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

## TL;DR

A plant virus causes inheritable apoptosis in insect vectors' ovaries, reducing female reproduction but aiding viral transmission.

## Contribution

RGDV uses capsid protein P2 to manipulate PI3K/AKT/FoxO signaling, inducing apoptosis in insect vectors for balanced viral transmission.

## Key findings

- RGDV induces mitochondria-dependent apoptosis in leafhopper ovaries via PI3K/AKT/FoxO signaling.
- Capsid protein P2 activates apoptosis by interacting with insulin-like peptides and PTEN.
- RGDV causes female reproductive costs but ensures efficient paternal transmission without male apoptosis.

## Abstract

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.

Rice gall dwarf virus (RGDV), transmitted biparentally by leafhopper vector to their offspring, exploits the capsid protein to induce inheritable ovarian apoptosis via insulin‐driven PI3K/AKT/FoxO signaling axis. This mechanism enhances infection but reduces female reproductive fitness, causing inefficient maternal transmission. RGDV spares male reproductive apoptosis and ensures efficient paternal transmission. This balanced strategy sustains viral persistence in China for 40+ years.