Gut-Expressed Vitellogenin Facilitates the Movement of a Plant Virus across the Midgut Wall in Its Insect Vector

An essential step in the life cycle of many viruses is transmission to a new host by insect vectors, and one critical step in the transmission of persistently transmitted viruses is overcoming the midgut barrier to enter vectors and complete their cycle. Most viruses enter vector midgut epithelial cells via specific interaction between viral structural proteins and vector cell surface receptor complexes.

How Does Vector Bemisia Tabaci use Visual and Olfactory Cues in Orientation to A Virus-Infected Host Plant?

Cucurbit chlorotic yellows virus (CCYV) has caused serious damage to melon crops in many countries in recent years. It is exclusively transmitted by the notorious pest Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) in a semi-persistent manner. Previous studies have shown that both persistently and non-persistently transmitted viruses can manipulate orientation and performance of vector insects through changing host phenotype to facilitate virus spread. However, as a semi-persistently transmitted virus, how CCYV affect vector B. tabaci in locating host plants by altering physiological traits of host plants is still unknown. In this study, we investigated B. tabaci visual and olfactory preference between healthy and CCYV-infected host plant Cucumis sativus. Volatile profiles of healthy and CCYV-infected C. sativus plants were analyzed by using gas chromatography-mass spectrometry (GC-MS). Initially, it was found that vector insects preferred to settle down CCYV-infected Cucumis sativus seedlings in free choice. The concentrations of total volatiles and terpenes in cucumber plants were notably decreased after CCYV infection, and especially, the concentrations of α-pinene, β-ocimene, α-farnesene, and nonanal, responsible for olfactory attraction of B. tabaci, dramatically reduced in CCYV-infected plants. Subsequently, we investigated the visual preference of B. tabaci to CCYV-infected and healthy host, and found that B. tabaci adults showed significant preference to CCYV-infected host. CCYV induced yellowing symptoms in host leaves may explain the visual preference of B. tabaci adults to infected hosts. This study indicated that visual cues could play a vital role in vector insects locating virus-infected host plants.

Tomato Yellow Leaf Curl Virus Infection Alters Bemisia tabaci MED (Hemiptera: Aleyrodidae) Vulnerability to Flupyradifurone

The whitefly, Bemisia tabaci Gennadius, is a major phloem-feeding pest of agricultural crops that is also an important vector of many plant diseases. The B. tabaci Mediterranean (‘MED’) biotype is a particularly effective vector of Tomato yellow leaf curl virus (TYLCV), a devastating plant pathogen. Although insecticides play an important role in the control of MED and TYLCV, little is known about how TYLCV infection affects MED susceptibility to insecticides. We conducted research addressing how MED susceptibility to flupyradifurone, the first commercially available systemic control agent derived from the butenolide class of insecticides, was affected by TYLCV infection. We first conducted bioassays determining the LC15 and LC50 for control and viruliferous MED feeding on either water- or insecticide-treated plants. We next measured several demographic parameters of control and viruliferous MED exposed to either insecticide- or water-treated plants. TYLCV infection increased MED tolerance of flupyradifurone: the LC15 and LC50 of viruliferous MED were double that of uninfected MED. Viral infection also altered MED demographic responses to flupyradifurone, but in an inconsistent manner. Although the ability of TYLCV and other persistently transmitted viruses to benefit Bemisia via manipulation of host plant defense is well known, this appears to be the first example of virally mediated changes in vector susceptibility to an insecticide.

Infection by the semi-persistently transmitted Tomato chlorosis virus alters the biology and behaviour of Bemisia tabaci on two potato clones

Insect-borne plant viruses usually alter the interactions between host plant and insect vector in ways conducive to their transmission (‘host manipulation hypothesis’). Most studies have tested this hypothesis with persistently and non-persistently transmitted viruses, while few have examined semi-persistently transmitted viruses. The crinivirus Tomato chlorosis virus (ToCV) is semi-persistently transmitted virus by whiteflies, and has been recently reported infecting potato plants in Brazil, where Bemisia tabaci Middle East Asia Minor 1 (MEAM1) is a competent vector. We investigated how ToCV infection modifies the interaction between potato plants and B. tabaci in ways that increase the likelihood of ToCV transmission, in two clones, one susceptible (‘Agata’) and the other moderately resistant (Bach-4) to B. tabaci. Whiteflies alighted and laid more eggs on ToCV-infected plants than mock-inoculated plants of Bach-4. When non-viruliferous whiteflies were released on ToCV-infected plants near mock-inoculated plants, adults moved more intensely towards non-infected plants than in the reverse condition for both clones. Feeding on ToCV-infected plants reduced egg-incubation period in both clones, but the egg–adult cycle was similar for whiteflies fed on ToCV-infected and mock-inoculated plants. Our results demonstrated that ToCV infection in potato plants alters B. tabaci behaviour and development in distinct ways depending on the host clone, with potential implications for ToCV spread.

In vitro association between the helper component–proteinase of zucchini yellow mosaic virus and cuticle proteins of Myzus persicae

Potyviruses, as typical non-persistently transmitted viruses, are carried within the stylets of aphids. Cuticle proteins (CuPs), which are a major component of the insect cuticle, were examined for in vitro binding to the potyviral helper component–proteinase (HC–Pro). Proteins in 8 M urea extracts from Myzus persicae were separated by SDS-PAGE, electroblotted onto membranes and identified as CuPs by using specific antibodies to M. persicae CuP. Blotted M. persicae protein extracts were overlaid with two HC–Pros, differing by the presence of K or E in the KLSC domain. The HC–Pro with KLSC, known to assist transmission, was found to bind M. persicae proteins, whereas the HC–Pro with ELSC, being deficient in assisting transmission, did not. To identify CuPs that react with HC–Pro, protein extracts were separated by two-dimensional gel electrophoresis. Nine proteins reacting with HC–Pro were sequenced by mass spectrometry. Sequences of peptides in four proteins, of molecular masses between 22 and 31 kDa, were identified as CuPs according to comparison with sequences in GenBank. The putative CuPs from M. persicae that bind HC–Pro are potentially of interest in locating receptors for virions bound to HC–Pro in aphids’ stylets.

Intracellular salivation is the aphid activity associated with inoculation of non-persistently transmitted viruses

Approximately 75 % of aphid-vectored viruses are transmitted in a non-persistent (non-circulative) manner. Localization studies indicate that such viruses are acquired via ingestion and retained in the food canal of the maxillary stylets, but the inoculation mechanism has remained unresolved. Electrical recording of stylet penetration activities reveals that inoculation is associated with the first intracellular activity (subphase II-1) following maxillary puncture of an epidermal cell. Subphase II-1 may represent virus inoculation via egestion (regurgitation of virions with food-canal contents) or salivation (saliva-mediated release of virions from the common food-salivary duct at the tips of the maxillary stylets). Here, inoculation of the circulatively transmitted Pea enation mosaic virus was used as a marker for intracellular salivation during epidermal cell punctures. The results confirmed that inoculation of non-persistently transmitted viruses (subphase II-1) is associated with active injection of saliva directly into the cytoplasm.

Improving Fiji disease resistance screening trials in sugarcane by considering virus transmission class and possible origin of Fiji disease virus

Fiji disease virus is a propagative, persistently transmitted virus that multiplies in species of the delphacid planthopper genus Perkinsiella, and in sugarcane, the feeding host of the insect. Efforts to improve and modify the disease rating system for Fiji disease have largely focussed on the planthopper as individual vectors of the virus, rather than as a population of the principal, or at least an alternative, host of the virus. This perspective has resulted in key parameters of disease incidence resulting from plant infection by propagative, persistently transmitted viruses being largely overlooked or misunderstood during efforts to improve the rating system. These parameters include the relatively long acquisition, latency, and transmission times, the percentage of the population containing virus, or viruliferous, in the above periods, and the effects of population density and number of plants visited on disease incidence. Suggestions to modify trial design to improve virus transmission to the plant, based on the disease incidence parameters of the propagative, persistent transmission class, are presented and the practical difficulties of implementing these proposals are discussed. In the context of fully understanding the underlying biology of this virus–insect–plant system, the hypothesis that Fiji disease virus, as a plant-infecting member of the Reoviridae, is primarily an insect virus with a secondary plant host, and may have diverged from an insect-infecting virus relatively recently is proposed and compared with other members of the family Reoviridae.