Petal abscission is promoted by jasmonic acid-induced autophagy at Arabidopsis petal bases

Yuki Furuta, Haruka Yamamoto, Takeshi Hirakawa, Akira Uemura, Margaret Anne Pelayo, Hideaki Iimura, Naoya Katagiri, Noriko Takeda-Kamiya, Kie Kumaishi, Makoto Shirakawa, Sumie Ishiguro, Yasunori Ichihashi, Takamasa Suzuki, Tatsuaki Goh, Kiminori Toyooka, Toshiro Ito, Nobutoshi Yamaguchi

Abstract

In angiosperms, the transition from floral-organ maintenance to abscission determines reproductive success and seed dispersion. For petal abscission, cell-fate decisions specifically at the petal-cell base are more important than organ-level senescence or cell death in petals. However, how this transition is regulated remains unclear. Here, we identify a jasmonic acid (JA)-regulated chromatin-state switch at the base of Arabidopsis petals that directs local cell-fate determination via autophagy. During petal maintenance, co-repressors of JA signaling accumulate at the base of petals to block MYC activity, leading to lower levels of ROS. JA acts as an airborne signaling molecule transmitted from stamens to petals, accumulating primarily in petal bases to trigger chromatin remodeling. This allows MYC transcription factors to promote chromatin accessibility for downstream targets, including NAC DOMAIN-CONTAINING PROTEIN102 (ANAC102). ANAC102 accumulates specifically at the petal base prior to abscission and triggers ROS accumulation and cell death via AUTOPHAGY-RELATED GENEs induction. Developmentally induced autophagy at the petal base causes maturation, vacuolar delivery, and breakdown of autophagosomes for terminal cell differentiation. Dynamic changes in vesicles and cytoplasmic components in the vacuole occur in many plants, suggesting JA–NAC-mediated local cell-fate determination by autophagy may be conserved in angiosperms.