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

• Published in: PLoS genetics Vol. 19; no. 1; p. e1010423
• Main Authors: Casey, Chloe, Köcher, Thomas, Champion, Clément, Jandrasits, Katharina, Mosiolek, Magdalena, Bonnot, Clémence, Dolan, Liam
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 06-01-2023; Public Library of Science (PLoS)
• Subjects: Biology and Life Sciences; Biosynthesis; Botanical research; Coenzyme Q; Coenzymes; Crop production; Electronics industry; Enzymes; Evolution; Gene amplification; Gene families; Genetic aspects; Herbicide resistance; Herbicides; Herbicides - pharmacology; International economic relations; Isoxaben; Life Sciences; Metabolism; Metabolites; Molecular modelling; Mutation; Physical Sciences; Physiological aspects; Plant Weeds - genetics; Polygenic inheritance; Proteins; Reactive Oxygen Species; Resistant mutant; Single nucleotide polymorphisms; Single-nucleotide polymorphism; Synthesis; Ubiquinone; Weeds; Austria; Thailand; Japan
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1010423

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 weakly resistant to thaxtomin A and cross resistant to isoxaben, suggesting that loss of MpRTN4IP1L function confers non-target site resistance. Mutants are also defective in thaxtomin A metabolism. We conclude that loss of MpRTN4IP1L function is a novel mechanism of non-target site herbicide resistance and propose that other mutations that increase ROS levels or decrease thaxtomin A metabolism could contribute to thaxtomin A resistance in the field.