Auxin transport at cellular level: new insights supported by mathematical modelling
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
22438304
PubMed Central
PMC3388834
DOI
10.1093/jxb/ers074
PII: ers074
Knihovny.cz E-zdroje
- MeSH
- biologický transport MeSH
- kultivované buňky MeSH
- kyselina 2,4-dichlorfenoxyoctová chemie metabolismus MeSH
- kyseliny indoloctové chemie metabolismus MeSH
- naftaleny chemie metabolismus MeSH
- regulátory růstu rostlin chemie metabolismus MeSH
- tabák chemie cytologie metabolismus MeSH
- teoretické modely MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- kyselina 2,4-dichlorfenoxyoctová MeSH
- kyseliny indoloctové MeSH
- naftaleny MeSH
- naphthalene MeSH Prohlížeč
- regulátory růstu rostlin MeSH
The molecular basis of cellular auxin transport is still not fully understood. Although a number of carriers have been identified and proved to be involved in auxin transport, their regulation and possible activity of as yet unknown transporters remain unclear. Nevertheless, using single-cell-based systems it is possible to track the course of auxin accumulation inside cells and to specify and quantify some auxin transport parameters. The synthetic auxins 2,4-dichlorophenoxyacetic acid (2,4-D) and naphthalene-1-acetic acid (NAA) are generally considered to be suitable tools for auxin transport studies because they are transported specifically via either auxin influx or efflux carriers, respectively. Our results indicate that NAA can be metabolized rapidly in tobacco BY-2 cells. The predominant metabolite has been identified as NAA glucosyl ester and it is shown that all NAA metabolites were retained inside the cells. This implies that the transport efficiency of auxin efflux transporters is higher than previously assumed. By contrast, the metabolism of 2,4-D remained fairly weak. Moreover, using data on the accumulation of 2,4-D measured in the presence of auxin transport inhibitors, it is shown that 2,4-D is also transported by efflux carriers. These results suggest that 2,4-D is a promising tool for determining both auxin influx and efflux activities. Based on the accumulation data, a mathematical model of 2,4-D transport at a single-cell level is proposed. Optimization of the model provides estimates of crucial transport parameters and, together with its validation by successfully predicting the course of 2,4-D accumulation, it confirms the consistency of the present concept of cellular auxin transport.
Institute of Experimental Botany the Academy of Sciences of the Czech Republic Prague Czech Republic
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Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewcz P, Kuhlemeier C. Integration of transport-based models for phyllotaxis and midvein formation. Genes and Development. 2009;23:373–384. PubMed PMC
Cho M, Lee SH, Cho HT. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. The Plant Cell. 2007;19:3930–3943. PubMed PMC
Cooke TJ, Poli D, Sztein AE, Cohen JD. Evolutionary patterns in auxin action. Plant Molecular Biology. 2002;49:319–338. PubMed
Davies PJ, editor. The plant hormones: biosynthesis, signal transduction, action! 3rd edn. Dordrecht, The Netherlands: Springer; 2010.
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. PubMed
Delbarre A, Muller P, Imhoff V, Morgat JL, Barbier-Brygoo H. Uptake, accumulation and metabolism of auxins in tobacco leaf protoplasts. Planta. 1994;195:159–167.
Dhonukshe P, Kleine-Vehn J, Friml J. Cell polarity, auxin transport, and cytoskeleton-mediated division planes: who comes first? Protoplasma. 2005;226:67–73. PubMed
Dhonukshe P, Tanaka H, Goh T, et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature. 2008;456:962–975. PubMed PMC
Dobrev PI, Havlíček L, Vágner M, Malbeck J, Kamínek M. Purification and determination of plant hormones auxin and abscisic acid using solid phase extraction and two-dimensional high performance liquid chromatography. Journal of Chromatography A. 2005;1075:159–166. PubMed
Dobrev PI, Kamínek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. Journal of Chromatography A. 2002;950:21–29. PubMed
Ferro N, Gallegos A, Bultinck P, Jacobsen HJ, Dorca R, Reinard T. Coulomb and overlap self-similarities: a comparative selectivity analysis of structure–function relationships for auxin-like molecules. Journal of Chemical Information and Modeling. 2006;46:1751–1762. PubMed
Feugier FG, Mochizuki A, Iwasa Y. Self-organization of the vascular system in plant leaves: inter-dependent dynamics of auxin flux and carrier proteins. Journal of Theoretical Biology. 2005;236:366–375. PubMed
Fujita H, Mochizuki A. Pattern formation by the positive feedback regulation between flow of diffusible signal molecule and localization of its carrier. Journal of Theoretical Biology. 2006;241:541–555. PubMed
Gailweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 1998;282:2226–2230. PubMed
Gamborg OL, Miller RA, Ojima K. Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research. 1968;15:148–151. PubMed
Garnett P, Steinacher A, Stepney S, Clayton R, Leyser O. Computer simulation: the imaginary friend of auxin transport biology. Bioessays. 2010;32:828–835. PubMed
Geisler M, Murphy AS. The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Letters. 2006;580:1094–1102. PubMed
Goldsmith MHM. The polar transport of auxin. Annual Review of Plant Physiology. 1977;28:439–478.
Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jönsson H, Traas J, Meyerowitz EM. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biolology. 2010;8:e1000516. doi:10.1371/journal.pbio.1000516. PubMed PMC
Heisler MG, Jönsson H. Modeling auxin transport and plant development. Journal of Plant Growth Regulation. 2006;25:302–312.
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. PubMed
Ito H, Gray WM. A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiology. 2006;142:63–74. PubMed PMC
Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E. An auxin-driven polarized transport model for phyllotaxis. Proceedings of the National Academy of Sciences, USA. 2006;103:1633–1638. PubMed PMC
Kai K, Nakamura S, Wakasa K, Miyagawa H. Facile preparation of deuterium-labeled indole-3-acetic acid (IAA) and its metabolites to quantitatively analyze the disposition of exogenous IAA in Arabidopsis thaliana . Bioscience Biotechnology and Biochemistry. 2007;71:1946–1954. PubMed
Katekar GF. Auxins: nature of the receptor-site and molecular requirements for auxin activity. Phytochemistry. 1979;18:223–233.
Kramer EM. Computer models of auxin transport: a review and commentary. Journal of Experimental Botany. 2008;59:45–53. PubMed
Kramer EM, Bennett MJ. Auxin transport: A field in flux. Trends in Plant Science. 2006;11:382–386. PubMed
Kubeš M, Yang H, Richter GL, et al. The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. The Plant Journal. 2012 (in press) doi: 10.1111/j.1365-313X.2011.04818.x. PubMed
Laňková M, Smith RS, Pešek B, Kubeš M, Zažímalová E, Petrášek J, Hoyerová K. Auxin influx inhibitors 1-NOA, 2-NOA, and CHPAA interfere with membrane dynamics in tobacco cells. Journal of Experimental Botany. 2010;61:3589–3598. PubMed PMC
Leyser O. Auxin, self-organisation, and the colonial nature of plants. Current Biology. 2011;21:331–337. PubMed
Ludwig-Muller J. Auxin conjugates: their role for plant development and in the evolution of land plants. Journal of Experimental Botany. 2011;62:1757–1773. PubMed
Merks RMH, Van de Peer Y, Inzé D, Beemster GTS. Canalization without flux sensors: a traveling-wave hypothesis. Trends in Plant Science. 2007;12:384–390. PubMed
Mitchison GJ. A model for vein formation in higher plants. Proceedings of the Royal Society of London, Series B. 1980a;207:79–109.
Mitchison GJ. The dynamics of auxin transport. Proceedings of the Royal Society of London, Series B. 1980b;209:489–511.
Mitchison GJ, Hanke DE, Sheldrake AR. The polar transport of auxin and vein patterns in plants. Philosophical Transactions of the Royal Society of London, Series B. 1981;295:461–471.
Mravec J, Skůpa P, Bailly A, et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature. 2009;459:1136–1140. PubMed
Muller JF, Goujaud J, Caboche M. Isolation in vitro of naphthalene-acetic-tolerant mutants of Nicotiana tabacum, which are impaired in root morphogenesis. Molecular and General Genetics. 1985;199:194–200.
Nagata T, Nemoto Y, Hasezava S. Tobacco BY-2 cell line as the ‘Hela’ cell in the cell biology of higher plants. International Review of Cytology. 1992;132:1–30.
Normanly J, Slovin JP, Cohen JD. Hormone biosynthesis, metabolism and its regulation. In: Davies PJ, editor. Plant hormones: biosynthesis, signal transduction, action! 3rd edn. Dordrecht, The Netherlands: Springer; 2010. pp. 36–62.
Paciorek T, Zažímalová E, Ruthardt N, et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005;435:1251–1256. PubMed
Parry G, Delbarre A, Marchant A, Swarup R, Napier R, Perrot-Rechenmann C, Bennett MJ. Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation aux1. The Plant Journal. 2001a;25:399–406. PubMed
Parry G, Marchant A, May S, et al. Quick on the uptake: Characterization of a family of plant auxin influx carriers. Journal of Plant Growth Regulation. 2001b;20:217–225.
Peer WA, Blakeslee JJ, Yang H, Murphy AS. Seven things we think we know about auxin transport. Molecular Plant. 2011;4:487–504. PubMed
Peer WA, Murphy AS. Flavonoids and auxin transport: modulators or regulators? Trends in Plant Science. 2007;12:556–563. PubMed
Petrášek J, Černá A, Schwarzerová K, Elčkner M, Morris DA, Zažímalová E. Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiology. 2003;131:254–263. PubMed PMC
Petrášek J, Elčkner M, Morris DA, Zažímalová E. Auxin efflux carrier activity and auxin accumulation regulate cell division and polarity in tobacco cells. Planta. 2002;216:302–308. PubMed
Petrášek J, Friml J. Auxin transport routes in plant development. Development. 2009;136:2675–2688. PubMed
Petrášek J, Mravec J, Bouchard R, et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006;312:914–918. PubMed
Rahman A, Ahamed A, Amakawa T, Goto N, Tsurumi S. Chromosaponin I specifically interacts with AUX1 protein in regulating the gravitropic response of arabidopsis roots. Plant Physiology. 2001;125:990–1000. PubMed PMC
Raven J. Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytologist. 1975;74:163–172.
Rubery P. Phytotropins-receptors and endogenous ligands. Hormone perception and signal transduction in animals and plants. Book Series. Symposia of the Society for Experimental Biology. 1990;44:119–146. PubMed
Rubery P, Sheldrake A. Carrier-mediated auxin transport. Planta. 1974;118:101–121. PubMed
Sachs T. Polarity and the induction of organized vascular tissues. Annals of Botany. 1969;33:263–275.
Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K. Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica . Proceedings of the National Academy of Sciences, USA. 2003;100:751–756. PubMed PMC
Smith RS, Bayer EM. Auxin transport-feedback models of patterning in plants. Plant, Cell and Environment. 2009;32:1258–1271. PubMed
Smith RS, Guyomarch S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P. A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences, USA. 2006;103:1301–1306. PubMed PMC
Steinacher A, Leyser O, Clayton RH. A computational model of auxin and pH dynamics in a single plant cell. Journal of Theoretical Biology. 2012;296:84–94. PubMed
Stoma S, Lucas M, Chopard J, Schaedel J, Traas J, Godin C. Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Computational Biology. 2008;4:e1000207. PubMed PMC
Terasaka K, Blakeslee JJ, Titapiwatanakun B, et al. PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. The Plant Cell. 2005;17:2922–2939. PubMed PMC
Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, et al. ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. The Plant Journal. 2009;57:27–44. PubMed
Titapiwatanakun B, Murphy AS. Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. Journal of Experimental Botany. 2009;60:1093–1097. PubMed
Tromas A, Paponov I, Perrot-Rechenmann C. AUXIN BINDING PROTEIN 1: functional and evolutionary aspects. Trends in Plant Science. 2010;15:436–446. PubMed
Wabnik K, Govaerts W, Friml J, Kleine-Vehn J. Feedback models for polarized auxin transport: an emerging trend. Molecular BioSystems. 2011;7:2352–2359. PubMed
Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinöhl V, Merks RMH, Goaverts W, Friml J. Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Molecular Systems Biology. 2010;6:447. PubMed PMC
Yamamoto M, Yamamoto KT. Differential effects of 1- naphthalene acetic acid, indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid on the gravitropic response of roots in an auxin resistant mutant of Arabidopsis Aux1 . Plant and Cell Physiology. 1998;39:660–664. PubMed
Yang HB, Murphy AS. Functional expression and characterization of Arabidopsis ABCB AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe . The Plant Journal. 2009;59:179–191. PubMed
Zažímalová E, Murphy A, Yang H, Hoyerová K, Hošek P. Auxin transporters: why so many? Cold Spring Harbor Perspectives in Biology. 2010;2:a001552. PubMed PMC
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