Integrated transcriptomics, proteomics, and metabolomics analyses reveal key regulatory pathways related to the development of viral symptoms in tomato plants

Abstract Background Viral infections of tomato plants present a significant threat to tomato production and yield. Mixed viral infections are common in field-grown tomatoes and are known to exacerbate disease symptoms; however, the molecular mechanisms affecting symptom severity remain poorly understood. This study used integrated omics analyses to identify tissue-specific molecular pathways associated with severe and mild disease symptoms in tomato plants naturally co-infected with multiple viruses. Results Our analyses revealed multiple pathways that were differentially expressed in tomato plants in response to viral disease. Among them, the phenylpropanoid biosynthesis enrichment pathway (ko00940) is associated with leaf symptoms, stem growth, and fruit-set rate, and is a key enrichment pathway in the development of viral disease symptoms in tomato plants. In addition, molecules of the porphyrin metabolism enrichment pathway (ko00860) were highly expressed in mature tomato leaf tissues with mild viral disease, which corresponded to better leaf development. qRT-PCR showed that expression of key genes in the phenylpropanoid biosynthesis and the porphyrin metabolism enrichment pathways differed among tissue types of tomato plants with severe and mild viral disease, and the trend was consistent with the transcriptome results. Weighted gene co-expression network analysis revealed that differentially expressed genes across three aggregation modules were significantly correlated with the severity of tomato viral disease symptoms. Conventional virus detection assays confirmed mixed infections with tomato leaf curl New Delhi virus, tomato chlorosis virus, and tomato mosaic virus in tomato plants exhibiting viral symptoms. Conclusions We present a multi-tissue, multi-omics systems view of mixed viral infections in a field setting, which provides a valuable reference for screening and exploring key regulatory molecular functions and mechanisms underlying the development of viral disease symptoms.