Tomato antiviral ubiquitin-proteasome system recognizes viral 59 kDa protein to confer tomato chlorosis virus resistance

Viral diseases critically impact crop yields, necessitating insights into plant-pathogen recognition and resistance. In tomato (Solanum lycopersicum), tomato chlorosis virus (ToCV) employs 59 kDa protein (p59) to facilitate movement and degrade the host Catalase1 (SlCAT1), disrupting redox homeostasis. Importantly, tomato has evolved an antiviral ubiquitin-proteasome system (UPS) featuring the Antiviral E2 ubiquitin-conjugating enzyme (SlAVE2) and Antiviral E3 ubiquitin ligase (SlAVE3) pair, which specifically recognizes p59 to trigger antiviral defenses. During infection, this system ubiquitinates SlWRKY6, alleviating its repression of SlAVE3 and creating a positive feedback loop that enhances SlAVE3 expression. SlAVE3 then targets p59 for ubiquitination and degradation, inhibiting viral spread. Notably, p59 co-opts this UPS to degrade SlCAT1, illustrating a counter-defense interplay. Domestication analysis reveals selection of AVE3 from S. pimpinellifolium to S. lycopersicum, with SpAVE3 conferring stronger ToCV resistance than SlAVE3 through improved p59 targeting and reduced SlCAT1 degradation. This study unveils a domesticated antiviral UPS, providing a foundation for breeding ToCV-resistant tomatoes. This study deciphers an arms race between the infected tomato plant that deploys a ubiquitin-proteasome system to target the viral pathogenic protein, p59. To counter, p59 hijacks the host system to degrade the defence protein SlCAT1 benefitting the virus.