Abstract
Positional information is essential for coordinating the development of multicellular organisms. In plants, positional information provided by the hormone auxin regulates rhythmic organ production at the shoot apex, but the spatio-temporal dynamics of auxin gradients is unknown. We used quantitative imaging to demonstrate that auxin carries high-definition graded information not only in space but also in time. We show that, during organogenesis, temporal patterns of auxin arise from rhythmic centrifugal waves of high auxin travelling through the tissue faster than growth. We further demonstrate that temporal integration of auxin concentration is required to trigger the auxin-dependent transcription associated with organogenesis. This provides a mechanism to temporally differentiate sites of organ initiation and exemplifies how spatio-temporal positional information can be used to create rhythmicity.
Highlights
Specification of differentiation patterns in multicellular organisms is regulated by gradients of biochemical signals providing positional information to cells (Rogers and Schier, 2011; Wolpert, 1969)
We provide evidence that organ initiation in the shoot apical meristem (SAM) is dependent on temporal integration of the auxin signal
Our results suggest that a time integration mechanism is essential for rhythmic organ patterning in the SAM since auxin-based spatial information pre-specifies several sites of organ initiation and is unlikely to provide sufficient information (Video 1)
Summary
Specification of differentiation patterns in multicellular organisms is regulated by gradients of biochemical signals providing positional information to cells (Rogers and Schier, 2011; Wolpert, 1969). Plant shoots develop post-embryonically through rhythmic organ generation in the shoot apical meristem (SAM), a specialized tissue with a stem cell niche in its central zone (CZ; Figure 1A). SAM organ patterning or phyllotaxis has been extensively analyzed using mathematical models (Douady and Couder, 1996; Mitchison, 1977; Veen and Lindenmayer, 1977). A widely accepted model proposes that the time interval between organ initiations (the plastochron) and the spatial position of organ initiation emerge from the combined action of inhibitory fields emitted by pre-existing organs and the SAM center (Douady and Couder, 1996). Tissue growth self-organizes organ patterning by moving organs away from the stem cells and leaving space for new ones
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