Annu. Rev. Phytopathol. 2005. 43:361–94 doi: 10.1146/annurev.phyto.43.040204.135939 Copyright c  2005 by Annual Reviews. All rights reserved First published online as a Review in Advance on May 27, 2005 EXPLOITING CHINKS IN THE PLANT’ S ARMOR: Evolution and Emergence of Geminiviruses Maria R. Rojas, 1,2 Charles Hagen, 1 William J. Lucas, 2 and Robert L. Gilbertson 1 1 Department of Plant Pathology, College of Agricultural and Environmental Sciences; 2 Section of Plant Biology, Division of Biological Sciences, University of California, Davis, California 95616; email: mrrojas@ucdavis.edu, chagen@ucdavis.edu, wjlucas@ucdavis.edu, rlgilbertson@ucdavis.edu Key Words plant virus movement, gene silencing, satellite DNA, plant diseases, insect-vectored viruses ■ Abstract The majority of plant-infecting viruses utilize an RNA genome, sug- gesting that plants have imposed strict constraints on the evolution of DNA viruses. The geminiviruses represent a family of DNA viruses that has circumvented these impediments to emerge as one of the most successful viral pathogens, causing severe economic losses to agricultural production worldwide. The genetic diversity reflected in present-day geminiviruses provides important insights into the evolution and biology of these pathogens. To maximize replication of their DNA genome, these viruses ac- quired and evolved mechanisms to manipulate the plant cell cycle machinery for DNA replication, and to optimize the number of cells available for infection. In addition, several strategies for cell-to-cell and long-distance movement of the infectious viral DNA were evolved and refined to be compatible with the constraints imposed by the host endogenous macromolecular trafficking machinery. Mechanisms also evolved to circumvent the host antiviral defense systems. Effectively combatting diseases caused by geminiviruses represents a major challenge and opportunity for biotechnology. INTRODUCTION In the world of plant-infecting viruses, the vast majority of families possess positive-sense RNA genomes, whereas only a few have evolved DNA genomes. This stands in marked contrast to prokaryotes, invertebrates and vertebrates, which are infected by a diversity of DNA viruses. This may indicate fundamental plant- specific challenges that had to be overcome during DNA virus evolution. Presently, there are three families of plant-infecting DNA viruses: the Caulimoviridae, which have a double-stranded (ds) DNA genome replicated via reverse transcription; and the Nanoviridae and Geminiviridae, both of which have small circular single- stranded (ss) DNA genomes. Obviously, these viruses must have evolved strategies to circumvent the constraints imposed on using DNA as their genetic material. 0066-4286/05/0908-0361$20.00 361 Annu. Rev. Phytopathol. 2005.43:361-394. Downloaded from arjournals.annualreviews.org by CAPES on 09/16/05. For personal use only.