# The βC1 protein encoded in betasatellites promotes begomovirus-whitefly coexistence by subverting vector infestation-induced plant antiviral defenses

## TL;DR

This study reveals how a viral protein helps viruses and whiteflies coexist on plants by weakening the plant's defenses triggered by whitefly feeding.

## Contribution

The study identifies a novel mechanism by which the βC1 protein promotes begomovirus-whitefly compatibility through suppression of plant antiviral defenses.

## Key findings

- Whitefly infestation on begomovirus-infected plants activates salicylic acid (SA)-mediated antiviral defenses.
- The βC1 protein suppresses SA accumulation and signaling by disrupting interactions between EDS1 and PAD4, and EDS1 and TGA2.
- βC1 promotes virus-whitefly coexistence, enhancing virus transmission by insect vectors.

## Abstract

The transmission of many plant viruses depends on arthropod vectors, which acquire viruses while feeding on infected plants and subsequently inoculate un-infected hosts. Efficient virus acquisition, particularly for persistently transmitted viruses, requires sustained vector feeding on infected plants. However, how vector infestation influences plant-virus interactions and the modulation of these impacts by viral factors remains poorly understood. Here, we show that whitefly infestation on begomovirus-infected plants activates host antiviral defenses through inducing salicylic acid (SA) accumulation. Betasatellites associated with begomoviruses, specifically the βC1 protein encoded therein, suppress these whitefly-induced defenses by interfering with SA accumulation and signaling. Mechanistically, βC1 interacts with Nicotiana benthamiana ENHANCED DISEASE SUSCEPTIBILITY 1 (NbEDS1), disrupting its interaction with NbPAD4 to reduce SA accumulation. Additionally, βC1 interferes with the association between NbEDS1 and NbTGA2, thereby attenuating NbTGA2-mediated transcription of SA-responsive genes. Our findings unravel a novel mechanism by which βC1 promotes begomovirus-whitefly compatibility, offering new insights into insect vector-mediated transmission of plant viruses.

The majority of plant viruses are transmitted by insect vectors. Insect vectors acquire viruses when feeding on infected plants and then translocate to un-infected plants to inoculate the viruses. Hence, the feeding of insect vectors on infected plants, or in another word, vector-virus coexistence on plants, determines virus acquisition by insect vectors and in turn vector-mediated virus spread. However, the factors and molecular mechanisms governing vector-virus coexistence on plants are barely known. Using begomoviruses and their whitefly vectors, here we decipher the role of salicylic acid (SA)-signaling pathway and βC1 proteins encoded in begomoviral betasatellites in modulating vector-virus coexistence on plants. Whitefly infestation on virus-infected plants induces SA accumulation and in turn plant defenses against begomoviruses. Begomoviral betasatellites and βC1 proteins encoded therein interfere with whitefly infestation-induced SA accumulation and SA signaling. Mechanistically, βC1 proteins dampen SA accumulation and signaling by subverting plant EDS1-PAD4 interaction and EDS1-TGA2 association, respectively. Our results uncover a novel mechanism by which viral proteins promotes virus transmission by insect vectors.