Pinstatic Acid Promotes Auxin Transport by Inhibiting PIN Internalization
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
P 29988
Austrian Science Fund FWF - Austria
BB/L009366/1
Biotechnology and Biological Sciences Research Council - United Kingdom
PubMed
30936248
PubMed Central
PMC6548234
DOI
10.1104/pp.19.00201
PII: pp.19.00201
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis účinky léků metabolismus MeSH
- biologický transport účinky léků MeSH
- buněčná membrána účinky léků metabolismus MeSH
- endocytóza * účinky léků MeSH
- fenotyp MeSH
- fenylacetáty farmakologie MeSH
- gravitropismus účinky léků MeSH
- hypokotyl účinky léků růst a vývoj MeSH
- kořeny rostlin účinky léků růst a vývoj MeSH
- kyseliny indoloctové metabolismus MeSH
- proteiny huseníčku metabolismus MeSH
- signální transdukce MeSH
- výhonky rostlin metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fenylacetáty MeSH
- kyseliny indoloctové MeSH
- phenylacetic acid MeSH Prohlížeč
- pinstatic acid MeSH Prohlížeč
- proteiny huseníčku MeSH
Polar auxin transport plays a pivotal role in plant growth and development. PIN-FORMED (PIN) auxin efflux carriers regulate directional auxin movement by establishing local auxin maxima, minima, and gradients that drive multiple developmental processes and responses to environmental signals. Auxin has been proposed to modulate its own transport by regulating subcellular PIN trafficking via processes such as clathrin-mediated PIN endocytosis and constitutive recycling. Here, we further investigated the mechanisms by which auxin affects PIN trafficking by screening auxin analogs and identified pinstatic acid (PISA) as a positive modulator of polar auxin transport in Arabidopsis (Arabidopsis thaliana). PISA had an auxin-like effect on hypocotyl elongation and adventitious root formation via positive regulation of auxin transport. PISA did not activate SCFTIR1/AFB signaling and yet induced PIN accumulation at the cell surface by inhibiting PIN internalization from the plasma membrane. This work demonstrates PISA to be a promising chemical tool to dissect the regulatory mechanisms behind subcellular PIN trafficking and auxin transport.
Centre for Plant Sciences Faculty of Biological Sciences University of Leeds Leeds LS2 9JT UK
Department of Biochemistry Okayama University of Science Okayama 700 0005 Japan
Graduate School of Science Nagoya University Chikusa Nagoya 464 8602 Japan
Institute of Science and Technology Austria 3400 Klosterneuburg Austria
Institute of Transformative Bio Molecules Nagoya University Chikusa Nagoya 464 8601 Japan
RIKEN Center for Sustainable Resource Science Yokohama Kanagawa 230 0045 Japan
School of Life Sciences University of Warwick Coventry CV4 7AL United Kingdom
Zobrazit více v PubMed
Abas L, Benjamins R, Malenica N, Paciorek T, Wiśniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol 8: 249–256 PubMed
Adamowski M, Friml J (2015) PIN-dependent auxin transport: Action, regulation, and evolution. Plant Cell 27: 20–32 PubMed PMC
Adamowski M, Narasimhan M, Kania U, Glanc M, De Jaeger G, Friml J (2018) A functional study of AUXILIN-LIKE1 and 2, two putative clathrin uncoating factors in Arabidopsis. Plant Cell 30: 700–716 PubMed PMC
Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2013) SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32: 260–274 PubMed PMC
Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001) The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128: 4057–4067 PubMed
Brumos J, Robles LM, Yun J, Vu TC, Jackson S, Alonso JM, Stepanova AN (2018) Local auxin biosynthesis is a key regulator of plant development. Dev Cell 47: 306–318 e305 PubMed
Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, et al. (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103–106 PubMed
Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16: 1191–1205 PubMed PMC
Chae K, Isaacs CG, Reeves PH, Maloney GS, Muday GK, Nagpal P, Reed JW (2012) Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J 71: 684–697 PubMed
Chen Q, Dai X, De-Paoli H, Cheng Y, Takebayashi Y, Kasahara H, Kamiya Y, Zhao Y (2014) Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol 55: 1072–1079 PubMed PMC
Ding Z, Galván-Ampudia CS, Demarsy E, Łangowski Ł, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, et al. (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13: 447–452 PubMed
Du Y, Tejos R, Beck M, Himschoot E, Li H, Robatzek S, Vanneste S, Friml J (2013) Salicylic acid interferes with clathrin-mediated endocytic protein trafficking. Proc Natl Acad Sci USA 110: 7946–7951 PubMed PMC
Fendrych M, Leung J, Friml J (2016) TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife 5: 5 PubMed PMC
Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, et al. (2004) A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862–865 PubMed
Fukui K, Hayashi KI (2018) Manipulation and sensing of auxin metabolism, transport and signaling. Plant Cell Physiol 59: 1500–1510 PubMed
Furutani M, Nakano Y, Tasaka M (2014) MAB4-induced auxin sink generates local auxin gradients in Arabidopsis organ formation. Proc Natl Acad Sci USA 111: 1198–1203 PubMed PMC
Ganguly A, Lee SH, Cho M, Lee OR, Yoo H, Cho HT (2010) Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol 153: 1046–1061 PubMed PMC
Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425–428 PubMed
Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219–230 PubMed
Hayashi K. (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53: 965–975 PubMed
Hayashi K, Neve J, Hirose M, Kuboki A, Shimada Y, Kepinski S, Nozaki H (2012) Rational design of an auxin antagonist of the SCF(TIR1) auxin receptor complex. ACS Chem Biol 7: 590–598 PubMed
He W, Brumos J, Li H, Ji Y, Ke M, Gong X, Zeng Q, Li W, Zhang X, An F, et al. (2011) A small-molecule screen identifies l-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23: 3944–3960 PubMed PMC
Jásik J, Bokor B, Stuchlík S, Mičieta K, Turňa J, Schmelzer E (2016) Effects of auxins on PIN-FORMED2 (PIN2) dynamics are not mediated by inhibiting PIN2 endocytosis. Plant Physiol 172: 1019–1031 PubMed PMC
Kasahara H. (2016) Current aspects of auxin biosynthesis in plants. Biosci Biotechnol Biochem 80: 34–42 PubMed
Kitakura S, Vanneste S, Robert S, Löfke C, Teichmann T, Tanaka H, Friml J (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23: 1920–1931 PubMed PMC
Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64: 2541–2555 PubMed PMC
Lee S, Sundaram S, Armitage L, Evans JP, Hawkes T, Kepinski S, Ferro N, Napier RM (2014) Defining binding efficiency and specificity of auxins for SCF(TIR1/AFB)-Aux/IAA co-receptor complex formation. ACS Chem Biol 9: 673–682 PubMed PMC
Lewis DR, Muday GK (2009) Measurement of auxin transport in Arabidopsis thaliana. Nat Protoc 4: 437–451 PubMed
Leyser O. (2018) Auxin signaling. Plant Physiol 176: 465–479 PubMed PMC
Lin D, Nagawa S, Chen J, Cao L, Chen X, Xu T, Li H, Dhonukshe P, Yamamuro C, Friml J, et al. (2012) A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr Biol 22: 1319–1325 PubMed PMC
Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Pařezová M, Petrášek J, Friml J, Kleine-Vehn J, et al. (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21: 796–804 PubMed
Muir RM, Fujita T, Hansch C (1967) Structure-activity relationship in the auxin activity of mono-substituted phenylacetic acids. Plant Physiol 42: 1519–1526 PubMed PMC
Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol 10: e1001299 PubMed PMC
Naramoto S, Kleine-Vehn J, Robert S, Fujimoto M, Dainobu T, Paciorek T, Ueda T, Nakano A, Van Montagu MC, Fukuda H, et al. (2010) ADP-ribosylation factor machinery mediates endocytosis in plant cells. Proc Natl Acad Sci USA 107: 21890–21895 PubMed PMC
Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M (2009) An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods 6: 917–922 PubMed
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19: 118–130 PubMed PMC
Paciorek T, Zazímalová E, Ruthardt N, Petrásek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jürgens G, Geldner N, et al. (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435: 1251–1256 PubMed
Pan J, Fujioka S, Peng J, Chen J, Li G, Chen R (2009) The E3 ubiquitin ligase SCFTIR1/AFB and membrane sterols play key roles in auxin regulation of endocytosis, recycling, and plasma membrane accumulation of the auxin efflux transporter PIN2 in Arabidopsis thaliana. Plant Cell 21: 568–580 PubMed PMC
Prát T, Hajný J, Grunewald W, Vasileva M, Molnár G, Tejos R, Schmid M, Sauer M, Friml J (2018) WRKY23 is a component of the transcriptional network mediating auxin feedback on PIN polarity. PLoS Genet 14: e1007177 PubMed PMC
Quareshy M, Uzunova V, Prusinska JM, Napier RM (2017) Assaying auxin receptor activity using SPR assays with F-Box proteins and Aux/IAA degrons. Methods Mol Biol 1497: 159–191 PubMed
Rakusová H, Fendrych M, Friml J (2015) Intracellular trafficking and PIN-mediated cell polarity during tropic responses in plants. Curr Opin Plant Biol 23: 116–123 PubMed
Rakusová H, Abbas M, Han H, Song S, Robert HS, Friml J (2016) Termination of shoot gravitropic responses by auxin feedback on PIN3 polarity. Curr Biol 26: 3026–3032 PubMed
Ren H, Gray WM (2015) SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant 8: 1153–1164 PubMed PMC
Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197: 1130–1141 PubMed
Robert HS, Grones P, Stepanova AN, Robles LM, Lokerse AS, Alonso JM, Weijers D, Friml J (2013) Local auxin sources orient the apical-basal axis in Arabidopsis embryos. Curr Biol 23: 2506–2512 PubMed
Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Čovanová M, et al. (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143: 111–121 PubMed PMC
Salanenka Y, Verstraeten I, Löfke C, Tabata K, Naramoto S, Glanc M, Friml J (2018) Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane. Proc Natl Acad Sci USA 115: 3716–3721 PubMed PMC
Sauer M, Paciorek T, Benková E, Friml J (2006) Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat Protoc 1: 98–103 PubMed
Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D, Peer WA, Murphy AS, Overvoorde PJ, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70: 978–990 PubMed PMC
Sugawara S, Mashiguchi K, Tanaka K, Hishiyama S, Sakai T, Hanada K, Kinoshita-Tsujimura K, Yu H, Dai X, Takebayashi Y, et al. (2015) Distinct characteristics of indole-3-acetic acid and phenylacetic acid, two common auxins in plants. Plant Cell Physiol 56: 1641–1654 PubMed PMC
Tsuda E, Yang H, Nishimura T, Uehara Y, Sakai T, Furutani M, Koshiba T, Hirose M, Nozaki H, Murphy AS, et al. (2011) Alkoxy-auxins are selective inhibitors of auxin transport mediated by PIN, ABCB, and AUX1 transporters. J Biol Chem 286: 2354–2364 PubMed PMC
Tsugafune S, Mashiguchi K, Fukui K, Takebayashi Y, Nishimura T, Sakai T, Shimada Y, Kasahara H, Koshiba T, Hayashi KI (2017) Yucasin DF, a potent and persistent inhibitor of auxin biosynthesis in plants. Sci Rep 7: 13992. PubMed PMC
Vieten A, Vanneste S, Wisniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132: 4521–4531 PubMed
Winicur ZM, Zhang GF, Staehelin LA (1998) Auxin deprivation induces synchronous Golgi differentiation in suspension-cultured tobacco BY-2 cells. Plant Physiol 117: 501–513 PubMed PMC
Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312: 883. PubMed