Viral Perturbation of Alternative Splicing of a Host Transcript Benefits Infection

• Published in: Plant physiology (Bethesda) 2020-11, Vol.184 (3), p.1514-1531
• Main Authors: Du, Kaitong, Jiang, Tong, Chen, Hui, Murphy, Alex M, Carr, John P, Du, Zhiyou, Li, Xiangdong, Fan, Zaifeng, Zhou, Tao
• Format: Article
• Language: English
• Subjects: Alternative Splicing; Crops, Agricultural - genetics; Crops, Agricultural - virology; Gene Expression Regulation, Plant; Genetic Variation; Genome, Viral; Genotype; Host-Pathogen Interactions; Mutation; Plant Diseases - genetics; Plant Diseases - virology; Potyvirus - genetics; Potyvirus - physiology; Transcription Factors - genetics; Zea mays - genetics; Zea mays - virology
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.20.00903

Pathogens disturb alternative splicing patterns of infected eukaryotic hosts. However, in plants it is unknown if this is incidental to infection or represents a pathogen-induced remodeling of host gene expression needed to support infection. Here, we compared changes in transcription and protein accumulation with changes in transcript splicing patterns in maize ( ) infected with the globally important pathogen sugarcane mosaic virus (SCMV). Our results suggested that changes in alternative splicing play a major role in determining virus-induced proteomic changes. Focusing on maize ( ), which encodes the key regulatory enzyme in carotenoid biosynthesis, we found that although SCMV infection decreases total transcript accumulation, the proportion of splice variant T001 increases by later infection stages so that ZmPSY1 protein levels are maintained. We determined that has two leaf-specific transcripts, T001 and T003, distinguished by differences between the respective 3'-untranslated regions (UTRs). The shorter 3'-UTR of T001 makes it the more efficient mRNA. Nonsense mutants or virus-induced silencing of expression suppressed SCMV accumulation, attenuated symptoms, and decreased chloroplast damage. Thus, ZmPSY1 acts as a proviral host factor that is required for virus accumulation and pathogenesis. Taken together, our findings reveal that SCMV infection-modulated alternative splicing ensures that ZmPSY1 synthesis is sustained during infection, which supports efficient virus infection.