Transcomplementation and synergism in plants: implications for viral transgenes?

In plants, viral synergisms occur when one virus enhances infection by a distinct or unrelated virus. Such synergisms may be unidirectional or mutualistic but, in either case, synergism implies that protein(s) from one virus can enhance infection by another. A mechanistically related phenomenon is transcomplementation, in which a viral protein, usually expressed from a transgene, enhances or supports the infection of a virus from a distinct species. To gain an insight into the characteristics and limitations of these helper functions of individual viral genes, and to assess their effects on the plant-pathogen relationship, reports of successful synergism and transcomplementation were compiled from the peer-reviewed literature and combined with data from successful viral gene exchange experiments. Results from these experiments were tabulated to highlight the phylogenetic relationship between the helper and dependent viruses and, where possible, to identify the protein responsible for the altered infection process. The analysis of more than 150 publications, each containing one or more reports of successful exchanges, transcomplementation or synergism, revealed the following: (i) diverse viral traits can be enhanced by synergism and transcomplementation; these include the expansion of host range, acquisition of mechanical transmission, enhanced specific infectivity, enhanced cell-to-cell and long-distance movement, elevated or novel vector transmission, elevated viral titre and enhanced seed transmission; (ii) transcomplementation and synergism are mediated by many viral proteins, including inhibitors of gene silencing, replicases, coat proteins and movement proteins; (iii) although more frequent between closely related viruses, transcomplementation and synergism can occur between viruses that are phylogenetically highly divergent. As indicators of the interoperability of viral genes, these results are of general interest, but they can also be applied to the risk assessment of transgenic crops expressing viral proteins. In particular, they can contribute to the identification of potential hazards, and can be used to identify data gaps and limitations in predicting the likelihood of transgene-mediated transcomplementation.