Attacks on plants by both viruses and their vectors is common in nature. Yet the dynamics of the plant-virus-vector tripartite system, in particular the effects of viral infection on plant-insect interactions, have only begun to emerge in the last decade. Viruses can modulate the interactions between insect vectors and plants via the jasmonate, salicylic acid and ethylene phytohormone pathways, resulting in changes in fitness and viral transmission capacity of their insect vectors. Virus infection of plants may also modulate other phytohormones, such as auxin, gibberellins, cytokinins, brassinosteroids and abscisic acid, with yet undefined consequences on plant-insect interactions. Moreover, virus infection in plants may incur changes to other plant traits, such as nutrition and secondary metabolites, that potentially contribute to virus-associated, phytohormone-mediated manipulation of plant-insect interactions. In this article, we review the research progress, discuss issues related to the complexity and variability of the viral modulation of plant interactions with insect vectors, and suggest future directions of research in this field.

Hemipteran insects transmit viruses when infesting plants, during which vectors activate salicylic acid (SA)-regulated antiviral defenses. How vector-borne plant viruses circumvent these antiviral defenses is largely unexplored. During co-infections of begomoviruses and betasatellites in plants, betasatellite-encoded βC1 proteins interfere with SA signaling and reduce the activation of antiviral resistance. βC1 inhibits SA-induced degradation of NbNPR3 (Nicotiana benthamiana nonexpressor of pathogenesis-related genes 3), a negative regulator of SA signaling. βC1 does not bind directly to NbNPR3, but regulates NbNPR3 degradation via heat shock protein 90s (NbHSP90s). NbHSP90s bind to both NbNPR3 and βC1 and suppress SA signaling. This viral success strategy appears to be conserved as it is also documented for viral proteins encoded by two aphid-borne viruses. Our findings reveal an exquisite mechanism that facilitates the persistence of vector-borne plant viruses and provide important insights into the intricacies of the virus life cycle.

A parasite-infected host may promote performance of associated insect vectors; but possible parasite effects on nonvector insects have been largely unexplored. Here, we show that Begomovirus, the largest genus of plant viruses and transmitted exclusively by whitefly, reprogram plant immunity to promote the fitness of the vector and suppress performance of nonvector insects (i.e., cotton bollworm and aphid). Infected plants accumulated begomoviral βC1 proteins in the phloem where they were bound to the plant transcription factor WRKY20. This viral hijacking of WRKY20 spatiotemporally redeployed plant chemical immunity within the leaf and had the asymmetrical benefiting effects on the begomoviruses and its whitefly vectors while negatively affecting two nonvector competitors. This type of interaction between a parasite and two types of herbivores, i.e., vectors and nonvectors, occurs widely in various natural and agricultural ecosystems; thus, our results have broad implications for the ecological significance of parasite-vector-host tripartite interactions.

Environments such as light condition influence the spread of infectious diseases by affecting insect vector behavior. However, whether and how light affects the host defense which further affects insect preference and performance, remains unclear, nor has been demonstrated how pathogens co-adapt light condition to facilitate vector transmission. We previously showed that begomoviral βC1 inhibits MYC2-mediated jasmonate signaling to establish plant-dependent mutualism with its insect vector. Here we show red-light as an environmental catalyzer to promote mutualism of whitefly-begomovirus by stabilizing βC1, which interacts with PHYTOCHROME-INTERACTING FACTORS (PIFs) transcription factors. PIFs positively control plant defenses against whitefly by directly binding to the promoter of terpene synthase genes and promoting their transcription. Moreover, PIFs interact with MYC2 to integrate light and jasmonate signaling and regulate the transcription of terpene synthase genes. However, begomovirus encoded βC1 inhibits PIFs' and MYC2' transcriptional activity via disturbing their dimerization, thereby impairing plant defenses against whitefly-transmitted begomoviruses. Our results thus describe how a viral pathogen hijacks host external and internal signaling to enhance the mutualistic relationship with its insect vector.