Functions of the sulfatase-modifying factor 1 (HaSumf1) in the development and host glucosinolate adaptation of Helicoverpa armigera

Abstract

The system of gulcosinoalte sulfatase–sulfatase-modifying factors (Sumfs) in herbivorous insects fulfils an essential function in defending host plant glucosinolates (GLSs)—the compounds of cruciferous plants—by swiftly desulfurising them. Previously, eight HaSulfs and one HaSumf1 were identified in Helicoverpa armigera. GLSs have a significant impact on the growth and development of H. armigera larvae. They can induce the expression of HaSulf in the midgut of H. armigera at both gene and protein levels. In the present study, we utilised RNAi technology to silence the HaSumf1 gene and explored its potential impact on the growth, development, and adaptation of GLSs. The sequence analysis has indicated that the HaSumf1 gene in H. armigera shares a high degree of sequence identity with other insect genes and is expressed at its highest level in the fifth-instar phase. Additionally, the qRT-PCR results reveal that the expression of HaSumf1 was upregulated by 1.26 and 0.07 times in third-instar and 1.65 and 0.19 times in fifth-instar when fed with 0.004% and 0.04% GLS, respectively. The effectiveness of dsSumf1 silencing was observed in both third- and fifth-instar stages, with silencing rates of 65.5%–88.9% and 61.3%–74.6%, respectively (p < 0.05). The findings of the bioassay indicate that H. armigera's body weight at fifth-instar significantly increased after treatment with 0.004% GLS and 0.04% GLS, while the larval survival rate, pupation rate, and pupa weight decreased. Notably, when feeding dsRNA-encapsulated carbon quantum dots (CQD-dsRNA), this trend was significantly strengthened (p < 0.05). Taken together, these findings provide evidence supporting HaSumf1's conservation involvement in the adaptation of host plant GLSs during lepidopteran insect evolution. Therefore, it plays a critical role in the growth and development of H. armigera, offering molecular targets for developing novel pesticides and targeted control measures against this vital pest.