Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
M 2379
Austrian Science Fund FWF - Austria
P 25931
Austrian Science Fund FWF - Austria
P 31493
Austrian Science Fund FWF - Austria
PubMed
31797871
PubMed Central
PMC6892858
DOI
10.1038/s41467-019-13543-1
PII: 10.1038/s41467-019-13543-1
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis účinky léků metabolismus MeSH
- biologický transport účinky léků MeSH
- brassinosteroidy metabolismus farmakologie MeSH
- endocytóza účinky léků MeSH
- gravitropismus účinky léků fyziologie MeSH
- kořeny rostlin účinky léků metabolismus MeSH
- kyseliny indoloctové metabolismus MeSH
- meristém účinky léků metabolismus MeSH
- proteiny huseníčku metabolismus MeSH
- regulátory růstu rostlin metabolismus farmakologie MeSH
- signální transdukce MeSH
- steroidy heterocyklické metabolismus farmakologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- brassinolide MeSH Prohlížeč
- brassinosteroidy MeSH
- kyseliny indoloctové MeSH
- PIN2 protein, Arabidopsis MeSH Prohlížeč
- proteiny huseníčku MeSH
- regulátory růstu rostlin MeSH
- steroidy heterocyklické MeSH
Arabidopsis PIN2 protein directs transport of the phytohormone auxin from the root tip into the root elongation zone. Variation in hormone transport, which depends on a delicate interplay between PIN2 sorting to and from polar plasma membrane domains, determines root growth. By employing a constitutively degraded version of PIN2, we identify brassinolides as antagonists of PIN2 endocytosis. This response does not require de novo protein synthesis, but involves early events in canonical brassinolide signaling. Brassinolide-controlled adjustments in PIN2 sorting and intracellular distribution governs formation of a lateral PIN2 gradient in gravistimulated roots, coinciding with adjustments in auxin signaling and directional root growth. Strikingly, simulations indicate that PIN2 gradient formation is no prerequisite for root bending but rather dampens asymmetric auxin flow and signaling. Crosstalk between brassinolide signaling and endocytic PIN2 sorting, thus, appears essential for determining the rate of gravity-induced root curvature via attenuation of differential cell elongation.
Boehringer Ingelheim RCV Doktor Boehringer Gasse 5 11 1120 Wien Austria
Institute of Science and Technology Austria Am Campus 1 3400 Klosterneuburg Austria
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Luschnig C, Vert G. The dynamics of plant plasma membrane proteins: PINs and beyond. Development. 2014;141:2924–2938. doi: 10.1242/dev.103424. PubMed DOI
Naramoto S. Polar transport in plants mediated by membrane transporters: focus on mechanisms of polar auxin transport. Curr. Opin. Plant Biol. 2017;40:8–14. doi: 10.1016/j.pbi.2017.06.012. PubMed DOI
Adamowski M, Friml J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell. 2015;27:20–32. doi: 10.1105/tpc.114.134874. PubMed DOI PMC
Feraru E, et al. BEX5/RabA1b regulates trans-Golgi network-to-plasma membrane protein trafficking in Arabidopsis. Plant Cell. 2012;24:3074–3086. doi: 10.1105/tpc.112.098152. PubMed DOI PMC
Geldner N, et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell. 2003;112:219–230. doi: 10.1016/S0092-8674(03)00003-5. PubMed DOI
Kitakura S, et al. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell. 2011;23:1920–1931. doi: 10.1105/tpc.111.083030. PubMed DOI PMC
Leitner J, et al. Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc. Natl Acad. Sci. USA. 2012;109:8322–8327. doi: 10.1073/pnas.1200824109. PubMed DOI PMC
Korbei B, et al. Arabidopsis TOL proteins act as gatekeepers for vacuolar sorting of PIN2 plasma membrane protein. Curr. Biol. 2013;23:2500–2505. doi: 10.1016/j.cub.2013.10.036. PubMed DOI
Kleine-Vehn J, et al. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc. Natl Acad. Sci. USA. 2008;105:17812–17817. doi: 10.1073/pnas.0808073105. PubMed DOI PMC
Ambrose C, et al. CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev. Cell. 2013;24:649–659. doi: 10.1016/j.devcel.2013.02.007. PubMed DOI
Paciorek T, et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005;435:1251–1256. doi: 10.1038/nature03633. 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. 2006;8:249–256. doi: 10.1038/ncb1369. PubMed DOI
Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C. Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell. 2011;23:2184–2195. doi: 10.1105/tpc.111.086355. PubMed DOI PMC
Löfke C, et al. Asymmetric gibberellin signaling regulates vacuolar trafficking of PIN auxin transporters during root gravitropism. Proc. Natl Acad. Sci. USA. 2013;110:3627–3632. doi: 10.1073/pnas.1300107110. PubMed DOI PMC
Sun J, et al. Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell. 2009;21:1495–1511. doi: 10.1105/tpc.108.064303. PubMed DOI PMC
Shinohara N, Taylor C, Leyser O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 2013;11:e1001474. doi: 10.1371/journal.pbio.1001474. PubMed DOI PMC
Marhavy P, et al. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev. Cell. 2011;21:796–804. doi: 10.1016/j.devcel.2011.08.014. PubMed DOI
Zhang J, et al. Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. Dev. Cell. 2011;20:855–866. doi: 10.1016/j.devcel.2011.05.013. PubMed DOI
Retzer Katarzyna, Lacek Jozef, Skokan Roman, del Genio Charo, Vosolsobě Stanislav, Laňková Martina, Malínská Kateřina, Konstantinova Nataliia, Zažímalová Eva, Napier Richard, Petrášek Jan, Luschnig Christian. Evolutionary Conserved Cysteines Function as cis-Acting Regulators of Arabidopsis PIN-FORMED 2 Distribution. International Journal of Molecular Sciences. 2017;18(11):2274. doi: 10.3390/ijms18112274. PubMed DOI PMC
Belkhadir Y, Jaillais Y. The molecular circuitry of brassinosteroid signaling. N. Phytol. 2015;206:522–540. doi: 10.1111/nph.13269. PubMed DOI
Jaillais Y, Vert G. Brassinosteroid signaling and BRI1 dynamics went underground. Curr. Opin. Plant Biol. 2016;33:92–100. doi: 10.1016/j.pbi.2016.06.014. PubMed DOI PMC
Hacham Y, et al. Brassinosteroid perception in the epidermis controls root meristem size. Development. 2011;138:839–848. doi: 10.1242/dev.061804. PubMed DOI PMC
Gonzalez-Garcia MP, et al. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development. 2011;138:849–859. doi: 10.1242/dev.057331. PubMed DOI
Wolf S, Mravec J, Greiner S, Mouille G, Hofte H. Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Curr. Biol. 2012;22:1732–1737. doi: 10.1016/j.cub.2012.07.036. PubMed DOI
Nemhauser JL, Mockler TC, Chory J. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2004;2:E258. doi: 10.1371/journal.pbio.0020258. PubMed DOI PMC
Oh E., et al. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife3, 10.7554/eLife.03031 (2014). PubMed PMC
Tian H, Lv B, Ding T, Bai M, Ding Z. Auxin-BR interaction regulates plant growth and development. Front Plant Sci. 2017;8:2256. doi: 10.3389/fpls.2017.02256. PubMed DOI PMC
Hacham Y, Sela A, Friedlander L, Savaldi-Goldstein S. BRI1 activity in the root meristem involves post-transcriptional regulation of PIN auxin efflux carriers. Plant Signal Behav. 2012;7:68–70. doi: 10.4161/psb.7.1.18657. PubMed DOI PMC
Lanza M, et al. Role of actin cytoskeleton in brassinosteroid signaling and in its integration with the auxin response in plants. Dev. Cell. 2012;22:1275–1285. doi: 10.1016/j.devcel.2012.04.008. PubMed DOI
Ruan Yuan, Halat Laryssa S., Khan Deirdre, Jancowski Sylwia, Ambrose Chris, Belmonte Mark F., Wasteneys Geoffrey O. The Microtubule-Associated Protein CLASP Sustains Cell Proliferation through a Brassinosteroid Signaling Negative Feedback Loop. Current Biology. 2018;28(17):2718-2729.e5. doi: 10.1016/j.cub.2018.06.048. PubMed DOI
Piper R. C., Dikic I., Lukacs G. L. Ubiquitin-Dependent Sorting in Endocytosis. Cold Spring Harbor Perspectives in Biology. 2014;6(1):a016808–a016808. doi: 10.1101/cshperspect.a016808. PubMed DOI PMC
Butt H, Graner S, Luschnig C. Expression analysis of Arabidopsis XH/XS-domain proteins indicates overlapping and distinct functions for members of this gene family. J. Exp. Bot. 2014;65:1217–1227. doi: 10.1093/jxb/ert480. PubMed DOI PMC
Fujioka S, et al. The Arabidopsis deetiolated2 mutant is blocked early in brassinosteroid biosynthesis. Plant Cell. 1997;9:1951–1962. PubMed PMC
Asami T, et al. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiol. 2000;123:93–100. doi: 10.1104/pp.123.1.93. PubMed DOI PMC
Unterholzner SJ, et al. Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell. 2015;27:2261–2272. doi: 10.1105/tpc.15.00433. PubMed DOI PMC
Li JM, Nam KH. Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science. 2002;295:1299–1301. PubMed
Youn JH, Kim TW. Functional insights of plant GSK3-like kinases: multi-taskers in diverse cellular signal transduction pathways. Mol. Plant. 2015;8:552–565. doi: 10.1016/j.molp.2014.12.006. PubMed DOI
De Rybel B, et al. Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling. Chem. Biol. 2009;16:594–604. doi: 10.1016/j.chembiol.2009.04.008. PubMed DOI PMC
Arcaro A, Wymann MP. Wortmannin Is a potent phosphatidylinositol 3-Kinase Inhibitor—the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J. 1993;296:297–301. doi: 10.1042/bj2960297. PubMed DOI PMC
Liao CY, et al. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods. 2015;12:207–210. doi: 10.1038/nmeth.3279. PubMed DOI PMC
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
Kim TW, et al. Elongation and gravitropic responses of Arabidopsis roots are regulated by brassinolide and IAA. Plant Cell Environ. 2007;30:679–689. doi: 10.1111/j.1365-3040.2007.01659.x. PubMed DOI
Kim SK, et al. Involvement of brassinosteroids in the gravitropic response of primary root of maize. Plant Physiol. 2000;123:997–1004. doi: 10.1104/pp.123.3.997. PubMed DOI PMC
Li L, Xu J, Xu ZH, Xue HW. Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell. 2005;17:2738–2753. doi: 10.1105/tpc.105.034397. PubMed DOI PMC
Dharmasiri N, et al. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell. 2005;9:109–119. doi: 10.1016/j.devcel.2005.05.014. PubMed DOI
Baster P, et al. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 2013;32:260–274. doi: 10.1038/emboj.2012.310. PubMed DOI PMC
Yin Y, et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell. 2002;109:181–191. doi: 10.1016/S0092-8674(02)00721-3. PubMed DOI
Band LR, et al. Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc. Natl Acad. Sci. USA. 2012;109:4668–4673. doi: 10.1073/pnas.1201498109. PubMed DOI PMC
Fendrych M, et al. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants. 2018;4:453–459. doi: 10.1038/s41477-018-0190-1. 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. 2005;7:1057–1065. doi: 10.1038/ncb1316. PubMed DOI
Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature. 2002;415:806–809. doi: 10.1038/415806a. PubMed DOI
Haughn GW, Somerville C. Sulfonylurea-resistant mutants of Arabidopsis-Thaliana. Mol. Gen. Genet. 1986;204:430–434. doi: 10.1007/BF00331020. DOI
Clough SJ, Bent AF. Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–743. doi: 10.1046/j.1365-313x.1998.00343.x. PubMed DOI
Noguchi T, et al. Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. Plant Physiol. 1999;121:743–752. doi: 10.1104/pp.121.3.743. PubMed DOI PMC
Silva-Navas J, et al. D-Root: a system for cultivating plants with the roots in darkness or under different light conditions. Plant J. 2015;84:244–255. doi: 10.1111/tpj.12998. PubMed DOI
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI
Abas L, Luschnig C. Maximum yields of microsomal-type membranes from small amounts of plant material without requiring ultracentrifugation. Anal. Biochem. 2010;401:217–227. doi: 10.1016/j.ab.2010.02.030. PubMed DOI PMC
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