Predicting the Stability of Homologous Gene Duplications in a Plant RNA Virus.
One of the striking features of many eukaryotes is the apparent amount of redundancy in coding and non-coding elements of their genomes. Despite the possible evolutionary advantages, there are fewer examples of redundant sequences in viral genomes, particularly those with RNA genomes. The factors constraining the maintenance of redundant sequences in present-day RNA virus genomes are not well known. Here, we use Tobacco etch virus, a plant RNA virus, to investigate the stability of genetically redundant sequences by generating viruses with potentially beneficial gene duplications. Subsequently, we tested the viability of these viruses and performed experimental evolution. We found that all gene duplication events resulted in a loss of viability or in a significant reduction in viral fitness. Moreover, upon analyzing the genomes of the evolved viruses, we always observed the deletion of the duplicated gene copy and maintenance of the ancestral copy. Interestingly, there were clear differences in the deletion dynamics of the duplicated gene associated with the passage duration and the size and position of the duplicated copy. Based on the experimental data, we developed a mathematical model to characterize the stability of genetically redundant sequences, and showed that fitness effects are not enough to predict genomic stability. A context-dependent recombination rate is also required, with the context being the duplicated gene and its position. Our results therefore demonstrate experimentally the deleterious nature of gene duplications in RNA viruses. Beside previously described constraints on genome size, we identified additional factors that reduce the likelihood of the maintenance of duplicated genes.
Instituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Campus UPV CPI 8E, Ingeniero Fausto Elio s/n, València, Spain Present address: MIVEGEC (UMR CNRS 5290, IRD 224, UM), National Center for Scientific Research (CNRS), 911 Avenue Agropolis, BP 64501, 34394 Montpellier, Cedex 5, France anouk.willemsen@ird.fr sfelena@ibmcp.upv.es.
Anouk
A
Willemsen
Instituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Campus UPV CPI 8E, Ingeniero Fausto Elio s/n, València, Spain Present address: Institute of Theoretical Physics, University of Cologne, Zülpicher Straße 77, 50937 Cologne, Germany.
Mark P
MP
Zwart
Instituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Campus UPV CPI 8E, Ingeniero Fausto Elio s/n, València, Spain.
Pablo
P
Higueras
ICREA Complex Systems Laboratory, Universitat Pompeu Fabra, Barcelona, Spain Institut de Biologia Evolutiva (Consejo Superior de Investigaciones Científicas-Universitat Pompeu Fabra), Barcelona, Spain.
Josep
J
Sardanyés
Instituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Campus UPV CPI 8E, Ingeniero Fausto Elio s/n, València, Spain Instituto de Biología Integrativa y de Sistems (I2SysBio), Consejo Superior de Investigaciones Científicas-Universitat de València, Parc Científic de la Universitat de València, Paterna, València, Spain The Santa Fe Institute, Santa Fe, New Mexico anouk.willemsen@ird.fr sfelena@ibmcp.upv.es.
Santiago F
SF
Elena
D019143:Evolution, Molecular; D020440:Gene Duplication; D005814:Genes, Viral; D056084:Genetic Fitness; D042822:Genomic Instability; D059765:Homologous Recombination; D008957:Models, Genetic; D010942:Plant Viruses / Q000235:genetics*; D012328:RNA Viruses / Q000235:genetics*; D014026:Nicotiana / Q000821:virology
experimental evolution; gene duplication; genome stability; virus evolution