Plastid perturbations trigger epigenetic programs during environmental sensing in plants

Plants adapt to environmental changes by adjusting growth and defense, and the role of epigenetic modifications in this process remains unclear. Sensing and adjusting to environmental changes are more pronounced in certain tissues such as epidermis, vasculature, meristem, and reproductive tissues. These tissues possess sensory plastids that are enriched in stress response proteins. We investigated the effects of perturbation of four sensory plastid-localized proteins, MutS HOMOLOG 1 (MSH1), PsbP DOMAIN-CONTAINING PROTEIN 3 (PPD3), CAB UNDEREXPRESSED 1 (CUE1), and 3'(2'),5'-BISPHOSPHATE NUCLEOTIDASE 1 (SAL1), on the Arabidopsis (Arabidopsis thaliana) epigenome, detecting gene expression and DNA methylation changes within gene networks associated with environmental sensing. These effects significantly overlapped with a set of CHG hypermethylated genes identified within the chromatin remodeler mutant histone deacetylase 6 (hda6) at 12-hr daylength. At 16-hr daylength, hda6 lost this CHG hypermethylation in gene bodies, and the sensory plastid mutants showed milder adjustments in phenotype and methylation- and gene expression- associated gene networks. We detected daylength-responsive epistatic interaction between sensory plastid mutants with hda6. We also found that the hda6 mutation conferred daylength memory and, with msh1, enhanced tolerance to heat and biotic stresses. These results support a model of epigenetically programmed adjustments in plant phenotype triggered by sensory plastid-to-nucleus retrograde signaling in direct response to daylength and environmental cues.