Reciprocity between a retrograde signal and a putative metalloprotease reconfigures plastidial metabolic and structural states.

Abstract

Reconfiguration of the plastidial proteome in response to environmental cues is central to tailoring adaptive responses. To define the underlying mechanisms and consequences of these reconfigurations, we performed a suppressor screen, using a mutant (<i>ceh1</i>) accumulating high levels of a plastidial retrograde signaling metabolite, MEcPP. We isolated a revertant partially suppressing the dwarf stature and high salicylic acid of <i>ceh1</i> and identified the mutation in a putative plastidial metalloprotease (VIR3). Biochemical analyses showed increased VIR3 levels in <i>ceh1</i>, accompanied by reduced abundance of VIR3-target enzymes, ascorbate peroxidase, and glyceraldehyde 3-phophate dehydrogenase B. These proteomic shifts elicited increased H₂O₂, salicylic acid, and MEcPP levels, as well as stromule formation. High light recapitulated VIR3-associated reconfiguration of plastidial metabolic and structural states. These results establish a link between a plastidial stress-inducible retrograde signaling metabolite and a putative metalloprotease and reveal how the reciprocity between the two components modulates plastidial metabolic and structural states, shaping adaptive responses.