Parallel and nonparallel genomic responses contribute to herbicide resistance in Ipomoea purpurea, a common agricultural weed

Abstract

The repeated evolution of herbicide resistance has been cited as an example of genetic parallelism, wherein separate species or genetic lineages utilize the same genetic solution in response to selection. However, most studies that investigate the genetic basis of herbicide resistance examine the potential for changes in the protein targeted by the herbicide rather than considering genome-wide changes. We used a population genomics screen and targeted exome re-sequencing to uncover the potential genetic basis of glyphosate resistance in the common morning glory, Ipomoea purpurea, and to determine if genetic parallelism underlies the repeated evolution of resistance across replicate resistant populations. We found no evidence for changes in 5‐enolpyruvylshikimate‐3‐phosphate synthase ( EPSPS), glyphosate’s target protein, that were associated with resistance, and instead identified five genomic regions that showed evidence of selection. Within these regions, genes involved in herbicide detoxification—cytochrome P450s, ABC transporters, and glycosyltransferases—are enriched and exhibit signs of selective sweeps. One region under selection shows parallel changes across all assayed resistant populations whereas other regions exhibit signs of divergence. Thus, while it appears that the physiological mechanism of resistance in this species is likely the same among resistant populations, we find patterns of both similar and divergent selection across separate resistant populations at particular loci.

Author summary

Although there are many examples of herbicide resistance among natural populations of weeds, it is unknown if the same genetic mechanism underlies its repeated evolution across the landscape. Using a population genomics screen and exome re-sequencing, we examined the genetic basis of RoundUp resistance across populations of Ipomoea purpurea, a noxious agricultural weed. We identified multiple regions of the genome that exhibit signs of selection, and found genes involved in herbicide detoxification to be enriched within these regions. Interestingly, while one genomic region under selection exhibited a similar haplotype among resistant populations, other regions of the genome under selection exhibited signs of divergence. Overall, our results find evidence for both parallel and nonparallel genetic changes associated with resistance, suggesting there are more genetic avenues underlying the adaptation to herbicide than previously considered.