The fall armyworm converts maize endophytes into its own probiotics to detoxify benzoxazinoids and promote caterpillar growth

作者：Jinfeng Qi, Fangjie Xiao, Xingxing Liu, Jìng Li, Haocai Wang, Wang Hao-cai, Shu Li, Hongwei D. Yu, Yuxing Xu, Hang Wang, Hang Wang · 发表于：Microbiome · 年份：2024 · DOI：10.1186/s40168-024-01957-z · 被引用次数：12 · 研究领域：Insect-Plant Interactions and Control、Insect Resistance and Genetics、Neurobiology and Insect Physiology Research

BACKGROUND: The fall armyworm (FAW, Spodoptera frugiperda) threatens maize production worldwide, and benzoxazinoids (Bxs) are known as the main secondary metabolites produced by maize to defend against FAW. However, we do not yet know whether and in what ways certain endophytes in the digestive system of FAW can metabolize Bxs, thus enhancing the fitness of FAW when feeding on maize. RESULTS: Using Bxs as the sole carbon and nitrogen source, we isolated Pantoea dispersa from the guts of FAW. P. dispersa can colonize maize roots and leaves as indicated by GFP-labeling and further successfully established itself as an endophyte in the Malpighian tubules and the gut of FAW after FAW feeding activities. Once established, it can be vertically transmitted through FAW eggs, suggesting the potential that FAW can convert maize-derived endophytes into symbiotic bacteria for intergenerational transmission. The prevalence of P. dispersa in FAW guts and maize leaves was also confirmed over large geographic regions, indicating its evolutionary adaptation in fields. Bxs determination in the gut and frass of FAW combined with bioassays performance on maize bx2 mutants revealed that the colonization of P. dispersa can promote FAW growth by metabolizing Bxs rather than other metabolites. Additionally, genome and transcriptome analyses identified plasmid-borne genes, rather than chromosomes of this species, were crucial for Bxs metabolism. This was further validated through in vitro prokaryotic...