The RhMPK3-RhLOB41-RhWRKY9 module orchestrates ethylene-induced petal abscission via dual control of ROS homeostasis in rose.

Abstract

Organ abscission represents a critical adaptive strategy for plant survival, yet the post-translational mechanisms ensuring its irreversible remain poorly understood. Here, we unveil a signaling module, MITOGEN-ACTIVATED PROTEIN KINASE 3 (RhMPK3)-LATERAL ORGAN BOUNDARIES DOMAIN 41 (RhLOB41)-WRKY DNA-BINDING PROTEIN 9 (RhWRKY9), that gates ethylene-induced petal abscission in rose (<i>Rosa hybrida</i>) by orchestrating reactive oxygen species (ROS) homeostasis. We demonstrate that the transcription factor RhWRKY9 acts as a dual-function regulator, concurrently activating ROS production via activation of <i>RESPIRATORY BURST OXIDASE HOMOLOGUE D</i> (<i>RhRBOHD</i>) and suppressing scavenging via repression of <i>CATALASE 2</i> (<i>RhCAT2</i>), thereby generating a ROS burst that locks abscission progression. Ethylene primes this process by destabilizing RhLOB41, a transcriptional repressor of <i>RhWRKY9</i>, through RhMPK3-mediated phosphorylation at Ser30. Phosphorylation creates a phosphodegron that targets RhLOB41 for autophagy-dependent degradation. Our findings redefine ROS as decisive executors of abscission and establish bidirectional ROS control as a paradigm for irreversible developmental transitions.