Integrative analysis identifies the safety of transgenic Cry1Ab rice to non-target spider Pardosa pseudoannulata

• Bioaccumulation of Cry1Ab protein harbors no adverse impact on the growth of spider. • Cry1Ab protein affects detoxifying enzyme activities at subcellular level . • Transcriptome analysis displays the altered genes involved in cuticle proteins. • Organ-level bioinformatics analysis identifies the safety of Cry1Ab on predation and sensitivity. • Cry1Ab protein constitutes no influence on foraging behavior of spiders. Cry1Ab toxin has been successfully integrated into crops (e.g., rice and cotton) for pest control. Concomitantly, the environmental safety assessment of non-target organisms exposed to transgenic crops has become an essential task. Spiders grant a new perspective on the influence of the transgenic toxin on invertebrates, but the mechanisms of Cry1Ab bioaccumulation, adaptation, and safety in spiders remain unclear. In this study, we identified that the wolf spider Pardosa pseudoannulata, fed with Nilaparvata lugens enriched with Cry1Ab protein, suffered no significant toxicity in terms of body mass, carapace width, and survival rate, except the prolonged developmental duration in 7th ∼ 8th instars. The overall activities of four detoxifying enzymes (SOD, POD, CAT, and GSH-Px) were not altered in four organs of adults and spiderlings. Comparison analyses of whole-body transcriptomes revealed 1,480 differentially expressed genes (DEGs), and down-regulated cuticle encoding genes were considered as a segment for the prolonged developmental duration under Cry1Ab exposure. Further venom gland transcriptome sequencing analysis found that a total of 31 toxin encoding genes were up-regulated under Cry1Ab protein stress, indicating that the spiders needed to inject more venom to digest the external protein. Furthermore, gene expression profiles of ganglia transcriptome showed that Cry1Ab protein did not generate DEGs involved in neuron sensitivity in spiders. Behavioral experiments verified that both Cry1Ab and Cry1Ab-free spiders were in line with the Holling type II functional response model. In summary, the data provide multi-level views to assess the safety of genetically modified crops on non-target arthropods.