Abstract
In RNA viruses, which have high mutation—and fast evolutionary— rates, gene overlapping (i.e., genomic regions that encode more than one protein) is a major factor controlling mutational load and therefore the virus evolvability. Although DNA viruses use host high-fidelity polymerases for their replication, and therefore should have lower mutation rates, it has been shown that some of them have evolutionary rates comparable to those of RNA viruses. Notably, these viruses have large proportions of their genes with at least one overlapping instance. Hence, gene overlapping could be a modulator of virus evolution beyond the RNA world. To test this hypothesis, we use the genus Begomovirus of plant viruses as a model. Through comparative genomic approaches, we show that terminal gene overlapping decreases the rate of virus evolution, which is associated with lower frequency of both synonymous and nonsynonymous mutations. In contrast, terminal overlapping has little effect on the pace of virus evolution. Overall, our analyses support a role for gene overlapping in the evolution of begomoviruses and provide novel information on the factors that shape their genetic diversity.
Highlights
Genomic regions that encode more than one protein, that is, gene overlapping, are commonplace among viruses [1,2]
Viruses are subjected to strong selection for maintaining smaller genomes because this (i) reduces the chances for deleterious mutations to become fixed in the virus genome, in viruses with high mutation rates; (ii) improves virus fitness due to faster replication; and (iii) optimizes virion formation due to physical limitations imposed by the capsid size [7,8,9]
Gene overlapping allows increasing the amount of genomic information in viral genomes while controlling for limited capsid space and speeding up the purification of deleterious mutations from the virus population by amplifying their effect, as in overlapping regions these mutations affect more than one gene at the same time [1,9,10]
Summary
Genomic regions that encode more than one protein, that is, gene overlapping, are commonplace among viruses [1,2]. The encoding for the AC3 protein(TGS (replication enhancer protein,and andgene post-transcriptional gene silencing and PTGS, respectively), REn), viral DNA accumulation, and isfor involved in protein interaction with the enhancer plantwithenhances the CP expression. Extensive gene overlapping in begomoviruses may contribute to modulate mutational load, and the rate of virus evolution, as it has been shown for RNA viruses [1]. Experimental evidence supporting this idea is scarce and sometimes contradictory. We explored whether the following evolutionary parameters vary between OV and NOV regions and among different types of gene overlap: (1) the rate of viral evolution, using overall tree length as a proxy, (2) the frequency of synonymous and nonsynonymous substitutions, (3) selection pressure and (4) magnitude of the effect of gene overlapping in the rate of virus evolution
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