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Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China

SIMPLE SUMMARY: Digitaria sanguinalis is considered one of the most malignant grass weeds worldwide and is widely distributed in Chinese maize fields. In this study, we explored the mechanism of metabolic resistance via cytochrome P450s of the LJ-01 population of Digitaria sanguinalis, which evolved...

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Autores principales: Wang, Xumiao, Hu, Wei, Li, Yuxi, Jiang, Minghao, Zhao, Ning, Cao, Haiqun, Liao, Min
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10525941/
https://www.ncbi.nlm.nih.gov/pubmed/37759591
http://dx.doi.org/10.3390/biology12091192
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author Wang, Xumiao
Hu, Wei
Li, Yuxi
Jiang, Minghao
Zhao, Ning
Cao, Haiqun
Liao, Min
author_facet Wang, Xumiao
Hu, Wei
Li, Yuxi
Jiang, Minghao
Zhao, Ning
Cao, Haiqun
Liao, Min
author_sort Wang, Xumiao
collection PubMed
description SIMPLE SUMMARY: Digitaria sanguinalis is considered one of the most malignant grass weeds worldwide and is widely distributed in Chinese maize fields. In this study, we explored the mechanism of metabolic resistance via cytochrome P450s of the LJ-01 population of Digitaria sanguinalis, which evolved high-level resistance to the ALS inhibitor nicosulfuron and evolved cross- and multiple resistance to thifensulfuron-methyl and pyrazosulfuron-ethyl, as well as the PS II inhibitors bromoxynil octanoate and atrazine. This study provides scientific and theoretical guidance for the control of resistant populations in D. sanguinalis. ABSTRACT: Large crabgrass (Digitaria sanguinalis (L.) Scop.) is one of the major malignant grass weeds in Chinese maize (Zea mays L.) fields, and it has recently developed resistance to the acetolactate synthase (ALS)-inhibiting herbicide nicosulfuron. This study focused on a suspected nicosulfuron-resistant (R) population (LJ-01) of D. sanguinalis, collected from Lujiang County in Anhui Province, China, to explore the resistance level and potential resistance mechanism. Whole-plant dose–response testing confirmed that the LJ-01 population evolved a high level of resistance to nicosulfuron (11.5-fold) compared to the susceptible (S) population, DY-02. The ALS gene sequencing and relative expression assay of the R plants indicated that target gene mutation and overexpression were not responsible for the resistance phenotype. However, pretreatment with malathion, a known cytochrome P450 monooxygenase (P450) inhibitor, alleviated the resistance of the R population to nicosulfuron by approximately 36%. High-performance liquid chromatography (HPLC) analysis revealed that the R plants metabolized nicosulfuron faster than the S plants. Moreover, cross-resistance testing suggested that the R population exhibited low levels of resistance to thifensulfuron-methyl and pyrazosulfuron-ethyl, but it remained susceptible to rimsulfuron. Multiple resistance patterns showed that the R population evolved low resistance to the photosystem inhibitors bromoxynil octanoate and atrazine and sensitivity to the acetyl-CoA carboxylase (ACCase) inhibitor cyhalofop-butyl and the 4-hydroxyphenylpyruvate dioxygenase (HPPD) inhibitors tembotrione, mesotrione, and topramezone. This study reports, for the first time, the simultaneous resistance to ALS and different photosystem inhibitors in D. sanguinalis. The nicosulfuron resistance observed in the R population could primarily be attributed to an enhanced metabolism involving P450 enzymes.
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spelling pubmed-105259412023-09-28 Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China Wang, Xumiao Hu, Wei Li, Yuxi Jiang, Minghao Zhao, Ning Cao, Haiqun Liao, Min Biology (Basel) Article SIMPLE SUMMARY: Digitaria sanguinalis is considered one of the most malignant grass weeds worldwide and is widely distributed in Chinese maize fields. In this study, we explored the mechanism of metabolic resistance via cytochrome P450s of the LJ-01 population of Digitaria sanguinalis, which evolved high-level resistance to the ALS inhibitor nicosulfuron and evolved cross- and multiple resistance to thifensulfuron-methyl and pyrazosulfuron-ethyl, as well as the PS II inhibitors bromoxynil octanoate and atrazine. This study provides scientific and theoretical guidance for the control of resistant populations in D. sanguinalis. ABSTRACT: Large crabgrass (Digitaria sanguinalis (L.) Scop.) is one of the major malignant grass weeds in Chinese maize (Zea mays L.) fields, and it has recently developed resistance to the acetolactate synthase (ALS)-inhibiting herbicide nicosulfuron. This study focused on a suspected nicosulfuron-resistant (R) population (LJ-01) of D. sanguinalis, collected from Lujiang County in Anhui Province, China, to explore the resistance level and potential resistance mechanism. Whole-plant dose–response testing confirmed that the LJ-01 population evolved a high level of resistance to nicosulfuron (11.5-fold) compared to the susceptible (S) population, DY-02. The ALS gene sequencing and relative expression assay of the R plants indicated that target gene mutation and overexpression were not responsible for the resistance phenotype. However, pretreatment with malathion, a known cytochrome P450 monooxygenase (P450) inhibitor, alleviated the resistance of the R population to nicosulfuron by approximately 36%. High-performance liquid chromatography (HPLC) analysis revealed that the R plants metabolized nicosulfuron faster than the S plants. Moreover, cross-resistance testing suggested that the R population exhibited low levels of resistance to thifensulfuron-methyl and pyrazosulfuron-ethyl, but it remained susceptible to rimsulfuron. Multiple resistance patterns showed that the R population evolved low resistance to the photosystem inhibitors bromoxynil octanoate and atrazine and sensitivity to the acetyl-CoA carboxylase (ACCase) inhibitor cyhalofop-butyl and the 4-hydroxyphenylpyruvate dioxygenase (HPPD) inhibitors tembotrione, mesotrione, and topramezone. This study reports, for the first time, the simultaneous resistance to ALS and different photosystem inhibitors in D. sanguinalis. The nicosulfuron resistance observed in the R population could primarily be attributed to an enhanced metabolism involving P450 enzymes. MDPI 2023-08-31 /pmc/articles/PMC10525941/ /pubmed/37759591 http://dx.doi.org/10.3390/biology12091192 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Wang, Xumiao
Hu, Wei
Li, Yuxi
Jiang, Minghao
Zhao, Ning
Cao, Haiqun
Liao, Min
Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China
title Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China
title_full Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China
title_fullStr Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China
title_full_unstemmed Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China
title_short Cytochrome P450s-Involved Enhanced Metabolism Contributes to the High Level of Nicosulfuron Resistance in Digitaria sanguinalis from China
title_sort cytochrome p450s-involved enhanced metabolism contributes to the high level of nicosulfuron resistance in digitaria sanguinalis from china
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10525941/
https://www.ncbi.nlm.nih.gov/pubmed/37759591
http://dx.doi.org/10.3390/biology12091192
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