Journal Article

Cytokinin signalling inhibitory fields provide robustness to phyllotaxis

Bishopp, Anthony, Chambrier, Pierre, Thévenon, Emmanuel, Rozier, Frédérique, Refahi, Yassin, Lainé, Stéphanie, Marteaux, Benjamin, Guédon, Yann, Cellier, Coralie, Dumas, Renaud, Helariutta, Ykä, Legrand, Jonathan, Farcot, Etienne, Godin, Christophe, Traas, Jan, Brunoud, Géraldine, Parcy, François, Vernoux, Teva, Besnard, Fabrice, Boudaoud, Arezki, Morin, Valérie, Mirabet, Vincent, Das, Pradeep

2014

Overview

The regularly spaced arrangement of plant organs around the stem known as phyllotaxis depends on auxin-based inhibitory fields; this study identifies another hormone-based inhibitory field downstream of auxin which is generated by movement of the cytokinin signalling inhibitor ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6 and regulates the periodicity of organ production. A second hormone for plant stem organization The regular arrangement of organs around the stem in plants is known as phyllotaxis. Accumulation of the hormone auxin triggers organ initiation, and auxin depletion around organs generates inhibitory fields that were thought to be sufficient to maintain these patterns. In this study, Teva Vernoux and colleagues demonstrate that a second type of hormone-based field may be involved. They find that intercellular movement of the cytokinin inhibitor AHP6 in the shoot apex generates fields downstream of auxin that create spatial patterns of cytokinin signalling activity in the meristem, thus providing robustness to phyllotaxis. How biological systems generate reproducible patterns with high precision is a central question in science 1 . The shoot apical meristem (SAM), a specialized tissue producing plant aerial organs, is a developmental system of choice to address this question. Organs are periodically initiated at the SAM at specific spatial positions and this spatiotemporal pattern defines phyllotaxis. Accumulation of the plant hormone auxin triggers organ initiation 2 , 3 , 4 , 5 , whereas auxin depletion around organs generates inhibitory fields that are thought to be sufficient to maintain these patterns and their dynamics 4 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 . Here we show that another type of hormone-based inhibitory fields, generated directly downstream of auxin by intercellular movement of the cytokinin signalling inhibitor ARABIDOPSIS HISTIDINE PHOSPHOTRANSFER PROTEIN 6 (AHP6) 14 , is involved in regulating phyllotactic patterns. We demonstrate that AHP6-based fields establish patterns of cytokinin signalling in the meristem that contribute to the robustness of phyllotaxis by imposing a temporal sequence on organ initiation. Our findings indicate that not one but two distinct hormone-based fields may be required for achieving temporal precision during formation of reiterative structures at the SAM, thus indicating an original mechanism for providing robustness to a dynamic developmental system.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14/19 / 38/35 / 631/449/2653/2660 / 96/35 / Arabidopsis - anatomy & histology / Arabidopsis - cytology / Arabidopsis - growth & development / Arabidopsis - metabolism / Arabidopsis Proteins - metabolism / Binding sites / Biological Transport / Computer Science / Cytokinins / Cytokinins - antagonists & inhibitors / Cytokinins - metabolism / Humanities and Social Sciences / Indoleacetic Acids - metabolism / Legumes / letter / Meristem - metabolism / Microscopy / Modeling and Simulation / multidisciplinary / Mutation / Other / Phyllotaxis / Plant Growth Regulators - antagonists & inhibitors / Plant Growth Regulators - metabolism / Plant physiology / Plant Shoots - metabolism / Science / Signal Transduction