The Incredible Journey of Begomoviruses in Their Whitefly Vector

Abstract

Begomoviruses are vectored in a circulative persistent manner by the whitefly Bemisia tabaci. The insect ingests viral particles with its stylets. Virions pass along the food canal and reach the esophagus and the midgut. They cross the filter chamber and the midgut into the haemolymph, translocate into the primary salivary glands and are egested with the saliva into the plant phloem. Begomoviruses have to cross several barriers and checkpoints successfully, while interacting with would-be receptors and other whitefly proteins. The bulk of the virus remains associated with the midgut and the filter chamber. In these tissues, viral genomes, mainly from the tomato yellow leaf curl virus (TYLCV) family, may be transcribed and may replicate. However, at the same time, virus amounts peak, and the insect autophagic response is activated, which in turn inhibits replication and induces the destruction of the virus. Some begomoviruses invade tissues outside the circulative pathway, such as ovaries and fat cells. Autophagy limits the amounts of virus associated with these organs. In this review, we discuss the different sites begomoviruses need to cross to complete a successful circular infection, the role of the coat protein in this process and the sites that balance between virus accumulation and virus destruction.

Keywords: TYLCV; autophagy; begomovirus; transcription and replication; whitefly.

Figure 1

Schematic drawing of a female whitefly longitudinal cross-section. The main organs and cells involved in begomovirus translocation (Arabic numerals in a circle) and the main processes affecting the viruses (Roman numerals in a rectangle) are shown in the drawing. The important virus translocation sites in the midgut and the primary salivary glands are enlarged. Organ and cells: 1. stylets; 2. maxillary stylet containing the food and salivary canals; 3. primary and accessory salivary glands; 4. cibarium; 5. esophagus; 6. filter chamber; 7. midgut; 8. section across the filter chamber; 9. microvilli; 10. bacteriosome and endosymbiotic bacteria; 11. haemolymph; 12. salivary gland lumen; 13. salivary gland secretory cells; 14. hindgut; 15. rectal sac; 16. ovaries; 17. fat cells. Processes: I. virus ingestion; II. cibarium: discrimination non-circulative and circulative viruses; III. entry of virus via microvilli; IV. endocytosis; V. virus accumulation; VI. transcription, replication, virion formation; VII. autophagy; VIII. interactions virus CP-whitefly proteins; IX. virus aggregation; X. GroEL production; XI. interaction endosymbiotic GroEL-begomovirus CP; XII. release of virion from GroEL near primary salivary glands; XIII. secretion of begomovirus in primary salivary glands, from secretory cells into central lumen; XIV. virus excretion with honeydew; XV. virus invasion of fat cells and ovaries; XVI. virus egestion and transmission to plants.