Submitted to: Virology
Publication Type: Peer reviewed journal
Publication Acceptance Date: 8/30/2005
Publication Date: 12/20/2005
Citation: French, R.C., Stenger, D.C. 2005. Population structure within lineages of wheat streak mosaic virus derived from a common founding event exhibits stochastic variation inconsistent with the deterministic quasi-species model. Virology 343:179-189. Interpretive Summary: Genetic variation within experimental populations of wheat streak mosaic virus (WSMV) was evaluated by nucleotide sequencing of viral genomes sampled from lineages of WSMV subjected to serial passage. The results indicated that viral populations varied in an unpredictable fashion with respect to the number and relative frequency of specific viral genomes present in the population at any given time. Attempts to artificially increase the complexity of WSMV populations by co-inoculation of wheat plants with inocula mixed from two different WSMV lineages did not result in increased genetic diversity of the population upon serial passage. The WSMV populations were apparently subject to severe genetic bottlenecks during systemic infection of plants. The results also indicated that relatively few individual viral genomes are responsible for the production of very high numbers of progeny in infected plants. Collectively, these results indicate that changes in plant virus population structure may occur randomly (e.g., genetic drift is possible), and that the currently accepted deterministic model of virus population genetics derived from animal and bacterial virus models do not apply to virus populations in plants.
Technical Abstract: Wheat streak mosaic virus (WSMV) populations derived from a common founding event and subjected to serial passage at high multiplicity of infection (MOI) was evaluated. The founding population was generated by limiting dilution inoculation. Lineages of known pedigree were sampled at passage 9 (two populations) and at passage 15, with (three populations) or without mixing (four populations) of lineages at passage 10. Polymorphism within each population was assessed by sequencing 17-21 clones containing a 1371 nt region (WSMV Sidney 81 nts 8001-9371) encompassing the entire coat protein cistron and flanking regions. Mutation frequency averaged ~5.0 X 10-4/nt across all populations and ranged from 2.4 to 11.6 X 10-4/nt within populations, but did not consistently increase or decrease with the number of passages removed from the founding population. Shared substitutions (19 nonsynonymous, 10 synonymous, and 3 noncoding) occurred at 32 sites among 44 haplotypes. Only four substitutions became fixed (frequency = 100%) within a population and nearly one third (10/32) never achieved a frequency of 10% or greater in any sampled population. Shared substitutions were randomly distributed with respect to genome position, with transitions outnumbering transversions 5.4 : 1 and a clear bias for A to G and U to C substitutions. Haplotype composition of each population was unique with complexity of each population varying unpredictably, in that the number and frequency of haplotypes within a lineage were not correlated with number of passages removed from the founding population or whether the population was derived from a single or mixed lineage. The simplest explanation is that plant virus lineages, even those propagated at high MOI, are subject to frequent and stringent genetic bottlenecks during systemic movement that result in low effective population size and stochastic changes in population structure upon serial passage.