Genetic and cytological evidence that heterocyst patterning is regulated by inhibitor gradients that promote activator decay

Date
2009-11
Authors
Risser, Douglas D.
Callahan, Sean M.
Journal Title
Journal ISSN
Volume Title
Publisher
Proceedings of the National Academy of Sciences of the United States of America
Abstract
The formation of a pattern of differentiated cells from a group of seemingly equivalent, undifferentiated cells is a central paradigm of developmental biology. Several species of filamentous cyanobacteria differentiate nitrogen-fixing heterocysts at regular intervals along unbranched filaments to form a periodic pattern of two distinct cell types. This patterning has been used to exemplify application of the activator-inhibitor model to periodic patterns in biology. The activator-inhibitor model proposes that activators and inhibitors of differentiation diffuse from source cells to form concentration gradients that in turn mediate patterning, but direct visualization of concentration gradients of activators and inhibitors has been difficult. Here we show that the periodic pattern of heterocysts produced by cyanobacteria relies on two inhibitors of heterocyst differentiation, PatS and HetN, in a manner consistent with the predictions of the activator-inhibitor model. Concentration gradients of the activator, HetR, were observed adjacent to heterocysts, the natural source of PatS and HetN, as well as adjacent to vegetative cells that were manipulated to overexpress a gene encoding either of the inhibitors. Gradients of HetR relied on posttranslational decay of HetR. Deletion of both patS and hetN genes prevented the formation of gradients of HetR, and a derivative of the inhibitors was shown to promote decay of HetR in a concentration-dependent manner. Our results provide strong support for application of the activator-inhibitor model to heterocyst patterning and, more generally, the formation of periodic patterns in biological systems.
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Keywords
activator-inhibitor, Anabaena, development
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