A horizontally acquired pantothenate gene drives vitellogenin's benefit to whitefly symbiosis persistence

Insects can survive in nutrient-poor environments owing to nutritional symbionts that produce vitamins and essential amino acids (EAAs). Nonetheless, how symbionts actively benefit from this nutritional symbiosis remains incompletely understood. Horizontally transferred genes (HTGs) expressed in bacteriocytes can function autonomously or cooperatively with symbionts to biosynthesize EAAs or B vitamins. We previously demonstrated that the horizontally transferred panBC and the symbiont Portiera cooperatively synthesize vitamin B5 (pantothenate), thereby enhancing whitefly fecundity. Beyond supporting host reproduction, this nutritional symbiosis also confers a fitness advantage on the symbionts. We further showed that induction of autophagy reduces symbiont abundance in bacteriocytes, whereas inhibition of autophagy increases it. Here, we found that silencing panBC reduced Portiera titer, impaired whitefly oogenesis, and disrupted vitellogenin (Vg) localization in ovarioles and bacteriocytes by modulating juvenile hormone biosynthesis. Pantothenate supplementation restored Vg localization in panBC RNAi whiteflies. Furthermore, silencing either Vg or panBC induced autophagy in bacteriocytes, and rapamycin-induced autophagy decreased symbiont titers. Taken together, our findings demonstrate that pantothenate, synthesized cooperatively by the horizontally transferred panBC and Portiera, regulates Vg localization in whiteflies and that Vg, in turn, protects symbionts from autophagic degradation. Our study suggests that horizontally transferred genes and symbionts jointly contribute to an important role of Vg in maintaining and shaping the evolution of insect-symbiont interactions. This study advances our understanding of how HTGs contribute to the persistence of nutritional symbiosis.