Geminiviral C2 Proteins Promote Virus Transmission by Subverting Plant Defenses Upon Infestation of Non-Vector Herbivores.

BACKGROUND:Insect vectors are responsible for transmitting the majority of plant viruses. While the interplays between insect vectors and viruses have been extensively investigated, how other organisms associated with the shared host plants of the insect and virus impact virus transmission dynamics, and the corresponding viral countermeasures, remain largely unknown. RESULTS:We explored the modulation of whitefly-mediated transmission of geminiviruses by two non-vector herbivores and the role of viral C2 proteins. The infestation of cotton bollworm induced the accumulation of jasmonic acid (JA) in plants, which in turn elicited plant repellence against whiteflies. Tomato yellow leaf curl virus (TYLCV) and its C2 inhibited JA-induced plant repellence against whiteflies. However, infestation by another non-vector insect, the green peach aphid, induced salicylic acid (SA) accumulation, thereby decreasing TYLCV infection in plants. TYLCV C2 dampens SA-induced antiviral defenses against TYLCV. The functions of TYLCV C2 in subverting both JA-induced plant repellence against the insect vector and SA-induced antiviral defenses seem conserved, as it was also observed in C2 proteins encoded by members of two other genera Becurtovirus and Topocuvirus. Mechanistically, geminiviral C2 proteins did not affect JA or SA biosynthesis but suppressed the signal transduction of both pathways. CONCLUSION:This study demonstrates that geminiviral C2 proteins suppress JA- and SA-mediated defenses induced by non-vector herbivores, thereby facilitating whitefly-mediated virus transmission. © 2026 Society of Chemical Industry.