Location: Plant Gene Expression CenterTitle: A mutually assured destruction mechanism attentuates light signaling in Arabidopsis) Author
Submitted to: Science
Publication Type: Peer reviewed journal
Publication Acceptance Date: 5/20/2014
Publication Date: 6/6/2014
Citation: Quail, P.H., Ni, W., Xu, S., Tepperman, J.M., Stanley, D.J., Maltby, D.A., Gross, J.D., Burlingame, A.L., Wang, Z. 2014. A mutually assured destruction mechanism attentuates light signaling in Arabidopsis. Science. 344:1160-1164. Interpretive Summary: Using plants’ responses to light, this paper identifies a new mechanism of signaling-attenuation. Signaling-attenuation is a way cells and organisms guard against potentially harmful over-reaction to the external cues that enable them to adapt to prevailing conditions. Attenuation of signaling is analogous to the brakes on a car. While acceleration is desirable, acceleration without restraint can be disastrous. This research describes the discovery of a nuclear-localized, bimolecular signaling configuration where the accelerator is directly linked to the braking mechanism, thereby providing simultaneous acceleration and controlled restraint of the plant’s adaptational response to the light signal. Light-signaling in Arabidopsis involves the binding of an activated photoreceptor molecule (called phytochrome (phyB)) to a transcription factor (gene-switch) called PIF. This binding destroys PIF, switching off its target genes. However, it was found that in imposing PIF's destruction, phytochrome signs its own death warrant and is simultaneously executed, thus reducing the incoming light-signaling intensity. This bimolecular mutually assured destruction (MAD) mechanism of signaling attenuation appears to represent a new configuration, thus broadening our understanding of the range of mechanisms nature has evolved to enact this critical function, and providing molecular targets with potential agricultural importance. By engineering either phyB or its PIF-interactor, to reduce or enhance this MAD activity, it should be possible to reduce or enhance the plant’s sensitivity to the available light. Since phyB regulates both seedling establishment (critical to out-competing neighboring weeds) and the shade-avoidance response (which regulates the distribution of captured carbon between the sugars and starches of seeds and the cellulose of stems), manipulating the plant's inherent light-sensitivity profile could have impact on those agriculturally-important facets of crop growth (food/feed or cellulosic biofuel yields).
Technical Abstract: Following light-induced nuclear translocation, phytochrome photoreceptors interact with and induce rapid phosphorylation and degradation of bHLH transcription factors, such as PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), to regulate gene expression. Concomitantly this interaction triggers feedback reduction of phytochrome B (phyB) levels. Light-induced phosphorylation of PIF3 is necessary for the degradation of both proteins. We report that this PIF3 phosphorylation induces, and is necessary for, recruitment of LRB (Light-Response Bric-a-Brack/Tramtrack/Broad (BTB)) E3 ubiquitin ligases to the PIF3-phyB complex. The recruited LRBs promote concurrent polyubiqutination and degradation of both PIF3 and phyB in vivo. These data reveal a linked signal-transmission and attenuation mechanism involving mutually assured destruction of the receptor and its immediate signaling partner.