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 329 (5997): 1306-1311

Copyright © 2010 by the American Association for the Advancement of Science

Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching

Miguel A. Moreno-Risueno,1 Jaimie M. Van Norman,1 Antonio Moreno,2 Jingyuan Zhang,1 Sebastian E. Ahnert,3 Philip N. Benfey1,*

Abstract: Plants and animals produce modular developmental units in a periodic fashion. In plants, lateral roots form as repeating units along the root primary axis; however, the developmental mechanism regulating this process is unknown. We found that cyclic expression pulses of a reporter gene mark the position of future lateral roots by establishing prebranch sites and that prebranch site production and root bending are periodic. Microarray and promoter-luciferase studies revealed two sets of genes oscillating in opposite phases at the root tip. Genetic studies show that some oscillating transcriptional regulators are required for periodicity in one or both developmental processes. This molecular mechanism has characteristics that resemble molecular clock–driven activities in animal species.

1 Department of Biology and Institute for Genome Sciences and Policy Center for Systems Biology, Duke University, Durham, NC 27708, USA.
2 Departamento de Acustica Ambiental, Instituto de Acustica, Consejo Superior de Investigaciones Cientificas, Serrano 144, Madrid 28006, Spain.
3 Theory of Condensed Matter Group, Cavendish Laboratory, University of Cambridge, Cambridge CB3 0HE, UK.

* To whom correspondence should be addressed. E-mail: philip.benfey{at}duke.edu

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 »
PFRU, a single dominant locus regulates the balance between sexual and asexual plant reproduction in cultivated strawberry.
A. Gaston, J. Perrotte, E. Lerceteau-Kohler, M. Rousseau-Gueutin, A. Petit, M. Hernould, C. Rothan, and B. Denoyes (2013)
J. Exp. Bot.
   Abstract »    Full Text »    PDF »
Interacting Glutamate Receptor-Like Proteins in Phloem Regulate Lateral Root Initiation in Arabidopsis.
E. D. Vincill, A. E. Clarin, J. N. Molenda, and E. P. Spalding (2013)
PLANT CELL 25, 1304-1313
   Abstract »    Full Text »    PDF »
Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence.
R. P. Kumpf, C.-L. Shi, A. Larrieu, I. M. Sto, M. A. Butenko, B. Peret, E. S. Riiser, M. J. Bennett, and R. B. Aalen (2013)
PNAS 110, 5235-5240
   Abstract »    Full Text »    PDF »
Rooting plant development.
B. Scheres (2013)
Development 140, 939-941
   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 »
Endodermal ABA Signaling Promotes Lateral Root Quiescence during Salt Stress in Arabidopsis Seedlings.
L. Duan, D. Dietrich, C. H. Ng, P. M. Y. Chan, R. Bhalerao, M. J. Bennett, and J. R. Dinneny (2013)
PLANT CELL 25, 324-341
   Abstract »    Full Text »    PDF »
Natural Variation in Small Molecule-Induced TIR-NB-LRR Signaling Induces Root Growth Arrest via EDS1- and PAD4-Complexed R Protein VICTR in Arabidopsis.
T.-H. Kim, H.-H. Kunz, S. Bhattacharjee, F. Hauser, J. Park, C. Engineer, A. Liu, T. Ha, J. E. Parker, W. Gassmann, et al. (2012)
PLANT CELL 24, 5177-5192
   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 »
Spatiotemporal Regulation of Lateral Root Organogenesis in Arabidopsis by Cytokinin.
A. Bielach, K. Podlesakova, P. Marhavy, J. Duclercq, C. Cuesta, B. Muller, W. Grunewald, P. Tarkowski, and E. Benkova (2012)
PLANT CELL 24, 3967-3981
   Abstract »    Full Text »    PDF »
Modeling Regulatory Networks to Understand Plant Development: Small Is Beautiful.
A. M. Middleton, E. Farcot, M. R. Owen, and T. Vernoux (2012)
PLANT CELL 24, 3876-3891
   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 »
Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies.
C. Smaczniak, R. G. H. Immink, G. C. Angenent, and K. Kaufmann (2012)
Development 139, 3081-3098
   Abstract »    Full Text »    PDF »
Ontogeny of the Maize Shoot Apical Meristem.
E. M. Takacs, J. Li, C. Du, L. Ponnala, D. Janick-Buckner, J. Yu, G. J. Muehlbauer, P. S. Schnable, M. C. P. Timmermans, Q. Sun, et al. (2012)
PLANT CELL 24, 3219-3234
   Abstract »    Full Text »    PDF »
Genetic approach towards the identification of auxin-cytokinin crosstalk components involved in root development.
A. Bielach, J. Duclercq, P. Marhavy, and E. Benkova (2012)
Phil Trans R Soc B 367, 1469-1478
   Abstract »    Full Text »    PDF »
Phloem-associated auxin response maxima determine radial positioning of lateral roots in maize.
L. Jansen, I. Roberts, R. De Rycke, and T. Beeckman (2012)
Phil Trans R Soc B 367, 1525-1533
   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 »
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 »
Analyzing Lateral Root Development: How to Move Forward.
I. De Smet, P. J. White, A. G. Bengough, L. Dupuy, B. Parizot, I. Casimiro, R. Heidstra, M. Laskowski, M. Lepetit, F. Hochholdinger, et al. (2012)
PLANT CELL 24, 15-20
   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 »
Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers.
D. R. Lewis, S. Negi, P. Sukumar, and G. K. Muday (2011)
Development 138, 3485-3495
   Abstract »    Full Text »    PDF »
Transcription Dynamics in Plant Immunity.
J. W. Moore, G. J. Loake, and S. H. Spoel (2011)
PLANT CELL 23, 2809-2820
   Abstract »    Full Text »    PDF »
Evolutionary plasticity of segmentation clock networks.
A. J. Krol, D. Roellig, M.-L. Dequeant, O. Tassy, E. Glynn, G. Hattem, A. Mushegian, A. C. Oates, and O. Pourquie (2011)
Development 138, 2783-2792
   Abstract »    Full Text »    PDF »
Three-Dimensional Root Phenotyping with a Novel Imaging and Software Platform.
R. T. Clark, R. B. MacCurdy, J. K. Jung, J. E. Shaff, S. R. McCouch, D. J. Aneshansley, and L. V. Kochian (2011)
Plant Physiology 156, 455-465
   Abstract »    Full Text »    PDF »
Brassinosteroid perception in the epidermis controls root meristem size.
Y. Hacham, N. Holland, C. Butterfield, S. Ubeda-Tomas, M. J. Bennett, J. Chory, and S. Savaldi-Goldstein (2011)
Development 138, 839-848
   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 »
The Arabidopsis D-Type Cyclin CYCD2;1 and the Inhibitor ICK2/KRP2 Modulate Auxin-Induced Lateral Root Formation.
L. Sanz, W. Dewitte, C. Forzani, F. Patell, J. Nieuwland, B. Wen, P. Quelhas, S. De Jager, C. Titmus, A. Campilho, et al. (2011)
PLANT CELL 23, 641-660
   Abstract »    Full Text »    PDF »
Oscillating Roots.
J. Traas and T. Vernoux (2010)
Science 329, 1290-1291
   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