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Transcriptome changes in chlorsulfuron-treated plants are caused by acetolactate synthase inhibition and not induction of a herbicide detoxification system in Marchantia polymorpha

Alexandra Casey, Thomas Köcher, Samuel Caygill, Clément Champion, Clémence Bonnot, View ORCID ProfileLiam Dolan
doi: https://doi.org/10.1101/2022.08.31.505973
Alexandra Casey
1Department of Biology, University of Oxford, Oxford OX1 3RB, United Kingdom
2Gregor Mendel Institute, Dr. Bohr-Gasse, 3, Vienna 1030, Austria
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Thomas Köcher
3Vienna BioCenter Core Facilities GmbH, Dr. Bohr-Gasse 3, Vienna 1030, Austria
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Samuel Caygill
1Department of Biology, University of Oxford, Oxford OX1 3RB, United Kingdom
2Gregor Mendel Institute, Dr. Bohr-Gasse, 3, Vienna 1030, Austria
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Clément Champion
1Department of Biology, University of Oxford, Oxford OX1 3RB, United Kingdom
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Clémence Bonnot
1Department of Biology, University of Oxford, Oxford OX1 3RB, United Kingdom
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Liam Dolan
1Department of Biology, University of Oxford, Oxford OX1 3RB, United Kingdom
2Gregor Mendel Institute, Dr. Bohr-Gasse, 3, 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

A sensing mechanism in mammals perceives xenobiotics and induces the transcription of genes encoding proteins that detoxify these molecules. However, it is unclear if plants sense xenobiotics, and activate an analogous signalling system leading to their detoxification. Using the liverwort Marchantia polymorpha, we tested the hypothesis that there is a sensing system in plants that perceives herbicides resulting in the increased transcription of genes encoding proteins that detoxify these herbicides. Consistent with the hypothesis, we show that chlorsulfuron-treatment induces changes in the M. polymorpha transcriptome. However, these transcriptome changes do not occur in chlorsulfuron (CS)-treated target site resistant mutants, where the gene encoding the target carries a mutation that confers resistance to chlorsulfuron. Instead, we show that inactivation of the chlorsulfuron target, acetolactate synthase (ALS) (also known as acetohydroxyacid synthase (AHAS)), is required for the transcriptome response. These data are consistent with the changes in the transcriptome of chlorsulfuron-treated plants being caused by disrupted amino acid synthesis and metabolism resulting from acetolactate synthase inhibition. These conclusions suggest that chlorsulfuron is not sensed in M. polymorpha leading to induce a detoxification system.

Author Summary Herbicide use is increasing throughout the world, however we know little about how plants respond to herbicide treatment and regulate their metabolism. Some plants have evolved resistance to herbicides such as chlorsulfuron by increasing the detoxification of the herbicide compared to sensitive plants. It has been suggested that plants can directly sense the herbicide chemical which activates a detoxification response, in a similar way to the detoxification of foreign chemicals in mammalian cells. The liverwort Marchantia polymorpha is an excellent system to study plant herbicide responses due to its short generation time, ease of propagation and low genetic redundancy. We show that chlorsulfuron treatment alters the expression of many genes in M. polymorpha, however plants with a resistance-conferring mutation in the molecular target of chlorsulfuron do not show any changes in gene expression in response to chlorsulfuron treatment. This result indicates that transcriptome changes caused by chlorsulfuron depend on the inhibition of the target by chlorsulfuron. This suggests that plants do not sense chlorsulfuron and activate a detoxification system. This finding has implications for herbicide use and discovery.

Competing Interest Statement

The authors have declared no competing interest.

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 01, 2022.
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Transcriptome changes in chlorsulfuron-treated plants are caused by acetolactate synthase inhibition and not induction of a herbicide detoxification system in Marchantia polymorpha
Alexandra Casey, Thomas Köcher, Samuel Caygill, Clément Champion, Clémence Bonnot, Liam Dolan
bioRxiv 2022.08.31.505973; doi: https://doi.org/10.1101/2022.08.31.505973
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Transcriptome changes in chlorsulfuron-treated plants are caused by acetolactate synthase inhibition and not induction of a herbicide detoxification system in Marchantia polymorpha
Alexandra Casey, Thomas Köcher, Samuel Caygill, Clément Champion, Clémence Bonnot, Liam Dolan
bioRxiv 2022.08.31.505973; doi: https://doi.org/10.1101/2022.08.31.505973

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