A premature termination codon mutation in the onion AcCER2 gene is associated with both glossy leaves and thrip resistance

Plant epicuticular waxes (EW) play a critical role in defending against biotic and abiotic stresses. Notably, onions (Allium cepa L.) present a distinctive case where the mutant with defect in leaf and stalk EW showed resistance to thrips compared with the wild type with integral EW. We identified a premature stop codon mutation in the AcCER2 gene, an ortholog of CER2 gene in Arabidopsis thaliana that has been proved essential for the biosynthesis of very long-chain fatty acids (VLCFAs), in the onions with glossy leaf and stalks in our experiments. The data hinted at the possibility that this mutation might impede the elongation process of VLCFAs from C28 to C32, thereby hindering the production of 16-hentriacontanone, a primary constituent of onion EW. Transcriptomic analysis revealed substantial alterations in expression of genes in the pathways related not only to lipid synthesis and transport but also to signal transduction and cell wall modification in glossy mutants. Meanwhile, metabolomic profiling indicates a remarkable increase in flavonoid accumulation and a significant reduction in soluble sugar content in glossy mutants. These findings suggested that the enhanced resistance of glossy mutants to thrips might be a consequence of multiple physiological changes, and our integrated multiomics analysis highlighting the regulatory role of AcCER2 in these processes. Our study has yielded valuable insights into the biosynthesis of onion EW and has provided an initial hypothesis for the mechanisms underlying thrip resistance. These findings hold significant promise for the breeding programs of thrip-resistant onion.