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.
Subscribe

Logo for

Science 319 (5868): 1384-1386

Copyright © 2008 by the American Association for the Advancement of Science

TOPLESS Mediates Auxin-Dependent Transcriptional Repression During Arabidopsis Embryogenesis

Heidi Szemenyei,1,2 Mike Hannon,1,2 Jeff A. Long1*

Abstract: The transcriptional response to auxin is critical for root and vascular development during Arabidopsis embryogenesis. Auxin induces the degradation of AUXIN/INDOLE-3-ACETIC ACID (AUX/IAA) transcriptional repressors, freeing their binding partners, the AUXIN RESPONSE FACTOR (ARF) proteins, which can activate transcription of auxin response genes. We show that TOPLESS (TPL) can physically interact with IAA12/BODENLOS (IAA12/BDL) through an ETHYLENE RESPONSE FACTOR (ERF)–associated amphiphilic repression (EAR) motif. TPL can repress transcription in vivo and is required for IAA12/BDL repressive activity. In addition, tpl-1 can suppress the patterning defects of the bdl-1 mutant. Direct interaction between TPL and ARF5/MONOPTEROS, which is regulated by IAA12/BDL, results in a loss-of-function arf5/mp phenotype. These observations show that TPL is a transcriptional co-repressor and further our understanding of how auxin regulates transcription during plant development.

1 Plant Biology Laboratory, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
2 Division of Biological Sciences, Section of Cell and Developmental Biology, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093, USA.

* To whom correspondence should be addressed. E-mail: long{at}salk.edu

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Mutations in the TIR1 Auxin Receptor That Increase Affinity for Auxin/Indole-3-Acetic Acid Proteins Result in Auxin Hypersensitivity.
H. Yu, B. L. Moss, S. S. Jang, M. Prigge, E. Klavins, J. L. Nemhauser, and M. Estelle (2013)
Plant Physiology 162, 295-303
   Abstract »    Full Text »    PDF »
Tuning the auxin transcriptional response.
E. Pierre-Jerome, B. L. Moss, and J. L. Nemhauser (2013)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
The TIE1 Transcriptional Repressor Links TCP Transcription Factors with TOPLESS/TOPLESS-RELATED Corepressors and Modulates Leaf Development in Arabidopsis.
Q. Tao, D. Guo, B. Wei, F. Zhang, C. Pang, H. Jiang, J. Zhang, T. Wei, H. Gu, L.-J. Qu, et al. (2013)
PLANT CELL 25, 421-437
   Abstract »    Full Text »    PDF »
Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription.
L. Wang, J. Kim, and D. E. Somers (2013)
PNAS 110, 761-766
   Abstract »    Full Text »    PDF »
Evolution of the ARF Gene Family in Land Plants: Old Domains, New Tricks.
C. Finet, A. Berne-Dedieu, C. P. Scutt, and F. Marletaz (2013)
Mol. Biol. Evol. 30, 45-56
   Abstract »    Full Text »    PDF »
Defence on demand: mechanisms behind optimal defence patterns.
S. Meldau, M. Erb, and I. T. Baldwin (2012)
Ann. Bot. 110, 1503-1514
   Abstract »    Full Text »    PDF »
APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19.
N. T. Krogan, K. Hogan, and J. A. Long (2012)
Development 139, 4180-4190
   Abstract »    Full Text »    PDF »
Systems Analysis of Shoot Apical Meristem Growth and Development: Integrating Hormonal and Mechanical Signaling.
J. A. H. Murray, A. Jones, C. Godin, and J. Traas (2012)
PLANT CELL 24, 3907-3919
   Abstract »    Full Text »    PDF »
Auxin and Epigenetic Regulation of SKP2B, an F-Box That Represses Lateral Root Formation.
C. Manzano, E. Ramirez-Parra, I. Casimiro, S. Otero, B. Desvoyes, B. De Rybel, T. Beeckman, P. Casero, C. Gutierrez, and J. C. del Pozo (2012)
Plant Physiology 160, 749-762
   Abstract »    Full Text »    PDF »
Phenotypes Associated with Down-Regulation of Sl-IAA27 Support Functional Diversity Among Aux/IAA Family Members in Tomato.
C. Bassa, I. Mila, M. Bouzayen, and C. Audran-Delalande (2012)
Plant Cell Physiol. 53, 1583-1595
   Abstract »    Full Text »    PDF »
Ubiquitin-Mediated Control of Plant Hormone Signaling.
D. R. Kelley and M. Estelle (2012)
Plant Physiology 160, 47-55
   Full Text »    PDF »
Stable establishment of cotyledon identity during embryogenesis in Arabidopsis by ANGUSTIFOLIA3 and HANABA TARANU.
M. Kanei, G. Horiguchi, and H. Tsukaya (2012)
Development 139, 2436-2446
   Abstract »    Full Text »    PDF »
The Arabidopsis Mediator Subunit MED25 Differentially Regulates Jasmonate and Abscisic Acid Signaling through Interacting with the MYC2 and ABI5 Transcription Factors.
R. Chen, H. Jiang, L. Li, Q. Zhai, L. Qi, W. Zhou, X. Liu, H. Li, W. Zheng, J. Sun, et al. (2012)
PLANT CELL 24, 2898-2916
   Abstract »    Full Text »    PDF »
The Interaction and Integration of Auxin Signaling Components.
K.-i. Hayashi (2012)
Plant Cell Physiol. 53, 965-975
   Abstract »    Full Text »    PDF »
Genome-Wide Identification, Functional Analysis and Expression Profiling of the Aux/IAA Gene Family in Tomato.
C. Audran-Delalande, C. Bassa, I. Mila, F. Regad, M. Zouine, and M. Bouzayen (2012)
Plant Cell Physiol. 53, 659-672
   Abstract »    Full Text »    PDF »
ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis.
D. R. Kelley, A. Arreola, T. L. Gallagher, and C. S. Gasser (2012)
Development 139, 1105-1109
   Abstract »    Full Text »    PDF »
JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis.
C. Shyu, P. Figueroa, C. L. DePew, T. F. Cooke, L. B. Sheard, J. E. Moreno, L. Katsir, N. Zheng, J. Browse, and G. A. Howe (2012)
PLANT CELL 24, 536-550
   Abstract »    Full Text »    PDF »
SPT6L Encoding a Putative WG/GW-Repeat Protein Regulates Apical-Basal Polarity of Embryo in Arabidopsis.
X.-L. Gu, H. Wang, H. Huang, and X.-F. Cui (2012)
Mol Plant 5, 249-259
   Abstract »    Full Text »    PDF »
Bipartite Promoter Element Required for Auxin Response.
C. L. Walcher and J. L. Nemhauser (2012)
Plant Physiology 158, 273-282
   Abstract »    Full Text »    PDF »
The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis.
B. Causier, M. Ashworth, W. Guo, and B. Davies (2012)
Plant Physiology 158, 423-438
   Abstract »    Full Text »    PDF »
A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development.
J. J. Ripoll, A. H. K. Roeder, G. S. Ditta, and M. F. Yanofsky (2011)
Development 138, 5167-5176
   Abstract »    Full Text »    PDF »
POPCORN Functions in the Auxin Pathway to Regulate Embryonic Body Plan and Meristem Organization in Arabidopsis.
D. Xiang, H. Yang, P. Venglat, Y. Cao, R. Wen, M. Ren, S. Stone, E. Wang, H. Wang, W. Xiao, et al. (2011)
PLANT CELL 23, 4348-4367
   Abstract »    Full Text »    PDF »
Stress-Responsive Mitogen-Activated Protein Kinases Interact with the EAR Motif of a Poplar Zinc Finger Protein and Mediate Its Degradation through the 26S Proteasome.
L.-P. Hamel, M. Benchabane, M.-C. Nicole, I. T. Major, M.-J. Morency, G. Pelletier, N. Beaudoin, J. Sheen, and A. Seguin (2011)
Plant Physiology 157, 1379-1393
   Abstract »    Full Text »    PDF »
Chromatin Configuration as a Battlefield in Plant-Bacteria Interactions.
K.-W. Ma, C. Flores, and W. Ma (2011)
Plant Physiology 157, 535-543
   Full Text »    PDF »
Arabidopsis Cys2/His2 Zinc-Finger Proteins AZF1 and AZF2 Negatively Regulate Abscisic Acid-Repressive and Auxin-Inducible Genes under Abiotic Stress Conditions.
K.-S. Kodaira, F. Qin, L.-S. P. Tran, K. Maruyama, S. Kidokoro, Y. Fujita, K. Shinozaki, and K. Yamaguchi-Shinozaki (2011)
Plant Physiology 157, 742-756
   Abstract »    Full Text »    PDF »
The Basic Helix-Loop-Helix Transcription Factor MYC2 Directly Represses PLETHORA Expression during Jasmonate-Mediated Modulation of the Root Stem Cell Niche in Arabidopsis.
Q. Chen, J. Sun, Q. Zhai, W. Zhou, L. Qi, L. Xu, B. Wang, R. Chen, H. Jiang, J. Qi, et al. (2011)
PLANT CELL 23, 3335-3352
   Abstract »    Full Text »    PDF »
RopGEF7 Regulates PLETHORA-Dependent Maintenance of the Root Stem Cell Niche in Arabidopsis.
M. Chen, H. Liu, J. Kong, Y. Yang, N. Zhang, R. Li, J. Yue, J. Huang, C. Li, A. Y. Cheung, et al. (2011)
PLANT CELL 23, 2880-2894
   Abstract »    Full Text »    PDF »
Taking the very first steps: from polarity to axial domains in the early Arabidopsis embryo.
S. Jeong, M. Bayer, and W. Lukowitz (2011)
J. Exp. Bot. 62, 1687-1697
   Abstract »    Full Text »    PDF »
Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis.
Y. Niu, P. Figueroa, and J. Browse (2011)
J. Exp. Bot. 62, 2143-2154
   Abstract »    Full Text »    PDF »
Identical Amino Acid Substitutions in the Repression Domain of Auxin/Indole-3-Acetic Acid Proteins Have Contrasting Effects on Auxin Signaling.
H. Li, S. B. Tiwari, G. Hagen, and T. J. Guilfoyle (2011)
Plant Physiology 155, 1252-1263
   Abstract »    Full Text »    PDF »
Context, Specificity, and Self-Organization in Auxin Response.
M. Del Bianco and S. Kepinski (2011)
Cold Spring Harb Perspect Biol 3, a001578
   Abstract »    Full Text »    PDF »
Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity.
R. Carranco, J. M. Espinosa, P. Prieto-Dapena, C. Almoguera, and J. Jordano (2010)
PNAS 107, 21908-21913
   Abstract »    Full Text »    PDF »
Ubiquitin Ligase-Coupled Receptors Extend Their Reach to Jasmonate.
G. A. Howe (2010)
Plant Physiology 154, 471-474
   Full Text »    PDF »
Odyssey of Auxin.
S. Abel and A. Theologis (2010)
Cold Spring Harb Perspect Biol 2, a004572
   Abstract »    Full Text »    PDF »
Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis.
M. J. Miller, G. A. Barrett-Wilt, Z. Hua, and R. D. Vierstra (2010)
PNAS 107, 16512-16517
   Abstract »    Full Text »    PDF »
The control of axillary meristem fate in the maize ramosa pathway.
A. Gallavotti, J. A. Long, S. Stanfield, X. Yang, D. Jackson, E. Vollbrecht, and R. J. Schmidt (2010)
Development 137, 2849-2856
   Abstract »    Full Text »    PDF »
Functional analysis of the structural domain of ARF proteins in rice (Oryza sativa L.).
C. Shen, S. Wang, Y. Bai, Y. Wu, S. Zhang, M. Chen, T. J. Guilfoyle, P. Wu, and Y. Qi (2010)
J. Exp. Bot. 61, 3971-3981
   Abstract »    Full Text »    PDF »
Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor.
Z. Zhu, F. Xu, Y. Zhang, Y. T. Cheng, M. Wiermer, X. Li, and Y. Zhang (2010)
PNAS 107, 13960-13965
   Abstract »    Full Text »    PDF »
Auxin Perception--Structural Insights.
L. I. Calderon-Villalobos, X. Tan, N. Zheng, and M. Estelle (2010)
Cold Spring Harb Perspect Biol 2, a005546
   Abstract »    Full Text »    PDF »
Putative Arabidopsis Transcriptional Adaptor Protein (PROPORZ1) is required to modulate histone acetylation in response to auxin.
J. M. Anzola, T. Sieberer, M. Ortbauer, H. Butt, B. Korbei, I. Weinhofer, A. E. Mullner, and C. Luschnig (2010)
PNAS 107, 10308-10313
   Abstract »    Full Text »    PDF »
Auxin Control of Root Development.
P. Overvoorde, H. Fukaki, and T. Beeckman (2010)
Cold Spring Harb Perspect Biol 2, a001537
   Abstract »    Full Text »    PDF »
MGOUN1 Encodes an Arabidopsis Type IB DNA Topoisomerase Required in Stem Cell Regulation and to Maintain Developmentally Regulated Gene Silencing.
P. Graf, A. Dolzblasz, T. Wurschum, M. Lenhard, U. Pfreundt, and T. Laux (2010)
PLANT CELL 22, 716-728
   Abstract »    Full Text »    PDF »
Genome-Wide Analysis of Ethylene-Responsive Element Binding Factor-Associated Amphiphilic Repression Motif-Containing Transcriptional Regulators in Arabidopsis.
S. Kagale, M. G. Links, and K. Rozwadowski (2010)
Plant Physiology 152, 1109-1134
   Abstract »    Full Text »    PDF »
Complex regulation of the TIR1/AFB family of auxin receptors.
G. Parry, L. I. Calderon-Villalobos, M. Prigge, B. Peret, S. Dharmasiri, H. Itoh, E. Lechner, W. M. Gray, M. Bennett, and M. Estelle (2009)
PNAS 106, 22540-22545
   Abstract »    Full Text »    PDF »
Auxin Control of Embryo Patterning.
B. Moller and D. Weijers (2009)
Cold Spring Harb Perspect Biol 1, a001545
   Abstract »    Full Text »    PDF »
Genome-wide analysis of the auxin-responsive transcriptome downstream of iaa1 and its expression analysis reveal the diversity and complexity of auxin-regulated gene expression.
D. J. Lee, J. W. Park, H. W. Lee, and J. Kim (2009)
J. Exp. Bot. 60, 3935-3957
   Abstract »    Full Text »    PDF »
Partitioning the Apical Domain of the Arabidopsis Embryo Requires the BOBBER1 NudC Domain Protein.
R. J. Jurkuta, N. J. Kaplinsky, J. E. Spindel, and M. K. Barton (2009)
PLANT CELL 21, 1957-1971
   Abstract »    Full Text »    PDF »
Functional Analysis of Transcription Factors in Arabidopsis.
N. Mitsuda and M. Ohme-Takagi (2009)
Plant Cell Physiol. 50, 1232-1248
   Abstract »    Full Text »    PDF »
DORNROSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo.
M. Cole, J. Chandler, D. Weijers, B. Jacobs, P. Comelli, and W. Werr (2009)
Development 136, 1643-1651
   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 »
Members of the GCN5 Histone Acetyltransferase Complex Regulate PLETHORA-Mediated Root Stem Cell Niche Maintenance and Transit Amplifying Cell Proliferation in Arabidopsis.
N. Kornet and B. Scheres (2009)
PLANT CELL 21, 1070-1079
   Abstract »    Full Text »    PDF »
COP9 Signalosome- and 26S Proteasome-dependent Regulation of SCFTIR1 Accumulation in Arabidopsis.
J. Stuttmann, E. Lechner, R. Guerois, J. E. Parker, L. Nussaume, P. Genschik, and L. D. Noel (2009)
J. Biol. Chem. 284, 7920-7930
   Abstract »    Full Text »    PDF »
Constitutive Repression and Activation of Auxin Signaling in Arabidopsis.
H. Li, Y. Cheng, A. Murphy, G. Hagen, and T. J. Guilfoyle (2009)
Plant Physiology 149, 1277-1288
   Abstract »    Full Text »    PDF »
The paramutated SULFUREA locus of tomato is involved in auxin biosynthesis.
B. Ehlert, M. A. Schottler, G. Tischendorf, J. Ludwig-Muller, and R. Bock (2008)
J. Exp. Bot. 59, 3635-3647
   Abstract »    Full Text »    PDF »
Cotyledon organogenesis.
J. W. Chandler (2008)
J. Exp. Bot. 59, 2917-2931
   Abstract »    Full Text »    PDF »
The Evolving Complexity of the Auxin Pathway.
S. Lau, G. Jurgens, and I. De Smet (2008)
PLANT CELL 20, 1738-1746
   Full Text »    PDF »
LEUNIG_HOMOLOG and LEUNIG Perform Partially Redundant Functions during Arabidopsis Embryo and Floral Development.
J. Sitaraman, M. Bui, and Z. Liu (2008)
Plant Physiology 147, 672-681
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882