The blackgrass genome reveals patterns of non‐parallel evolution of polygenic herbicide resistance

Cai, Lichun; Comont, David; MacGregor, Dana R.; Lowe, C. C.; Beffa, Roland; Neve, Paul; Saski, Christopher

doi:10.1111/nph.18655

Cited by 19 publications

(54 citation statements)

References 105 publications

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“…While there is an increasing appreciation for the role of nontarget‐site mechanisms underlying herbicide resistance in agricultural weeds (Délye et al ., 2011; Ghanizadeh & Harrington, 2017; Jugulam & Shyam, 2019; Gaines et al ., 2020), there are strikingly few comprehensive whole‐genome assays of resistant weeds (Kreiner et al ., 2021b; Van Etten et al ., 2020; Cai et al ., 2022) suggesting that many of the genes responsible for the NTSR response are rarely captured. Our study using a sequenced and assembled genome, whole‐genome resequencing of natural populations, and a gene expression survey offers a unique and a more comprehensive opportunity to identify loci associated with NTSR compared with previous assays and to further investigate the evolutionary forces that underlie the maintenance of resistance alleles in natural populations.…”

Section: Discussionmentioning

confidence: 99%

Interchromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

et al. 2023

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Summary The adaptation of weeds to herbicide is both a significant problem in agriculture and a model of rapid adaptation. However, significant gaps remain in our knowledge of resistance controlled by many loci and the evolutionary factors that influence the maintenance of resistance. Here, using herbicide‐resistant populations of the common morning glory (Ipomoea purpurea), we perform a multilevel analysis of the genome and transcriptome to uncover putative loci involved in nontarget‐site herbicide resistance (NTSR) and to examine evolutionary forces underlying the maintenance of resistance in natural populations. We found loci involved in herbicide detoxification and stress sensing to be under selection and confirmed that detoxification is responsible for glyphosate (RoundUp) resistance using a functional assay. We identified interchromosomal linkage disequilibrium (ILD) among loci under selection reflecting either historical processes or additive effects leading to the resistance phenotype. We further identified potential fitness cost loci that were strongly linked to resistance alleles, indicating the role of genetic hitchhiking in maintaining the cost. Overall, our work suggests that NTSR glyphosate resistance in I. purpurea is conferred by multiple genes which are potentially maintained through generations via ILD, and that the fitness cost associated with resistance in this species is likely a by‐product of genetic hitchhiking.

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Section: Discussionmentioning

confidence: 99%

Interchromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

et al. 2023

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“…Nevertheless, many studies do not proceed to functionally validate these candidate genes and the actual cause for resistance remains undetermined. In order to validate the function of the computationally predicted genes, the full‐length cDNA sequences of three tau and one phi class GST were obtained and later also identified in the recently assembled black‐grass genome 35 . The three tau class GSTs ALOMY3G13667, ALOMY3G13668, and ALOMY3G13670 had a high sequence identity of >80%.…”

Section: Discussionmentioning

confidence: 99%

“…The three tau class GSTs ALOMY3G13667, ALOMY3G13668, and ALOMY3G13670 had a high sequence identity of >80%. Interestingly, those three upregulated GSTs were located next to each other on the same chromosome, only separated by a pseudogene (ALOMY3G13669 35 ). The sequence similarity and their location in the genome suggests that these genes may be coregulated in the same signaling pathway, as previously described in eukaryotic organisms 42 …”

Section: Discussionmentioning

confidence: 99%

“…2.1 Characterization of the cDNA sequences of four candidate GSTs After an RNA-Seq approach, 31 four candidate GSTs (GST1, GST2, GST4 and GST5), which are differentially expressed in flufenacet resistant black-grass, were chosen for cloning and thus a 3 0 and 5' RACE PCR technique was used. Once the black-grass genome 35 was available, those candidate genes were identified as ALO-MY3G13667 (GST1), ALOMY3G13668 (GST2), ALOMY3G13670 (GST8; derived by the realignment of the RNA-Seq reads against the black-grass genome using STAR aligner; version 2.6.1d) and ALOMY5G35766 (GST4 and GST5 contigs correspond to the same gene), respectively. Prior to genome availability, the total RNA of pooled untreated samples of the flufenacet resistant Kehdingen2 population 16 was extracted using the RNeasy Plant Mini Kit (Qiagen, Hilden, Germany) in order to obtain the full-length sequences of the candidate GSTs.…”

Section: Methodsmentioning

confidence: 99%

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Recombinant glutathione transferases from flufenacet‐resistant black‐grass (Alopecurus myosuroides Huds.) form different flufenacet metabolites and differ in their interaction with pre‐ and post‐emergence herbicides

Parcharidou

Dücker

Zöllner

et al. 2023

Pest Management Science

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BACKGROUND: Black-grass (Alopecurus myosuroides Huds.) has become a problematic weed in cereals in Europe. Besides resistance to post-emergent herbicides becoming increasingly widespread, enhanced metabolism of inhibitors of the synthesis of very-long-chain fatty acids (VLCFAs), such as flufenacet, is evolving. Yet, cross-resistance patterns and evolution of this resistance remains poorly understood. RESULTS:The cDNA sequences of five glutathione transferases (GSTs) upregulated in flufenacet resistant black-grass were identified and used for recombinant protein expression. Moderate to slow detoxification of flufenacet was verified for all candidate GSTs expressed in E. coli, and the most active protein produced flufenacet-alcohol instead of a glutathione conjugate, in the presence of reduced glutathione (GSH). Moreover, cross-resistance to other VLCFA-inhibitors e.g., acetochlor and pyroxasulfone and the ACCase inhibitor fenoxaprop was verified in vitro. Various other herbicides of different modes of action including VLCFA-inhibitors were not detoxified by the candidate GSTs.CONCLUSIONS: As several in planta upregulated GSTs detoxified flufenacet in vitro, the shift in sensitivity observed in blackgrass populations, is likely a result of an additive effect. The polygenic character and the relatively low turnover rate of the individual GSTs may explain the slow evolution of flufenacet resistance. In addition, flufenacet resistance was accompanied by cross-resistance with some, but not all, herbicides of the same mode of action, and furthermore to the ACCase inhibitor fenoxaprop-ethyl. Hence, not only the rotation of herbicide modes of action, but also of individual active ingredients is important for resistance management.

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“…NTSR refers to processes that degrade or physically prevent the active ingredient from reaching its target, such as enhanced metabolization, decreased absorption or translocation and sequestration (Devine and Shukla, 2000; Heap, 2014b). NTSR typically involves multiple genes (Cai et al ., 2022; Franco‐Ortega et al ., 2021; Kreiner et al ., 2021; Van Etten et al ., 2020), resistance is often quantitative and several candidate gene families contribute to it, including cytochromes P450 monooxygenases, glycosyltransferases or glutathione S‐transferases (reviewed in Gaines et al ., 2020). TSR has more qualitative effects, it is usually characterized by resistance to high levels of the herbicide, and it can often be traced back to large‐effect gene mutations that change individual amino acids in herbicide target enzymes.…”

Section: Introductionmentioning

confidence: 99%

Deep haplotype analyses of target‐site resistance locus ACCase in blackgrass enabled by pool‐based amplicon sequencing

Kersten

Rabanal

Herrmann³

et al. 2023

Plant Biotechnology Journal

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Summary Rapid adaptation of weeds to herbicide applications in agriculture through resistance development is a widespread phenomenon. In particular, the grass Alopecurus myosuroides is an extremely problematic weed in cereal crops with the potential to manifest resistance in only a few generations. Target‐site resistances (TSRs), with their strong phenotypic response, play an important role in this rapid adaptive response. Recently, using PacBio's long‐read amplicon sequencing technology in hundreds of individuals, we were able to decipher the genomic context in which TSR mutations occur. However, sequencing individual amplicons are costly and time‐consuming, thus impractical to implement for other resistance loci or applications. Alternatively, pool‐based approaches overcome these limitations and provide reliable allele frequencies, although at the expense of not preserving haplotype information. In this proof‐of‐concept study, we sequenced with PacBio High Fidelity (HiFi) reads long‐range amplicons (13.2 kb), encompassing the entire ACCase gene in pools of over 100 individuals, and resolved them into haplotypes using the clustering algorithm PacBio amplicon analysis (pbaa), a new application for pools in plants and other organisms. From these amplicon pools, we were able to recover most haplotypes from previously sequenced individuals of the same population. In addition, we analysed new pools from a Germany‐wide collection of A. myosuroides populations and found that TSR mutations originating from soft sweeps of independent origin were common. Forward‐in‐time simulations indicate that TSR haplotypes will persist for decades even at relatively low frequencies and without selection, highlighting the importance of accurate measurement of TSR haplotype prevalence for weed management.

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The blackgrass genome reveals patterns of non‐parallel evolution of polygenic herbicide resistance

Abstract: The output can be accessed at: https://repository.rothamsted.ac.uk/item/98769/theblackgrass-genome-reveals-patterns-of-non-parallel-evolution-of-polygenic-herbicideresistance.

Cited by 19 publications

References 105 publications

Interchromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

Interchromosomal linkage disequilibrium and linked fitness cost loci associated with selection for herbicide resistance

Recombinant glutathione transferases from flufenacet‐resistant black‐grass (Alopecurus myosuroides Huds.) form different flufenacet metabolites and differ in their interaction with pre‐ and post‐emergence herbicides

Deep haplotype analyses of target‐site resistance locus ACCase in blackgrass enabled by pool‐based amplicon sequencing

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