Local and terminal cell differentiation mediated by the jasmonic acid-mediated autophagy evokes petal abscission in Arabidopsis thaliana

Abstract In angiosperms, transition from floral organ maintenance to abscission determines plant reproductive success and seed dispersion. For petal abscission, local cell fate decision at petal cell base is more important than general senescence or cell death of petals at organ levels. However, how this decision is regulated in a spatiotemporal manner remains unclear. Here, we describe a jasmonic acid (JA)–regulated chromatin state change that directs the local cell fate determination via autophagy at the base of petals. During petal maintenance phase, transcriptional co-repressors of JA signaling accumulate at the base of petals to block MYC activity, leading to lower reactive oxygen species (ROS) levels. JA acts as an airborne signaling molecule transmitted from stamens to petals and accumulates primarily in petal bases to trigger epigenetic reprograming, allowing MYC transcription factors to interact with MEDIATOR25 and to increase chromatin accessibility for key downstream targets, such as Arabidopsis NAC DOMAIN-CONTAINING PROTEIN102 (ANAC102). ANAC102 specifically accumulates at the base of petals just prior to petal abscission and triggers local ROS accumulation and cell death via AUTOPHAGY-RELATED GENES induction. Notably, this ANAC102-triggered autophagy at the petal base causes maturation, vacuolar delivery, and breakdown of autophagosome for terminal cell differentiation. Because dynamic changes in the number of vesicles and cytoplasmic components in the vacuole are often seen in many plants, the local cell fate determination by autophagy may be conserved for petal abscission across angiosperms and may have been recruited under the JA/NAC module to pattern plant organ detachment systems.