Plants have several means of registering and adapting to stress. While many stress-responsive pathways in plants involve organellar functions, little is known about the role of organelle perturbation in reprogramming for stress. Our system of study is MSH1, a plant-specific, nuclear gene that encodes a dual-targeting protein. MSH1 is spatially regulated, functional in both mitochondrial and plastid genome stability, and accumulates in a specialized plastid type. Perturbation of this plastid is accompanied by both organellar and epigenetic responses that are programmed and conserved across species. Investigating the networks regulating this coordinated organellar-epigenomic response appears to be relevant not only to understanding trans-generational stress adaptation, but also growth enhancement behavior akin to heterosis.