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

文献类型： 外文期刊

第一作者： Qi, Jinfeng

作者： Qi, Jinfeng;Xiao, Fangjie;Liu, Xingxing;Li, Jing;Xu, Yuxing;Qi, Jinfeng;Xiao, Fangjie;Liu, Xingxing;Qi, Jinfeng;Xiao, Fangjie;Liu, Xingxing;Li, Jing;Xu, Yuxing;Wang, Haocai;Wang, Hang;Li, Shu;Yu, Hongwei

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关键词： Spodoptera frugiperda; Maize; Benzoxazinoids; Pantoea dispersa; Pest-microbe-plant interactions

期刊名称：MICROBIOME （ 影响因子：12.7； 五年影响因子：16.6 ）

ISSN： 2049-2618

年卷期： 2024 年 12 卷 1 期

页码：

收录情况： SCI

摘要： BackgroundThe 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.ResultsUsing 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 expression assays by expressing two candidate genes form the plasmid.ConclusionsFAW can convert maize endophytes into its own probiotics to detoxify Bxs and thus enhance caterpillar growth. This represents a novel strategy for lepidopteran pests-transforming allies of the host into its own-thereby shedding light on the rapid spread of FAW and enhancing our understanding of ecological and evolutionary mechanisms underlying the pest-microbe-plant interactions.2f6JcKQYnKTEdqap9saLkxVideo AbstractConclusionsFAW can convert maize endophytes into its own probiotics to detoxify Bxs and thus enhance caterpillar growth. This represents a novel strategy for lepidopteran pests-transforming allies of the host into its own-thereby shedding light on the rapid spread of FAW and enhancing our understanding of ecological and evolutionary mechanisms underlying the pest-microbe-plant interactions.2f6JcKQYnKTEdqap9saLkxVideo Abstract

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