Standing genetic variation fuels rapid evolution of herbicide resistance in blackgrass

Abstract

DATA, MATERIALS, AND SOFTWARE AVAILABILITY : Raw data including PacBio CLR and Iso-seq reads, Illumina PCR-free, Hi-C, and RNA-seq reads can be accessed in the European Nucleotide Archive (ENA; https://www.ebi.ac.uk/ena/browser/ home) under project accession number PRJEB49257 (78), assembly accession CASDCE010000000 (79). Raw ddRAD-seq data for the population study, and PacBio CCS q20 reads can be downloaded from the ENA project accession number PRJEB49288 (80). Annotation files for the genome assembly, the SNP matrix for the ddRAD-seq experiment, and the fasta files with the haplotypes of ACCase and ALS can be found at https://doi.org/10.5281/zenodo.7634530 (81). Scripts and experimental protocols to reproduce the analyses in this study are deposited in the GitHub repository of this study (https://github.com/SonjaKersten/ Herbicide_resistance_evolution_in_blackgrass_2022) (82).Repeated herbicide applications in agricultural fields exert strong selection on weeds such as blackgrass (Alopecurus myosuroides), which is a major threat for temperate climate cereal crops. This inadvertent selection pressure provides an opportunity for investigating the underlying genetic mechanisms and evolutionary processes of rapid adaptation, which can occur both through mutations in the direct targets of herbicides and through changes in other, often metabolic, pathways, known as non-target-site resistance. How much target-site resistance (TSR) relies on de novo mutations vs. standing variation is important for developing strategies to manage herbicide resistance. We first generated a chromosome-level reference genome for A. myosuroides for population genomic studies of herbicide resistance and genome-wide diversity across Europe in this species. Next, through empirical data in the form of highly accurate long-read amplicons of alleles encoding acetyl-CoA carboxylase (ACCase) and acetolactate synthase (ALS) variants, we showed that most populations with resistance due to TSR mutations—23 out of 27 and six out of nine populations for ACCase and ALS, respectively—contained at least two TSR haplotypes, indicating that soft sweeps are the norm. Finally, through forward-in-time simulations, we inferred that TSR is likely to mainly result from standing genetic variation, with only a minor role for de novo mutations.The Landesgraduiertenförderung (State Graduate Scholarship, LGFG) of the State of Baden-Württemberg; a Human Frontiers Science Program Long-Term Fellowship, BASF and the Max Planck Society.https://www.pnas.org/am2024Biochemistry, Genetics and Microbiology (BGM)SDG-15:Life on lan

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