Fine-tuning of MYC2-mediated Botrytis defense response by the LBD40/42-CRL3BPM4 module in tomato

Abstract Gray mold caused by the fungal pathogen Botrytis cinerea is a major disease of vegetable and fruit crops. This study elucidates mechanism that fine-tunes B. cinerea resistance mediated by the transcription factor SlMYC2 in tomato (Solanum lycopersicum), characterized by a dynamic balance between “active braking” and “brake release”. The Lateral Organ Boundaries Domain (LBD) transcription factor family members SlLBD40 and SlLBD42 repress transcription and form homodimers or heterodimers, with heterodimers demonstrating higher activity. SlLBD40 and SlLBD42 are transcriptionally up-regulated by SlMYC2, but SlLBD40 and SlLBD42 attenuate SlMYC2-orchestrated defenses against B. cinerea, thereby safeguarding the plant from immune over-activation. Moreover, the BTB/POZ-MATH (BPM) protein family member SlBPM4 targets and degrades SlLBD40 and SlLBD42, releasing the defense response and enhancing B. cinerea resistance. Genetic analyses demonstrated that SlLBD40 and SlLBD42 are epistatic to SlBPM4. Additionally, SlLBD40 and SlLBD42 play dual roles in fruit development and B. cinerea defense, and SlBPM4 functions as a protective factor under pathogen attack. Our study uncovered a MYC2-LBD40/42-CRL3BPM4 module in tomato that allocates growth and defense resources by finely regulating gene expression and balancing immune response activation levels. This module also provides potential targets for optimizing the balance between plant growth and defense through gene-editing technologies.