Whitefly (Bemisia tabaci) causes extensive crop damage throughout the world by feeding directly on plants and by vectoring hundreds of species of begomoviruses. Yet little is understood about its genes involved in development, insecticide resistance, host range plasticity and virus transmission.

The begomoviruses are the largest and most economically important group of plant viruses transmitted exclusively by the whitefly Bemisia tabaci in a circulative, persistent manner. The circulation of the viruses within the insect vectors involves complex interactions between virus and vector components; however, the molecular mechanisms of these interactions remain largely unknown. Here we investigated the transcriptional response of the invasive B. tabaci Middle East-Asia Minor 1 species to Tomato yellow leaf curl China virus (TYLCCNV) using Illumina sequencing technology. Results showed that 1,606 genes involved in 157 biochemical pathways were differentially expressed in the viruliferous whiteflies. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis indicated that TYLCCNV can perturb the cell cycle and primary metabolism in the whitefly, which explains the negative effect of this virus on the longevity and fecundity of B. tabaci . Our data also demonstrated that TYLCCNV can activate whitefly immune responses, such as autophagy and antimicrobial peptide production, which might lead to a gradual decrease of viral particles within the body of the viruliferous whitefly. Furthermore, PCR results showed that TYLCCNV can invade the ovary and fat body tissues of the whitefly, and Lysotracker and Western blot analyses revealed that the invasion of TYLCCNV induced autophagy in both the ovary and fat body tissues. Surprisingly, TYLCCNV also suppressed the whitefly immune responses by downregulating the expression of genes involved in Toll-like signaling and mitogen-activated protein kinase (MAPK) pathways. Taken together, these results reveal the relationship of coevolved adaptations between begomoviruses and whiteflies and will provide a road map for future investigations into the complex interactions between plant viruses and their insect vectors.

Summary: Plant hormones play a vital role in plant immune responses. However, in contrast to the relative wealth of information on hormone‐mediated immunity in dicot plants, little information is available on monocot–virus defense systems. We used a high‐throughput‐sequencing approach to compare the global gene expression of Rice black‐streaked dwarf virus (RBSDV)‐infected rice plants with that of healthy plants. Exogenous hormone applications and transgenic rice were used to test RBSDV infectivity and pathogenicity. Our results revealed that the jasmonic acid (JA) pathway was induced while the brassinosteroid (BR) pathway was suppressed in infected plants. Foliar application of methyl jasmonate (MeJA) or brassinazole (BRZ) resulted in a significant reduction in RBSDV incidence, while epibrassinolide (BL) treatment increased RBSDV infection. Infection studies using coi1‐13 and Go mutants demonstrated JA‐mediated resistance and BR‐mediated susceptibility to RBSDV infection. A mixture of MeJA and BL treatment resulted in a significant reduction in RBSDV infection compared with a single BL treatment. MeJA application efficiently suppressed the expression of BR pathway genes, and this inhibition depended on the JA coreceptor OsCOI1. Collectively, our results reveal that JA‐mediated defense can suppress the BR‐mediated susceptibility to RBSDV infection.

OsGSK2 directly interacts with and destabilizes OsJAZ4 to activate JA-mediated defense signaling.

Significance: Auxin signaling plays essential roles in almost every aspect of plant growth and development. Auxin response factors (ARFs) are key transcriptional regulators of auxin signaling. However, it is not clear what roles ARF transcription factors may play in plant–pathogen, and specifically plant–virus, interactions. This study reveals that an ARF transcription factor is targeted by several independently evolved viral proteins of very different plant RNA viruses. These viral proteins impede the ARF activity in different ways, but in each case, these interactions benefit viral infection. These findings demonstrate that manipulation of the auxin signaling by viral proteins is a common pathogenicity strategy in plant RNA viruses.