Abstract

Numerous herbivores orally secrete defense compounds to detoxify plant toxins. However, little is known about the role of orally secreted enzymes by a specialized pest, Plutella xylostella, in the detoxification of plant defense compounds. Three glucosinolate sulfatases (GSSs) or two sulfatase-modifying factors (SUMF1s) mutant strains were established on the basis of CRISPR/Cas9 technology to validate the existence of a species-specific GSSs–SUMF1s system. In comparison to the bioassay data from mutant strains of GSS1/GSS2 or SUMF1a/SUMF1b, GSS3 had a minimal role because no significant change was found in GSS3–/– under different feeding contexts. Antibody-based technologies were used to examine GSSs-related deficient strains, and the results showed that the GSS1 protein was primarily released through larval oral secretion. On the basis of high-performance liquid chromatography, we found that GSS1 was secreted to pre-desulfate the typical plant defensive glucosinolates known as 4-(methylsulfinyl)butyl glucosinolate (4MSOB-GL) to suppress the production of the toxic substance, which is referred to as pre-detoxification strategy. These findings highlighted that the GSSs–SUMF1s system is the key factor for counteradaptation of P. xylostella to cruciferous plants, which strengthens the concept that herbivores deploy pre-detoxification strategies to disrupt the plant chemical defenses to facilitate the colonization process.