Sulforaphane, A Mustard Oil Bomb Product, Reprograms Herbivore Gene Expression and Alters Chromatin Structure Across Generations

Sulforaphane (SFN), an isothiocyanate produced by the mustard oil bomb defense system of cruciferous plants, is a natural inhibitor of class I and II histone deacetylases (HDACs). We previously showed that dietary SFN inhibits HDAC activity, delays larval development, and alters the expression of more than 1,600 genes in the agricultural pests Spodoptera exigua and Trichoplusia ni. Here we investigated the mechanisms underlying these responses and whether their effects extend across generations. RNA-seq analyses revealed that SFN rapidly disrupted the normal developmental progression of gene expression in both somatic and germline tissues. ATAC-seq analyses indicated that these transcriptional changes in S. exigua were accompanied by widespread alterations in chromatin accessibility. In this species, we detected the suppression of genes involved in energy metabolism, consistent with the observed developmental delays. We observed that many SFN-induced changes in chromatin accessibility and gene expression persisted in the offspring of exposed insects despite the offspring never consuming SFN themselves. These findings demonstrate that SFN acts through chromatin-associated mechanisms to alter transcriptional programs during development, with intergenerational effects. We propose that SFN, and perhaps other HDAC inhibitors produced by plants in nature, may act as an "epigenetic weapon" with the potential to influence herbivore gene expression across generations.