The genetic architecture and population genomic signatures of glyphosate resistance in Amaranthus tuberculatus

Abstract

Much of what we know about the genetic basis of herbicide resistance has come from detailed investigations of monogenic adaptation at known target-sites, despite the increasingly recognized importance of polygenic resistance. Little work has been done to characterize the broader genomic basis of herbicide resistance, including the number and distribution of genes involved, their effect sizes, allele frequencies and signatures of selection. In this work, we implemented genome-wide association (GWA) and population genomic approaches to examine the genetic architecture of glyphosate (Round-up) resistance in the problematic agricultural weed Amaranthus tuberculatus.A GWA was able to correctly identify the known target-gene but statistically controlling for two causal target-site mechanisms revealed an additional 250 genes across all 16 chromosomes associated with non-target-site resistance (NTSR). The encoded proteins had functions that have been linked to NTSR, the most significant of which is response to chemicals, but also showed pleiotropic roles in reproduction and growth.Compared to an empirical null that accounts for complex population structure, the architecture of NTSR was enriched for large effect sizes and low allele frequencies, suggesting the role of pleiotropic constraints on its evolution. The enrichment of rare alleles also suggested that the genetic architecture of NTSR may be population-specific and heterogeneous across the range. Despite their rarity, we found signals of recent positive selection on NTSR-alleles by both window-and haplotype-based statistics, and an enrichment of amino acid changing variants. In our samples, genome-wide single nucleotide polymorphisms explain a comparable amount of the total variation in glyphosate resistance to monogenic mechanisms, even in a collection of individuals where 80% of resistant individuals have large-effect TSR mutations, indicating an underappreciated polygenic contribution to the evolution of herbicide resistance in weed populations.

Repeated origins, widespread gene flow, and allelic interactions of target-site herbicide resistance mutations

“…In conclusion, adaptation to herbicides and the emergence of well-characterized target-site resistance mutations provide a powerful system for characterizing rapid and repeated evolution in plant populations, as well as the consequences of extreme selection on local and genome-wide patterns of diversity. Studies of herbicide resistance evolution have highlighted how extreme selection can modify life-history and plant mating systems ( Kuester et al, 2017 ; Van Etten et al, 2020 ) and vice versa ( Kreiner et al, 2018 ), as well as the role of small- versus large-effect mutations (or monogenic versus polygenic adaptation) ( Kreiner et al, 2021 ; reviewed in Délye, 2013 ; Powles and Yu, 2010 ), costs of adaptation under fluctuating environments ( Vila-Aiub, 2019 ; Vila-Aiub et al, 2009 ), and mutational repeatability (e.g. Heap, 2014 ; Menchari et al, 2006 ) (see Baucom, 2019 ).…”

The effect of recent habitat change on genetic diversity at putatively adaptive and neutral loci in Primula veris in semi-natural grasslands

“…In contrast, such validations are common practice in genome wide association studies (e.g. Kreiner, Tranel, Weigel, Stinchcombe, & Wright, 2021;Tibbs Cortes, Zhang, & Yu, 2021) which, together with our results, might call for their wider application in landscape genomic analyses.…”

Evidence of hard-selective sweeps suggest independent adaptation to insecticides in Colorado potato beetle (Coleoptera:Chrysomelidae) populations

“…Classical expectations for single locus adaptive mutations have been challenged by growing evidence of polygenic resistance traits (Pélissié et al, 2022; Kreiner et al, 2021; Wybouw et al, 2019). However, there are well documented examples of both single locus and polygenic resistance evolution (ffrench-Constant 2013) and the relative importance of these selective regimes might relate to fundamental population genetic properties (Barton 2010; Hermisson and Pennings 2005).…”