Factors Influencing Begomovirus Evolution and Their Increasing Global Significance: Implications for Sustainable Control

Begomoviruses (Family Geminiviridae, Genus Begomovirus) have become the most destructive group of plant viruses in tropical and subtropical regions of the world. The recent emergence of begomoviruses is notable, as these viruses have been co-evolving with their dicotyledonous plant hosts for millennia. Agricultural intensification has been proposed as one of the main causes, together with increases in populations of their vector Bemisia tabaci, partly due to the worldwide spread of the more fecund B-biotype. Reports of new diseases and associated epidemics are frequent. Many such reports describe the evolution of more aggressive virus variants through recombination. Little is known about the selection pressures that seem to operate and drive begomovirus evolution towards increased virulence and an extended host range. It is apparent, however, that the genomes of begomoviruses show extreme plasticity leading to an ability to evolve very rapidly in response to changing cropping systems. Genetic diversity is created not only by recombination between genomic components, but also by exchange (pseudorecombination) of their genomic components, and even by acquiring DNA sequences from viruses of other genera. Recently, associations with some satellite molecules, termed DNA-β and DNA1, have also been shown to be widespread in the Old World. Functional DNA-β molecules encode pathogenicity determinants and are often critical for disease symptom development. They appear to act by suppressing host plant defense mechanism(s), such as post-transcriptional gene silencing (PTGS), enabling a diverse range of begomoviruses to infect particular hosts. In this review, suppression of PTGS is one of the driving forces discussed as a likely and important influence on the evolution of begomoviruses. The known sources of genetic variation in begomoviruses are also considered together with the factors driving evolutionary change, the potential for limiting the extent and rate of adverse change, and therefore the potential for achieving more sustainable control of crop disease epidemics.

Referee: Professor J.O. Strandberg, Mid-Florida Research and Education Center, University of Florida/IFAS, 2725 Binion Road, Apopka, FL 32704 USA

Keywords:

• Bemisia tabaci
• emerging disease epidemics
• geminiviruses
• gene silencing
• recombination
• DNA satellite molecules

ACKNOWLEDGEMENTS

The authors thank Drs R Briddon, J Colvin, MN Maruthi and JM Thresh for their comments on this manuscript, and Dr Maruthi for providing virus genome maps. We are also indebted to Drs R Gibson, L Kenyon, J Legg, F Morales, V Muniyappa, J Polston, P Sseruwagi and F Zerbini for helpful discussions. This review is an output from a project funded by the Crop Protection Programme, Department for International Development, UK.

Notes

Referee: Professor J.O. Strandberg, Mid-Florida Research and Education Center, University of Florida/IFAS, 2725 Binion Road, Apopka, FL 32704 USA