Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors

Most plant viruses are vectored by insects and the interactions of virus-plant-vector have important ecological and evolutionary implications. Insect vectors often perform better on virus-infected plants. This indirect mutualism between plant viruses and insect vectors promotes the spread of virus and has significant agronomical effects. However, few studies have investigated how plant viruses manipulate plant defenses and promote vector performance. Begomoviruses are a prominent group of plant viruses in tropical and sub-tropical agro-ecosystems and are transmitted by whiteflies. Working with the whitefly Bemisia tabaci, begomoviruses and tobacco, we revealed that C2 protein of begomoviruses lacking DNA satellites was responsible for the suppression of plant defenses against whitefly vectors. We found that infection of plants by tomato yellow leaf curl virus (TYLCV), one of the most devastating begomoviruses worldwide, promoted the survival and reproduction of whitefly vectors. TYLCV C2 protein suppressed plant defenses by interacting with plant ubiquitin. This interaction compromised the degradation of JAZ1 protein, thus inhibiting jasmonic acid defense and the expression of MYC2-regulated terpene synthase genes. We further demonstrated that function of C2 protein among begomoviruses not associated with satellites is well conserved and ubiquitination is an evolutionarily conserved target of begomoviruses for the suppression of plant resistance to whitefly vectors. Taken together, these results demonstrate that ubiquitination inhibition by begomovirus C2 protein might be a general mechanism in begomovirus, whitefly and plant interactions. Author summary In the long evolutionary history, plants, vector-borne viruses and insects have built complicated relationships. A growing body of evidence has shown that virus infection of the plant can influence vector physiology and behavior to increase virus transmission. However, the underlying mechanisms are largely unknown. Working with begomoviruses, a group of over 300 single-stranded plant DNA virus species, which are transmitted by the whitefly Bemisia tabaci and have caused extensive damage to many crops worldwide, we addressed whether and how begomovirus infection suppresses plant defense responses to insect vectors. We found that begomovirus C2 protein was responsible for the suppression of plant defenses and contributed to the virus-vector mutualism. Viral C2 directly interacted with plant ubiquitin to compromise the degradation of JAZ1 protein and therefore inhibited the expression of down-stream defense genes. We further demonstrated that function of C2 was well conserved among begomoviruses for the suppression of plant resistance to vectors. This study also shows how sophisticated mutualism has evolved in the begomovirus-insect vector system. Our findings expand fascinating new horizons in the field of research on the interactions among plants, vectors and viruses and might lead to new strategies to combat begomovirus spread.