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Sugarcane mosaic virus (SCMV) is a pathogen of worldwide importance that causes dwarf mosaic disease on maize (Zea mays). Until now, few maize genes/proteins have been shown to be involved in resistance to SCMV. In this study, we characterized the role of maize phenylalanine ammonia-lyases (ZmPALs) in accumulation of the defence signal salicylic acid (SA) and in resistance to virus infection. SCMV infection significantly increased SA accumulation and expression of SA-responsive pathogenesis-related protein genes (PRs). Interestingly, exogenous SA treatment decreased SCMV accumulation and enhanced resistance. Both reverse transcription-coupled quantitative PCR and RNA-Seq data confirmed that expression levels of at least four ZmPAL genes were significantly up-regulated upon SCMV infection. Knockdown of ZmPAL expression led to enhanced SCMV infection symptom severity and virus multiplication, and simultaneously resulted in decreased SA accumulation and PR gene expression. Intriguingly, application of exogenous SA to SCMV-infected ZmPAL-silenced maize plants decreased SCMV accumulation, showing that ZmPALs are required for SA-mediated resistance to SCMV infection. In addition, lignin measurements and metabolomic analysis showed that ZmPALs are also involved in SCMV-induced lignin accumulation and synthesis of other secondary metabolites via the phenylpropanoid pathway. In summary, our results indicate that ZmPALs are required for SA accumulation in maize and are involved in resistance to virus infection by limiting virus accumulation and moderating symptom severity.

Pathogens disturb alternative splicing patterns of infected eukaryotic hosts. However, in plants it is not known 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 Zea mays phytoene synthase 1 (ZmPSY1), which encodes the key regulatory enzyme in carotenoid biosynthesis, we found although SCMV infection decreases total ZmPSY1 transcript accumulation, the proportion of splice variant T001 increases by later infection stages so that ZmPSY1 protein levels are maintained. We determined that ZmPSY1 has two leaf-specific transcripts, T001 and T003, distinguished by differences between the respective 3ʹ-untranslated regions (UTRs). The shorter 3ʹ-UTR of T001 makes it the more efficient mRNA. Nonsense ZmPSY1 mutants or virus-induced silencing of ZmPSY1 expression suppressed SCMV accumulation, attenuated symptoms, and decreased chloroplast damage. Thus, ZmPSY1 acts as a pro-viral host factor 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., This work was supported by grants from Ministry of Agriculture and Rural Affairs of China (2016ZX08010-001, 2018YFD020062), the National Natural Science Foundation of China (Grants 31371912, 31871930), and the Chinese Universities Scientific Fund (2019TC064) and a grant from the Ministry of Education of China (the 111 Project B13006). Work on SCMV by AMM and JPC is funded by BBSRC-Global Challenges Research Fund-Connected Grant BB/R005397/1.