Diverse Begomoviruses Evolutionarily Hijack Plant Terpenoid-Based Defense to Promote Whitefly Performance.

ABSTRACT

Arthropod-borne pathogens and parasites are major threats to human health and global agriculture. They may directly or indirectly manipulate behaviors of arthropod vector for rapid transmission between hosts. The largest genus of plant viruses, Begomovirus, is transmitted exclusively by whitefly (Bemisia tabaci), a complex of at least 34 morphologically indistinguishable species. We have previously shown that plants infected with the tomato yellowleaf curl China virus (TYLCCNV) and its associated betasatellite (TYLCCNB) attract their whitefly vectors by subverting plant MYC2-regulated terpenoid biosynthesis, therefore forming an indirect mutualism between virus and vector via plant. However, the evolutionary mechanism of interactions between begomoviruses and their whitefly vectors is still poorly understood. Here we present evidence to suggest that indirect mutualism may happen over a millennium ago and at present extensively prevails. Detailed bioinformatics and functional analysis identified the serine-33 as an evolutionary conserved phosphorylation site in 105 of 119 Betasatellite species-encoded ßC1 proteins, which are responsible for suppressing plant terpenoid-based defense by interfering with MYC2 dimerization and are essential to promote whitefly performance. The substitution of serine-33 of ßC1 proteins with either aspartate (phosphorylation mimic mutants) or cysteine, the amino acid in the non-functional sßC1 encoded by Siegesbeckia yellow vein betasatellite SiYVB) impaired the ability of ßC1 functions on suppression of MYC2 dimerization, whitefly attraction and fitness. Moreover the gain of function mutation of cysteine-31 to serine in sßC1 protein of SiYVB restored these functions of ßC1 protein. Thus, the dynamic phosphorylation of serine-33 in ßC1 proteins helps the virus to evade host defense against insect vectors with an evolutionarily conserved manner. Our data provide a mechanistic explanation of how arboviruses evolutionarily modulate host defenses for rapid transmission.