Sensory plastid-associated PsbP DOMAIN-CONTAINING PROTEIN 3 triggers plant growth- and defense-related epigenetic responses.

Sensory plastids are important in plant response to environmental changes. Previous studies show that MutS HOMOLOG 1 (MSH1) perturbation in sensory plastids induces heritable epigenetic phenotype adjustment. PsbP DOMAIN-CONTAINING PROTEIN 3 (PPD3), a protein of unknown function, was earlier postulated to be an interactor of MSH1. This study investigates the relationship of PPD3 to MSH1 and to plant environmental sensing. The ppd3 mutant displays a whole-plant phenotype variably altered in growth rate, flowering time, ROS modulation and response to salt, with effects on meristem growth. Present in both chloroplasts and sensory plastids, PPD3 co-localized with MSH1 in root tips but not in leaf tissues. Suppression or overexpression of PPD3 affected plant growth rate and stress tolerance, and led to a heritable, heterogenous memory state with both dwarfed and vigorous growth phenotypes. Gene expression and DNA methylome datasets from PPD3-OX and derived memory states showed enrichment in growth versus defense networks and meristem effects. Our results support a model of sensory plastid influence on nuclear epigenetic behavior and ppd3 as a second trigger, functioning within meristem plastids to recalibrate growth plasticity.