BSPP Presidential Meeting 1999

Biotic Interactions in Plant-pathogen Associations

Session IV - Virus-Vector associations: homoptera

The evolution of virus vectors within the leafhoppers and whiteflies.
Peter G. Markham.

John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK. 

Although unknown millions of species of insects inhabit the planet only about 400 species are known to transmit plant viruses. The majority of these are in the Order Homoptera divided into the two main clades of Auchenorrhyncha and Sternorrhyncha. The former includes, as vectors, the plant-, tree- and leafhoppers while the latter includes aphids, whiteflies, psyllids, scale insects etc. Leafhoppers and whiteflies both contain species that are significant pests to the worlds economic crops.

The majority of mans crops have been developed in recent times, in the evolutionary sense, in the last 10,000 years. Insects with their ability to rapidly adapt to their environment have successfully colonised mans evolving crops. Some of these associations are measured in thousands and some in hundreds of years, while others in several decades. For example, the co-evolution of maize and Dalbulus maidis probably occurred over 7-10,000 years, while the association in Africa of cassava with whiteflies and maize with Cicadulina species developed over 300-400 years; while more recently the green revolution in rice has encouraged the increase of insects such as the Brown Planthopper and the Rice Green Leafhopper. In the last few decades the whitefly, Bemisia tabaci, with the assistance of modern agricultural practice, has devastated crops on a worldwide basis. In each of these cases one species within a genus appears to have become a "superpest". This status is often associated with high fecundity, extreme mobility and exacerbated by the association with viruses and other plant pathogens, often giving rise to well documented epidemics of considerable economic impact.

The relationships between virus, plant host and vector is a complex of interactions. However for this talk, the emphasis will be on factors that contribute to specificity and will focus on hosts (varieties and crops), the coat protein gene, and viral movement proteins. The key issues with the vectors are taxonomy (and molecular markers) and the evolution of feeding strategies. The dependence of some viruses on their vectors for dissemination in the field has resulted in highly specific interactions and may give insights into the co-evolution of the virus and the insects. One such interesting virus group is the Geminiviridae, with examples of different vector specificities and virus interactions. If the virus genes are highly conserved there may be clues to the evolution of vector species. L.R. Nault suggested that geminiviruses evolved before the Sternorrhyncha and the Auchenorrhyncha diverged (about 250mya), which suggests that 150 mya the geminiviruses and vectors all shared a common land mass. Conversely geminiviruses and their vectors could have radiated from a common geographical region and undergone speciation in the process. Suitable molecular markers may offer a means to resolve these issues; not only for phylogenies but to investigate genetic evolution. We need to know a great deal more about the vectors and their lineages. Preliminary data will be presented on the use of molecular markers (such as ITS, 16S and COI) to explore the evolution of some important vector groups, such as Nephotettix, Cicadulina and Bemisia. The evolution of Bemisia species (or species complex) and the usefulness of studying vector genetics within the homoptera will be discussed.

Biotic interactions and whitefly-borne virus epidemics.
John Colvin.

University of Greenwich, Natural Resources Institute, Chatham Maritime, Kent ME4 4TB, UK. E-Mail: /

The epidemiologies of plant-virus diseases are the product of interactions that occur between viruses, host-plant species, the environment and, if present, vectors. Changes in any one of these factors, such as the introduction of a non-indigenous vector biotype or virus strain, can affect the system dynamics significantly and cause epidemics.

In this presentation, two whitefly-borne virus disease epidemics are described and data presented that suggests that they are driven by different mechanisms. In the first case, in May-July 1999, an unusually severe outbreak of tomato leaf curl virus (ToLCV) caused failure of the tomato crop in the Kolar district of Karnataka State in South India. ToLCV disease incidence reached 100% in most fields only 30 days after transplanting and unusually high populations of Bemisia tabaci were observed on the infected tomato plants. B. tabaci collected from eight sites within the epidemic area were characterised by RAPD-PCR and the non-indigenous B-biotype, responsible for spreading plant-virus disease outbreaks in many parts of the world, was found to be present at all sites.

In the second case, an epidemic of cassava mosaic disease has been spreading steadily southwards across Uganda since the late 1980s, and has recently moved into the cassava growing areas of Kenya and Tanzania. Within the epidemic and at its leading edge, infected plants expressed very severe symptoms and unusually large B. tabaci populations were associated with rapid disease spread. Molecular analysis of diseased plants collected from within the epidemic region revealed the presence of a hybrid geminivirus, termed the Uganda variant (Harrison et al., 1998). Unlike the Indian situation, in this case the epidemic and non-epidemic zone B. tabaci were not different biotypes and readily interbred. To investigate whether an interaction effect might account for the increased B. tabaci numbers associated with the epidemic, either virus-free or Uganda variant-infected B. tabaci were used to colonise three-week-old, healthy cassava plants (var. Ebwanateraka). Vector fecundity increased on plants infected successfully with the Uganda variant, as did the concentration of the amino acid asparagine, which was ca. five times higher in diseased plants, irrespective of the presence or absence of whiteflies. In the field, the density of B. tabaci per unit green leaf area was significantly higher on symptomatic than on non-symptomatic plants, indicating a preference for feeding on infected plants. Uganda variant virus and the cassava biotype B. tabaci, therefore, apparently interact in a mutually beneficial manner that provides an important component of the mechanism responsible for driving this epidemic.


Harrison et al. (1998). Ann. Appl. Biol. 131, 437-448.

A theoretical assessment of the effects of vector-virus transmission mechanism on plant virus disease epidemics
Larry V. Madden

Department of Plant Pathology, Ohio State University, Wooster, OH 44691-4096 USA. 

There are four general transmission classes of plant viruses transmitted by Homopteran insects, 1) non-persistently transmitted (stylet-borne [NP]), 2) semi-persistently transmitted (foregut borne [SP]), 3) circulative-persistent (CP), and 4) propagative-persistent (PP). These classes are characterized by rate of acquisition of the virus by the insect from an infective (and infectious) host plant, rate of inoculation of host plants by infective insects, and length of the latent period in the vector. The influence of these three factors on virus disease dynamics was explored using the linked-differential-equation deterministic model of the host and vector populations developed by Jeger, van den Bosch, Madden and Holt (IMA Journal of Mathematics Applied in Medicine and Biology 15, 1-18 [1998]). During an epidemic, four categories of plant-host status are considered, namely healthy (disease-free; H), latent (L), infectious (S), and removed (R); diseased plants "move" through the categories at rates specified in the model. Three categories of vector status are considered, namely virus-free (X), latent (Y), and infective (inoculative; Z), although Y may be, by definition, zero for the non-persistent and semi-persistent classes. Rate of change of new diseased plants is a function of the density of disease-free plants (H), infective insects (Z) and a contact rate, with the rate being a function of number of plants visited by a vector per time period and the probability of transmitting the virus per plant visit (a function of feeding time per visit and mean time that a vector must feed to inoculate a plant). Rate of change in infective insects is a function of density of infectious plants (S), number of plants visited per time by an insect, and the probability of acquiring the virus per plant visit (also a function of feeding time per visit and mean time that a vector must feed to acquire the virus).

Numerical solutions of the differential equations were used to determine transitional and steady-state levels of disease incidence (d*); d* was also determined directly from the model parameters. Clear differences were found in disease development among the four transmission classes, with the highest disease incidence (d) for the semi-persistent (SP) and circulative-persistent (CP) viruses relative to the others, especially at low insect density, when there was no insect migration or when the vector status of emigrating insects was the same as immigrating ones. The persistent viruses (PP and CP) were most affected by changes in vector longevity and rates of acquisition and inoculation of the virus by vectors, whereas the persistent-propagative (PP) viruses were least affected by changes in insect mobility. When vector migration was explicitly considered, results depended on the fraction of infective insects in the immigration pool and the fraction of dying and emigrating vectors replaced by immigrants. The persistent viruses (PP and CP) were most sensitive to changes in these factors, where d could change from ~0 to ~1 with small changes in these migration terms.

Based on model parameters, the basic reproductive number (R0)number of new infected plants resulting from an infected plant introduced into a susceptible plant populationwas derived for some circumstances and used to determine the steady-state level of disease incidence and an approximate exponential rate of disease increase early in the epidemic. Results can be used to evaluate disease management strategies.