Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-06-13T05:25:38.852Z Has data issue: false hasContentIssue false

Resistance patterns and molecular basis to ACCase-inhibiting herbicides

Published online by Cambridge University Press:  08 May 2024

Qian Yang
Affiliation:
Associate Research Fellow, Jiangsu Lixiahe District Institute of Agricultural Sciences, Yangzhou, PR China
Wei Deng
Affiliation:
Associate Professor, College of Plant Protection, Yangzhou University, Yangzhou, PR China
Longwei Liu
Affiliation:
Undergraduate, College of Plant Protection, Yangzhou University, Yangzhou, PR China
Tian Wei
Affiliation:
Research Associate, Jiangsu Lixiahe District Institute of Agricultural Sciences, Yangzhou, PR China
Xia Yang
Affiliation:
Research Fellow, Institute of Germplasm Resources and Biotechnology, Jiangsu Academy of Agricultural Sciences, Nanjing, PR China
Jinlei Zhu
Affiliation:
Research Associate, Jiangsu Lixiahe District Institute of Agricultural Sciences, Yangzhou, PR China
Min Lv*
Affiliation:
Associate Research Fellow, Jiangsu Lixiahe District Institute of Agricultural Sciences, Yangzhou, PR China
Yongfeng Li*
Affiliation:
Research Fellow, Institute of Germplasm Resources and Biotechnology, Jiangsu Academy of Agricultural Sciences, Nanjing, PR China
*
Corresponding authors: Min Lv; Email: lvmin8889@126.com and Yongfeng Li; Email: liyongfeng_2020@aliyun.com
Corresponding authors: Min Lv; Email: lvmin8889@126.com and Yongfeng Li; Email: liyongfeng_2020@aliyun.com

Abstract

Digitaria ciliaris var. chrysoblephara (Fig. & De Not.) R.R. Stewart is an annual xeromorphic weed that severely infests direct-seeded rice fields in China. Herbicide resistance is emerging in D. ciliaris var. chrysoblephara owing to extensive and recurrent use of the acetyl-CoA carboxylase (ACCase)-inhibiting herbicide metamifop. In this study, a total of 53 D. ciliaris var. chrysoblephara populations randomly sampled from direct-seeded rice fields across Jiangsu Province were investigated for metamifop resistance and potential resistance-endowing mutations. Single-dose assays revealed that 17 (32.1%) populations evolved resistance to metamifop and 5 (9.4%) populations were in the process of developing resistance. The resistance index (RI) of metamifop-resistant populations ranged from 2.7 to 32.1. Amino acid substitutions (Ile-1781-Leu, Trp-2027-Cys/Ser, and Ile-2041-Asn) in ACCase genes were detected in resistant D. ciliaris var. chrysoblephara plants and caused various cross-resistance patterns to ACCase-inhibiting herbicides. All of four resistant populations (YC07, YZ09, SQ03, and HA06), with different ACCase mutations, exhibited cross-resistance to the aryloxyphenoxypropionate (APP) herbicides cyhalofop-butyl (RI values: 10.0 to 19.9), fenoxaprop-P-ethyl (RI values: 53.7 to 132.8), and haloxyfop-P-methyl (RI values: 6.2 to 62.6), and the phenylpyrazoline (DEN) pinoxaden (RI values: 2.3 to 5.4), but responded differently to the cyclohexanedione (CHD) herbicides clethodim and sethoxydim. It is noteworthy that four postemergence herbicides used for rice cropping, including bispyribac-sodium, pyraclonil, quinclorac, and anilofos, showed poor control effect against D. ciliaris var. chrysoblephara, suggesting few alternations for managing this weed in rice fields except ACCase inhibitors. In conclusion, this work demonstrated that the D. ciliaris var. chrysoblephara had developed resistance to ACCase-inhibiting herbicides in rice cultivation of China, and target-site amino acid substitutions in ACCase were primarily responsible for metamifop resistance.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of Weed Science Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Gulshan Mahajan, Punjab Agricultural University

References

Bagavathiannan, MV, Norsworthy, JK, Smith, KL, Neve, P (2014) Modeling the simultaneous evolution of resistance to ALS- and ACCase-inhibiting herbicides in barnyardgrass (Echinochloa crus-galli) in Clearfield® rice. Weed Technol 28:89103 CrossRefGoogle Scholar
Basak, S, McElroy, JS, Brown, AM, Gonçalves, CG, Patel, JD, McCullough, PE (2020) Plastidic ACCase Ile-1781-Leu is present in pinoxaden-resistant southern crabgrass (Digitaria ciliaris). Weed Sci 68:4150 Google Scholar
Beckie, HJ, Tardif, FJ (2012) Herbicide cross resistance in weeds. Crop Prot 35:1528 CrossRefGoogle Scholar
Cao, J, Tao, Y, Zhang, Z, Gu, T, Li, G, Lou, Y, Wang, H (2023) Mechanism of metamifop resistance in Digitaria ciliaris var. chrysoblephara from Jiangsu, China. Front Plant Sci 14:1133798 CrossRefGoogle ScholarPubMed
de Carvalho, LB, Alves, PL, González-Torralva, F, Cruz-Hipolito, HE, Rojano-Delgado, AM, De Prado, R, Gil-Humanes, J, Barro, F, de Castro, MD (2012) Pool of resistance mechanisms to glyphosate in Digitaria insularis . J Agric Food Chem 60:615622 CrossRefGoogle ScholarPubMed
Délye, C, Jasieniuk, M, Le Corre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649658 CrossRefGoogle ScholarPubMed
Deng, W, Cai, J, Zhang, J, Chen, Y, Chen, Y, Di, Y, Yuan, S (2019) Molecular basis of resistance to ACCase-inhibiting herbicide cyhalofop-butyl in Chinese sprangletop (Leptochloa chinensis (L.) Nees) from China. Pestic Biochem Physiol 158:143148 CrossRefGoogle ScholarPubMed
Deng, W, Li, Y, Yao, S, Duan, Z, Yang, Q, Yuan, S (2023a) ACCase gene mutations and P450-mediated metabolism contribute to cyhalofop-butyl resistance in Eleusine indica biotypes from direct-seeding paddy fields. Pestic Biochem Physiol 194:105530 CrossRefGoogle ScholarPubMed
Deng, W, Li, Y, Yao, S, Wu, J, Zhu, A, Yang, Q, Yuan, S (2023b) Current status of cyhalofop-butyl and metamifop resistance and diversity of the ACCase gene mutations in Chinese sprangletop (Leptochloa chinensis) from China. Pestic Biochem Physiol 197:105648 CrossRefGoogle ScholarPubMed
Deng, W, Yang, M, Li, Y, Xia, Z, Chen, Y, Yuan, S, Yang, Q (2021) Enhanced metabolism confers a high level of cyhalofop-butyl resistance in a Chinese sprangletop (Leptochloa chinensis (L.) Nees) population. Pest Manag Sci 77:25762583 CrossRefGoogle Scholar
Gaines, TA, Duke, SO, Morran, S, Rigon, CAG, Tranel, PJ, Küpper, A, Dayan, FE (2020) Mechanisms of evolved herbicide resistance. J Biol Chem 295:1030710330 CrossRefGoogle ScholarPubMed
Golmohammadzadeh, S, Rojano-Delgado, AM, Vázquez-García, JG, Romano, Y, Osuna, MD, Gherekhloo, J, De Prado, R (2020) Cross-resistance mechanisms to ACCase-inhibiting herbicides in short-spike canarygrass (Phalaris brachystachys). Plant Physiol Biochem 151:681688 CrossRefGoogle ScholarPubMed
Guo, W, Zhang, TJ, Zhang, C, Tian, XS (2022) Response of seed germination and seedling establishment of Digitaria sanguinalis to different environmental factors. Plant Prot 48:8593. ChineseGoogle Scholar
Iwakami, S, Ishizawa, H, Sugiura, K, Kashiwagi, K, Oga, T, Niwayama, S, Uchino, A (2024) Syntenic analysis of ACCase loci and target-site-resistance mutations in cyhalofop-butyl resistant Echinochloa crus-galli var. crus-galli in Japan. Pest Manag Sci 80:627636 CrossRefGoogle ScholarPubMed
Jiang, M, Wang, Y, Li Wei, Li Q, Zhang, J, Liao, M, Zhao, N, Cao, H (2022) Investigating resistance levels to cyhalofop-butyl and mechanisms involved in Chinese sprangletop (Leptochloa chinensis L.) from Anhui Province, China. Pestic Biochem Physiol 186:105165 CrossRefGoogle ScholarPubMed
Jiang, Y, Chen, G, Dong, L (2017) Resistance level of Digitaria sanguinalis to post-emergence herbicides frequently used in rice fields. J Weed Sci 35:6772. ChineseGoogle Scholar
Jin, M, Chen, L, Deng, XW, Tang, X (2022) Development of herbicide resistance genes and their application in rice. Crop J 10:2635 CrossRefGoogle Scholar
Kaundun, SS (2014) Resistance to acetyl-CoA carboxylase-inhibiting herbicides. Pest Manag Sci 70:14051417 CrossRefGoogle ScholarPubMed
Khammassi, M, Hajri, H, Menchari, Y, Chaabane, H, Souissi, T (2019) Current status in resistance to ACCase and ALS-inhibiting herbicides in rigid ryegrass populations from cereal crops in North of Tunisia. J Agric Sci 157: 676683 CrossRefGoogle Scholar
Laforest, M, Soufiane, B, Simard, MJ, Obeid, K, Page, E, Nurse, RE (2017) Acetyl-CoA carboxylase overexpression in herbicide-resistant large crabgrass (Digitaria sanguinalis). Pest Manag Sci 73:22272235 CrossRefGoogle ScholarPubMed
Li, J, Li, M, Gao, X, Fang, F (2017) A novel amino acid substitution Trp574Arg in acetolactate synthase (ALS) confers broad resistance to ALS-inhibiting herbicides in crabgrass (Digitaria sanguinalis). Pest Manag Sci 73:25382543 CrossRefGoogle ScholarPubMed
Li, Q, Zhao, N, Jiang, M, Wang, M, Zhang, J, Cao, H, Liao, M (2023) Metamifop resistance in Echinochloa glabrescens via glutathione S-transferase-involved enhanced metabolism. Pest Manag Sci 79:27252736 CrossRefGoogle ScholarPubMed
Liu, X, Hou, Z, Zhang, Y, Merchant, A, Zhong, M, Ma, G, Zeng, Q, Wu, L, Zhou, X, Luo, K, Ding, C (2023) Cloning and functional characterization of a tau class glutathione transferase associated with haloxyfop-P-methyl resistance in Digitaria sanguinalis . Pest Manag Sci 79:39503958 CrossRefGoogle ScholarPubMed
Petit, C, Bay, G, Pernin, F, Délye, C (2010) Prevalence of cross or multiple resistance to the acetylcoenzyme A carboxylase inhibitors fenoxaprop, clodinafop and pinoxaden in black-grass (Alopecurus myosuroides Huds.) in France. Pest Manag Sci 66:168177 CrossRefGoogle ScholarPubMed
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347 CrossRefGoogle ScholarPubMed
Seefeldt, SS, Jensen, JE, Fuerst, EP (1995) Log-logistic analysis of herbicide dose-response relationships. Weed Technol 9:218227 CrossRefGoogle Scholar
Sun, P, Niu, L, Lan, X, Yu, H, Cui, H, Chen, J, Li, X (2023) Enhanced metabolic resistance mechanism endows resistance to metamifop in Echinochloa crus-galli (L.) P. Beauv. Pestic Biochem Physiol 197:105656 CrossRefGoogle ScholarPubMed
Takano, HK, Melo, MSC, Ovejero, RFL, Ovejero, RFL, Westra, PH, Todd, A, Gaines, TA, Dayan, FE (2020) Trp2027Cys mutation evolves in Digitaria insularis with cross-resistance to ACCase inhibitors. Pestic Biochem Physiol 164:16 CrossRefGoogle ScholarPubMed
Tang, W, Zhou, F, Zhang, Y, Chen, J (2015) Resistance of American sloughgrass (Bechmannia syzigachne) populations to ACCase-inhibiting herbicides involves three different target site mutations from China. Pestic Biochem Physiol 124: 9396 CrossRefGoogle ScholarPubMed
Yang, Q, Yang, X, Zhang, Z, Wang, J, Fu, W, Li, Y (2021) Investigating the resistance levels and mechanisms to penoxsulam and cyhalofop-butyl in barnyardgrass (Echinochloa crus-galli) from Ningxia Province, China. Weed Sci 69:422429 CrossRefGoogle Scholar
Yang, Q, Yang, X, Zhu, J, Wei, T, Lv, M, Li, Y (2022) Metabolic resistance to acetyl-CoA carboxylase-inhibiting herbicide cyhalofop-butyl in a Chinese Echinochloa crus-galli population. Agronomy 12:2724 CrossRefGoogle Scholar
Yang, Q, Zhu, J, Yang, X, Wei, T, Lv, M, Li, Y (2023) Ile-1781-Leu target mutation and non-target-site mechanism confer resistance to acetyl-CoA carboxylase-inhibiting herbicides in Digitaria ciliaris var. chrysoblephara . J Agric Food Chem 71:79887995 CrossRefGoogle ScholarPubMed
Yanniccari, M, Vázquez-García, JG, Gigón, R, Palma-Bautista, C, Vila-Aiub, M, De Prado, D (2022) A novel EPSPS Pro-106-His mutation confers the first case of glyphosate resistance in Digitaria sanguinalis . Pest Manag Sci 78:31353143 CrossRefGoogle ScholarPubMed
Yu, J, McCullough, PE, Czarnota, MA (2017) First report of acetyl-CoA carboxylase–resistant southern crabgrass (Digitaria ciliaris) in the United States. Weed Technol 31:252259 CrossRefGoogle Scholar
Yu, Q, Ahmad-Hamdani, MS, Han, H, Christoffers, MJ, Powles, SB (2013) Herbicide resistance-endowing ACCase gene mutations in hexaploidy wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity 110:220231 CrossRefGoogle Scholar
Yu, Q, Collavo, A, Zheng, MQ, Owen, M, Sattin, M, Powles, SB (2007) Diversity of acetyl-coenzyme A carboxylase mutations in resistant Lolium populations: evaluation using clethodim. Plant Physiol 145:547558 CrossRefGoogle ScholarPubMed
Yuan, S, Di, Y, Chen, Y, Chen, Y, Cai, J, Deng, W (2019) Target-site resistance to cyhalofop-butyl in bearded sprangletop (Diplachne fusca) from China. Weed Sci 67:534538 CrossRefGoogle Scholar
Zhang, L, Wang, W, Du, Y, Deng, Y, Bai, T, Ji, M (2023) Multiple resistance of Echinochloa phyllopogon to synthetic auxin, ALS-, and ACCase-inhibiting herbicides in northeast China. Pestic Biochem Physiol 193:105450 CrossRefGoogle ScholarPubMed
Zhang, Y, Chen, L, Song, W, Cang, T, Xu, M, Wu, C (2022) Diverse mechanisms associated with cyhalofop-butyl resistance in Chinese sprangletop (Leptochloa chinensis (L.) Nees): characterization of target-site mutations and metabolic resistance-related genes in two resistant populations. Front Plant Sci 13:990085 CrossRefGoogle ScholarPubMed
Zhang, Z, Li, R, Zhao, C, Qiang, S (2021) Reduction in weed infestation through integrated depletion of the weed seed bank in a rice-wheat cropping system. Agron Sustain Dev 41:10 CrossRefGoogle Scholar
Zhao, B, Xu, X, Li, B, Qi, Z, Huang, J, Hu, A, Wang, G, Liu, X (2023) Target-site mutation and enhanced metabolism endow resistance to nicosulfuron in a Digitaria sanguinalis population. Pestic Biochem Physiol 194:105488 CrossRefGoogle Scholar
Zhao, N, Ge, L, Yan, Y, Bai, S, Wang, D, Liu, W, Wang, J (2019) Trp-1999-Ser mutation of acetyl-CoA carboxylase and cytochrome P450s-involved metabolism confer resistance to fenoxaprop-P-ethyl in Polypogon fugax . Pest Manag Sci 75:31753183 CrossRefGoogle ScholarPubMed
Zhao, N, Jiang, M, Li, Q, Gao, Q, Zhang, J, Liao, M, Cao, H (2022) Cyhalofop-butyl resistance conferred by a novel Trp-2027-Leu mutation of acetyl-CoA carboxylase and enhanced metabolism in Leptochloa chinensis . Pest Manag Sci 78:11761186 CrossRefGoogle ScholarPubMed
Zhu, J, Wang, J, DiTommaso, A, Zhang, C, Zheng, G, Liang, W, Islam, F, Yang, C, Chen, X, Zhou, W (2020) Weed research status, challenges, and opportunities in China. Crop Prot 134:104449 CrossRefGoogle Scholar
Supplementary material: File

Yang et al. supplementary material

Yang et al. supplementary material
Download Yang et al. supplementary material(File)
File 18.9 KB