OpenLB
Open Library of Bioscience
Advanced Search
Proceedings of the National Academy of Sciences of the United States of America
04 18, 2023;120 (16): e2206808120.

Standing genetic variation fuels rapid evolution of herbicide resistance in blackgrass.

Sonja Kersten, Jiyang Chang, Christian D Huber, Yoav Voichek, Christa Lanz, Timo Hagmaier, Patricia Lang, Ulrich Lutz, Insa Hirschberg, Jens Lerchl, Aimone Porri, Yves Van de Peer, Karl Schmid, Detlef Weigel, Fernando A Rabanal
Author Information
  1. Sonja Kersten: Institute of Plant Breeding, Seed Science and Population Genetics, University of Hohenheim, 70599 Stuttgart, Germany.
  2. Jiyang Chang: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium. ORCID
  3. Christian D Huber: Department of Biology, The Eberly College of Science, Penn State University, State College, PA 16801. ORCID
  4. Yoav Voichek: Gregor Mendel Institute, Austrian Academy of Sciences, Vienna Bio Center, 1030 Vienna, Austria.
  5. Christa Lanz: Department of Molecular Biology, Max Planck Institute for Biology Tübingen, 72076 Tübingen, Germany.
  6. Timo Hagmaier: Department of Molecular Biology, Max Planck Institute for Biology Tübingen, 72076 Tübingen, Germany.
  7. Patricia Lang: Department of Molecular Biology, Max Planck Institute for Biology Tübingen, 72076 Tübingen, Germany. ORCID
  8. Ulrich Lutz: Department of Molecular Biology, Max Planck Institute for Biology Tübingen, 72076 Tübingen, Germany.
  9. Insa Hirschberg: Friedrich Miescher Laboratory 72076 Tübingen, Germany.
  10. Jens Lerchl: Agricultural Research Station, BASF SE, 67117 Limburgerhof, Germany.
  11. Aimone Porri: Agricultural Research Station, BASF SE, 67117 Limburgerhof, Germany.
  12. Yves Van de Peer: Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium.
  13. Karl Schmid: Institute of Plant Breeding, Seed Science and Population Genetics, University of Hohenheim, 70599 Stuttgart, Germany. ORCID
  14. Detlef Weigel: Department of Molecular Biology, Max Planck Institute for Biology Tübingen, 72076 Tübingen, Germany. ORCID
  15. Fernando A Rabanal: Department of Molecular Biology, Max Planck Institute for Biology Tübingen, 72076 Tübingen, Germany. ORCID
PMID: 37043536 DOI: 10.1073/pnas.2206808120

Abstract

Repeated herbicide applications in agricultural fields exert strong selection on weeds such as blackgrass (), 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 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 and , 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.

Keywords

Alopecurus myosuroides blackgrass herbicide resistance rapid adaptation

References

Mol Biol Evol. 2019 Mar 1;36(3):632-637 [PMID: 30517680]
Genetics. 2019 Feb;211(2):703-714 [PMID: 30514707]
Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W116-20 [PMID: 15980438]
Nat Commun. 2018 Jul 16;9(1):2750 [PMID: 30013096]
Proc Natl Acad Sci U S A. 2013 May 21;110(21):8615-20 [PMID: 23650353]
Pest Manag Sci. 2004 Jan;60(1):35-41 [PMID: 14727739]
Elife. 2022 Jan 17;11: [PMID: 35037853]
Pest Manag Sci. 2013 Feb;69(2):176-87 [PMID: 22614948]
Heredity (Edinb). 2010 Oct;105(4):394-400 [PMID: 20087387]
Mol Ecol. 2007 Aug;16(15):3161-72 [PMID: 17651194]
PLoS One. 2013 Oct 16;8(10):e75117 [PMID: 24146749]
New Phytol. 2020 Apr;226(2):301-305 [PMID: 31608445]
Nat Commun. 2020 Jun 18;11(1):3086 [PMID: 32555156]
PLoS Genet. 2018 Feb 12;14(2):e1007155 [PMID: 29432421]
Proc Natl Acad Sci U S A. 2010 Jan 19;107(3):1029-34 [PMID: 20018685]
Genome Biol. 2013;14(9):R103 [PMID: 24050704]
Nat Rev Genet. 2009 Mar;10(3):195-205 [PMID: 19204717]
Mol Biol Evol. 2013 Apr;30(4):772-80 [PMID: 23329690]
Mol Ecol. 2013 Jun;22(11):3179-90 [PMID: 23551379]
Proc Natl Acad Sci U S A. 2023 Apr 18;120(16):e2206808120 [PMID: 37043536]
Heredity (Edinb). 2005 Dec;95(6):485-92 [PMID: 16175194]
BMC Evol Biol. 2016 Nov 8;16(1):240 [PMID: 27825303]
Pest Manag Sci. 2014 Dec;70(12):1894-901 [PMID: 24497328]
Mol Biol Evol. 2004 May;21(5):884-92 [PMID: 15014166]
Ecol Evol. 2019 Jan 28;9(4):2220-2230 [PMID: 30847106]
Pest Manag Sci. 2014 Sep;70(9):1340-50 [PMID: 24338926]
PLoS Biol. 2012;10(9):e1001388 [PMID: 22984349]
Heredity (Edinb). 2002 Jan;88(1):8-13 [PMID: 11813100]
BMC Bioinformatics. 2011 Jun 18;12:246 [PMID: 21682921]
Bioinformatics. 2015 Oct 1;31(19):3210-2 [PMID: 26059717]
Nature. 2012 Nov 29;491(7426):711-6 [PMID: 23075845]
Nat Commun. 2017 Nov 30;8(1):1874 [PMID: 29187731]
Bioinformatics. 2019 Nov 1;35(21):4453-4455 [PMID: 31070718]
Nucleic Acids Res. 2011 Jul;39(Web Server issue):W475-8 [PMID: 21470960]
PeerJ. 2014 Jun 10;2:e431 [PMID: 24949246]
Evolution. 2015 Jan;69(1):271-8 [PMID: 25255698]
Genetics. 2017 Apr;205(4):1573-1586 [PMID: 28213477]
Trends Ecol Evol. 2013 Nov;28(11):659-69 [PMID: 24075201]
Genetics. 2005 Apr;169(4):2335-52 [PMID: 15716498]
Mol Ecol Resour. 2020 Sep;20(5):1228-1247 [PMID: 32306514]
Plant Genome. 2018 Mar;11(1): [PMID: 29505643]
Science. 1986 Jul 25;233(4762):478-81 [PMID: 17794571]
Bioinformatics. 2020 May 1;36(9):2896-2898 [PMID: 31971576]
Genome Biol. 2019 Dec 16;20(1):275 [PMID: 31843001]
BMC Bioinformatics. 2014 Nov 25;15:356 [PMID: 25420514]
Nat Sustain. 2020 Jan;3(1):63-71 [PMID: 31942455]
Plant Physiol. 2005 Mar;137(3):794-806 [PMID: 15579665]
Nat Methods. 2016 Dec;13(12):1050-1054 [PMID: 27749838]
Ann Bot. 2013 Apr;111(4):681-91 [PMID: 23393095]
Curr Protoc Bioinformatics. 2013;43:11.10.1-11.10.33 [PMID: 25431634]
Plants (Basel). 2019 Sep 19;8(9): [PMID: 31546893]
New Phytol. 2006;171(4):861-73 [PMID: 16918556]
Am J Bot. 2016 Feb;103(2):181-3 [PMID: 26823379]
Pest Manag Sci. 2021 Mar;77(3):1520-1529 [PMID: 33155426]
Genome Res. 2016 Mar;26(3):342-50 [PMID: 26848124]
Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10274-9 [PMID: 8816790]
Nat Ecol Evol. 2018 Mar;2(3):529-536 [PMID: 29434350]
Nature. 2005 Aug 11;436(7052):793-800 [PMID: 16100779]

Grants

  1. /Landesgraduiertenfoerderung des Landes Baden-Württemberg
  2. LT000819/2018-L/Human Frontier Science Program (HFSP)
  3. /Max-Planck-Gesellschaft (MPG)

MeSH Term

Herbicide Resistance
Poaceae
Mutation
Haplotypes
Europe
Herbicides
Acetyl-CoA Carboxylase

Chemicals

Herbicides
Acetyl-CoA Carboxylase
Journal Article Research Support, Non-U.S. Gov't

Word Cloud

Similar Articles

Cited By