Transmission of Cereal Geminiviruses

The following sections are excerpted (with modification) from Dr Fiona Hughes' PhD Thesis: "Molecular Investigations of Subgroup I Geminiviruses"; University of Cape Town, June 1991, 150 pp.

Cereal geminiviruses can be transmitted neither mechanically nor by seed, their only natural mode of transmission being by leafhoppers (Storey, 1928; Harrison, 1985). Unlike the dicot-infecting geminiviruses, which are all transmitted by a single whitefly species, grass geminiviruses are transmitted by a wide range of genera and species in the Cicadellideae. MSV is transmitted by several Cicadulina spp. (see refs. below). DSV is transmitted by Nesoclutha declivata (Linnavuori) (Julia & Dollet, 1989) and cannot be transmitted by Cicadulina spp. (Julia & Dollet, 1989; Pinner et al., 1989). WDV is transmitted by Psammotettix alienus (Dhalb.) (Lindsten et al., 1980). CSMV and related viruses are transmitted by Nesoclutha pallida (Evans) (Grylls, 1963), and the vector of MiSV is unknown (Ikegami et al., 1989).

The best-studied vector/virus system for this geminivirus genus is that of MSV, investigated in great detail by Storey (1928, 1932).

In southern and central Africa, MSV is transmitted chiefly by Cicadulina mbila (Storey, 1924, 1925). In West Africa, C. triangula Ruppel is the major vector (Soto & Buddenhagen, 1982; Okoth et al., 1987), while in Egypt the main streak vector is C. bipunctella-zeae China (Ammar et al., 1982). Other species of Cicadulina capable of transmitting MSV are C. bipunctata bipunctata (Melichar) (C. zeae) (Storey, 1936), C. latens Fennah, C. parazeae Ghauri, C. storeyi China, (Bock et al., 1974), C. ghaurii (Dabrowski, 1987a), and C. hartmansi Dabrowski (Okoth et al., 1987).

Not all races of a vector species are active, ie. capable of virus transmission (Storey, 1928). A bioassay of C. ghaurii showed that an average of 10% of males and 30% of females were capable of transmission after a 4h acquisition feed (Dabrowski, 1987b). The ability to transmit virus seems to be controlled by a dominant sex-linked gene (Storey, 1928, 1932b).

MSV can be acquired by active races of C. mbila after an acquisition probe into the mesophyll of less than 1 hour (minimum acquisition time 15 seconds) and inoculation can occur in as brief a probe as 5 minutes, during which time the insect's stylets are thought to reach the phloem (Storey, 1938). However, the frequency of transmission by, and persistence of MSV in, individual insects increases with the virus concentration in the plant, the length of the acquisition access period, and on the duration of inoculation (Okoth et al., 1987). Similar findings have been made for CSMV and its vector, N. pallida (Grylls, 1963).

MSV undergoes a latent period in the vector before transmission can occur. The length of this period is temperature dependent. At 30øC, the minimum latent period is 6 - 12 hours (Storey, 1928), the medium period being 16 - 20 hours (Okoth et al., 1987). At 16øC, the minimum latent period is 85 hours (Storey, 1928). The latent period represents the time required for the virus to pass from the insect's gut lumen to the haemocoel and thence to the salivary glands, where it becomes available for inoculation (Storey, 1932b).

The gene that controls the insect's virus transmitting ability appears to act by controlling the passage of virus to the haemolymph. This is so, since inactive leafhoppers can be rendered active by puncturing the gut with a needle (Storey, 1932b). This evidence has been taken to imply that a single vector protein regulates virus passage through the gut wall (Harrison, 1985). However, since individual insects transmit virus with differing degrees of efficiency, it has been assumed that other autosomal genes modify the effect of the major gene controlling transmission (Storey, 1932b). Indeed, Medina et al. (1990) have shown that there are two barriers to infection; transport of virus across the insect's gut lining, and virus entry into the salivary glands. They demonstrated that MSV particles are taken up into cells of the filter chamber in active vectors only. Virus-vector specificity is consistent with receptor-mediated endocytosis, followed by envelopment of aggregated virus by the endoplasmic reticulum. A rapid transcytotic pathway was proposed for virus in cells of the ventriculus, with inclusions probably breaking up in the haemolymph. From there, virions enter the salivary glands via specialized secretory cells (Medina et al., 1990). It appears that a protease inhibitor motif exists in the virion coat protein sequence, which may be responsible for resistance to proteolysis in the insect gut (P. G. Markham, pers. comm. to E. P. Rybicki).

MSV can be acquired and transmitted by all 5 nymphal instars of C. mbila and is retained through ecdysis, although the virus does not appear to be capable of replication in the vector (Boulton & Markham, 1986). The virus cannot be transmitted to the following insect generation through the egg (Storey, 1928).

For CSMV at least, the proportion of insects transmitting virus, the length of the latent period, and the duration of transmission are dependent on the specific acquisition source (Greber, 1989). Thus, for field-infected Chloris gayana, 10% of feeding insects could transmit virus over 3 - 10 days after a latent period of 3 - 7 days. Using freshly infected C. gayana or wheat as acquisition sources, 50% of feeding insects could transmit virus for up to 9 weeks after a latent period of only 12 hours.

Little is known definitively about whether specific viruses or strains of a virus are preferentially adapted to particular species or races of vector. It has been shown recently though that paspalum striate mosaic virus (PSMV), which is related to CSMV, is transmitted by only one specific biotype of N. pallida (Greber, 1989).