Toxicity assessment and transcriptomic analysis of Metarhizium rileyi (Hypocreales: Clavicipitaceae) against Spodoptera frugiperda (Lepidoptera: Noctuidae): identification of tyrosol as a key quorum sensing regulator of pathogenicity.

Abstract

The fall armyworm, Spodoptera frugiperda, a severe crop pest, gained significant attention following its invasion of China in 2019. This study aimed to investigate the virulence and in vivo pathogenic transition of Metarhizium rileyi on S. frugiperda to understand biological control strategies. Using the immersion method, M. rileyi exhibited higher lethality toward third-instar larvae compared to fourth-instar larvae, with LC50 values of 3.15 × 107 conidia/ml and 1.04 × 108 conidia/ml, respectively. Microscopic observations revealed that M. rileyi initially existed as a yeast-like nonpathogenic form within the host but later transformed into a mycelial-like pathogenic form to effectively kill the host insect. De novo transcriptome analysis identified 89,498 unigenes. KEGG analysis highlighted genes associated with "metabolic pathways" and "quorum sensing." Differentially expressed gene (DEG) analysis identified 2,988 DEGs during the morphological transformation of M. rileyi, with increased tyrosine levels due to 13 down-regulated genes in the "biosynthesis of various plant secondary metabolites" pathway. DAHP synthase, an up-regulated enzyme from the quorum sensing pathway, also facilitated tyrosine biosynthesis. Given tyrosine's role as a precursor to tyrosol, we hypothesized tyrosol served as quorum sensing molecule regulating the pathogenic switch of M. rileyi. The hypothesis was validated in vitro, confirming 1000 mg/L as the effective inducible concentration.