Plant Virus-Induced Inheritable Apoptosis Drives Reproductive Costs in Female Insect Vectors to Balance Viral Biparental Transmission.

Insect-borne pathogens often reduce the reproductive fitness of insect vectors. Rice gall dwarf virus (RGDV) is biparentally transmitted to the offspring of its leafhopper vector. However, maternal transmission of RGDV decreases female fecundity and disrupts egg development via an unknown mechanism. This study reveals that RGDV induces mitochondria-dependent apoptosis in leafhopper ovaries, promoting viral infection but impairing ovary development. This apoptosis is transmitted to eggs during maternal RGDV transmission, promoting viral infection while harming eggs. RGDV in the ovary activates insulin-like peptide-driven PI3K signaling but reverses the downstream AKT/FoxO signaling axis. This reversal activates FoxO, which in turn transcribes pro-apoptotic Bcl-2-related ovarian killer, triggering mitochondria-dependent apoptosis. Moreover, RGDV capsid protein P2 is the key viral protein responsible for inducing apoptosis through the PI3K/AKT/FoxO signaling axis. Specifically, P2 initiates mitochondria-dependent apoptosis by activating the PI3K signaling pathway upon recognition by insulin-like peptide 2. Furthermore, P2 reverses the AKT/FoxO signaling axis via its interaction with PTEN. In contrast, two rice viruses, which are exclusively maternally transmitted, do not induce apoptosis in the ovary of insect vectors. These findings uncover how this biparentally transmitted plant virus induces inheritable apoptosis, thereby imposing female reproductive costs, and highlight viral manipulation of vector reproduction to optimize transmission.