A Conserved Planthopper MATH-BTB Protein Regulates Fecundity in Nilaparvata legens Stål

The meprin and TRAF-C homology (MATH) family of proteins plays essential roles in diverse biological processes across eukaryotes. Fecundity is a key determinant underlying the rapid outbreaks of agricultural insect pests. Nevertheless, the potential involvement of MATH proteins in the regulation of fecundity in agriculturally important insects, particularly planthoppers, remains largely uncharacterized. This study identified key members of the MATH protein family that are conserved in planthoppers and involved in the regulation of insect fecundity. A total of 121 identified MATH proteins from 31 insect species were classified into five distinct clades based on protein structures, predominantly represented by the MATH-BTB, MATH-USP7, and MATH-Zf-Box subtypes, which are largely conserved across most agricultural insect species. In planthoppers, the MATH-BTB subtype gene cluster <i>SfMATH1</i>-<i>NlMATH3</i>-<i>LsMATH3</i> constitutes a tripartite collinear gene set conserved across all three species. Among the four ovary-specific expressed <i>MATH</i> genes, <i>NlMATH3</i> exhibited the highest expression level in the ovary. Moreover, silencing <i>NlMATH3</i> significantly impaired ovarian development in adult females and reduced both the number of deposited and hatched eggs, which was associated with downregulation of vitellogenin (<i>Vg</i>) and its receptor <i>VgR</i>, as well as elevating activity in metabolic and immune signaling pathways. In summary, this study provides novel insights into the evolutionary dynamics of the MATH family in agricultural insects, particularly planthoppers, and elucidates the critical regulatory role of the planthopper conserved MATH-BTB protein NlMATH3 in insect fecundity. The conservation of NlMATH3 homologs across planthoppers highlights their potential as targets for RNAi-based pest control strategies.