Probing the actin-auxin oscillator

Abstract

The directional transport of the plant hormone auxin depends on transcellular gradients of auxin-efflux carriers that continuously cycle between plasma membrane and intracellular compartments. This cycling has been proposed to depend on actin filaments. However, the role of actin for the polarity of auxin transport has been disputed. To get insight into this question, actin bundling was induced by overexpression of the actin-binding domain of talin in tobacco BY-2 cells and in rice plants. This bundling can be reverted by addition of auxins, which allows to address the role of actin organization on the flux of auxin. In both systems, the reversion of a normal actin configuration can be restored by addition of exogenous auxins and this fully restores the respective auxin-dependent functions. These findings lead to a model of a self-referring regulatory circuit between polar auxin transport and actin organization. To further dissect the actin-auxin oscillator, we used photoactivated release of caged auxin in tobacco cells to demonstrate that auxin gradients can be manipulated at a subcellular level.

Figure 1

Model of the actin-auxin oscillator. In the absence of auxin, actin is organized in bundles that do not support the localization of auxin-efflux carriers in the plasma membrane, such that these carriers are clustered inside the cell. Upon addition of IAA or NAA (but not 2,4-D that is perceived by a different receptor), these bundles detach into fine actin strands that efficiently support the polar localization of the auxin-efflux carriers. The altered auxin efflux will transiently reduce the intracellular concentration of auxin (which will be later compensated by auxin drainage from neighboring cells) such that actin returns to a more bundled configuration. This will again affect the localization and thus the activity of efflux-carriers such that intracellular auxin concentration increases again. Since the cycling of transporters is a rapid process, the frequency of the oscillator is mainly determined by the velocity of actin reorganization (in the range of around 20 min).