Advances in Understanding the Mechanism of Action of the Auxin Permease AUX1

. 2018 Oct 30 ; 19 (11) : . [epub] 20181030

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid30380696

Grantová podpora
MSM200381701 Akademie Věd České Republiky
16-10948S Grantová Agentura České Republiky
CZ.02.1.01/0.0/0.0/16_019/0000738 Ministry of Education, Youth and Sports of Czech Republic from European Regional Development Fund "Centre for Experimental Plant Biology"
SB/OS/PDF-336/2016-17 Science and Engineering Research Board, Department of Science and Technology, India
NPUI no. LO1417 Ministry of Education, Youth and Sport of the Czech Republic

In over 40 years of research on the cellular uptake of auxin it is somewhat chastening that we have elaborated so little on the original kinetic descriptions of auxin uptake by plant cells made by Rubery and Sheldrake in 1974. Every aspect of that seminal work has been investigated in detail, and the uptake activity they measured is now known to be attributed to the AUX1/LAX family of permeases. Recent pharmacological studies have defined the substrate specificity of AUX1, biochemical studies have evaluated its permeability to auxin in plant cell membranes, and rigourous kinetic studies have confirmed the affinity of AUX1 for IAA and synthetic auxins. Advances in genome sequencing have provided a rich resource for informatic analysis of the ancestry of AUX1 and the LAX proteins and, along with models of topology, suggest mechanistic links to families of eukaryotic proton co-transporters for which crystal structures have been presented. The insights gained from all the accumulated research reflect the brilliance of Rubery and Sheldrake's early work, but recent biochemical analyses are starting to advance further our understanding of this vitally important family of auxin transport proteins.

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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

Lacek J., Retzer K., Luschnig C., Zažímalová E. ELS. John Wiley & Sons Ltd.; Chichester, UK: 2017. [(accessed on 17 April 2017)]. Polar Auxin Transport. Available online: http://www.els.net.

Swarup R., Péret B. AUX/LAX family of auxin influx carriers-an overview. Front Plant Sci. 2012;3:225. doi: 10.3389/fpls.2012.00225. PubMed DOI PMC

Terasaka K., Blakeslee J.J., Titapiwatanakun B., Peer W.A., Bandyopadhyay A., Makam S.N., Lee O.R., Richards E.L., Murphy A.S., Sato F., et al. PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. Plant Cell. 2005;17:2922–2939. doi: 10.1105/tpc.105.035816. PubMed DOI PMC

Krouk G., Lacombe B., Bielach A., Perrine-Walker F., Malinska K., Mounier E., Hoyerova K., Tillard P., Leon S., jung K., et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell. 2010;18:927–937. doi: 10.1016/j.devcel.2010.05.008. PubMed DOI

Kamimoto Y., Terasaka K., Hamamoto M., Takanashi K., Fukuda S., Shitan N., Sugiyama A., Suzuki H., Shibata D., Wang B., et al. Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration. Plant Cell Physiol. 2012;53:2090–2100. doi: 10.1093/pcp/pcs149. PubMed DOI

Kubeš M., Yang H., Richter G.L., Cheng Y., Młodzińska E., Wang X., Blakeslee J.J., Carraro N., Petrášek J., Zažímalová E., et al. The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J. 2012;69:640–654. doi: 10.1111/j.1365-313X.2011.04818.x. PubMed DOI

Swarup R., Friml J., Marchant A., Ljung K., Sandberg G., Palme K., Bennett M. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 2001;15:2648–2653. doi: 10.1101/gad.210501. PubMed DOI PMC

Marchant A., Kargul J., May S.T., Muller P., Delbarre A., Perrot-Rechenmann C., Bennett M.J. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 1999;18:2066–2073. doi: 10.1093/emboj/18.8.2066. PubMed DOI PMC

Vandenbussche F., Petrásek J., Zádníková P., Hoyerová K., Pesek B., Raz V., Bennett M., Zažímalová E., Benková E., Van Der Straeten D. The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development. 2010;137:597–606. doi: 10.1242/dev.040790. PubMed DOI

Swarup K., Benková E., Swarup R., Casimiro I., Péret B., Yang Y., Parry G., Nielsen E., De Smet I., Vanneste S., et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 2008;10:946–954. doi: 10.1038/ncb1754. PubMed DOI

Kasprzewska A., Carter R., Swarup R., Bennett M., Monk N., Hobbs J.K., Fleming A. Auxin influx importers modulate serration along the leaf margin. Plant J. 2015;83:705–718. doi: 10.1111/tpj.12921. PubMed DOI PMC

Bhosale R., Giri J., Pandey B.K., Giehl R.F.H., Hartmann A., Traini R., Truskina J., Leftley N., Hanlon M., Swarup K., et al. A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun. 2018;9:1409. doi: 10.1038/s41467-018-03851-3. PubMed DOI PMC

Dindas J., Scherzer S., Roelfsema M.R.G., von Meyer K., Müller H.M., Al-Rasheid K.A.S., Palme K., Dietrich P., Becker D., Bennett M.J., et al. AUX1-mediated root hair auxin influx governs SCF. Nat. Commun. 2018;9:1174. doi: 10.1038/s41467-018-03582-5. PubMed DOI PMC

Fendrych M., Akhmanova M., Merrin J., Glanc M., Hagihara S., Takahashi K., Uchida N., Torii K.U., Friml J. 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

O’Leary B.M., Neale H.C., Geilfus C.M., Jackson R.W., Arnold D.L., Preston G.M. Early changes in apoplast composition associated with defence and disease in interactions between Phaseolus vulgaris and the halo blight pathogen Pseudomonas syringae Pv. phaseolicola. Plant Cell Environ. 2016;39:2172–2184. doi: 10.1111/pce.12770. PubMed DOI PMC

Rubery P.H., Sheldrake A.R. Carrier-mediated auxin transport. Planta. 1974;118:101–121. doi: 10.1007/BF00388387. PubMed DOI

Parry G., Delbarre A., Marchant A., Swarup R., Napier R., Perrot-Rechenmann C., Bennett M.J. Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. Plant J. 2001;25:399–406. doi: 10.1046/j.1365-313x.2001.00970.x. PubMed DOI

Rubery P.H., Sheldrake A.R. Effect of pH and surface charge on cell uptake of auxin. Nat. New Biol. 1973;244:285–288. doi: 10.1038/newbio244285a0. PubMed DOI

Jacobs M., Hertel R. Auxin binding to subcellular fractions from Cucurbita hypocotyls: In vitro evidence for an auxin transport carrier. Planta. 1978;142:1–10. doi: 10.1007/BF00385113. PubMed DOI

Hertel R., Lomax T.L., Briggs W.R. Auxin transport in membrane vesicles from Cucurbita pepo L. Planta. 1983;157:193–201. doi: 10.1007/BF00405182. PubMed DOI

Lomax T.L., Mehlhorn R.J., Briggs W.R. Active auxin uptake by zucchini membrane vesicles: Quantitation using ESR volume and delta pH determinations. Proc. Natl. Acad. Sci. USA. 1985;82:6541–6545. doi: 10.1073/pnas.82.19.6541. PubMed DOI PMC

Benning C. Evidence supporting a model of voltage-dependent uptake of auxin into Cucurbita vesicles. Planta. 1986;169:228–237. doi: 10.1007/BF00392319. PubMed DOI

Geier U., Werner O., Bopp M. Indole-3-acetic acid uptake in isolated protoplasts of the moss Funaria hygrometrica. Planta. 1990;80:584–592. doi: 10.1111/j.1399-3054.1990.tb05682.x. DOI

Barbez E., Dünser K., Gaidora A., Lendl T., Busch W. Auxin steers root cell expansion via apoplastic pH regulation in. Proc. Natl. Acad. Sci. USA. 2017;114:E4884–E4893. doi: 10.1073/pnas.1613499114. PubMed DOI PMC

Inoue S.I., Takahashi K., Okumura-Noda H., Kinoshita T. Auxin Influx Carrier AUX1 Confers Acid Resistance for Arabidopsis Root Elongation Through the Regulation of Plasma Membrane, H+-ATPase. Plant Cell Physiol. 2016;57:2194–2201. doi: 10.1093/pcp/pcw136. PubMed DOI PMC

Bennett M.J., Marchant A., Green H.G., May S.T., Ward S.P., Millner P.A., Walker A.R., Schulz B., Feldmann K.A. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science. 1996;273:948–950. doi: 10.1126/science.273.5277.948. PubMed DOI

Maher E.P., Martindale S.J. Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem. Genet. 1980;18:1041–1053. doi: 10.1007/BF00484337. PubMed DOI

Okada K., Shimura Y. Reversible root tip rotation in Arabidopsis seedlings induced by obstacle-touching stimulus. Science. 1990;250:274–276. doi: 10.1126/science.250.4978.274. PubMed DOI

Swarup R., Kargul J., Marchant A., Zadik D., Rahman A., Mills R., Yemm A., May S., Williams L., Millner P., et al. Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell. 2004;16:3069–3083. doi: 10.1105/tpc.104.024737. PubMed DOI PMC

Péret B., Swarup K., Ferguson A., Seth M., Yang Y., Dhondt S., James N., Casimiro I., Perry P., Syed A., et al. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell. 2012;24:2874–2885. doi: 10.1105/tpc.112.097766. PubMed DOI PMC

Swarup R., Kramer E.M., Perry P., Knox K., Leyser H.M., Haseloff J., Beemster G.T.S., Bhalerao R., Bennett M.J. 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

Kramer E.M., Bennett M.J. Auxin transport: A field in flux. Trends Plant Sci. 2006;11:382–386. doi: 10.1016/j.tplants.2006.06.002. PubMed DOI

Omasits U., Ahrens C.H., Müller S., Wollscheid B. Protter: Interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics. 2014;30:884–886. doi: 10.1093/bioinformatics/btt607. PubMed DOI

Yang Y., Hammes U.Z., Taylor C.G., Schachtman D.P., Nielsen E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 2006;16:1123–1127. doi: 10.1016/j.cub.2006.04.029. PubMed DOI

Carrier D.J., Bakar N.T., Swarup R., Callaghan R., Napier R.M., Bennett M.J., Kerr I.D. The binding of auxin to the Arabidopsis auxin influx transporter AUX1. Plant Physiol. 2008;148:529–535. doi: 10.1104/pp.108.122044. PubMed DOI PMC

Lanková M., Smith R.S., Pesek B., Kubes M., Zazímalová E., Petrásek J., Hoyerová K. Auxin influx inhibitors 1-NOA, 2-NOA, and CHPAA interfere with membrane dynamics in tobacco cells. J. Exp. Bot. 2010;61:3589–3598. doi: 10.1093/jxb/erq172. PubMed DOI PMC

Delbarre A., Muller P., Imhoff V., Guern J. Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta. 1996;198:532–541. doi: 10.1007/BF00262639. PubMed DOI

Imhoff V., Muller P., Guern J., Delbarre A. Inhibitors of the carrier-mediated influx of auxin in suspension-cultured tobacco cells. Planta. 2000;210:580–588. doi: 10.1007/s004250050047. PubMed DOI

Hošek P., Kubes M., Lanková M., Dobrev P.I., Klíma P., Kohoutová M., Petrášek J., Hoyerová K., Jiřina M., Zažímalová E. Auxin transport at cellular level: New insights supported by mathematical modelling. J. Exp. Bot. 2012;63:3815–3827. doi: 10.1093/jxb/ers074. PubMed DOI PMC

Simon S., Kubeš M., Baster P., Robert S., Dobrev P.I., Friml J., Petrášek J., Zažímalová E. Defining the selectivity of processes along the auxin response chain: A study using auxin analogues. New Phytol. 2013;200:1034–1048. doi: 10.1111/nph.12437. PubMed DOI

Sussman M.R., Goldsmith M.H. Auxin uptake and action of N-1-naphthylphthalamic acid in corn coleoptiles. Planta. 1981;151:15–25. doi: 10.1007/BF00384232. PubMed DOI

Tsuda E., Yang H., Nishimura T., Uehara Y., Sakai T., Furutani M., Koshiba T., Hirose M., Nozaki H., Murphy A.S., et al. Alkoxy-auxins are selective inhibitors of auxin transport mediated by PIN, ABCB, and AUX1 transporters. J. Biol. Chem. 2011;286:2354–2364. doi: 10.1074/jbc.M110.171165. PubMed DOI PMC

Hoyerova K., Hosek P., Quareshy M., Li J., Klima P., Kubes M., Yemm A.A., Neve P., Tripathi A., Bennett M.J., et al. Auxin molecular field maps define AUX1 selectivity: Many auxin herbicides are not substrates. New Phytol. 2018;217:1625–1639. doi: 10.1111/nph.14950. PubMed DOI

Quareshy M., Prusinska J., Kieffer M., Fukui K., Pardal A.J., Lehmann S., Schafer P., del Genio C.I., Kepinski S., Hayashi K., et al. The Tetrazole Analogue of the Auxin Indole-3-acetic Acid Binds Preferentially to TIR1 and Not AFB5. ACS Chem. Biol. 2018;13:2585–2594. doi: 10.1021/acschembio.8b00527. PubMed DOI

Kell D.B. Implications of endogenous roles of transporters for drug discovery: Hitchhiking and metabolite-likeness. Nat. Rev. Drug Discov. 2016;15:143. doi: 10.1038/nrd.2015.44. PubMed DOI

Busi R., Goggin D.E., Heap I., Horak M.J., Jugulam M., Masters R.A., Napier R.M., Riar D.S., Satchivi N.M., Torra J., et al. Weed resistance to synthetic auxin herbicides. Pest Manag. Sci. 2018;74:2265–2276. doi: 10.1002/ps.4823. PubMed DOI PMC

Bennett T., Brockington S.F., Rothfels C., Graham S.W., Stevenson D., Kutchan T., Rolf M., Thomas P., Wong G.K.-S., Leyser O., et al. Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure. Mol. Biol. Evol. 2014;31:2042–2060. doi: 10.1093/molbev/msu147. PubMed DOI PMC

De Smet I., Voss U., Lau S., Wilson M., Shao N., Timme R.E., Swarup R., Kerr I., Hodgman C., Bock R., et al. Unraveling the evolution of auxin signaling. Plant Physiol. 2011;155:209–221. doi: 10.1104/pp.110.168161. PubMed DOI PMC

Fischer W.N., Kwart M., Hummel S., Frommer W.B. Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol. Chem. 1995;270:16315–16320. doi: 10.1074/jbc.270.27.16315. PubMed DOI

Fowler P.W., Orwick-Rydmark M., Radestock S., Solcan N., Dijkman P.M., Lyons J.A., Kwok J., Caffrey M., Watts A., Forrest L.R., et al. Gating topology of the proton-coupled oligopeptide symporters. Structure. 2015;23:290–301. doi: 10.1016/j.str.2014.12.012. PubMed DOI PMC

Jardetzky O. Protein dynamics and conformational transitions in allosteric proteins. Prog. Biophys. Mol. Biol. 1996;65:171–219. doi: 10.1016/S0079-6107(96)00010-7. PubMed DOI

Kramer E.M., Rutschow H.L., Mabie S.S. AuxV: A database of auxin transport velocities. Trends Plant Sci. 2011;16:461–463. doi: 10.1016/j.tplants.2011.05.003. 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

Band L.R., Wells D.M., Fozard J.A., Ghetiu T., French A.P., Pound M.P., Wilson M.H., Yu L., Li W., Hijazi H.I., et al. Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell. 2014;26:862–875. doi: 10.1105/tpc.113.119495. PubMed DOI PMC

Band L.R., Wells D.M., Larrieu A., Sun J., Middleton A.M., French A.P., Brunoud G., Sato E.M., Wilson M.H., Péret B., 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

Mironova V.V., Omelyanchuk N.A., Novoselova E.S., Doroshkov A.V., Kazantsev F.V., Kochetov A.V., Kolchanov N.A., Mjolsness E., Likhoshvai V.A. Combined in silico/in vivo analysis of mechanisms providing for root apical meristem self-organization and maintenance. Ann. Bot. 2012;110:349–360. doi: 10.1093/aob/mcs069. PubMed DOI PMC

Grieneisen V.A., Xu J., Marée A.F., Hogeweg P., Scheres B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature. 2007;449:1008–1013. doi: 10.1038/nature06215. PubMed DOI

Wabnik K., Kleine-Vehn J., Balla J., Sauer M., Naramoto S., Reinöhl V., Merks R.M., Govaerts W., Friml J. Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol. Syst. Biol. 2010;6:447. doi: 10.1038/msb.2010.103. PubMed DOI PMC

Rutschow H.L., Baskin T.I., Kramer E.M. The carrier AUXIN RESISTANT (AUX1) dominates auxin flux into Arabidopsis protoplasts. New Phytol. 2014;204:536–544. doi: 10.1111/nph.12933. PubMed DOI

Moore S., Liu J., Zhang X., Lindsey K. A recovery principle provides insight into auxin pattern control in the Arabidopsis root. Sci. Rep. 2017;7:43004. doi: 10.1038/srep43004. PubMed DOI PMC

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