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 322 (5901): 594-597

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

Receptor-Like Kinase ACR4 Restricts Formative Cell Divisions in the Arabidopsis Root

Ive De Smet,1,2,4* Valya Vassileva,1,2*{dagger} Bert De Rybel,1,2 Mitchell P. Levesque,3{ddagger} Wim Grunewald,1,2 Daniël Van Damme,1,2 Giel Van Noorden,1,2 Mirande Naudts,1,2 Gert Van Isterdael,1,2 Rebecca De Clercq,1,2 Jean Y. Wang,3 Nicholas Meuli,5 Steffen Vanneste,1,2 Jirí Friml,1,2 Pierre Hilson,1,2 Gerd Jürgens,4 Gwyneth C. Ingram,5 Dirk Inzé,1,2 Philip N. Benfey,3 Tom Beeckman1,2§

Abstract: During the development of multicellular organisms, organogenesis and pattern formation depend on formative divisions to specify and maintain pools of stem cells. In higher plants, these activities are essential to shape the final root architecture because the functioning of root apical meristems and the de novo formation of lateral roots entirely rely on it. We used transcript profiling on sorted pericycle cells undergoing lateral root initiation to identify the receptor-like kinase ACR4 of Arabidopsis as a key factor both in promoting formative cell divisions in the pericycle and in constraining the number of these divisions once organogenesis has been started. In the root tip meristem, ACR4 shows a similar action by controlling cell proliferation activity in the columella cell lineage. Thus, ACR4 function reveals a common mechanism of formative cell division control in the main root tip meristem and during lateral root initiation.

1 Department of Plant Systems Biology, Flanders Institute for Biotechnology (VIB), B-9052 Ghent, Belgium.
2 Department of Molecular Genetics, Ghent University, B-9052 Ghent, Belgium.
3 Department of Biology and Institute for Genome Sciences and Policy, Center for Systems Biology, Duke University, Box 90338, Durham, NC 27708, USA.
4 Center for Plant Molecular Biology (ZMBP), Auf der Morgenstelle 3, University of Tübingen, D-72076 Tübingen, Germany.
5 Institute of Molecular Plant Science, Rutherford Building, Kings Buildings, University of Edinburgh, Edinburgh, EH9 3JR, UK.

* These authors contributed equally to this work.

{dagger} Present address: Academik Metodi Popov Institute of Plant Physiology, Bulgarian Academy of Sciences, Academik Georgi Bonchev Street, Building 21, 1113 Sofia, Bulgaria.

{ddagger} Present address: Max Planck Institute for Developmental Biology, Department of Genetics and Genomics, Spemannstrasse 35/III, D-72076 Tübingen, Germany.

§ To whom correspondence should be addressed. E-mail: tom.beeckman{at}psb.ugent.be

THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Lateral root initiation is a probabilistic event whose frequency is set by fluctuating levels of auxin response.
M. Laskowski (2013)
J. Exp. Bot. 64, 2609-2617
   Abstract »    Full Text »    PDF »
Quantitative Phosphoproteomics after Auxin-stimulated Lateral Root Induction Identifies an SNX1 Protein Phosphorylation Site Required for Growth.
H. Zhang, H. Zhou, L. Berke, A. J. R. Heck, S. Mohammed, B. Scheres, and F. L. H. Menke (2013)
Mol. Cell. Proteomics 12, 1158-1169
   Abstract »    Full Text »    PDF »
Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3.
S. Depuydt, A. Rodriguez-Villalon, L. Santuari, C. Wyser-Rmili, L. Ragni, and C. S. Hardtke (2013)
PNAS 110, 7074-7079
   Abstract »    Full Text »    PDF »
Tissue-Specific Expression of SMALL AUXIN UP RNA41 Differentially Regulates Cell Expansion and Root Meristem Patterning in Arabidopsis.
Y. Kong, Y. Zhu, C. Gao, W. She, W. Lin, Y. Chen, N. Han, H. Bian, M. Zhu, and J. Wang (2013)
Plant Cell Physiol. 54, 609-621
   Abstract »    Full Text »    PDF »
Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues.
M. Lucas, K. Kenobi, D. von Wangenheim, U. Voss, K. Swarup, I. De Smet, D. Van Damme, T. Lawrence, B. Peret, E. Moscardi, et al. (2013)
PNAS 110, 5229-5234
   Abstract »    Full Text »    PDF »
Hormonal regulation of stem cell maintenance in roots.
Y. Lee, W. S. Lee, and S.-H. Kim (2013)
J. Exp. Bot. 64, 1153-1165
   Abstract »    Full Text »    PDF »
GNOM/FEWER ROOTS is Required for the Establishment of an Auxin Response Maximum for Arabidopsis Lateral Root Initiation.
K.-i. Okumura, T. Goh, K. Toyokura, H. Kasahara, Y. Takebayashi, T. Mimura, Y. Kamiya, and H. Fukaki (2013)
Plant Cell Physiol. 54, 406-417
   Abstract »    Full Text »    PDF »
Formative Cell Divisions: Principal Determinants of Plant Morphogenesis.
M. Smolarkiewicz and P. Dhonukshe (2013)
Plant Cell Physiol. 54, 333-342
   Abstract »    Full Text »    PDF »
Transcriptional and Functional Classification of the GOLVEN/ROOT GROWTH FACTOR/CLE-Like Signaling Peptides Reveals Their Role in Lateral Root and Hair Formation.
A. Fernandez, A. Drozdzecki, K. Hoogewijs, A. Nguyen, T. Beeckman, A. Madder, and P. Hilson (2013)
Plant Physiology 161, 954-970
   Abstract »    Full Text »    PDF »
Cell cycle regulates cell type in the Arabidopsis sepal.
A. H. K. Roeder, A. Cunha, C. K. Ohno, and E. M. Meyerowitz (2012)
Development 139, 4416-4427
   Abstract »    Full Text »    PDF »
Endocytic Trafficking towards the Vacuole Plays a Key Role in the Auxin Receptor SCFTIR-Independent Mechanism of Lateral Root Formation in A. thaliana.
P. Perez-Henriquez, N. V. Raikhel, and L. Norambuena (2012)
Mol Plant 5, 1195-1209
   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 »
Rapid Phosphoproteomic and Transcriptomic Changes in the Rhizobia-legume Symbiosis.
C. M. Rose, M. Venkateshwaran, J. D. Volkening, P. A. Grimsrud, J. Maeda, D. J. Bailey, K. Park, M. Howes-Podoll, D. den Os, L. H. Yeun, et al. (2012)
Mol. Cell. Proteomics 11, 724-744
   Abstract »    Full Text »    PDF »
Small Signaling Peptides in Arabidopsis Development: How Cells Communicate Over a Short Distance.
E. Murphy, S. Smith, and I. De Smet (2012)
PLANT CELL 24, 3198-3217
   Abstract »    Full Text »    PDF »
In silico analyses of pericycle cell populations reinforce their relation with associated vasculature in Arabidopsis.
B. Parizot, I. Roberts, J. Raes, T. Beeckman, and I. De Smet (2012)
Phil Trans R Soc B 367, 1479-1488
   Abstract »    Full Text »    PDF »
Root system architecture: insights from Arabidopsis and cereal crops.
S. Smith and I. De Smet (2012)
Phil Trans R Soc B 367, 1441-1452
   Abstract »    Full Text »    PDF »
Peptides and receptors controlling root development.
Y. Stahl and R. Simon (2012)
Phil Trans R Soc B 367, 1453-1460
   Abstract »    Full Text »    PDF »
Tackling Drought Stress: RECEPTOR-LIKE KINASES Present New Approaches.
A. Marshall, R. B. Aalen, D. Audenaert, T. Beeckman, M. R. Broadley, M. A. Butenko, A. I. Cano-Delgado, S. de Vries, T. Dresselhaus, G. Felix, et al. (2012)
PLANT CELL 24, 2262-2278
   Abstract »    Full Text »    PDF »
Plasma Membrane Calcium ATPases Are Important Components of Receptor-Mediated Signaling in Plant Immune Responses and Development.
N. Frei dit Frey, M. Mbengue, M. Kwaaitaal, L. Nitsch, D. Altenbach, H. Haweker, R. Lozano-Duran, M. F. Njo, T. Beeckman, B. Huettel, et al. (2012)
Plant Physiology 159, 798-809
   Abstract »    Full Text »    PDF »
The establishment of asymmetry in Arabidopsis lateral root founder cells is regulated by LBD16/ASL18 and related LBD/ASL proteins.
T. Goh, S. Joi, T. Mimura, and H. Fukaki (2012)
Development 139, 883-893
   Abstract »    Full Text »    PDF »
Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis.
W. Grunewald, I. De Smet, D. R. Lewis, C. Lofke, L. Jansen, G. Goeminne, R. Vanden Bossche, M. Karimi, B. De Rybel, B. Vanholme, et al. (2012)
PNAS 109, 1554-1559
   Abstract »    Full Text »    PDF »
CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis.
L. Meng, B. B. Buchanan, L. J. Feldman, and S. Luan (2012)
PNAS 109, 1760-1765
   Abstract »    Full Text »    PDF »
Quantitative Analysis of Lateral Root Development: Pitfalls and How to Avoid Them.
J. G. Dubrovsky and B. G. Forde (2012)
PLANT CELL 24, 4-14
   Abstract »    Full Text »    PDF »
The Arabidopsis RETARDED ROOT GROWTH Gene Encodes a Mitochondria-Localized Protein That Is Required for Cell Division in the Root Meristem.
X. Zhou, Q. Li, X. Chen, J. Liu, Q. Zhang, Y. Liu, K. Liu, and J. Xu (2011)
Plant Physiology 157, 1793-1804
   Abstract »    Full Text »    PDF »
Measuring cell identity in noisy biological systems.
K. D. Birnbaum and E. Kussell (2011)
Nucleic Acids Res. 39, 9093-9107
   Abstract »    Full Text »    PDF »
Auxin-Dependent Cell Cycle Reactivation through Transcriptional Regulation of Arabidopsis E2Fa by Lateral Organ Boundary Proteins.
B. Berckmans, V. Vassileva, S. P. C. Schmid, S. Maes, B. Parizot, S. Naramoto, Z. Magyar, C. L. A. Kamei, C. Koncz, L. Bogre, et al. (2011)
PLANT CELL 23, 3671-3683
   Abstract »    Full Text »    PDF »
Intercellular Communication during Plant Development.
J. M. Van Norman, N. W. Breakfield, and P. N. Benfey (2011)
PLANT CELL 23, 855-864
   Abstract »    Full Text »    PDF »
Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching.
M. A. Moreno-Risueno, J. M. Van Norman, A. Moreno, J. Zhang, S. E. Ahnert, and P. N. Benfey (2010)
Science 329, 1306-1311
   Abstract »    Full Text »    PDF »
Auxin regulates distal stem cell differentiation in Arabidopsis roots.
Z. Ding and J. Friml (2010)
PNAS 107, 12046-12051
   Abstract »    Full Text »    PDF »
VisuaLRTC: A New View on Lateral Root Initiation by Combining Specific Transcriptome Data Sets.
B. Parizot, B. De Rybel, and T. Beeckman (2010)
Plant Physiology 153, 34-40
   Abstract »    Full Text »    PDF »
Information processing without brains - the power of intercellular regulators in plants.
W. Busch and P. N. Benfey (2010)
Development 137, 1215-1226
   Abstract »    Full Text »    PDF »
The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division.
J. P. Etchells and S. R. Turner (2010)
Development 137, 767-774
   Abstract »    Full Text »    PDF »
Bimodular auxin response controls organogenesis in Arabidopsis.
I. De Smet, S. Lau, U. Voss, S. Vanneste, R. Benjamins, E. H. Rademacher, A. Schlereth, B. De Rybel, V. Vassileva, W. Grunewald, et al. (2010)
PNAS 107, 2705-2710
   Abstract »    Full Text »    PDF »
The MYB96 Transcription Factor Mediates Abscisic Acid Signaling during Drought Stress Response in Arabidopsis.
P. J. Seo, F. Xiang, M. Qiao, J.-Y. Park, Y. N. Lee, S.-G. Kim, Y.-H. Lee, W. J. Park, and C.-M. Park (2009)
Plant Physiology 151, 275-289
   Abstract »    Full Text »    PDF »
Identification of Nutrient-Responsive Arabidopsis and Rapeseed MicroRNAs by Comprehensive Real-Time Polymerase Chain Reaction Profiling and Small RNA Sequencing.
B. D. Pant, M. Musialak-Lange, P. Nuc, P. May, A. Buhtz, J. Kehr, D. Walther, and W.-R. Scheible (2009)
Plant Physiology 150, 1541-1555
   Abstract »    Full Text »    PDF »
The lateral root initiation index: an integrative measure of primordium formation.
J. G. Dubrovsky, A. Soukup, S. Napsucialy-Mendivil, Z. Jeknic, and M. G. Ivanchenko (2009)
Ann. Bot. 103, 807-817
   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