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Reduced coenzyme Q synthesis confers non-target site resistance to the herbicide thaxtomin A

Chloe Casey, Thomas Köcher, Clément Champion, Katharina Jandrasits, Magdalena Mosiolek, Clémence Bonnot, View ORCID ProfileLiam Dolan
doi: https://doi.org/10.1101/2022.09.13.507736
Chloe Casey
1Department of Biology, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
2Gregor Mendel Institute, Dr Bohr-Gasse, Vienna, 1030, Austria
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Thomas Köcher
3Vienna Biocenter Core Facilities, Dr Bohr-Gasse, Vienna, 1030, Austria
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Clément Champion
1Department of Biology, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
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Katharina Jandrasits
2Gregor Mendel Institute, Dr Bohr-Gasse, Vienna, 1030, Austria
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Magdalena Mosiolek
2Gregor Mendel Institute, Dr Bohr-Gasse, Vienna, 1030, Austria
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Clémence Bonnot
1Department of Biology, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
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Liam Dolan
1Department of Biology, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom
2Gregor Mendel Institute, Dr Bohr-Gasse, Vienna, 1030, Austria
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  • ORCID record for Liam Dolan
  • For correspondence: liam.dolan@gmi.oeaw.ac.at
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ABSTRACT

Herbicide resistance in weeds is a growing threat to global crop production. Non-target site resistance is problematic because a single resistance allele can confer tolerance to many herbicides (cross resistance), and it is often a polygenic trait so it can be difficult to identify the molecular mechanisms involved. Most characterized molecular mechanisms of non-target site resistance are caused by gain-of-function mutations in genes from a few key gene families – the mechanisms of resistance caused by loss-of-function mutations remain unclear. In this study, we first show that the mechanism of non-target site resistance to the herbicide thaxtomin A conferred by loss-of-function of the gene PAM16 is conserved in Marchantia polymorpha, validating its use as a model species with which to study non-target site resistance. To identify mechanisms of non-target site resistance caused by loss-of-function mutations, we generated 107 UV-B mutagenized M. polymorpha spores and screened for resistance to the herbicide thaxtomin A. We isolated 13 thaxtomin A-resistant mutants and found that 3 mutants carried candidate resistance-conferring SNPs in the MpRTN4IP1L gene. Mprtn4ip1l mutants are defective in coenzyme Q biosynthesis and accumulate higher levels of reactive oxygen species (ROS) than wild-type plants. Mutants are also defective in thaxtomin A metabolism, consistent with the hypothesis that loss of MpRTN4IP1L function confers non-target site resistance. We conclude that loss of MpRTN4IP1L function is a novel mechanism of non-target site herbicide resistance, and propose that other mutations which increase ROS levels or decrease thaxtomin A metabolism could confer thaxtomin A resistance in the field.

AUTHOR SUMMARY Modern agriculture relies on herbicides to control weed populations. However, herbicide resistance in weeds threatens the efficacy of herbicides and global crop production, similar to how antibiotic resistance poses a global health threat. Understanding the molecular mechanisms behind herbicide resistance helps to prevent resistance from evolving and to better manage herbicide resistant weeds in the field. Here, we use a forward genetic approach in the model species Marchantia polymorpha to discover novel mechanisms of herbicide resistance. We report the discovery of a novel mechanism of herbicide resistance caused by loss-of-function mutations in the MpRTN4IP1L gene. We find that Mprtn4ip1l mutants are resistant to the herbicides thaxtomin A and isoxaben, accumulate higher levels of reactive oxygen species than wild type plants, and are defective in thaxtomin A metabolism. We predict that loss-of-function mutations or treatments that increase reactive oxygen species production could contribute to thaxtomin A tolerance.

Competing Interest Statement

I have read the journal's policy and the authors of this manuscript have the following competing interests: L.D. and C.C. are co-founders of MoA Technology Ltd.

Footnotes

  • Competing interests: L. D. and C. C. are co-founders of MoA Technology Ltd.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted September 15, 2022.
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Reduced coenzyme Q synthesis confers non-target site resistance to the herbicide thaxtomin A
Chloe Casey, Thomas Köcher, Clément Champion, Katharina Jandrasits, Magdalena Mosiolek, Clémence Bonnot, Liam Dolan
bioRxiv 2022.09.13.507736; doi: https://doi.org/10.1101/2022.09.13.507736
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Reduced coenzyme Q synthesis confers non-target site resistance to the herbicide thaxtomin A
Chloe Casey, Thomas Köcher, Clément Champion, Katharina Jandrasits, Magdalena Mosiolek, Clémence Bonnot, Liam Dolan
bioRxiv 2022.09.13.507736; doi: https://doi.org/10.1101/2022.09.13.507736

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