Abstract
Genetic recombination is an important process during the evolution of many virus species and occurs particularly frequently amongst begomoviruses in the single stranded DNA virus family, Geminiviridae. As in many other recombining viruses it is apparent that non-random recombination breakpoint distributions observable within begomovirus genomes sampled from nature are the product of variations both in basal recombination rates across genomes and in the over-all viability of different recombinant genomes. Whereas factors influencing basal recombination rates might include local degrees of sequence similarity between recombining genomes, nucleic acid secondary structures and genomic sensitivity to nuclease attack or breakage, the viability of recombinant genomes could be influenced by the degree to which their co-evolved protein-protein and protein-nucleotide and nucleotide-nucleotide interactions are disreputable by recombination. Here we investigate patterns of recombination that occur over 120 day long experimental infections of tomato plants with the begomoviruses Tomato yellow leaf curl virus and Tomato leaf curl Comoros virus. We show that patterns of sequence exchange between these viruses can be extraordinarily complex and present clear evidence that factors such as local degrees of sequence similarity but not genomic secondary structure strongly influence where recombination breakpoints occur. It is also apparent from our experiment that over-all patterns of recombination are strongly influenced by selection against individual recombinants displaying disrupted intra-genomic interactions such as those required for proper protein and nucleic acid folding. Crucially, we find that selection favoring the preservation of co-evolved longer-range protein-protein and protein DNA interactions is so strong that its imprint can even be used to identify the exact sequence tracts involved in these interactions.
Highlights
Variations in the basal mechanistic predispositions of different regions of nucleic acid molecules to recombine is certainly a primary determinant of recombination patterns detectable within some viral genomes [1,2,3,4,5], it is becoming increasingly apparent that an important secondary determinant is natural selection [6,7,8]
We cannot know whether over the long-term upon this flattish landscape some of the recombinants we observed could have out-competed their parental genomes under natural conditions, it is apparent that TYX and TOX are possibly more ‘‘genetically compatible’’ when it comes to making recombinants than other geminivirus combinations that have been tested in the past [13,26,65]
We show here that within begomovirus co-infections, local degrees of sequence similarity, but not genomic secondary structure, strongly influences the genesis of recombinant sequences
Summary
Variations in the basal mechanistic predispositions of different regions of nucleic acid molecules to recombine is certainly a primary determinant of recombination patterns detectable within some viral genomes [1,2,3,4,5], it is becoming increasingly apparent that an important secondary determinant is natural selection [6,7,8]. Analyses of bacterial [14,15,16] and viral recombination [6,12,13,17] and protein engineering studies utilising DNAshuffling methodologies [9,10,15,18] have indicated that the probability of a given recombination event being deleterious depends on the modularity of the specific gene(s) or sub-gene module(s) that are transferred and tends to increase with decreasing parental sequence relatedness This effect is caused, at least in part, by the tendency of recombination to disrupt the networks of genome encoded sequence specific interactions that underpin the biology of all organisms. It might be expected that the survival of recombinant genomes
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