Temporal dynamics of potyviral regulation and aphid-induced changes to volatile-related transcripts

Insect-vectored plant viruses cause significant losses in all major crops and result in economic impacts and threats to food security. Virus-plant dynamics change over the course of infection and influence plant ecological interactions, including interactions with insect vectors. At early infection stages, insect vectors are often attracted to virus-infected plants, while later there often a change in preference which should enhance transmission. Viruses alter plant attractiveness through changes in host traits; however, the mechanistic basis for the temporal impact of virus-vector interactions remains unknown. We performed transcriptomic and proteomic profiling of Nicotiana benthamiana to examine the effect of early- and late-stage Potato virus Y (PVYO) infection and Myzus persicae herbivory on volatile biosynthetic pathways. We used virus-induced gene silencing (VIGS) to silence a target volatile gene and assessed vector preference. PVYO had larger impacts on the N. benthamiana transcriptome at early-stage infection and that many volatile-related transcripts were differentially regulated by stage of PVYO infection and M. persicae herbivory. We identified a major transcriptional regulator of aphid choice, 5-epi-aristolochene synthase (5-EAS), that is differentially regulated over the course of infection and found that silencing this volatile gene altered aphid preference toward infected plants. In sum, these results suggest that PVYO can mediate plant-vector interactions through transcriptional reprogramming of volatile biosynthetic pathways. Understanding the mechanisms that mediate plant-vector-virus interactions could improve current management strategies and offer new avenues for relevant agricultural pest control to provide plant protection.