The chloroplast translocon subunit TOC33 relays singlet oxygen-induced chloroplast-to-nucleus retrograde signaling in Arabidopsis

In the fluEX1 sof1, all 1O2-induced stress responses are largely suppressed, despite 1O2 levels being similar to those in the fluEX1. SOF1 encodes the chloroplast outer envelope-anchored preprotein import receptor TOC33. While TOC33 loss does not affect EX1 import, abundance, localization, and 1O2-induced proteolysis in the chloroplast, it blocks 1O2-induced chloroplast-to-nucleus retrograde signaling.

TOC33 interacts with the UVR domain of EX1 (EX1-UVR) in the chloroplast envelope, facilitating 1O2-induced decrease of the chloroplast EX1-UVR and increase of the nucleus EX1-UVR. Moreover, ectopic expression of EX1-UVR outside of the chloroplast bypasses the restrictive barrier imposed by the chloroplast envelope, activating 1O2 signaling and inducing stress responses. Our findings demonstrate that SOF1/TOC33 mediates 1O2-EX1 signaling from the chloroplast to the nucleus and that the EX1-UVR domain can substitute for full-length EX1 in this signaling pathway.