Tomato brown rugose fruit virus and pepino mosaic virus differentially modulate disease severity of bacterial pith necrosis and bacterial canker in tomato

Abstract

Tomato worldwide production is increasingly challenged by complex disease outbreaks involving multiple interacting pathogens. In Israel, recent years have seen a marked rise in vascular collapse symptoms in greenhouse-grown tomatoes, coinciding with the widespread emergence of tomato brown rugose fruit virus (ToBRFV) and pepino mosaic virus (PepMV). Here, we investigated the bacterial and viral agents associated with these outbreaks and examined how viral infection influences the development and severity of bacterial diseases that cause vascular collapse. Surveys conducted between 2021 and 2026 revealed that tomato pith necrosis outbreaks were associated with a diverse bacterial community dominated by members of the Pseudomonadales and Enterobacterales, while bacterial canker outbreaks were exclusively linked to Clavibacter michiganensis. Multilocus sequence analysis showed that pith necrosis-associated Pseudomonas isolates clustered primarily within the P. syringae, and P. corrugata phylogroups. Pathogenicity assays demonstrated that only a subset of pith necrosis-associated bacteria, P. mediterranea, P. capsici, P. viridiflava, and Xanthomonas euvesicatoria pv. perforans, induced pith necrosis under controlled conditions, with high variability in symptom severity. Co-inoculation experiments showed that ToBRFV- and PepMV-infected plants exhibited a 40-100% increase in lesion size following inoculation with pith necrosis-associated bacteria, without a corresponding increase in bacterial colonization, whereas the same viral infections attenuated wilt symptoms caused by C. michiganensis. Together, our findings demonstrate that endemic viral infections differentially modulate bacterial disease outcomes, either exacerbating or attenuating symptoms depending on the pathogen. These results highlight the importance of multi-pathogen interactions in disease severity and have important implications for tomato disease management.