Auxin: A Trigger for Change in Plant Development

Cell

Volumn 136, Issue 6, 2009, Pages 1005-1016

  Vanneste, Steffen ^a   Friml, Jiří ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; F BOX PROTEIN; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1;

ARABIDOPSIS; AUXIN TRANSPORT; CELL NUCLEUS; CELL TRANSPORT; NONHUMAN; PLANT DEVELOPMENT; PLANT GROWTH; PLANT MORPHOLOGY; PLANT ROOT; PLANT TISSUE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; UBIQUITINATION;

EID: 62149148505     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.03.001     Document Type: Review

References (98)

1. Abel S., and Theologis A. Early genes and auxin action. Plant Physiol. 111 (1996) 9-17
2. Abas L., Benjamins R., Malenica N., Paciorek T., Wiśniewska J., Moulinier-Anzola J.C., Sieberer T., Friml J., and Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8 (2006) 249-256
3. Bailly A., Sovero V., Vincezetti V., Santelia D., Bartnik D., Koenig B.W., Mancuso S., Martinoia E., and Geisler M. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J. Biol. Chem. 283 (2008) 21817-21826
4. Bainbridge K., Guyomarc'h S., Bayer E., Swarup R., Bennett M., Mandel T., and Kuhlemeier C. Auxin influx carriers stabilize phyllotactic patterning. Genes Dev. 22 (2008) 810-823
5. Benjamins R., and Scheres B. Auxin: the looping star in plant development. Annu. Rev. Plant Biol. 59 (2008) 443-465
6. Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., and Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115 (2003) 591-602
7. Bennett M.J., Marchant A., Green H.G., May S.T., Ward S.P., Millner P.A., Walker A.R., Schulz B., and Feldmann K.A. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273 (1996) 948-950
8. Blakeslee J.J., Bandyopadhyay A., Lee O.R., Mravec J., Tipapiwatanakun B., Sauer M., Makam S.N., Cheng Y., Bouchard R., Adamec J., et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19 (2007) 131-147
9. Blilou I., Xu J., Wildwater M., Willemsen V., Paponov I., Friml J., Heidstra R., Aida M., Palme K., and Scheres B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433 (2005) 39-44
10. Braun N., Wyrzykowska J., Muller P., David K., Couch D., Perrot-Reichenmann C., and Fleming A.J. Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell 20 (2008) 2746-2762
11. Chen J.-G., Ullah H., Young J.C., Sussman M.R., and Jones A.M. ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev. 15 (2001) 902-911
12. Cheng Y., Dai X., and Zhao Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 20 (2006) 1790-1799
13. Cheng Y., Dai X., and Zhao Y. Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19 (2007) 2430-2439
14. Cho M., Lee S.H., and Cho H.-T. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19 (2007) 3930-3943
15. Davies P.J. Plant Hormones: Biosynthesis, Signal Transduction, Action! (2004), Kluwer Academic Publishers, London
16. Dharmasiri N., Dharmasiri S., and Estelle M. The F-box protein TIR1 is an auxin receptor. Nature 435 (2005) 441-445
17. Dharmasiri N., Dharmasiri S., Weijers D., Lechner E., Yamada M., Hobbie L., Ehrismann J.S., Jürgens G., and Estelle M. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9 (2005) 109-119
18. Dhonukshe P., Aniento F., Hwang I., Robinson D.G., Mravec J., Stierhof Y.-D., and Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17 (2007) 520-527
19. Dhonukshe P., Grigoriev I., Fischer R., Tominaga M., Robinson D.G., Hašek J., Paciorek T., Petrášek J., Seifertová D., Tejos R., et al. Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc. Natl. Acad. Sci. USA 105 (2008) 4489-4494
20. Dhonukshe D., Tanaka H., Goh T., Ebine K., Mähönen A.P., Prasad K., Blilou I., Geldner N., Xu J., Uemura T., et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456 (2008) 962-966
21. Dreher K.A., Brown J., Saw R.E., and Callis J. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18 (2006) 699-714
22. Dubrovsky J.G., Sauer M., Napsucialy-Mendivil S., Ivanchenko M., Friml J., Shishkova S., Celenza J., and Benková E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl. Acad. Sci. USA 105 (2008) 8790-8794
23. Entchev E.V., and González-Gaitán M.A. Morphogen gradient formation and vesicular trafficking. Traffic 3 (2002) 98-109
24. Friml J. Auxin transport-shaping the plant. Curr. Opin. Plant Biol. 6 (2003) 7-12
25. Friml J., Benková E., Blilou I., Wisniewska J., Hamann T., Ljung K., Woody S., Sandberg G., Scheres B., Jürgens G., and Palme K. AtPIN4 mediates sink driven auxin gradients and root patterning in Arabidopsis. Cell 108 (2002) 661-673
26. Friml J., Wiśniewska J., Benková E., Mendgen K., and Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415 (2002) 806-809
27. Friml J., Vieten A., Sauer M., Weijers D., Schwarz H., Hamann T., Offringa R., and Jürgens G. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426 (2003) 147-153
28. Friml J., Yang X., Michniewicz M., Weijers D., Quint A., Tietz O., Benjamins R., Ouwerkerk P.B.F., Ljung K., Sandberg G., et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306 (2004) 862-865
29. Gälweiler L., Guan C., Müller A., Wisman E., Mendgen K., Yephremov A., and Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282 (1998) 2226-2230
30. Geisler M., Blakeslee J.J., Bouchard R., Lee O.R., Vincenzetti V., Bandyopadhyay A., Titapiwatanakun B., Peer W.A., Bailly A., Richards E.L., et al. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 44 (2005) 179-194
31. Geldner N., Friml J., Stierhof Y.-D., Jürgens G., and Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413 (2001) 425-428
32. TIR1-dependent degradation of AUX/IAA proteins. Nature 414 (2001) 271-276
33. Guilfoyle T.J., and Hagen G. Auxin response factors. Curr. Opin. Plant Biol. 10 (2007) 453-460
34. Hardtke C.S., Ckurshumova W., Vidaurre D.P., Singh S.A., Stamatiou G., Tiwari S.B., Hagen G., Guilfoyle T.J., and Berleth T. Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131 (2004) 1089-1100
35. Heisler M.G., Ohno C., Das P., Sieber P., Reddy G.V., Long J.A., and Meyerowitz E.M. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15 (2005) 1899-1911
36. Hertel R., Thompson K.-S., and Russo V.E.A. In-vitro auxin binding to particulate cell fractions from corn coleoptiles. Planta 107 (1972) 325-340
37. Jones A.M., Im K.-H., Savka M.A., Wu M.-J., DeWitt N.G., Shillito R., and Binns A.N. Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282 (1998) 1114-1117
38. Jones A.R., Kramer E.M., Knox K., Swarup R., Bennett M.J., Lazarus C.M., Leyser H.M.O., and Grierson C.S. Auxin transport through non-hair cells sustains root-hair development. Nat. Cell Biol. 11 (2009) 78-84
39. Kepinski S., and Leyser O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435 (2005) 446-451
40. Kim J., Harter K., and Theologis A. Protein-protein interactions among the Aux/IAA proteins. Proc. Natl. Acad. Sci. USA 94 (1997) 11786-11791
41. Kleine-Vehn J., Dhonukshe P., Sauer M., Brewer P., Wiśniewka J., Paciorek T., Benková E., and Friml J. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 18 (2008) 526-531
42. Kovtun Y., Chiu W.-L., Zeng W., and Sheen J. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395 (1998) 716-720
43. Leblanc N., David K., Grosclaude J., Pradier J.-M., Barbier-Brygoo H., Labiau S., and Perrot-Rechenmann C. A novel immunological approach establishes that the auxin-binding protein, Nt-abp1, is an element involved in auxin signaling at the plasma membrane. J. Biol. Chem. 274 (1999) 28314-28320
44. Lee J.S., Wang S., Sritubtim S., Chen J.-G., and Ellis B.E. Arabidopsis mitogen-activated protein kinase MPK12 interacts with the MAPK phosphatase IBR5 and regulates auxin signaling. Plant J. 57 (2009) 975-985
45. Leyser H.M.O., Lincoln C.A., Timpte C., Lammer D., Turner J., and Estelle M. Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364 (1993) 161-164
46. +-PPase AVP1 regulates auxin-mediated organ development. Science 310 (2005) 121-125
47. Luschnig C., Gaxiola R.A., Grisafi P., and Fink G.R. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12 (1998) 2175-2187
48. Marchant A., Bhalerao R., Casimiro I., Eklöf J., Casero P.J., Bennett M., and Sandberg G. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14 (2002) 589-597
49. Mattsson J., Ckurshumova W., and Berleth T. Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol. 131 (2003) 1327-1339
50. Merks R.M.H., Van de Peer Y., Inzé D., and Beemster G.T.S. Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci. 12 (2007) 384-390
51. Michniewicz M., Zago M.K., Abas L., Weijers D., Schweighofer A., Meskiene I., Heisler M.G., Ohno C., Zhang J., Huang F., et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130 (2007) 1044-1056
52. Mockaitis K., and Howell S.H. Auxin induces mitogenic activated protein kinase (MAPK) activation in roots of Arabidopsis seedlings. Plant J. 24 (2000) 785-796
53. Mockaitis K., and Estelle M. Auxin receptors and plant development: A new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24 (2008) 55-80
54. Mravec J., Kubeš M., Bielach A., Gaykova V., Petrášek J., Skůpa P., Chand S., Benková E., Zažímalová E., and Friml J. Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135 (2008) 3345-3354
55. Murphy A.S., Hoogner K.R., Peer W.A., and Taiz L. Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiol. 128 (2002) 935-950
56. Muto H., Watahiki M.K., Nakamoto D., Kinjo M., and Yamamoto K.T. Specificity and similarity of functions of the Aux/IAA genes in auxin signaling of Arabidopsis revealed by promoter-exchange experiments among MSG2/IAA19, AXR2/IAA7, and SLR/IAA14. Plant Physiol. 144 (2007) 187-196
57. Paciorek T., Zažímalová E., Ruthardt N., Petrášek J., Stierhof Y.-D., Kleine-Vehn J., Morris D.A., Emans N., Jürgens G., Geldner N., and Friml J. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435 (2005) 1251-1256
58. Petrášek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertová D., Wiśniewska J., Tadele Z., Kubeš M., Čovanová M., et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312 (2006) 914-918
59. Pickett F.B., Wilson A.K., and Estelle M. The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. 94 (1990) 1462-1466
60. Raven J.A. Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol. 74 (1975) 163-172
61. Reinhardt D., Pesce E.-R., Stieger P., Mandel T., Baltensperger K., Bennett M., Traas J., Friml J., and Kuhlemeier C. Regulation of phyllotaxis by polar auxin transport. Nature 426 (2003) 255-260
62. Rensing S.A., Lang D., Zimmer A.D., Terry A., Salamov A., Shapiro H., Nishiyama T., Perroud P.-F., Lindquist E.A., Kamisugi Y., et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319 (2008) 64-69
63. Rouse D., Mackay P., Stirnberg P., Estelle M., and Leyser O. Changes in auxin response from mutations in an AUX/IAA gene. Science 279 (1998) 1371-1373
64. Rubery P.H., and Sheldrake A.R. Carrier-mediated auxin transport. Planta 118 (1974) 101-121
65. Ruegger M., Dewey E., Gray W.M., Hobbie L., Turner J., and Estelle M. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev. 12 (1998) 198-207
66. Sabatini S., Beis D., Wolkenfelt H., Murfett J., Guilfoyle T., Malamy J., Benfey P., Leyser O., Bechtold N., Weisbeek P., and Scheres B. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99 (1999) 463-472
67. Sachs T. Cell polarity and tissue patterning in plants. Dev. Suppl. 1 (1991) 83-93
68. Sauer M., Balla J., Luschnig C., Wišniewska J., Reinöhl V., Friml J., and Benková E. Canalization of auxin flow by Aux/IAA-ARF-dependent feed-back regulation of PIN polarity. Genes Dev. 20 (2006) 2902-2911
69. Scarpella E., Marcos D., Friml J., and Berleth T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 20 (2006) 1015-1027
70. Senn A.P., and Goldsmith M.H.M. Regulation of electrogenic proton pumping by auxin and fusicoccin as related to the growth of Avena coleoptiles. Plant Physiol. 88 (1988) 131-138
71. Shin R., Burch A.Y., Huppert K.A., Tiwari S.B., Murphy A.S., Guilfoyle T.J., and Schachtman D.P. The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19 (2007) 2440-2453
72. 2+ concentration in the cytosol of wheat leaf protoplasts. J. Plant Physiol. 161 (2004) 937-945
73. Sieberer T., Seifert G.J., Hauser M.-T., Grisafi P., Fink G.R., and Luschnig C. Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr. Biol. 10 (2000) 1595-1598
74. Sorefan K., Girin T., Liljegren S.J., Ljung K., Robles P., Galván-Ampudia C.S., Offringa R., Friml J., Yanofsky M.F., and Østergaard L. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature (2009) 10.1038/nature07875
75. Stepanova A.N., Robertson-Hoyt J., Yun J., Benavente L.M., Xie D.-Y., Doležal K., Schlereth A., Jürgens G., and Alonso J.M. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133 (2008) 177-191
76. Stone B.B., Stowe-Evans E.L., Harper R.M., Celaya R.B., Ljung K., Sandberg G., and Liscum E. Disruptions in AUX1-dependent auxin influx alter hypocotyl phototropism in Arabidopsis. Mol. Plant 1 (2008) 129-144
77. Strader L.C., Monroe-Augustus M., and Bartel B. The IBR5 phosphatase promotes Arabidopsis auxin responses through a novel mechanism distinct from TIR1-mediated repressor degradation. BMC Plant Biol. 8 (2008) 41.1-41.15
78. 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. 10 (2008) 946-954
79. Szemenyei H., Hannon M., and Long J.A. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319 (2008) 1384-1386
80. Tan X., Calderon-Villalobos L.I.A., Sharon M., Zheng C., Robinson C.V., Estelle M., and Zheng N. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446 (2007) 640-645
81. Tanaka H., Dhonukshe P., Brewer P.B., and Friml J. Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell. Mol. Life Sci. 63 (2006) 2738-2754
82. Tao Y., Ferrer J.-L., Ljung K., Pojer F., Hong F., Long J.A., Li L., Moreno J.E., Bowman M.E., Ivans L.J., et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133 (2008) 164-176
83. Teleman A.A., Strigini M., and Cohen S.M. Shaping morphogen gradients. Cell 105 (2001) 559-562
84. Theologis A., Huynh T.V., and Davis R.W. Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J. Mol. Biol. 183 (1985) 53-68
85. Thimann K.V. Hormones and the analysis of growth. Plant Physiol. 13 (1938) 437-449
86. Tiwari S.B., Hagen G., and Guilfoyle T.J. Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16 (2004) 533-543
87. Uggla C., Moritz T., Sandberg G., and Sundberg B. Auxin as a positional signal in pattern formation in plants. Proc. Natl. Acad. Sci. USA 93 (1996) 9282-9286
88. Ulmasov T., Hagen G., and Guilfoyle T.J. ARF1, a transcription factor that binds to auxin response elements. Science 276 (1997) 1865-1868
89. Vieten A., Vanneste S., Wiśniewska J., Benková E., Benjamins R., Beeckman T., Luschnig C., and Friml J. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132 (2005) 4521-4531
90. Vieten A., Sauer M., Brewer P.B., and Friml J. Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 12 (2007) 160-168
91. Weijers D., Benková E., Jäger K.E., Schlereth A., Hamann T., Kientz M., Wilmoth J.C., Reed J.W., and Jürgens G. Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J. 24 (2005) 1874-1885
92. Whippo C.W., and Hangarter R.P. Phototropism: bending towards enlightenment. Plant Cell 18 (2006) 1110-1119
93. Wiśniewska J., Xu J., Seifertová D., Brewer P.B., Růžička K., Blilou I., Rouquié D., Benková E., Scheres B., and Friml J. Polar PIN localization directs auxin flow in plants. Science 312 (2006) 883
94. Woodward A.W., and Bartel B. Auxin: regulation, action, and interaction. Ann. Bot. (Lond.) 95 (2005) 707-735
95. Xu J., Hofhuis H., Heidstra R., Sauer M., Friml J., and Scheres B. A molecular framework for plant regeneration. Science 311 (2006) 385-388
96. Yang Y., Hammes U.Z., Taylor C.G., Schachtman D.P., and Nielsen E. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16 (2006) 1123-1127
97. Yu R.C., Pesce C.G., Colman-Lerner A., Lok L., Pincus D., Serra E., Holl M., Benjamin K., Gordon A., and Brent R. Negative feedback that improves information transmission in yeast signalling. Nature 456 (2008) 755-761
98. Zhao Y., Christensen S.K., Fankhauser X., Cashman J.R., Cohen J.D., Weigel D., and Chory J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291 (2001) 306-309