Integrated transcriptome and metabolite profiling highlights the role of benzoxazinoids in wheat resistance against Fusarium crown rot

Abstract Fusarium crown rot (FCR), caused by Fusarium spp., is a chronic and severe plant disease worldwide. In the last years, the incidence and severity of FCR in China has increased to the point that it is now considered a threat to local wheat crops. In this study, for the first time, the metabolites and transcripts responsive to FCR infection in the partial resistant wheat cultivar 04 Zhong 36 (04z36) and susceptible cultivar Xinmai 26 (XM) were investigated and compared at 20 and 25 days post inoculation (dpi). A total of 443 metabolites were detected, of which 102 were significantly changed because of pathogen colonization. Most of these 102 metabolites belonged to the flavonoid, phenolic acid, amino acid and derivative classes. Some metabolites, such as proline betaine, lauric acid, ribitol, and arabitol, were stably induced by Fusarium pseudograminearum (Fp) infection at two time points and may have important roles in FCR resistance. In line with the reduced seedling height of 04z36 and XM plants, RNA-seq analysis revealed that FCR infection significantly affected the photosynthesis activities in two cultivars. Furthermore, 15 jasmonate ZIM-domain genes (JAZ) in the significantly enriched ‘regulation of jasmonic acid mediated signaling pathway’ in 04z36 were down-regulated. The down-regulation of these JAZ genes in 04z36 may cause a strong activation of the jasmonate signaling pathway. Based on combined data from gene expression and metabolite profiles, two metabolites, benzoxazolin-2-one (BOA) and 6-methoxy-benzoxazolin-2-one (MBOA), involved in the benzoxazinoid-biosynthesis pathway, were tested for their effects on FCR resistance. Both BOA and MBOA significantly reduced fungal growth in vitro and in vivo, and, thus, a higher content of BOA and MBOA in 04z36 may contribute to FCR resistance. Above all, the current analysis extends our understanding of the molecular mechanisms of FCR resistance/susceptibility in wheat and will benefit further efforts for the genetic improvement of disease resistance.