Most plant viruses require a biological vector to spread from plant to plant in nature. Among biological vectors for plant viruses, hemipteroid insects are the most common, including phloem-feeding aphids, whiteflies, mealybugs, planthoppers, and leafhoppers. A majority of the emerging diseases challenging agriculture worldwide are insect borne, with those transmitted by whiteflies (Hemiptera: Aleyrodidae) topping the list. Most damaging whitefly-transmitted viruses include begomoviruses (Geminiviridae), criniviruses (Closteroviridae), and torradoviruses (Secoviridae). Among the whitefly vectors, Bemisia tabaci, now recognized as a complex of cryptic species, is the most harmful in terms of virus transmission. Here, we review the available information on the differential transmission efficiency of begomoviruses and other whitefly-borne viruses by different species of whiteflies, including the cryptic species of the B. tabaci complex. In addition, we summarize the factors affecting transmission of viruses by whiteflies and point out some future research prospects.

Summary: 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.

Cotton leaf curl disease is one of the most significant constraints to the production of cotton. In the past decades our understanding of the begomoviruses (family Geminiviridae) causing the disease has improved, but little is known regarding transmission of these viruses by the different species of whiteflies in the Bemisia tabaci complex. We compared transmission efficiency of cotton leaf curl Multan virus (CLCuMuV), one of the major begomoviruses associated with cotton leaf curl disease, by four whitefly species, of which two are indigenous to Asia and two are invasive worldwide. Only the indigenous Asia II 1 species was able to transmit this virus with high efficiency. By quantifying the virus and using immunoflorescence assays, we found that the differential transmission was associated with the varying efficiency of CLCuMuV to cross the midgut of various whitefly species. Further, we verified the role of coat protein in the whitefly transmission of CLCuMuV. Based on a phylogenetic analysis of the virus coat proteins, we found that most begomoviruses associated with cotton leaf curl disease might share similar whitefly transmission characteristics. These findings advance our understanding of the nature of cotton leaf curl disease and provide information for the development of control and preventive strategies against this disease.

For many crop pathogens including viruses, high genetic variation provides them with potential to adapt to and prevail in a changing environment. Understanding genetic variation in viruses and their significance is a key to elaborate virus epidemiology and evolution. While genetic variation of plant viruses has been documented to impact virus–host interactions, how it affects virus–insect vector interactions remains elusive. Here, we report the impact of mutations in the coat protein of squash leaf curl China virus (SLCCNV), a begomovirus, on the interaction between the virus and its whitefly vectors. We characterized mutations in the coat protein of SLCCNV and found that some residues exhibited higher mutation frequency than the others. We assayed the impact of mutation on infectivity using agroinoculation and found these mutations marginally affect virus infectivity. We further analyze their functions using virus acquisition and transmission trials and found some of mutations resulted in altered transmission of SLCCNV by different species of the whitefly Bemisia tabaci complex. We then identified the key amino acid residue(s) involved by constructing several mutant viruses and found that a single-residue mutation in the coat protein of SLCCNV was sufficient to significantly alter the whitefly transmission characteristics of SLCCNV. We examined the competition between different genotypes of SLCCNV in plant infection and whitefly transmission. We found that mutations in the coat protein did not alter the fitness of SLCCNV in plants, but they rendered the virus more competitive in transmission by certain species of whiteflies. Our findings indicate that mutations in the coat protein may play a key role in both the adaptation of begomoviruses to the changing vector populations and the evolution of begomoviruses.

Plants face constant threats from insect herbivores, which limit plant distribution and abundance in nature and crop productivity in agricultural ecosystems. In recent decades, the whitefly Bemisia tabaci, a group of phloem-feeding insects, has emerged as pests of global significance. In this article, we summarize current knowledge on plant defenses against whitefly and approaches to engineer plant resistance to whitefly. Physically, plants deploy trichome and acylsugar-based strategies to restrain nutrient extraction by whitefly. Chemically, toxic secondary metabolites such as terpenoids confer resistance against whitefly in plants. Moreover, the jasmonate (JA) signaling pathway seems to be the major regulator of whitefly resistance in many plants. We next review advances in interfering with whitefly-plant interface by engineering of plant resistance using conventional and biotechnology-based breeding. These breeding programs have yielded many plant lines with high resistance against whitefly, which hold promises for whitefly control in the field. Finally, we conclude with an outlook on several issues of particular relevance to the nature and engineering of plant resistance against whitefly.

Whiteflies of the Bemisia tabaci complex transmit hundreds of plant viruses belonging to the genera Begomovirus and Crinivirus, among others. Tripartite interactions of whitefly–virus–plant frequently occur during virus infection and transmission. Specifically, virus transmission-related behavior of whitefly, such as preference and feeding, may be altered by viruses and thus exert significant impacts on the outcome of virus spread and epidemics. Here, we provide an overview on the current understanding of the manipulation of whitefly behavior by plant viruses. Plant viruses can significantly modulate whitefly preference and feeding behavior, either directly or in a plant-mediated manner. In general, non-viruliferous whiteflies tend to prefer virus-infected plants, and viruliferous whiteflies are more likely to prefer uninfected plants. In most cases, virus infection of plants and/or whitefly seems to exhibit positive or no effects on whitefly feeding on plants. The significance and evolution of these patterns are then discussed. Finally, we suggest several future directions of research, such as the exploration of temporal dynamics and the dissection of underlying mechanisms of virus-induced changes in whitefly behavior.