Hijacking the Plant Spliceosome: Alternative Splicing as a Driver of Viral Infection and Tomato Fruit Development

Abstract:

To cope with a constantly changing environment, plants fine-tune gene expression through multiple layers of regulation. Among these, alternative splicing (AS) has emerged as a crucial co- and posttranscriptional mechanism reshaping plant transcriptome and proteome in response to developmental and environmental cues. Although the plant spliceosome remains incompletely characterized, compelling evidence demonstrated its targeting by unrelated pathogens to promote infection. We discovered that tomato yellow leaf curl virus –which replicates in the host nucleus– usurps the plant spliceosome to splice its own transcripts, thereby expanding its limited coding capacity. We further uncover that functionally specialized isoforms required for viral infectivity are generated through AS.

Beyond plant-pathogen interactions, the regulation and functional relevance of AS in crop development remain largely unexplored.

Intriguingly, splicing factors of the serine/arginine-rich (SR) family, which drive spliceosome assembly onto pre-mRNAs, are highly expressed, yet with contrasting patterns, during tomato fruit development and ripening. We found that one SR factor, RS2Z35, may contribute to the regulation of the carbon flux towards specialized metabolite synthesis in ripe fruits, providing the first evidence that the spliceosome can directly influence fruit quality. In the future, we plan to dissect fruit-specific functions of AS in tomato, to get deeper insights into the intricate metabolic reprogramming that underpins reproductive growth.

Publications:

D.M. Pott, M. Gao, C. Shi, L. Wang, L. Medina-Puche, Z. Yagci, S.A. Acatay, J. Zhang, L. Gonzalo, C. Merchante, L. Gu, R. Lozano-Durán (2025) Pervasive splicing in a plant DNA virus. BioRxiv. DOI: 10.1101/2025.10.01.679800

L. Ge, F. Pan, M. Jia, D.M. Pott, H. He, H. Shan, R. Lozano-Durán, X. Zhou, F. Li (2025). RNA modifications in plant biotic interactions. Plant Communications 6, 101232. DOI: 10.1016/j.xplc.2024.101232.

D.M. Pott, S. Durán-Soria, J.W. Allwood, S. Pont, S.L. Gordon, N. Jennings, C. Austin, D. Stewart, R.M. Brennan, A. Masny, A. Sonsteby, E. Krüger, D. Jarret, J.G. Vallarino, B. Usadel, S. Osorio (2023) Dissecting the impact of environment, season and genotype on blackcurrant fruit quality traits. Food Chemistry 402, 134360. DOI: 10.1016/j.foodchem.2022.134360.