ZmSKI3 coordinates plant growth and immunity in maize

Disease resistance is often associated with compromised plant growth and yield due to defense-growth tradeoffs. However, key components and mechanisms underlying the defense-growth tradeoffs are rarely explored in maize. In this study, we find that ZmSKI3, a putative subunit of the SKI complex that mediates the 3-to-5 degradation of RNA, positively regulates plant development but negatively regulates disease resistance in maize. Dysfunction of either ZmSKI3 or its interacting protein ZmSKI2 leads to retarded kernel development and severe dwarfism. Intriguingly, the Zmski3 mutants show constitutively activated defense responses and enhanced resistance to Curvularia lunata. In contrast, the ZmSKI3 overexpression lines were more susceptible to C. lunata and B. maydis. Consistently, the biosynthesis of defense-associated phytohormones including salicylic acid and jasmonic acid was activated. According to the transcriptomics analysis, expressions of defense-related genes were generally upregulated while growth-related gene expressions were mostly downregulated in leaves of Zmski3-1 mutant compared to that of wild type. In addition, 223 differentially expressed genes (DEGs) that were up-regulated in Zmski3-1 mutant but down-regulated in the ZmSKI3-OE were identified as potential target genes of ZmSKI3. Among them, defense-related genes were dominantly enriched, implying that ZmSKI3 regulates plant defense by targeting the defense-related genes for degradation. Moreover, small interfering RNAs (siRNAs) targeting the defense and growth-related genes were differentially accumulated to combat the overaccumulation of defense-related RNAs but decrease of growth-related RNAs in Zmski3-1 mutant. Taken together, our study indicates that ZmSKI3 acts as an essential coordinator of plant growth and immunity at different post-transcriptional levels in maize. These findings expand our knowledge of the function of SKI complex and provide a valuable target for genetic modification towards balanced plant growth and disease resistance of maize.