimer C (2016) Phospholipid composition and a polybasic motif determine D6 PROTEIN KINASE polar association with the plasma membrane and tropic responses. Development  143: 4687–4700 PubMed

Baskin JM, Wu X, Christiano R, Oh MS, Schauder CM, Gazzerro E, Messa M, Baldassari S, Assereto S, Biancheri R, et al. (2016) The leukodystrophy protein FAM126A/Hyccin regulates PI4P synthesis at the plasma membrane. Nat Cell Biol  18: 132–138 PubMed PMC

Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell  23: 886–895 PubMed

Bloch D, Pleskot R, Pejchar P, Potocký M, Trpkošová P, Cwiklik L, Vukašinović N, Sternberg H, Yalovsky S, Žárský V (2016) Exocyst SEC3 and phosphoinositides define sites of exocytosis in pollen tube initiation and growth. Plant Physiol  172: 980–1002 PubMed PMC

Borg M, Twell D (2011). Pollen: structure and development. In eLS. John Wiley & Sons, Ltd: Chichester. American Cancer Society, Atlanta, GA. pp 1–11 10.1002/9780470015902.a0002039.pub2 DOI

Bürstenbinder K, Savchenko T, Müller J, Adamson AW, Stamm G, Kwong R, Zipp BJ, Dinesh DC, Abel S (2013) Arabidopsis calmodulin-binding protein IQ67-domain 1 localizes to microtubules and interacts with kinesin light chain-related protein-1. J Biol Chem  288: 1871–1882 PubMed PMC

Bürstenbinder K, Möller B, Plötner R, Stamm G, Hause G, Mitra D, Abel S (2017) The IQD family of calmodulin-binding proteins links calcium signaling to microtubules, membrane subdomains, and the nucleus. Plant Physiol  173: 1692–1708 PubMed PMC

Carroll AD, Moyen C, Kesteren PV, Tooke F, Battey NH, Brownlee C (1998) Ca2+, annexins, and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell  10: 1267–1276 PubMed PMC

de Jong F, Munnik T (2021) Attracted to membranes: lipid-binding domains in plants. Plant Physiol. 185:707–723 PubMed PMC

Delage E, Ruelland E, Guillas I, Zachowski A, Puyaubert J (2012) Arabidopsis type-III phosphatidylinositol 4-kinases β1 and β2 are upstream of the phospholipase C pathway triggered by cold exposure. Plant Cell Physiol  53: 565–576 PubMed

Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res  32: W665–W667 PubMed PMC

Dornan GL, Dalwadi U, Hamelin DJ, Hoffmann RM, Yip CK, Burke JE (2018) Probing the architecture, dynamics, and inhibition of the PI4KIIIα/TTC7/FAM126 complex. J Mol Biol  430: 3129–3142 PubMed

Dubois Gwennogan A, Jaillais Y (2021) Anionic phospholipid gradients: an uncharacterized frontier of the plant endomembrane network. Plant Physiol  185: 577–592 PubMed PMC

Elsayad K, Werner S, Gallemi M, Kong J, Sanchez Guajardo ER, Zhang L, Jaillais Y, Greb T, Belkhadir Y (2016) Mapping the subcellular mechanical properties of live cells in tissues with fluorescence emission-Brillouin imaging. Sci Signal  9: rs5. PubMed

Foti M, Audhya A, Emr SD (2001) Sac1 lipid phosphatase and Stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology. MBoC  12: 2396–2411 PubMed PMC

Fratini M, Krishnamoorthy P, Stenzel I, Riechmann M, Matzner M, Bacia K, Heilmann M, Heilmann I (2021) Plasma membrane nano-organization specifies phosphoinositide effects on Rho-GTPases and actin dynamics in tobacco pollen tubes. Plant Cell  33: 642–670 PubMed PMC

Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell  153: 1494–1509 PubMed PMC

Golovkin M, Reddy ASN (2003) A calmodulin-binding protein from Arabidopsis has an essential role in pollen germination. Proc Natl Acad Sci U S A  100: 10558–10563 PubMed PMC

Hammond GRV, Schiavo G, Irvine RF (2009) Immunocytochemical techniques reveal multiple, distinct cellular pools of PtdIns4P and PtdIns(4,5)P2. Biochem J  422: 23–35 PubMed PMC

Hammond GRV, Machner MP, Balla T (2014) A novel probe for phosphatidylinositol 4-phosphate reveals multiple pools beyond the Golgi. J Cell Biol  205: 113–126 PubMed PMC

Hepler PK (2016) The cytoskeleton and its regulation by calcium and protons. Plant Physiol  170: 3–22 PubMed PMC

Himschoot E, Pleskot R, Van Damme D, Vanneste S (2017) The ins and outs of Ca2+ in plant endomembrane trafficking. Curr Opin Plant Biol  40: 131–137 PubMed

Hirano T, Stecker K, Munnik T, Xu H, Sato MH (2017) Visualization of phosphatidylinositol 3,5-bisphosphate dynamics by a tandem ML1N-based fluorescent protein probe in Arabidopsis. Plant Cell Physiol  58: 1185–1195 PubMed PMC

Honkanen S, Jones VAS, Morieri G, Champion C, Hetherington AJ, Kelly S, Proust H, Saint-Marcoux D, Prescott H, Dolan L (2016) The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr Biol  26: 3238–3244 PubMed PMC

Idevall-Hagren O, Lü A, Xie B, De Camilli P (2015) Triggered Ca2+ influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering. EMBO J  34: 2291–2305 PubMed PMC

Jaillais Y, Ott T (2020) The nanoscale organization of the plasma membrane and its importance in signaling: a proteolipid perspective. Plant Physiol  182: 1682–1696 PubMed PMC

Jaillais Y, Hothorn M, Belkhadir Y, Dabi T, Nimchuk ZL, Meyerowitz EM, Chory J (2011) Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor. Genes Dev  25: 232–237 PubMed PMC

Källberg M, Wang H, Wang S, Peng J, Wang Z, Lu H, Xu J (2012) Template-based protein structure modeling using the RaptorX web server. Nat Protoc  7: 1511–1522 PubMed PMC

Kang B-H, Nielsen E, Preuss ML, Mastronarde D, Staehelin LA (2011) Electron tomography of RabA4b- and PI-4Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic  12: 313–329 PubMed

Karimi M, Bleys A, Vanderhaeghen R, Hilson P (2007) Building blocks for plant gene assembly. Plant Physiol  145: 1183–1191 PubMed PMC

Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci  7: 193–195 PubMed

Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol  145: 317–330 PubMed PMC

Kumar M, Carr P, Turner S (2020) An atlas of Arabidopsis protein S-Acylation reveals its widespread role in plant cell organisation of and function. DOI: 10.1101/2020.05.12.090415 PubMed

Lee BH, Weber ZT, Zourelidou M, Hofmeister BT, Schmitz RJ, Schwechheimer C, Dobritsa AA (2018) Arabidopsis protein kinase D6PKL3 is involved in the formation of distinct plasma membrane aperture domains on the pollen surface. Plant Cell  30: 2038–2056 PubMed PMC

Lee E, Vanneste S, Pérez-Sancho J, Benitez-Fuente F, Strelau M, Macho AP, Botella MA, Friml J, Rosado A (2019) Ionic stress enhances ER–PM connectivity via phosphoinositide-associated SYT1 contact site expansion in Arabidopsis. Proc Natl Acad Sci U S A  116: 1420–1429 PubMed PMC

Lees JA, Zhang Y, Oh MS, Schauder CM, Yu X, Baskin JM, Dobbs K, Notarangelo LD, Camilli PD, Walz T, et al. (2017) Architecture of the human PI4KIIIα lipid kinase complex. Proc Natl Acad Sci U S A  114: 13720–13725 PubMed PMC

Lemmon MA (2008) Membrane recognition by phospholipid-binding domains. Nat Rev Mol Cell Biol  9: 99–111 PubMed

Levine TP, Munro S (1998) The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr Biol  8: 729–739 PubMed

Levine TP, Munro S (2002) Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr Biol  12: 695–704 PubMed

Li L, Shi X, Guo X, Li H, Xu C (2014) Ionic protein–lipid interaction at the plasma membrane: what can the charge do?  Trends Biochem Sci  39: 130–140 PubMed

Li Y, Tan X, Wang M, Li B, Zhao Y, Wu C, Rui Q, Wang J, Liu Z, Bao Y (2017) Exocyst subunit SEC3A marks the germination site and is essential for pollen germination in Arabidopsis thaliana. Sci Rep  7: 1–11 PubMed PMC

Lin F, Krishnamoorthy P, Schubert V, Hause G, Heilmann M, Heilmann I (2019) A dual role for cell plate-associated PI4Kβ in endocytosis and phragmoplast dynamics during plant somatic cytokinesis. EMBO J  38: 1–26 PubMed PMC

Marquès-Bueno MM, Morao AK, Cayrel A, Platre MP, Barberon M, Caillieux E, Colot V, Jaillais Y, Roudier F, Vert G (2016) A versatile multisite gateway-compatible promoter and transgenic line collection for cell type-specific functional genomics in Arabidopsis. Plant J  85: 320–333 PubMed PMC

Martinière A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L, Luu D-T, Botchway SW, Webb SED, Mongrand S, Maurel C, et al. (2012) Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci U S A  109: 12805–12810 PubMed PMC

McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature  438: 605–611 PubMed

Miyamoto Y, Torii T, Eguchi T, Nakamura K, Tanoue A, Yamauchi J (2014) Hypomyelinating leukodystrophy-associated missense mutant of FAM126A/hyccin/DRCTNNB1A aggregates in the endoplasmic reticulum. J Clin Neurosci  21: 1033–1039 PubMed

Mueller-Roeber B, Pical C (2002) Inositol phospholipid metabolism in Arabidopsis. Characterized and Putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol  130: 22–46 PubMed PMC

Munnik T, Nielsen E (2011) Green light for polyphosphoinositide signals in plants. Curr Opin Plant Biol  14: 489–497 PubMed

Munnik T, Vermeer JEM (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ  33: 655–669 PubMed

Munnik T, Zarza X (2013) Analyzing plant signaling phospholipids through 32Pi-labeling and TLC. Methods Mol Biol  1009: 3–15 PubMed

Nakatsu F, Baskin JM, Chung J, Tanner LB, Shui G, Lee SY, Pirruccello M, Hao M, Ingolia NT, Wenk MR, et al. (2012) PtdIns4P synthesis by PI4KIIIα at the plasma membrane and its impact on plasma membrane identity. J Cell Biol  199: 1003–1016 PubMed PMC

Noack LC, Jaillais Y (2017) Precision targeting by phosphoinositides: how PIs direct endomembrane trafficking in plants. Curr Opin Plant Biol  40: 22–33 PubMed

Noack LC, Jaillais Y (2020) Functions of anionic lipids in plants. Annu Rev Plant Biol  71: 71–102 PubMed

Okazaki K, Miyagishima S, Wada H  (2015).  Phosphatidylinositol 4-phosphate negatively regulates chloroplast division in Arabidopsis. The Plant Cell  27: 663–674 PubMed PMC

Omnus DJ, Cadou A, Chung GHC, Bader JM, Stefan CJ (2018) A cytoplasmic GOLD protein controls cell polarity. BioRxiv  379057: 1–44 10.1101/379057

Pérez-Sancho J, Vanneste S, Lee E, McFarlane HE, Valle AE, Valpuesta V, Friml J, Botella MA, Rosado A (2015) The Arabidopsis synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol  168: 132–143 PubMed PMC

Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci U S A  104: 15566–15571 PubMed PMC

Pettersen EF, Goddard TD, Huang CC, Meng EC, Couch GS, Croll TI, Morris JH, Ferrin TE (2021) UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci  30: 70–82 PubMed PMC

Platre MP, Noack LC, Doumane M, Bayle V, Simon MLA, Maneta-Peyret L, Fouillen L, Stanislas T, Armengot L, Pejchar P, et al. (2018) A combinatorial lipid code shapes the electrostatic landscape of plant endomembranes. Dev Cell  45: 465–480 PubMed

Preuss ML, Schmitz AJ, Thole JM, Bonner HKS, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol  172: 991–998 PubMed PMC

Roy A, Levine TP (2004) Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p. J Biol Chem  279: 44683–44689 PubMed

Rozier F, Mirabet V, Vernoux T, Das P (2014) Analysis of 3D gene expression patterns in plants using whole-mount RNA in situ hybridization. Nat Protoc  9: 2464–2475 PubMed

Ruiz-Lopez N, Pérez-Sancho J, Valle AE, Haslam RP, Vanneste S, Catalá R, Perea-Resa C, Damme DV, García-Hernández S, Albert A, et al. (2021) Synaptotagmins at the endoplasmic reticulum-plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. Plant Cell:1–23 10.1093/plcell/koab122. Epub ahead of print. PMID: 33944955 PubMed DOI PMC

Šašek V, Janda M, Delage E, Puyaubert J, Guivarc’h A, López Maseda E, Dobrev PI, Caius J, Bóka K, Valentová O, et al. (2014) Constitutive salicylic acid accumulation in pi4kIIIβ1β2 Arabidopsis plants stunts rosette but not root growth. New Phytol  203: 805–816 PubMed

Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, et al. (2008) Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell  20: 3374–3388 PubMed PMC

Shin S-B, Golovkin M, Reddy ASN (2014) A pollen-specific calmodulin-binding protein, NPG1, interacts with putative pectate lyases. Sci Rep  4: 1–8 PubMed PMC

Siligato R, Wang X, Yadav SR, Lehesranta S, Ma G, Ursache R, Sevilem I, Zhang J, Gorte M, Prasad K, et al. (2016) Multisite gateway-compatible cell type-specific gene-inducible system for plants. Plant Physiol  170: 627–641 PubMed PMC

Simon MLA, Platre MP, Assil S, van Wijk R, Chen WY, Chory J, Dreux M, Munnik T, Jaillais Y (2014) A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J  77: 322–337 PubMed PMC

Simon MLA, Platre MP, Marquès-Bueno MM, Armengot L, Stanislas T, Bayle V, Caillaud M-C, Jaillais Y (2016) A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nat Plants  2: 1–10 PubMed PMC

Simon-Plas F, Elmayan T, Blein J-P (2002) The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J  31: 137–147 PubMed

Stevenson JM, Perera IY, Boss WF (1998) A phosphatidylinositol 4-kinase pleckstrin homology domain that binds phosphatidylinositol 4-monophosphate. J Biol Chem  273: 22761–22767 PubMed

Stevenson-Paulik J, Love J, Boss WF (2003) Differential regulation of two Arabidopsis type III phosphatidylinositol 4-kinase isoforms. A regulatory role for the pleckstrin homology domain. Plant Physiol  132: 1053–1064 PubMed PMC

Szumlanski AL, Nielsen E (2010) Phosphatidylinositol 4-phosphate is required for tip growth in Arabidopsis thaliana. In  Munnik T, ed, Lipid Signaling in Plants. Springer, Berlin, Heidelberg, pp 65–77

Van Damme D, Coutuer S, De Rycke R, Bouget F-Y, Inzé D, Geelen D (2006) Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell  18: 3502–3518 PubMed PMC

Vermeer JEM, Thole JM, Goedhart J, Nielsen E, Munnik T, Gadella TWJ Jr (2009) Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant J  57: 356–372 PubMed

Wang YJ, Wang J, Sun HQ, Martinez M, Sun YX, Macia E, Kirchhausen T, Albanesi JP, Roth MG, Yin HL (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell  114: 299–310 PubMed

Wang Z-P, Xing H-L, Dong L, Zhang H-Y, Han C-Y, Wang X-C, Chen Q-J (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol  16: 144. PubMed PMC

Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, et al. (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res  46: W296–W303 PubMed PMC

Wei YJ, Sun HQ, Yamamoto M, Wlodarski P, Kunii K, Martinez M, Barylko B, Albanesi JP, Yin HL (2002) Type II phosphatidylinositol 4-kinase beta is a cytosolic and peripheral membrane protein that is recruited to the plasma membrane and activated by Rac-GTP. J Biol Chem  277: 46586–46593 PubMed

Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res  35: W407–410 PubMed PMC

Wu X, Chi RJ, Baskin JM, Lucast L, Burd CG, De Camilli P, Reinisch KM (2014) Structural insights into assembly and regulation of the plasma membrane phosphatidylinositol 4-kinase complex. Dev Cell  28: 19–29 PubMed PMC

Xing H-L, Dong L, Wang Z-P, Zhang H-Y, Han C-Y, Liu B, Wang X-C, Chen Q-J (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol  14: 327. PubMed PMC

Xue H-W, Pical C, Brearley C, Elge S, Müller-Röber B (1999) A plant 126-kDa phosphatidylinositol 4-kinase with a novel repeat structure CLONING AND FUNCTIONAL EXPRESSION IN BACULOVIRUS-INFECTED INSECT CELLS. J Biol Chem  274: 5738–5745 PubMed

Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell  20: 3389–3404 PubMed PMC

Yan Y, Tao H, He J, Huang S-Y (2020) The HDOCK server for integrated protein-protein docking. Nat Protoc  15: 1829–1852 PubMed

Zaballa M-E, Goot FG (2018). The molecular era of protein S-acylation: spotlight on structure, mechanisms, and dynamics. Crit Rev Biochem Mol Biol  53: 420–451 PubMed

Zarza X, Van Wijk R, Shabala L, Hunkeler A, Lefebvre M, Rodriguez-Villalón A, Shabala S, Tiburcio AF, Heilmann I, Munnik T (2020) Lipid kinases PIP5K7 and PIP5K9 are required for polyamine-triggered K+ efflux in Arabidopsis roots. Plant J  104: 416–432 PubMed PMC

Zhao B, Shi H, Wang W, Liu X, Gao H, Wang X, Zhang Y, Yang M, Li R, Guo Y (2016) Secretory COPII protein SEC31B is required for pollen wall development. Plant Physiol  172: 1625–1642 PubMed PMC

Zimmermann L, Stephens A, Nam S-Z, Rau D, Kübler J, Lozajic M, Gabler F, Söding J, Lupas AN, Alva V (2018) A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol  430: 2237–2243 PubMed

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...