Abstract
Genomic‐based epidemiology can provide insight into the origins and spread of herbicide resistance mechanisms in weeds. We used kochia (Bassia scoparia) populations resistant to the herbicide glyphosate from across western North America to test the alternative hypotheses that (i) a single EPSPS gene duplication event occurred initially in the Central Great Plains and then subsequently spread to all other geographical areas now exhibiting glyphosate‐resistant kochia populations or that (ii) gene duplication occurred multiple times in independent events in a case of parallel evolution. We used qPCR markers previously developed for measuring the structure of the EPSPS tandem duplication to investigate whether all glyphosate‐resistant individuals had the same EPSPS repeat structure. We also investigated population structure using simple sequence repeat markers to determine the relatedness of kochia populations from across the Central Great Plains, Northern Plains and the Pacific Northwest. We found that the original EPSPS duplication genotype was predominant in the Central Great Plains where glyphosate resistance was first reported. We identified two additional EPSPS duplication genotypes, one having geographical associations with the Northern Plains and the other with the Pacific Northwest. The EPSPS duplication genotype from the Pacific Northwest seems likely to represent a second, independent evolutionary origin of a resistance allele. We found evidence of gene flow across populations and a general lack of population structure. The results support at least two independent evolutionary origins of glyphosate resistance in kochia, followed by substantial and mostly geographically localized gene flow to spread the resistance alleles into diverse genetic backgrounds.
Highlights
The rate at which herbicide resistance evolves in plant populations is dictated by the interplay of genetic and ecological factors (Hawkins et al, 2019; Kreiner et al, 2018), which determine whether resistance emerges and spreads via (i) a small number of initial evolutionary origins, or even a single evolutionary origin, followed by subsequent dispersal across landscapes; or (ii) via numerous local, independent evolutionary origins with limited and localized dispersal (Baucom, 2019)
Important genetic determinants include the potential for resistance to evolve from standing genetic variation versus the requirement for populations to “wait” for de novo variation to arise via mutation after the onset of selection (Barrett & Schluter, 2008), which in turn dictates the likelihood of soft versus hard selective sweeps for herbicide resistance in plant populations (Hermisson & Pennings, 2005; Messer & Petrov, 2013)
Genome sequencing has revealed that the structural rearrangement that caused duplication of the gene encoding the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase, EPSPS) in glyphosate-resistant kochia is due to complex interactions between mobile genetic elements and local tandem rearrangements (Jugulam et al, 2014; Patterson et al, 2019)
Summary
The rate at which herbicide resistance evolves in plant populations is dictated by the interplay of genetic and ecological factors (Hawkins et al, 2019; Kreiner et al, 2018), which determine whether resistance emerges and spreads via (i) a small number of initial evolutionary origins, or even a single evolutionary origin, followed by subsequent dispersal across landscapes; or (ii) via numerous local, independent evolutionary origins with limited and localized dispersal (Baucom, 2019). Genome sequencing has revealed that the structural rearrangement that caused duplication of the gene encoding the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase, EPSPS) in glyphosate-resistant kochia is due to complex interactions between mobile genetic elements and local tandem rearrangements (Jugulam et al, 2014; Patterson et al, 2019) These molecular mechanisms are unlikely to spontaneously generate the same genotype in multiple kochia populations and we are presented with a unique opportunity to employ genomic- based epidemiology to address questions about the evolutionary origins of glyphosate resistance in kochia. An EPSPS gene duplication with a different structural rearrangement could provide evidence for a shared evolutionary origin followed by a subsequent rearrangement
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