Stability of Begomoviral pathogenicity determinant [beta]C1 is modulated by mutually antagonistic SUMOylation and SIM interactions

To successfully invade new hosts, plant viruses must break host resistance and be competent to move within and between plant cells. As a means, viral proteins known as pathogenicity determinants have evolved to coordinate a network of protein interactions. The [beta]C1 protein encoded by specific geminiviral satellites acts as a key pathogenicity determinant for this disease-causing family of plant viruses. Post-translational modifications (PTMs) such as ubiquitination and phosphorylation of the [beta]C1 protein have been shown to occur in diverse viruses. However, the relevance of these and other layers of PTMs in host-geminiviral interactions has not been fully understood. Here we identified the significance of a novel layer of PTMs in the [beta]C1 protein of Synedrella yellow vein clearing virus (SyYVCV), a newly identified member of the Begomovirus genus of Geminiviruses. This protein has conserved SUMOylation and SUMO-interacting motifs (SIMs), and we observed SUMOylation of SyYVCV [beta]C1 in host plants as a defensive strategy against ubiquitin-mediated degradation. Counteracting this, SIMs encoded in [beta]C1 mediate the degradation of [beta]C1; however, both these PTMs are essential for the function of [beta]C1 protein since SIM and SUMOylation motif mutants failed to promote pathogenicity and viral replication in vivo. SUMOylation in different motifs of [beta]C1 led to functionally distinct outcomes, regulating the stability and function of the [beta]C1 protein, as well as increased global SUMOylation of host proteins. Our results indicate the presence of a novel mechanism mediating a fine balance between defence and counter-defence in which a SIM site is competitively sought for degradation and, as a counter-defence, [beta]C1 undergoes SUMOylation to escape from its degradation.