An Arabidopsis mutant deficient in phosphatidylinositol-4-phosphate kinases ß1 and ß2 displays altered auxin-related responses in roots

. 2022 Apr 28 ; 12 (1) : 6947. [epub] 20220428

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35484296
Odkazy

PubMed 35484296
PubMed Central PMC9051118
DOI 10.1038/s41598-022-10458-8
PII: 10.1038/s41598-022-10458-8
Knihovny.cz E-zdroje

Phosphatidylinositol 4-kinases (PI4Ks) are the first enzymes that commit phosphatidylinositol into the phosphoinositide pathway. Here, we show that Arabidopsis thaliana seedlings deficient in PI4Kβ1 and β2 have several developmental defects including shorter roots and unfinished cytokinesis. The pi4kβ1β2 double mutant was insensitive to exogenous auxin concerning inhibition of root length and cell elongation; it also responded more slowly to gravistimulation. The pi4kß1ß2 root transcriptome displayed some similarities to a wild type plant response to auxin. Yet, not all the genes displayed such a constitutive auxin-like response. Besides, most assessed genes did not respond to exogenous auxin. This is consistent with data with the transcriptional reporter DR5-GUS. The content of bioactive auxin in the pi4kß1ß2 roots was similar to that in wild-type ones. Yet, an enhanced auxin-conjugating activity was detected and the auxin level reporter DII-VENUS did not respond to exogenous auxin in pi4kß1ß2 mutant. The mutant exhibited altered subcellular trafficking behavior including the trapping of PIN-FORMED 2 protein in rapidly moving vesicles. Bigger and less fragmented vacuoles were observed in pi4kß1ß2 roots when compared to the wild type. Furthermore, the actin filament web of the pi4kß1ß2 double mutant was less dense than in wild-type seedling roots, and less prone to rebuilding after treatment with latrunculin B. A mechanistic model is proposed in which an altered PI4K activity leads to actin filament disorganization, changes in vesicle trafficking, and altered auxin homeostasis and response resulting in a pleiotropic root phenotypes.

Zobrazit více v PubMed

Retzer K, Weckwerth W. The TOR–auxin connection upstream of root hair growth. Plants. 2021;10:150. doi: 10.3390/plants10010150. PubMed DOI PMC

Waldie T, Leyser O. Cytokinin targets auxin transport to promote shoot branching. Plant Physiol. 2018;177:803–818. doi: 10.1104/pp.17.01691. PubMed DOI PMC

Luschnig C, Vert G. The dynamics of plant plasma membrane proteins: PINs and beyond. Development (Cambridge, England) 2014;141:2924–2938. doi: 10.1242/dev.103424. PubMed DOI

Habets M, Offringa R. PIN-driven polar auxin transport in plant developmental plasticity: A key target for environmental and endogenous signals. The New Phytol. 2014;203:1. doi: 10.1111/nph.12831. PubMed DOI

Semeradova H, Montesinos JC, Benkova E. All roads lead to Auxin: Post-translational regulation of Auxin transport by multiple hormonal pathways. Plant Commun. 2020;1:100048. doi: 10.1016/j.xplc.2020.100048. PubMed DOI PMC

Pokotylo I, Kravets V, Martinec J, Ruelland E. The phosphatidic acid paradox: Too many actions for one molecule class? Lessons from plants. Prog. Lipid Res. 2018;71:43–53. doi: 10.1016/j.plipres.2018.05.003. PubMed DOI

Noack LC, Jaillais Y. Functions of anionic lipids in plants. Annu. Rev. Plant. Biol. 2020;71:71–102. doi: 10.1146/annurev-arplant-081519-035910. PubMed DOI

Jaillais Y, Ott T. The nanoscale organization of the plasma membrane and its importance in signaling: A proteolipid perspective1. Plant Physiol. 2020;182:1682–1696. doi: 10.1104/pp.19.01349. PubMed DOI PMC

Gronnier, J. et al. Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains. eLife6, e26404 (2017). PubMed PMC

Galvan-Ampudia, C. S. et al. Temporal integration of auxin information for the regulation of patterning. eLife9, e55832 (2020). PubMed PMC

Ke M, et al. Salicylic acid regulates PIN2 auxin transporter hyperclustering and root gravitropic growth via Remorin-dependent lipid nanodomain organisation in Arabidopsis thaliana. New Phytol. 2021;229:963–978. doi: 10.1111/nph.16915. PubMed DOI PMC

McKenna JF, et al. The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis. PNAS. 2019;116:12857–12862. doi: 10.1073/pnas.1819077116. PubMed DOI PMC

Akhter S, et al. Role of Arabidopsis AtPI4Kγ3, a type II phosphoinositide 4-kinase, in abiotic stress responses and floral transition. Plant Biotechnol. J. 2016;14:215–230. doi: 10.1111/pbi.12376. PubMed DOI PMC

Galvão RM, Kota U, Soderblom EJ, Goshe MB, Boss WF. Characterization of a new family of protein kinases from Arabidopsis containing phosphoinositide 3/4-kinase and ubiquitin-like domains. Biochem. J. 2008;409:117–127. doi: 10.1042/BJ20070959. PubMed DOI

Cacas J-L, et al. Revisiting plant plasma membrane lipids in tobacco: A focus on sphingolipids. Plant Physiol. 2016;170:367–384. doi: 10.1104/pp.15.00564. PubMed DOI PMC

Delage E, Ruelland E, Guillas I, Zachowski A, Puyaubert J. Arabidopsis type-III phosphatidylinositol 4-kinases β1 and β2 are upstream of the phospholipase C pathway triggered by cold exposure. Plant Cell Physiol. 2012;53:565–576. doi: 10.1093/pcp/pcs011. PubMed DOI

Djafi N, et al. The Arabidopsis DREB2 genetic pathway is constitutively repressed by basal phosphoinositide-dependent phospholipase C coupled to diacylglycerol kinase. Front. Plant Sci. 2013;4:307. doi: 10.3389/fpls.2013.00307. PubMed DOI PMC

Krinke O, Novotná Z, Valentová O, Martinec J. Inositol trisphosphate receptor in higher plants: Is it real? J. Exp. Bot. 2007;58:361–376. doi: 10.1093/jxb/erl220. PubMed DOI

Ruelland E, et al. Salicylic acid modulates levels of phosphoinositide dependent-phospholipase C substrates and products to remodel the Arabidopsis suspension cell transcriptome. Front. Plant Sci. 2014;5:608. doi: 10.3389/fpls.2014.00608. PubMed DOI PMC

Kalachova T, et al. The inhibition of basal phosphoinositide-dependent phospholipase C activity in Arabidopsis suspension cells by abscisic or salicylic acid acts as a signalling hub accounting for an important overlap in transcriptome remodelling induced by these hormones. Environ. Exp. Bot. 2016;123:37–49. doi: 10.1016/j.envexpbot.2015.11.003. DOI

Šašek V, et al. Constitutive salicylic acid accumulation in pi4kIIIβ1β2 Arabidopsis plants stunts rosette but not root growth. New Phytol. 2014;203:805–816. doi: 10.1111/nph.12822. PubMed DOI

Pluhařová K, et al. “Salicylic Acid Mutant Collection” as a Tool to Explore the Role of Salicylic Acid in Regulation of Plant Growth under a Changing Environment. Int. J. Mol. Sci. 2019;20:1. doi: 10.3390/ijms20246365. PubMed DOI PMC

Lin, F. et al. A dual role for cell plate-associated PI4Kβ in endocytosis and phragmoplast dynamics during plant somatic cytokinesis. The EMBO Journal38, e100303 (2019). PubMed PMC

Kang B-H, Nielsen E, Preuss ML, Mastronarde D, Staehelin LA. Electron tomography of RabA4b- and PI-4Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic. 2011;12:313–329. doi: 10.1111/j.1600-0854.2010.01146.x. PubMed DOI

Preuss ML, et al. A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J. Cell Biol. 2006;172:991–998. doi: 10.1083/jcb.200508116. PubMed DOI PMC

Singh SK, Fischer U, Singh M, Grebe M, Marchant A. Insight into the early steps of root hair formation revealed by the procuste1 cellulose synthase mutant of Arabidopsis thaliana. BMC Plant Biol. 2008;8:57. doi: 10.1186/1471-2229-8-57. PubMed DOI PMC

Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ. Composite structure of auxin response elements. Plant Cell. 1995;7:1611–1623. PubMed PMC

Brunoud G, et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature. 2012;482:103–106. doi: 10.1038/nature10791. PubMed DOI

Hruz, T. et al. Genevestigator V3: A Reference Expression Database for the Meta-Analysis of Transcriptomes. Adv. Bioinf.2008, e420747 (2008). PubMed PMC

Preuss ML, Serna J, Falbel TG, Bednarek SY, Nielsen E. The arabidopsis rab GTPase RabA4b localizes to the tips of growing root hair cells. Plant Cell. 2004;16:1589–1603. doi: 10.1105/tpc.021634. PubMed DOI PMC

Sassi M, et al. COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis. Development. 2012;139:3402–3412. doi: 10.1242/dev.078212. PubMed DOI

Staswick PE. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous Auxin inhibitors. Plant Physiol. 2009;150:1310–1321. doi: 10.1104/pp.109.138529. PubMed DOI PMC

Löfke, C., Dünser, K., Scheuring, D. & Kleine-Vehn, J. Auxin regulates SNARE-dependent vacuolar morphology restricting cell size. eLife4, e05868 (2015). PubMed PMC

Kang B-H, Busse JS, Bednarek SY. Members of the arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth[W] Plant Cell. 2003;15:899–913. doi: 10.1105/tpc.009670. PubMed DOI PMC

Caillaud M-C, et al. MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in arabidopsis. Plant Cell. 2008;20:423–437. doi: 10.1105/tpc.107.057422. PubMed DOI PMC

Glanc M, Fendrych M, Friml J. PIN2 polarity establishment in arabidopsis in the absence of an intact cytoskeleton. Biomolecules. 2019;9:222. doi: 10.3390/biom9060222. PubMed DOI PMC

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. doi: 10.1038/35096571. PubMed DOI

Goldstein RE, van de Meent J-W. A physical perspective on cytoplasmic streaming. Interface Focus. 2015;5:20150030. doi: 10.1098/rsfs.2015.0030. PubMed DOI PMC

Nagawa, S. et al. ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLOS Biol.10, e1001299 (2012). PubMed PMC

Antignani V, et al. 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. 2015;27:243–261. doi: 10.1105/tpc.114.134262. PubMed DOI PMC

Smokvarska M, Jaillais Y, Martinière A. Function of membrane domains in rho-of-plant signaling. Plant Physiol. 2021;185:663–681. doi: 10.1093/plphys/kiaa082. PubMed DOI PMC

Smokvarska M, et al. A plasma membrane nanodomain ensures signal specificity during osmotic signaling in plants. Curr. Biol. 2020;30:4654–4664.e4. doi: 10.1016/j.cub.2020.09.013. PubMed DOI

Ischebeck T, et al. Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis. Plant Cell. 2013;25:4894–4911. doi: 10.1105/tpc.113.116582. PubMed DOI PMC

Mei Y, Jia W-J, Chu Y-J, Xue H-W. 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. 2012;22:581–597. doi: 10.1038/cr.2011.150. PubMed DOI PMC

Reyes-Hernández BJ, et al. Root stem cell niche maintenance and apical meristem activity critically depend on threonine synthase1. J. Exp. Bot. 2019;70:3835–3849. doi: 10.1093/jxb/erz165. PubMed DOI

Retzer K, et al. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nat. Commun. 2019;10:5516. doi: 10.1038/s41467-019-13543-1. PubMed DOI 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;8:249–256. doi: 10.1038/ncb1369. PubMed DOI

Luschnig C, Gaxiola RA, Grisafi P, Fink GR. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998;12:2175–2187. doi: 10.1101/gad.12.14.2175. PubMed DOI PMC

Kleine-Vehn J, et al. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. PNAS. 2008;105:17812–17817. doi: 10.1073/pnas.0808073105. PubMed DOI PMC

Ketelaar T. The actin cytoskeleton in root hairs: all is fine at the tip. Curr Opin Plant Biol. 2013;16:749–756. doi: 10.1016/j.pbi.2013.10.003. PubMed DOI

Grierson, C., Nielsen, E., Ketelaarc, T. & Schiefelbein, J. Root Hairs. Arabidopsis Book12, e0172 (2014). PubMed PMC

Wu C-Y, et al. The role of phosphoinositide-regulated actin reorganization in chemotaxis and cell migration. Br. J. Pharmacol. 2014;171:5541–5554. doi: 10.1111/bph.12777. PubMed DOI PMC

Sun T, Li S, Ren H. Profilin as a regulator of the membrane-actin cytoskeleton interface in plant cells. Front. Plant Sci. 2013;4:512. doi: 10.3389/fpls.2013.00512. PubMed DOI PMC

Molendijk, A. et al. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J.20, 2779–2788 (2001). PubMed PMC

Pleskot R, Pejchar P, Staiger C, Potocký M. When fat is not bad: the regulation of actin dynamics by phospholipid signaling molecules. Front. Plant Sci. 2014;5:5. doi: 10.3389/fpls.2014.00005. PubMed DOI PMC

Janmey PA, Bucki R, Radhakrishnan R. Regulation of actin assembly by PI(4,5)P2 and other inositol phospholipids: An update on possible mechanisms. Biochem. Biophys. Res. Commun. 2018;506:307–314. doi: 10.1016/j.bbrc.2018.07.155. PubMed DOI PMC

Marquès-Bueno MM, et al. Auxin-regulated reversible inhibition of TMK1 signaling by MAKR2 modulates the dynamics of root gravitropism. Curr. Biol. 2021;31:228–237.e10. doi: 10.1016/j.cub.2020.10.011. PubMed DOI PMC

Lin W, et al. TMK-based cell-surface auxin signalling activates cell-wall acidification. Nature. 2021;599:278–282. doi: 10.1038/s41586-021-03976-4. PubMed DOI PMC

Chakraborty S, et al. Cyclic nucleotide-gated ion channel 2 modulates Auxin homeostasis and signaling. Plant Physiol. 2021;187:1690–1703. doi: 10.1093/plphys/kiab332. PubMed DOI PMC

Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P. Spatio-temporal analysis of mitotic activity with a labile cyclin–GUS fusion protein. Plant J. 1999;20:503–508. doi: 10.1046/j.1365-313x.1999.00620.x. PubMed DOI

Kalachova T, et al. Interplay between phosphoinositides and actin cytoskeleton in the regulation of immunity related responses in Arabidopsis thaliana seedlings. Environ. Experim. Bot. 2019;167:103867. doi: 10.1016/j.envexpbot.2019.103867. DOI

Schindelin J, et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC

Figueroa-Balderas RE, García-Ponce B, Rocha-Sosa M. Hormonal and stress induction of the gene encoding common bean acetyl-coenzyme A carboxylase. Plant Physiol. 2006;142:609–619. doi: 10.1104/pp.106.085597. PubMed DOI PMC

Marhava P, et al. Plasma membrane domain patterning and self-reinforcing polarity in Arabidopsis. Dev. Cell. 2020;52:223–235.e5. doi: 10.1016/j.devcel.2019.11.015. PubMed DOI

Sauer M, et al. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev. 2006;20:2902–2911. doi: 10.1101/gad.390806. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Kopylova E, Noé L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–3217. doi: 10.1093/bioinformatics/bts611. PubMed DOI

Dobin A, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21. doi: 10.1093/bioinformatics/bts635. PubMed DOI PMC

Rigaill G, et al. Synthetic data sets for the identification of key ingredients for RNA-seq differential analysis. Brief Bioinform. 2018;19:65–76. PubMed

McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucl. Acids Res. 2012;40:4288–4297. doi: 10.1093/nar/gks042. PubMed DOI PMC

R Core Team. R: A Language and Environment for Statistical Computing. (2018).

Zhu, T. A browser-based functional classification SuperViewer for Arabidopsis genomics. (2003).

Ashburner M, et al. Gene Ontology: tool for the unification of biology. Nat. Genet. 2000;25:25–29. doi: 10.1038/75556. PubMed DOI PMC

Prerostova S, et al. Light quality and intensity modulate cold acclimation in Arabidopsis. Int. J. Mol. Sci. 2021;22:2736. doi: 10.3390/ijms22052736. PubMed DOI PMC

Gagnot S, et al. CATdb: A public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucl. Acids Res. 2008;36:D986–990. doi: 10.1093/nar/gkm757. PubMed DOI PMC

Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucl. Acids Res. 2002;30:207–210. doi: 10.1093/nar/30.1.207. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...