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Cytochrome P450 CYP709C56 metabolizing mesosulfuron-methyl confers herbicide resistance in Alopecurus aequalis

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Abstract

Multiple herbicide resistance in diverse weed species endowed by enhanced herbicide detoxification or degradation is rapidly growing into a great threat to herbicide sustainability and global food safety. Although metabolic resistance is frequently documented in the economically damaging arable weed species shortawn foxtail (Alopecurus aequalis Sobol.), relevant molecular knowledge has been lacking. Previously, we identified a field population of A. aequalis (R) that had evolved metabolic resistance to the commonly used acetolactate synthase (ALS)-inhibiting herbicide mesosulfuron-methyl. RNA sequencing was used to discover potential herbicide metabolism-related genes, and four cytochrome P450s (CYP709C56, CYP71R18, CYP94C117, and CYP94E14) were identified with higher expressions in the R vs. susceptible (S) plants. Here the full-length P450 complementary DNA transcripts were each cloned with identical sequences between the S and R plants. Transgenic Arabidopsis overexpressing CYP709C56 became resistant to the sulfonylurea herbicide mesosulfuron-methyl and the triazolo-pyrimidine herbicide pyroxsulam. This resistance profile generally but does not completely in accordance with what is evident in the R A. aequalis. Transgenic lines exhibited enhanced capacity for detoxifying mesosulfuron-methyl into O-demethylated metabolite, which is in line with the detection of O-demethylated herbicide metabolite in vitro in transformed yeast. Structural modeling predicted that mesosulfuron-methyl binds to CYP709C56 involving amino acid residues Thr-328, Thr-500, Asn-129, Gln-392, Phe-238, and Phe-242 for achieving O-demethylation. Constitutive expression of CYP709C56 was highly correlated with the metabolic mesosulfuron-methyl resistance in A. aequalis. These results indicate that CYP709C56 degrades mesosulfuron-methyl and its up-regulated expression in A. aequalis confers resistance to mesosulfuron-methyl.

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Acknowledgements

We would like to thank Dr. David Nelson (Department of Microbiology, Immunology and Biochemistry, University of Tennessee) for naming the P450 genes, Dr. Hailong An (State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University) for providing the expression vector pPZP211, and Dr. Xingqi Guo (State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University) for providing Arabidopsis seeds (ecotype Columbia-0).

Funding

This work was funded by grants from the National Natural Science Foundation of China (No. 32102237 and 31772181), the Anhui Provincial Natural Science Foundation (No. 2108085QC115), and the Talent Research Project of Anhui Agricultural University (No. rc342004).

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  1. Anhui Province Key Laboratory of Integrated Pest Management On Crops, School of Plant Protection, Anhui Agricultural University, Hefei, 230036, China

    Ning Zhao

  2. College of Plant Protection, Shandong Agricultural University, Tai’an, 271018, China

    Ning Zhao, Yanyan Yan, Weitang Liu & Jinxin Wang

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NZ, WL, and JW designed the study. NZ and YY performed the experimental works and statistical analyses. NZ, YY, WL, and JW drafted and critically revised the manuscript.

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Zhao, N., Yan, Y., Liu, W. et al. Cytochrome P450 CYP709C56 metabolizing mesosulfuron-methyl confers herbicide resistance in Alopecurus aequalis. Cell. Mol. Life Sci. 79, 205 (2022). https://doi.org/10.1007/s00018-022-04171-y

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