Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 29 October 2004:
Vol. 306. no. 5697, pp. 862 - 865
DOI: 10.1126/science.1100618
Prev | Table of Contents | Next

Reports

A PINOID-Dependent Binary Switch in Apical-Basal PIN Polar Targeting Directs Auxin Efflux

Jirí Friml,1 Xiong Yang,2,3 Marta Michniewicz,1 Dolf Weijers,1,2 Ab Quint,2 Olaf Tietz,4 René Benjamins,2,6 Pieter B. F. Ouwerkerk,2 Karin Ljung,5 Göran Sandberg,5 Paul J. J. Hooykaas,2 Klaus Palme,4 Remko Offringa2*

Polar transport–dependent local accumulation of auxin provides positional cues for multiple plant patterning processes. This directional auxin flow depends on the polar subcellular localization of the PIN auxin efflux regulators. Overexpression of the PINOID protein kinase induces a basal-to-apical shift in PIN localization, resulting in the loss of auxin gradients and strong defects in embryo and seedling roots. Conversely, pid loss of function induces an apical-to-basal shift in PIN1 polar targeting at the inflorescence apex, accompanied by defective organogenesis. Our results show that a PINOID-dependent binary switch controls PIN polarity and mediates changes in auxin flow to create local gradients for patterning processes.

1 Developmental Genetics, Center for Molecular Biology of Plants, University Tübingen, Auf der Morgenstelle 3, D-72076 Tübingen, Germany.
2 Developmental Genetics, Institute of Biology, Leiden University, Clusius Laboratory, Wassenaarseweg 64, 2333 AL Leiden, Netherlands.
3 College of Life Sciences, Peking University, Beijing 100871, China.
4 Albert-Ludwigs-Universität, Biologie II, Schaenzlestrasse 1, D-79104 Freiburg, Germany.
5 Umeå Plant Science Center, Department of Forest and Plant Physiology, Swedish University of Agricultural Sciences, S 901 83 Umeå, Sweden.
6 Institute of Applied Genetics and Cell Biology, BOKU–University of Natural Resources and Applied Life Sciences, Muthgasse 8, A-1190 Vienna, Austria.

* To whom correspondence should be addressed. E-mail: offringa{at}rulbim.leidenuniv.nl

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Genome-Wide Analysis Revealed the Complex Regulatory Network of Brassinosteroid Effects in Photomorphogenesis.
L. Song, X.-Y. Zhou, L. Li, L.-J. Xue, X. Yang, and H.-W. Xue (2009)
Mol Plant
   Abstract »    Full Text »    PDF »
PINOID Kinase Regulates Root Gravitropism through Modulation of PIN2-Dependent Basipetal Auxin Transport in Arabidopsis.
P. Sukumar, K. S. Edwards, A. Rahman, A. DeLong, and G. K. Muday (2009)
Plant Physiology 150, 722-735
   Abstract »    Full Text »    PDF »
A gain-of-function mutation in IAA18 alters Arabidopsis embryonic apical patterning.
S. E. Ploense, M.-F. Wu, P. Nagpal, and J. W. Reed (2009)
Development 136, 1509-1517
   Abstract »    Full Text »    PDF »
Meristematic sculpting in fruit development.
T. Girin, K. Sorefan, and L. Ostergaard (2009)
J. Exp. Bot. 60, 1493-1502
   Abstract »    Full Text »    PDF »
Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition.
B. Titapiwatanakun and A. S. Murphy (2009)
J. Exp. Bot. 60, 1093-1107
   Abstract »    Full Text »    PDF »
BARREN INFLORESCENCE2 Interaction with ZmPIN1a Suggests a Role in Auxin Transport During Maize Inflorescence Development.
A. Skirpan, A. H. Culler, A. Gallavotti, D. Jackson, J. D. Cohen, and P. McSteen (2009)
Plant Cell Physiol. 50, 652-657
   Abstract »    Full Text »    PDF »
The ESCRT-Related CHMP1A and B Proteins Mediate Multivesicular Body Sorting of Auxin Carriers in Arabidopsis and Are Required for Plant Development.
C. Spitzer, F. C. Reyes, R. Buono, M. K. Sliwinski, T. J. Haas, and M. S. Otegui (2009)
PLANT CELL 21, 749-766
   Abstract »    Full Text »    PDF »
The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana.
M. Zourelidou, I. Muller, B. C. Willige, C. Nill, Y. Jikumaru, H. Li, and C. Schwechheimer (2009)
Development 136, 627-636
   Abstract »    Full Text »    PDF »
Tobacco Arp3 is localized to actin-nucleating sites in vivo.
J. Maisch, J. Fiserova, L. Fischer, and P. Nick (2009)
J. Exp. Bot. 60, 603-614
   Abstract »    Full Text »    PDF »
Developmental disaster1: A novel mutation causing defects during vegetative and inflorescence development in maize (Zea mays, Poaceae).
K. A. Phillips, A. L. Skirpan, N. J. Kaplinsky, and P. McSteen (2009)
Am. J. Botany 96, 420-430
   Abstract »    Full Text »    PDF »
Thigmomorphogenesis: a complex plant response to mechano-stimulation.
E. W. Chehab, E. Eich, and J. Braam (2009)
J. Exp. Bot. 60, 43-56
   Abstract »    Full Text »    PDF »
Hormonal Regulation of Branching in Grasses.
P. McSteen (2009)
Plant Physiology 149, 46-55
   Full Text »    PDF »
Mechanical induction of lateral root initiation in Arabidopsis thaliana.
F. A. Ditengou, W. D. Teale, P. Kochersperger, K. A. Flittner, I. Kneuper, E. van der Graaff, H. Nziengui, F. Pinosa, X. Li, R. Nitschke, et al. (2008)
PNAS 105, 18818-18823
   Abstract »    Full Text »    PDF »
Cell Polarity Signaling: Focus on Polar Auxin Transport.
X. Gao, S. Nagawa, G. Wang, and Z. Yang (2008)
Mol Plant
   Abstract »    Full Text »    PDF »
Flavonoids Redirect PIN-mediated Polar Auxin Fluxes during Root Gravitropic Responses.
D. Santelia, S. Henrichs, V. Vincenzetti, M. Sauer, L. Bigler, M. Klein, A. Bailly, Y. Lee, J. Friml, M. Geisler, et al. (2008)
J. Biol. Chem. 283, 31218-31226
   Abstract »    Full Text »    PDF »
Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development.
J. Mravec, M. Kubes, A. Bielach, V. Gaykova, J. Petrasek, P. Skupa, S. Chand, E. Benkova, E. Zazimalova, and J. Friml (2008)
Development 135, 3345-3354
   Abstract »    Full Text »    PDF »
Multiple MONOPTEROS-Dependent Pathways Are Involved in Leaf Initiation.
M. Schuetz, T. Berleth, and J. Mattsson (2008)
Plant Physiology 148, 870-880
   Abstract »    Full Text »    PDF »
sparse inflorescence1 encodes a monocot-specific YUCCA-like gene required for vegetative and reproductive development in maize.
A. Gallavotti, S. Barazesh, S. Malcomber, D. Hall, D. Jackson, R. J. Schmidt, and P. McSteen (2008)
PNAS 105, 15196-15201
   Abstract »    Full Text »    PDF »
PIN Polar Targeting.
E. Feraru and J. Friml (2008)
Plant Physiology 147, 1553-1559
   Full Text »    PDF »
The Relationship between Auxin Transport and Maize Branching.
A. Gallavotti, Y. Yang, R. J. Schmidt, and D. Jackson (2008)
Plant Physiology 147, 1913-1923
   Abstract »    Full Text »    PDF »
Hormone interactions and regulation of PsPK2::GUS compared with DR5::GUS and PID::GUS in Arabidopsis thaliana.
F. Bai and D. A. DeMason (2008)
Am. J. Botany 95, 133-145
   Abstract »    Full Text »    PDF »
Determinate Root Growth and Meristem Maintenance in Angiosperms.
S. Shishkova, T. L. Rost, and J. G. Dubrovsky (2008)
Ann. Bot. 101, 319-340
   Abstract »    Full Text »    PDF »
P-Glycoprotein4 Displays Auxin Efflux Transporter-Like Action in Arabidopsis Root Hair Cells and Tobacco Cells.
M. Cho, S. H. Lee, and H.-T. Cho (2007)
PLANT CELL 19, 3930-3943
   Abstract »    Full Text »    PDF »
NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis.
Y. Cheng, G. Qin, X. Dai, and Y. Zhao (2007)
PNAS 104, 18825-18829
   Abstract »    Full Text »    PDF »
The role of auxin transport during inflorescence development in maize (Zea mays, Poaceae).
X. Wu and P. McSteen (2007)
Am. J. Botany 94, 1745-1755
   Abstract »    Full Text »    PDF »
The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level.
M. Furutani, T. Kajiwara, T. Kato, B. S. Treml, C. Stockum, R. A. Torres-Ruiz, and M. Tasaka (2007)
Development 134, 3849-3859
   Abstract »    Full Text »    PDF »
yucca6, a Dominant Mutation in Arabidopsis, Affects Auxin Accumulation and Auxin-Related Phenotypes.
J. I. Kim, A. Sharkhuu, J. B. Jin, P. Li, J. C. Jeong, D. Baek, S. Y. Lee, J. J. Blakeslee, A. S. Murphy, H. J. Bohnert, et al. (2007)
Plant Physiology 145, 722-735
   Abstract »    Full Text »    PDF »
RTE1 Is a Golgi-Associated and ETR1-Dependent Negative Regulator of Ethylene Responses.
X. Zhou, Q. Liu, F. Xie, and C.-K. Wen (2007)
Plant Physiology 145, 75-86
   Abstract »    Full Text »    PDF »
barren inflorescence2 Encodes a Co-Ortholog of the PINOID Serine/Threonine Kinase and Is Required for Organogenesis during Inflorescence and Vegetative Development in Maize.
P. McSteen, S. Malcomber, A. Skirpan, C. Lunde, X. Wu, E. Kellogg, and S. Hake (2007)
Plant Physiology 144, 1000-1011
   Abstract »    Full Text »    PDF »
The AP2 transcription factors DORNROSCHEN and DORNROSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA.
J. W. Chandler, M. Cole, A. Flier, B. Grewe, and W. Werr (2007)
Development 134, 1653-1662
   Abstract »    Full Text »    PDF »
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.
H. Muto, M. K. Watahiki, D. Nakamoto, M. Kinjo, and K. T. Yamamoto (2007)
Plant Physiology 144, 187-196
   Abstract »    Full Text »    PDF »
Flowering and determinacy in maize.
E. Bortiri and S. Hake (2007)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Characterization of OsPID, the Rice Ortholog of PINOID, and its Possible Involvement in the Control of Polar Auxin Transport.
Y. Morita and J. Kyozuka (2007)
Plant Cell Physiol. 48, 540-549
   Abstract »    Full Text »    PDF »
KANADI and Class III HD-Zip Gene Families Regulate Embryo Patterning and Modulate Auxin Flow during Embryogenesis in Arabidopsis.
A. Izhaki and J. L. Bowman (2007)
PLANT CELL 19, 495-508
   Abstract »    Full Text »    PDF »
Interactions among PIN-FORMED and P-Glycoprotein Auxin Transporters in Arabidopsis.
J. J. Blakeslee, A. Bandyopadhyay, O. R. Lee, J. Mravec, B. Titapiwatanakun, M. Sauer, S. N. Makam, Y. Cheng, R. Bouchard, J. Adamec, et al. (2007)
PLANT CELL 19, 131-147
   Abstract »    Full Text »    PDF »
Flavonoid Accumulation in Arabidopsis Repressed in Lignin Synthesis Affects Auxin Transport and Plant Growth.
S. Besseau, L. Hoffmann, P. Geoffroy, C. Lapierre, B. Pollet, and M. Legrand (2007)
PLANT CELL 19, 148-162
   Abstract »    Full Text »    PDF »
Arabidopsis PLD{zeta}2 Regulates Vesicle Trafficking and Is Required for Auxin Response.
G. Li and H.-W. Xue (2007)
PLANT CELL 19, 281-295
   Abstract »    Full Text »    PDF »
Structural and Functional Insights into the Regulation of Arabidopsis AGC VIIIa Kinases.
H. Zegzouti, W. Li, T. C. Lorenz, M. Xie, C. T. Payne, K. Smith, S. Glenny, G. S. Payne, and S. K. Christensen (2006)
J. Biol. Chem. 281, 35520-35530
   Abstract »    Full Text »    PDF »
Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity..
M. Sauer, J. Balla, C. Luschnig, J. Wisniewska, V. Reinohl, J. Friml, and E. Benkova (2006)
Genes & Dev. 20, 2902-2911
   Abstract »    Full Text »    PDF »
Down-Regulation of the 26S Proteasome Subunit RPN9 Inhibits Viral Systemic Transport and Alters Plant Vascular Development.
H. Jin, S. Li, and A. Villegas Jr. (2006)
Plant Physiology 142, 651-661
   Abstract »    Full Text »    PDF »
ZmPIN1a and ZmPIN1b Encode Two Novel Putative Candidates for Polar Auxin Transport and Plant Architecture Determination of Maize.
N. Carraro, C. Forestan, S. Canova, J. Traas, and S. Varotto (2006)
Plant Physiology 142, 254-264
   Abstract »    Full Text »    PDF »
RCN1-Regulated Phosphatase Activity and EIN2 Modulate Hypocotyl Gravitropism by a Mechanism That Does Not Require Ethylene Signaling.
G. K. Muday, S. R. Brady, C. Argueso, J. Deruere, J. J. Kieber, and A. DeLong (2006)
Plant Physiology 141, 1617-1629
   Abstract »    Full Text »    PDF »
Hormone Interactions and Regulation of Unifoliata, PsPK2, PsPIN1 and LE Gene Expression in Pea (Pisum sativum) Shoot Tips.
F. Bai and D. A. DeMason (2006)
Plant Cell Physiol. 47, 935-948
   Abstract »    Full Text »    PDF »
PINOID Positively Regulates Auxin Efflux in Arabidopsis Root Hair Cells and Tobacco Cells.
S. H. Lee and H.-T. Cho (2006)
PLANT CELL 18, 1604-1616
   Abstract »    Full Text »    PDF »
Differential Roles of Arabidopsis Heterotrimeric G-Protein Subunits in Modulating Cell Division in Roots.
J.-G. Chen, Y. Gao, and A. M. Jones (2006)
Plant Physiology 141, 887-897
   Abstract »    Full Text »    PDF »
Meristems in the movies: live imaging as a tool for decoding intercellular signaling in shoot apical meristems..
F. E. Tax and A. Durbak (2006)
PLANT CELL 18, 1331-1337
   Full Text »    PDF »
SCARFACE Encodes an ARF-GAP That Is Required for Normal Auxin Efflux and Vein Patterning in Arabidopsis.
L. E. Sieburth, G. K. Muday, E. J. King, G. Benton, S. Kim, K. E. Metcalf, L. Meyers, E. Seamen, and J. M. Van Norman (2006)
PLANT CELL 18, 1396-1411
   Abstract »    Full Text »    PDF »
Role of Cytokinin and Auxin in Shaping Root Architecture: Regulating Vascular Differentiation, Lateral Root Initiation, Root Apical Dominance and Root Gravitropism.
R. ALONI, E. ALONI, M. LANGHANS, and C. I. ULLRICH (2006)
Ann. Bot. 97, 883-893
   Abstract »    Full Text »    PDF »
Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis.
H. Zegzouti, R. G. Anthony, N. Jahchan, L. Bogre, and S. K. Christensen (2006)
PNAS 103, 6404-6409
   Abstract »    Full Text »    PDF »
Polar auxin transport and patterning: grow with the flow.
B. Scheres and J. Xu (2006)
Genes & Dev. 20, 922-926
   Full Text »    PDF »
The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins.
Y. Boutte, M.-T. Crosnier, N. Carraro, J. Traas, and B. Satiat-Jeunemaitre (2006)
J. Cell Sci. 119, 1255-1265
   Abstract »    Full Text »    PDF »
DNA Methylation Is Critical for Arabidopsis Embryogenesis and Seed Viability.
W. Xiao, K. D. Custard, R. C. Brown, B. E. Lemmon, J. J. Harada, R. B. Goldberg, and R. L. Fischer (2006)
PLANT CELL 18, 805-814
   Abstract »    Full Text »    PDF »
Ethylene Modulates Flavonoid Accumulation and Gravitropic Responses in Roots of Arabidopsis.
C. S. Buer, P. Sukumar, and G. K. Muday (2006)
Plant Physiology 140, 1384-1396
   Abstract »    Full Text »    PDF »
ramosa2 Encodes a LATERAL ORGAN BOUNDARY Domain Protein That Determines the Fate of Stem Cells in Branch Meristems of Maize.
E. Bortiri, G. Chuck, E. Vollbrecht, T. Rocheford, R. Martienssen, and S. Hake (2006)
PLANT CELL 18, 574-585
   Abstract »    Full Text »    PDF »
Increased Expression of MAP KINASE KINASE7 Causes Deficiency in Polar Auxin Transport and Leads to Plant Architectural Abnormality in Arabidopsis.
Y. Dai, H. Wang, B. Li, J. Huang, X. Liu, Y. Zhou, Z. Mou, and J. Li (2006)
PLANT CELL 18, 308-320
   Abstract »    Full Text »    PDF »
A Molecular Framework for Plant Regeneration.
J. Xu, H. Hofhuis, R. Heidstra, M. Sauer, J. Friml, and B. Scheres (2006)
Science 311, 385-388
   Abstract »    Full Text »    PDF »
Interactions between the Cell Cycle and Embryonic Patterning in Arabidopsis Uncovered by a Mutation in DNA Polymerase {varepsilon}.
P. D. Jenik, R. E.J. Jurkuta, and M. K. Barton (2005)
PLANT CELL 17, 3362-3377
   Abstract »    Full Text »    PDF »
The Arabidopsis STV1 Protein, Responsible for Translation Reinitiation, Is Required for Auxin-Mediated Gynoecium Patterning.
T. Nishimura, T. Wada, K. T. Yamamoto, and K. Okada (2005)
PLANT CELL 17, 2940-2953
   Abstract »    Full Text »    PDF »
Cell Cycle Progression in the Pericycle Is Not Sufficient for SOLITARY ROOT/IAA14-Mediated Lateral Root Initiation in Arabidopsis thaliana.
S. Vanneste, B. De Rybel, G. T.S. Beemster, K. Ljung, I. De Smet, G. Van Isterdael, M. Naudts, R. Iida, W. Gruissem, M. Tasaka, et al. (2005)
PLANT CELL 17, 3035-3050
   Abstract »    Full Text »    PDF »
The rib1 Mutant of Arabidopsis Has Alterations in Indole-3-Butyric Acid Transport, Hypocotyl Elongation, and Root Architecture.
J. Poupart, A. M. Rashotte, G. K. Muday, and C. S. Waddell (2005)
Plant Physiology 139, 1460-1471
   Abstract »    Full Text »    PDF »
Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression.
A. Vieten, S. Vanneste, J. Wisniewska, E. Benkova, R. Benjamins, T. Beeckman, C. Luschnig, and J. Friml (2005)
Development 132, 4521-4531
   Abstract »    Full Text »    PDF »
Cell-to-Cell Movement of Green Fluorescent Protein Reveals Post-Phloem Transport in the Outer Integument and Identifies Symplastic Domains in Arabidopsis Seeds and Embryos.
R. Stadler, C. Lauterbach, and N. Sauer (2005)
Plant Physiology 139, 701-712
   Abstract »    Full Text »    PDF »
The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo.
B. S. Treml, S. Winderl, R. Radykewicz, M. Herz, G. Schweizer, P. Hutzler, E. Glawischnig, and R. A. T. Ruiz (2005)
Development 132, 4063-4074
   Abstract »    Full Text »    PDF »
Surge and destroy: the role of auxin in plant embryogenesis.
P. D. Jenik and M. K. Barton (2005)
Development 132, 3577-3585
   Abstract »    Full Text »    PDF »
Auxin: Regulation, Action, and Interaction.
A. W. WOODWARD and B. BARTEL (2005)
Ann. Bot. 95, 707-735
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)