Inter-chromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

Gupta, Sonal; Harkess, Alex; Soble, Anah; Etten, Megan Van; Leebens‐Mack, James H.; Baucom, Regina S.

doi:10.1101/2021.04.04.438381

Cited by 12 publications

(13 citation statements)

References 118 publications

(167 reference statements)

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“…We find particularly extreme signed LD between TSR mutations and alleles on different chromosomes. LD between resistance alleles on different chromosomes has been interpreted as epistasis ( Gupta et al, 2021 ), but LD between alleles that are not physically linked may also result from the effects of additive alleles with correlated responses to selection (e.g. the stacking of resistance alleles; Busi et al, 2013 ).…”

Section: Discussionmentioning

confidence: 99%

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

Kreiner

Sandler

Stern

et al. 2022

eLife

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Causal mutations and their frequency in agricultural fields are well-characterized for herbicide resistance. However, we still lack understanding of their evolutionary history: the extent of parallelism in the origins of target-site resistance (TSR), how long these mutations persist, how quickly they spread, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of common waterhemp (Amaranthus tuberculatus), which we show to have undergone a massive expansion over the past century, with a contemporary effective population size (Ne) estimate of 8x107. We found variation at seven characterized TSR loci, two of which had multiple amino acid substitutions, and three of which were common. These three common resistance variants show parallelism in their mutational origins, with gene flow having shaped their distribution across the landscape. Allele age estimates supported a strong role of adaptation from de novo mutations, with a median allele age of 30 suggesting that most resistance alleles arose soon after the onset of herbicide use. However, resistant lineages varied in both their age and evidence for selection over two different timescales, implying considerable heterogeneity in the forces that govern their persistence. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We report a signal of extended haplotype competition between two common TSR alleles, and extreme linkage with genome-wide alleles with known functions in resistance adaptation. Together, this work reveals a remarkable example of spatial parallel evolution in a metapopulation, with important implications for the management of herbicide resistance.

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Section: Discussionmentioning

confidence: 99%

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

Kreiner

Sandler

Stern

et al. 2022

eLife

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“…We aligned single‐end (1 × 52nt) adapter‐trimmed Illumina RNA‐seq reads separately for all samples to the Ipomoea purpurea version 2.0 genome (Gupta et al. 2021) using the splice aware STAR aligner in its basic two‐pass mode (Dobin et al. 2013).…”

Section: Methodsmentioning

confidence: 99%

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed

et al. 2021

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Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (Ipomoea purpurea) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide to the expression changes that evolve in response to artificial selection for herbicide resistance. We identify a number of genes that show plastic and evolved responses to herbicide and find that for the majority of genes with both plastic and evolved responses, plastic responses appear to be adaptive. We also find that selection for herbicide response increases gene expression plasticity. Overall, these results show the importance of adaptive plasticity for herbicide resistance in a common weed and that expression changes in response to strong environmental change can be adaptive.

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“…We aligned single-end (1x52nt) adapter-trimmed Illumina RNA-seq reads separately for all samples to the Ipomoea purpurea v 2.0 genome [41] using the splice aware STAR aligner in its basic two-pass mode [42]. Genome annotation for STAR was generated using GATK's CreateSequenceDictionary (v4, [43]), samtools' v1.3 faidx function [44] and STAR's genomeGenerate option together with an Augustus-derived GFF3 annotation [45] provided with the v.2.0 assembly.…”

Section: Transcriptome Data Generationmentioning

confidence: 99%

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed

Josephs

Etten

Harkess

et al. 2020

Preprint

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Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (Ipomoea purpurea) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide spray to the expression changes that evolve in response to artificial selection for herbicide resistance. We identify a number of genes that show plastic and evolved responses to herbicide and find that for the majority of genes with both plastic and evolved responses, plastic responses appear to be adaptive. We also find that selection for herbicide response increases gene expression plasticity. Overall, these results show the importance of adaptive plasticity for herbicide resistance in a common weed and that expression changes in response to strong environmental change can be adaptive.

show abstract

Inter-chromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

Cited by 12 publications

References 118 publications

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

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

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed

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