Abstract
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.
Data availability
All data are presented in this manuscript and Supplementary Information. Raw data of RNA-seq have been deposited to Sequence Read Archive (SRA; https://www.ncbi.nlm.nih.gov/sra) under the accession number PRJNA1369304 with the referee access code or the clickable URL link (https://www.ncbi.nlm.nih.gov/sra/PRJNA1369304). Source data are provided with this paper.
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Acknowledgements
This work is supported by National Natural Science Foundation of China (32502807 to D.Z., 32573008 to B.G., 3227269 to B.G.), Taishan Scholars Program (tsqn202306139 to B.G.), China Postdoctoral Science Foundation (2024M761852 to D.Z.), Postdoctoral Fellowship Program of CPSF (GZC20252471 to D.Z.). We are grateful to Dr. Xueping Zhou (Chinese Academy of Agricultural Sciences) for providing the Turnip mosaic virus movement deficiency mutant.
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B.G. designed the study and wrote the manuscript. D.Z., X.L., T.X., Q.J., P.L., Q.S., C.L., H.L., L.Z., J.W., and B.G. performed the experiment and data analysis. H.L. and Y.G. carried out the tomato domestication analysis. T.L., T.Z., and X.Z. provided the materials and gave guidance.
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Zhao, D., Liu, X., Li, H. et al. Tomato antiviral ubiquitin-proteasome system recognizes viral 59 kDa protein to confer tomato chlorosis virus resistance. Nat Commun (2026). https://doi.org/10.1038/s41467-026-68832-3
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DOI: https://doi.org/10.1038/s41467-026-68832-3
