Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution

Abstract

BackgroundMaize streak virus -strain A (MSV-A; Genus Mastrevirus, Family Geminiviridae), the maize-adapted strain of MSV that causes maize streak disease throughout sub-Saharan Africa, probably arose between 100 and 200 years ago via homologous recombination between two MSV strains adapted to wild grasses. MSV recombination experiments and analyses of natural MSV recombination patterns have revealed that this recombination event entailed the exchange of the movement protein - coat protein gene cassette, bounded by the two genomic regions most prone to recombination in mastrevirus genomes; the first surrounding the virion-strand origin of replication, and the second around the interface between the coat protein gene and the short intergenic region. Therefore, aside from the likely adaptive advantages presented by a modular exchange of this cassette, these specific breakpoints may have been largely predetermined by the underlying mechanisms of mastrevirus recombination. To investigate this hypothesis, we constructed artificial, low-fitness, reciprocal chimaeric MSV genomes using alternating genomic segments from two MSV strains; a grass-adapted MSV-B, and a maize-adapted MSV-A. Between them, each pair of reciprocal chimaeric genomes represented all of the genetic material required to reconstruct - via recombination - the highly maize-adapted MSV-A genotype, MSV-MatA. We then co-infected a selection of differentially MSV-resistant maize genotypes with pairs of reciprocal chimaeras to determine the efficiency with which recombination would give rise to high-fitness progeny genomes resembling MSV-MatA.ResultsRecombinants resembling MSV-MatA invariably arose in all of our experiments. However, the accuracy and efficiency with which the MSV-MatA genotype was recovered across all replicates of each experiment depended on the MSV susceptibility of the maize genotypes used and the precise positions - in relation to known recombination hotspots - of the breakpoints required to re-create MSV-MatA. Although the MSV-sensitive maize genotype gave rise to the greatest variety of recombinants, the measured fitness of each of these recombinants correlated with their similarity to MSV-MatA.ConclusionsThe mechanistic predispositions of different MSV genomic regions to recombination can strongly influence the accessibility of high-fitness MSV recombinants. The frequency with which the fittest recombinant MSV genomes arise also correlates directly with the escalating selection pressures imposed by increasingly MSV-resistant maize hosts.

Extensive Recombination-Induced Disruption of Genetic Interactions Is Highly Deleterious but Can Be Partially Reversed by Small Numbers of Secondary Recombination Events

“…In addition, recombination breakpoint distributions found in both field-isolated geminiviruses and geminiviruses arising during recombination experiments display well-defined hot and cold spots (26,45,46,(48)(49)(50) that can strongly influence the efficiency of adaptive evolution via recombination (27). Here, however, we observed little evidence of recombination occurring at known recombination hot spots in the MSV genome and, in fact, found a number of breakpoints falling within known recombination cold spots (Fig.…”

“…Although maintenance of favorable genetic interactions appears to be a key determinant of whether newly emerged recombinants will survive, it is also evident that nonfatal recombinationinduced disruptions of genetic interactions can be very rapidly repaired by either compensatory mutations (10,13,14) or secondary recombination events (26,27). However, part of the reason why recombination-induced genetic disruptions appear to be so easily overcome is that studies investigating this phenomenon have focused on recombination events involving transfers of complete genes.…”

“…We therefore computationally inferred secondary structures of MSV-A, MSV-B, sMSV1, sMSV2, and the secondary recombinant (A) (data taken from a previous study examining the efficiency of secondary recombination to restore fitness deficits in recombinants with only two breakpoints [27]) or sMSV1 and sMSV2 (B). Whereas panels A and B indicate genetic distances between the recombinant viruses and the four reference viruses (one reference virus at each corner of the colored rhombus), panel C indicates estimated genomic secondary-structure folding distances between recombinants and the reference viruses.…”

“…Such exchanges would have no disruptive impacts on the genetic interactions that underlie the functional intraprotein amino acid contacts that determine proper protein folding (which certainly account for a large proportion of intragenome genetic interactions). It is perhaps unsurprising, therefore, that in the experimental systems that have investigated the repair of recombination-induced genetic disruption via secondary recombination events, many of the secondary events observed were essentially "reversion recombination events," in that they approximately reversed the primary recombination events (26,27).…”

Potential linkage between compound microsatellites and recombination in geminiviruses: Evidence from comparative analysis

“…Notably, position of recombination events has been mapped in the genome of many plant-infecting ssDNA viruses (Monjane et al, 2011;Martin et al, 2011;Prasanna and Rai, 2007;Padidam et al, 1999). The factors that could complicate an association between the cSSR repeats and recombination are likely to be less in geminiviruses as compared to eukaryotes such as yeast and human.…”