Auxin transport during root gravitropism: Transporters and techniques

Plant Biology

Volumn 16, Issue SUPPL.1, 2014, Pages 50-57

  Geisler, M ^a   Wang, B ^a   Zhu, J ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

ABC transporters; Chemiosmotic model; Cholodny Went hypothesis; Gravity sensing; IAA; PIN proteins

Indexed keywords

GRAVITY FIELD; HORMONE; NUMERICAL MODEL; PHYTOCHEMISTRY; PROTEIN; RESOLUTION; ROOT SYSTEM;

ABC TRANSPORTER; CARRIER PROTEIN; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE;

CHEMIOSMOTIC MODEL; CHOLODNY-WENT HYPOTHESIS; GRAVITROPISM; GRAVITY SENSING; METABOLISM; METHODOLOGY; PHYSIOLOGY; PIN PROTEINS; PLANT ROOT; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

ABC TRANSPORTERS; CHEMIOSMOTIC MODEL; CHOLODNY-WENT HYPOTHESIS; GRAVITY SENSING; IAA; PIN PROTEINS;

BIOLOGICAL TRANSPORT; GRAVITROPISM; INDOLEACETIC ACIDS; MEMBRANE TRANSPORT PROTEINS; PHYSIOLOGY; PLANT ROOTS;

EID: 84890918102     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/plb.12030     Document Type: Review

References (87)

1. Abel S., Oeller P.W., Theologis A. (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proceedings of the National Academy of Sciences of the United States of America, 91, 326-330.
2. Allen G.J., Kwak J.M., Chu S.P., Llopis J., Tsien R.Y., Harper J.F., Schroeder J.I. (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. The Plant Journal, 19, 735-747.
3. Armstrong J.I., Yuan S., Dale J.M., Tanner V.N., Theologis A. (2004) Identification of inhibitors of auxin transcriptional activation by means of chemical genetics in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 101, 14978-14983.
4. Bailly A., Sovero V., Vincenzetti V., Santelia D., Bartnik D., Koenig B.W., Mancuso S., Martinoia E., Geisler M. (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. Journal of Biological Chemistry, 283, 21817-21826.
5. 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., Oliva M., Swarup R., Sairanen I., Parry G., Ljung K., Beeckman T., Garibaldi J.M., Estelle M., Owen M.R., Vissenberg K., Hodgman T.C., Pridmore T.P., King J.R., Vernoux T., Bennett M.J. (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proceedings of the National Academy of Sciences of the United States of America, 109, 4668-4673.
6. Barbez E., Kubeš M., Rolčík J., Béziat C., Pěnčík A., Wang B., Rosquete M.R., Zhu J., Dobrev P.I., Lee Y., Zažímalovà E., Petrášek J., Geisler M., Friml J., Kleine-Vehn J. (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature, 485, 119-122.
7. Bargmann B.O., Birnbaum K.D. (2009) Positive fluorescent selection permits precise, rapid, and in-depth overexpression analysis in plant protoplasts. Plant Physiology, 149, 1231-1239.
8. Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., Friml J. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115, 591-602.
9. 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. (1996) Arabidopsis AUX1 gene, a permease-like regulator of root gravitropism. Science, 273, 948-950.
10. Blakeslee J.J., Bandyopadhyay A, Lee O.R., Mravec J., Titapiwatanakun B., Sauer M., Makam S.N., Cheng Y., Bouchard R., Adamec J., Geisler M., Nagashima A., Sakai T., Martinoia E., Friml J., Peer W.A., Murphy A.S. (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. The Plant Cell, 19, 131-147.
11. Blancaflor E.B., Masson P.H. (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiology, 133, 1677-1690.
12. Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., Scheres B. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433, 39-44.
13. Bouchard R., Bailly A., Blakeslee J.J., Oehring S.C., Vincenzetti V., Lee O.R., Paponov I., Palme K., Mancuso S., Murphy A.S., Schulz B., Geisler M. (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. Journal of Biological Chemistry, 281, 30603-30612.
14. Brunoud G., Wells D.M., Oliva M., Larrieu A., Mirabet V., Burrow A.H., Beeckman T., Kepinski S., Traas J., Bennett M.J., Vernoux T. (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature, 482, 103-106.
15. Caruso J., Pence V., Leverone L. (1995) Immunoassay methods of plant hormone analysis. Davies P.J. (Ed.), Plant Hormones: Physiology, Biochemistry and Molecular Biology. Kluwer Academic, Norwell, MA, USA, pp 433-447.
16. Chen D., Zhao J. (2008) Free IAA in stigmas and styles during pollen germination and pollen tube growth of Nicotiana tabacum. Physiologia Plantarum, 134, 202-215.
17. Chen R., Hilson P., Sedbrook J., Rosen E., Caspar T., Masson P.H. (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proceedings of the National Academy of Sciences of the United States of America, 95, 15112-15117.
18. Cohen J.D., Bausher M.G., Bialek K., Buta J.G., Gocal G.F., Janzen L.M., Pharis R.P., Reed A.N., Slovin J.P. (1987) Comparison of a commercial ELISA assay for indole-3-acetic acid at several stages of purification and analysis by gas chromatography-selected ion monitoring-mass spectrometry using a c(6)-labeled internal standard. Plant Physiology, 84, 982-686.
19. Dal Bosco C., Dovzhenko A., Liu X., Woerner N., Rensch T., Eismann M., Eimer S., Hegermann J., Paponov I.A., Ruperti B., Heberle-Bors E., Touraev A., Cohen J.D., Palme K. (2012) The endoplasmic reticulum localized PIN8 is a pollen-specific auxin carrier involved in intracellular auxin homeostasis. The Plant Journal, 71, 860-870.
20. Ding Z., Wang B., Moreno I., Dupláková N., Simon S., Carraro N., Reemmer J., Pěnčík A., Chen X., Tejos R., Skůpa P., Pollmann S., Mravec J., Petrášek J., Zažímalová E., Honys D., Rolčík J., Murphy A., Orellana A., Geisler M., Friml J. (2012) ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nature communications, 3, 941.
21. Friml J., Palme K. (2002) Polar auxin transport - old questions and new concepts? Plant Molecular Biology, 49, 273-284.
22. Friml J., Wisniewska J., Benkova E., Mendgen K., Palme K. (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature, 415, 806-809.
23. Gälweiler L., Guan C., Müller A., Wisman E., Mendgen K., Yephremov A., Palme K. (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science, 282, 2226-2230.
24. Geisler M., Murphy A.S. (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Letters, 580, 1094-1102.
25. Geisler M., Kolukisaoglu H.U., Bouchard R., Billion K., Berger J., Saal B., Frangne N., Koncz-Kalman Z., Koncz C., Dudler R., Blakeslee J.J., Murphy A.S., Martinoia E., Schulz B. (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Molecular Biology of the Cell, 14, 4238-4249.
26. Geisler M., Blakeslee J.J., Bouchard R., Lee O.R., Vincenzetti V., Bandyopadhyay A., Titapiwatanakun B., Peer W.A., Bailly A., Richards E.L., Ejenda K.F.K., Smith A.P., Baroux C., Grossniklaus U., Muller A., Hrycyna C.A., Dudler R., Murphy A.S., Martinoia E. (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. The Plant Journal, 44, 179-194.
27. Gjetting K.S., Ytting C.K., Schulz A., Fuglsang A.T. (2012) Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. Journal of Experimental Botany, 63, 3207-3218.
28. Goldsmith M., Goldsmith T. (1977) Chemisomotic model for polar transport of auxin. Plant Physiology, 59, 90-90.
29. Grunewald W., Friml J. (2010) The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO Journal, 29, 2700-2714.
30. Hager A., Menzel H., Krauss A. (1971) Versuche und Hypothese zur Primärwirkung des Auxins beim Streckungswachstum. Planta, 100, 47-75.
31. Hayashi K. (2012) Visualization of cellular auxin distribution by chemical biology approach. Abstract book of the AUXIN 2012 Conference, Hawai'i, USA: 15 pp.
32. Henrichs S., Wang B., Fukao Y., Zhu J., Charrier L., Bailly A., Oehring S.C., Linnert M., Weiwad M., Endler A., Nanni P., Pollmann S., Mancuso S., Schulz A., Geisler M. (2012) Regulation of ABCB1/PGP1-catalysed auxin transport by linker phosphorylation. EMBO Journal, 31, 2965-2980.
33. Kamimoto Y., Terasaka K., Hamamoto M., Takanashi K., Fukuda S., Shitan N., Sugiyama A., Suzuki H., Shibata D., Wang B., Pollmann S., Geisler M., Yazaki K. (2012) Arabidopsis ABCB21 is a Facultative Auxin Importer/Exporter Regulated by Cytoplasmic Auxin Concentration. Plant and Cell Physiology, 53, 2090-2100.
34. Kim J.Y., Henrichs S., Bailly A., Vincenzetti V., Sovero V., Mancuso S., Pollmann S., Kim D., Geisler M., Nam H.G. (2010) Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. Journal of Biological Chemistry, 285, 23309-23317.
35. Krouk G., Lacombe B., Bielach A., Perrine-Walker F., Malinska K., Mounier E., Hoyerova K., Tillard P., Leon S., Ljung K., Zazimalova E., Benkova E., Nacry P., Gojon A. (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell, 18, 927-937.
36. Kubeš M., Yang H., Richter G.L., Cheng Y., Mlodzińska E., Wang X., Blakeslee J.J., Carraro N., Petrášek J., Zažímalová E., Hoyerová K., Peer W.A., Murphy A.S. (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. The Plant Journal, 69, 640-654.
37. Lewis D.R., Muday G.K. (2009) Measurement of auxin transport in Arabidopsis thaliana. Nature Protocols, 4, 437-451.
38. Luschnig C., Gaxiola R.A., Grisafi P., Fink G.R. (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes & Development, 12, 2175-2187.
39. Maher E.P., Martindale S.J. (1980) Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochemical Genetics, 18, 1041-1053.
40. Mancuso S., Marras A.M., Magnus V., Baluska F. (2005) Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. Analytical Biochemistry, 341, 344-351.
41. Matsuda S., Kajizuka T., Kadota A., Nishimura T., Koshiba T. (2011) NPH3- and PGP-like genes are exclusively expressed in the apical tip region essential for blue-light perception and lateral auxin transport in maize coleoptiles. Journal of Experimental Botany, 62, 3459-3466.
42. McLamore E.S., Diggs A., Calvo Marzal P., Shi J., Blakeslee J.J., Peer W.A., Murphy A.S., Porterfield D.M. (2010) Non-invasive quantification of endogenous root auxin transport using an integrated flux microsensor technique. The Plant Journal, 63, 1004-1016.
43. Michniewicz M., Brewer P., Friml J. (2007) Polar auxin transport and asymmetric auxin distribution. The Arabidopsis Book. The American Society of Plant Biologists, Rockville, MA, USA, doi: 10.1199/tab.0108.
44. Mitchell E.K., Davies P.J. (1975) Evidence for three different systems of movement of indole acetic acid in intact roots of Phaseolus coccineus. Physiologia Plantarum, 33, 290-294.
45. 2+ measurements using improved cameleons. Proceedings of the National Academy of Sciences of the United States of America, 96, 2135-2140.
46. Mravec J., Skůpa P., Bailly A., Hoyerová K., Krecek P., Bielach A., Petrásek J., Zhang J., Gaykova V., Stierhof Y.D., Dobrev P.I., Schwarzerová K., Rolcík J., Seifertová D., Luschnig C., Benková E., Zazímalová E., Geisler M., Friml J. (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature, 459, 1136-1140.
47. Muday G.K., DeLong A. (2001) Polar auxin transport: controlling where and how much. Trends in Plant Science, 11, 535-542.
48. Muday G.K., Rahman A. (2008) Auxin transport and the integration of gravitropic growth. Gilroy S., Masson P.H. (Eds), Plant Tropisms. Blackwell, Ames, IA, USA, pp 47-77.
49. Muller A., Guan C., Galweiler L., Tanzler P., Huijser P., Marchant A., Parry G., Bennett M., Wisman E., Palme K. (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO Journal, 17, 6903-6911.
50. Murphy A.S., Hoogner K.R., Peer W.A., Taiz L. (2002) Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiology, 128, 935-950.
51. Nemhauser J.L., Mockler T.C., Chory J. (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biology, 2, E258.
52. Noh B., Murphy A.S., Spalding E.P. (2001) Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. The Plant Cell, 13, 2441-2454.
53. Okada K., Ueda J., Komaki M.K., Bell C.J., Shimura Y. (1991) Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. The Plant Cell, 3, 677-684.
54. Ottenschläger I., Wolff P., Wolverton C., Bhalerao R.P., Sandberg G., Ishikawa H., Evans M., Palme K. (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 2987-2991.
55. Palme K., Dovzhenko A., Ditengou F.A. (2006) Auxin transport and gravitational research: perspectives. Protoplasma, 229, 175-181.
56. Péret B., Swarup K., Ferguson A., Seth M., Yang Y., Dhondt S., James N., Casimiro I., Perry P., Syed A., Yang H., Reemmer J., Venison E., Howells C., Perez-Amador M.A., Yun J., Alonso J., Beemster G.T., Laplaze L., Murphy A., Bennett M.J., Nielsen E., Swarup R. (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. The Plant Cell, 24, 2874-2885.
57. Petersson S.V., Johansson A.I., Kowalczyk M., Makoveychuk A., Wang J.Y., Moritz T., Grebe M., Benfey P.N., Sandberg G., Ljung K. (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. The Plant Cell, 21, 1659-1668.
58. Petrášek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertová D., Wiśniewska J., Tadele J., Čovanová M., Dhonukshe P., Skůpa P., Benková E., Perry L., Křeček P., Lee O.R., Fink G.R., Geisler M., Murphy A.S., Luschnig C., Zažímalová E., Friml J. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science, 312, 914-918.
59. Pollmann S., Müller A., Piotrowski M., Weiler E.W. (2002) Occurrence and formation of indole-3-acetamide in Arabidopsis thaliana. Planta, 216, 155-161.
60. Rahman A., Takahashi M., Shibasaki K., Wu S., Inaba T., Tsurumi S., Baskin T.I. (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. The Plant Cell, 22, 1762-1776.
61. Rashotte A.M., Brady S.R., Reed R.C., Ante S.J., Muday G.K. (2000) Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiology, 122, 481-490.
62. Rashotte A.M., DeLong A., Muday G.K. (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. The Plant Cell, 13, 1683-1697.
63. Raven J.A. (1975) Transport of indole-3-acetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytologist, 74, 163-172.
64. Rayle D.L., Cleland R.E. (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiology, 99, 1271-1274.
65. Rayle D.L., Zenk M.H. (1973) Cell extension growth: some recent advances. Biochemical Society Symposium, 38, 235-246.
66. Rayle D.L., Haughton P.M., Cleland R. (1970) An in vitro system simulates plant cell extension growth. Proceedings of the National Academy of Sciences of the United States of America, 67, 1814-1817.
67. Rosquete M.R., Barbez E., Kleine-vehn J. (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Molecular Plant, 5, 772-786.
68. Rubery P.H., Sheldrake A.R. (1973) Effect of pH and surface charge on cell uptake of auxin. Nature New Biology, 244, 285-288.
69. Ruzicka K., Strader L.C., Bailly A., Yang H., Blakeslee J., Langowski L., Nejedlá E., Fujita H., Itoh H., Syono K., Hejátko J., Gray W.M., Martinoia E., Geisler M., Bartel B., Murphy A.S., Friml J. (2010) Arabidopsis PIS1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proceedings of the National Academy of Sciences of the United States of America, 107, 10749-10753.
70. Santelia D., Vincenzetti V., Azzarello E., Bovet L., Fukao Y., Duchtig P., Mancuso S., Martinoia E., Geisler M. (2005) MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Letters, 579, 5399-5406.
71. Schlicht M., Strnad M., Scanlon M.J., Mancuso S., Hochholdinger F., Palme K., Volkmann D., Menzel D., Baluska F. (2006) Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signaling & Behavior, 1, 122-133.
72. Shi L., Miller I., Moore R. (1993) Immunocytochemical localization of indole-3-acetic acid in primary root of Zea mays. Plant, Cell & Environment, 16, 967-973.
73. Swarup R., Péret B. (2012) AUX/LAX family of auxin influx carriers - an overview. Frontiers in plant science, 3, 225.
74. Swarup K., Benková E., Swarup R., Casimiro I., Péret B., Yang Y., Parry G., Nielsen E., De Smet I., Vanneste S., Levesque M.P., Carrier D., James N., Calvo V., Ljung K., Kramer E., Roberts R., Graham N., Marillonnet S., Patel K., Jones J.D., Taylor C.G., Schachtman D.P., May S., Sandberg G., Benfey P., Friml J., Kerr I., Beeckman T., Laplaze L., Bennett M.J. (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nature Cell Biology, 10, 946-954.
75. 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., Yazaki K. (2005) PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots. The Plant Cell, 17, 2922-2939.
76. Tsuda E., Yang H., Nishimura T., Uehara Y., Sakai T., Furutani M., Koshiba T., Hirose M., Nozaki H., Murphy A.S., Hayashi K. (2011) Alkoxy-auxins are selective inhibitors of auxin transport mediated by PIN, ABCB, and AUX1 transporters. Journal of Biological Chemistry, 286, 2354-2364.
77. 14C-labeled indoleacetic acid in Vicia root segments. Plant and Cell Physiology, 19, 1195-1206.
78. Ulmasov T., Murfett J., Hagen G., Guilfoyle T. (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant Cell, 9, 1963-1971.
79. Utsuno K., Shikanai T., Yamada Y., Hashimoto T. (1998) AGR, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant and Cell Physiology, 39, 1111-1118.
80. Wan Y., Jasik J., Wang L., Hao H., Volkmann D., Menzel D., Mancuso S., Baluška F., Lin J. (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. The Plant Cell, 24, 551-565.
81. Wang B., Bailly A., Zwiewka M., Henrichs S., Azzarello E., Mancuso S., Maeshima M., Friml J., Schulz A., Geisler M. (2013) Arabidopsis TWISTED DWARF1 functionally interacts with auxin exporter ABCB1 on the root plasma membrane. The Plant Cell, doi: 10.1105/tpc.112.105999.
82. Went F.W. (1974) Reflections and speculations. Annual Review of Plant Physiology, 25, 1-26.
83. Wisniewska J., Xu J., Seifertová D., Brewer P.B., Ruzicka K., Blilou I., Rouquié D., Benková E., Scheres B., Friml J. (2006) Polar PIN localization directs auxin flow in plants. Science, 312, 883.
84. Wu G., Otegui M.S., Spalding E.P. (2010) The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. The Plant Cell, 22, 3295-3304.
85. Yang H., Murphy A.S. (2009) Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. The Plant Journal, 59, 179-191.
86. Young L.M., Evans M.L., Hertel R. (1990) Correlations between gravitropic curvature and auxin movement across gravistimulated roots of Zea mays. Plant Physiology, 92, 792-796.
87. Zažímalová E., Murphy A.S., Yang H., Hoyerová K., Hošek P. (2009) Auxin transporters - Why So Many? Cold Springs Harbor Perspectives in Biology, 2, a001552-a001552.