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Investigating the resistance levels and mechanisms to penoxsulam and cyhalofop-butyl in barnyardgrass (Echinochloa crus-galli) from Ningxia Province, China

Published online by Cambridge University Press:  21 May 2021

Qian Yang
Affiliation:
Postdoctoral Research Associate, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China; Research Associate, Institute of Agricultural Sciences for Lixiahe Region in Jiangsu, Yangzhou, P. R. China
Xia Yang
Affiliation:
Associate Professor, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China
Zichang Zhang
Affiliation:
Associate Professor, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China
Jieping Wang
Affiliation:
Associate Professor, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China
Weiguo Fu
Affiliation:
Professor, Key Laboratory of Modern Agricultural Equipment and Technology, Ministry of Education and Jiangsu Province, Jiangsu University, Zhenjiang, P. R. China
Yongfeng Li*
Affiliation:
Professor, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, P. R. China
*
Author for correspondence: Yongfeng Li, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, P. R. China. (Email: [email protected])

Abstract

Barnyardgrass [Echinochloa crus-galli (L.) P. Beauv.] is a noxious grass weed that infests rice fields and causes huge crop yield losses. In this study, we collected 12 E. crus-galli populations from rice fields of Ningxia Province in China and investigated the resistance levels to the acetolactate synthase (ALS) inhibitor penoxsulam and the acetyl-CoA carboxylase (ACCase) inhibitor cyhalofop-butyl. The results showed that eight populations exhibited resistance to penoxsulam and four populations evolved resistance to cyhalofop-butyl. Moreover, all four cyhalofop-butyl–resistant populations (NX3, NX4, NX6, and NX7) displayed multiple herbicide resistance to both penoxsulam and cyhalofop-butyl. The alternative herbicides bispyribac-sodium, metamifop, and fenoxaprop-p-ethyl cannot effectively control the multiple herbicide–resistant (MHR) plants. To characterize the molecular mechanisms of resistance, we amplified and sequenced the target site–encoding genes in resistant and susceptible populations. Partial sequences of three ALS genes and six ACCase genes were examined. A Trp-574-Leu mutation was detected in EcALS1 and EcALS3 in two high-level (65.84- and 59.30-fold) penoxsulam-resistant populations, NX2 and NX10, respectively. In addition, one copy (EcACC4) of ACCase genes encodes a truncated aberrant protein due to a frameshift mutation in E. crus-galli populations. None of the amino acid substitutions that are known to confer herbicide resistance were detected in ALS and ACCase genes of MHR populations. Our study reveals the wide spread of MHR E. crus-galli populations in Ningxia Province that exhibit resistance to several ALS and ACCase inhibitors. Non–target site based mechanisms are likely to be involved in E. crus-galli resistance to the herbicides, at least in four MHR populations.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Weed Science Society of America

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Footnotes

Associate Editor: Mithila Jugulam, Kansas State University

References

Bai, S, Zhang, F, Li, Z, Wang, H, Wang, Q, Wang, J, Liu, W, Bai, L (2019) Target-site and non-target-site-based resistance to tribenuron-methyl in multiply-resistant Myosoton aquaticum L. Pestic Biochem Physiol 155:814 CrossRefGoogle ScholarPubMed
Bai, S, Zhao, Y, Zhou, Y, Wang, M, Li, Y, Luo, X, Li, L (2020) Identification and expression of main genes involved in non-target site resistance mechanisms to fenoxaprop-p-ethyl in Beckmannia syzigachne . Pest Manage Sci 76:26192626 CrossRefGoogle ScholarPubMed
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
Beckie, HJ, Tardif, FJ (2012) Herbicide cross resistance in weeds. Crop Prot 35:1518 CrossRefGoogle Scholar
Chen, GQ, Wang, Q, Yao, ZW, Zhu, LF, Dong, LY (2016) Penoxsulam-resistant barnyardgrass (Echinochloa crus-galli) in rice fields in China. Weed Biol Manag 16:1623 CrossRefGoogle Scholar
Délye, C (2013) Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: a major challenge for weed science in the forthcoming decade. Pest Manag Sci 69:176187 CrossRefGoogle Scholar
Deng, W, Cai, J, Zhang, J, Chen, Y, Chen, Y, Di, Y, Yuan, S (2019a) 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, Di, Y, Cai, J, Chen, Y, Yuan, S (2019b) Target-site resistance mechanisms to tribenuron-methyl and cross-resistance patterns to ALS-inhibiting herbicides of catchweed bedstraw (Galium aparine) with different ALS mutations. Weed Sci 67:183188 CrossRefGoogle Scholar
Deng, W, Yang, Q, Zhang, Y, Jiao, H, Mei, Y, Li, X, Zheng, M (2017). Cross-resistance patterns to acetolactate synthase (ALS)-inhibiting herbicides of flixweed (Descurainia sophia L.) conferred by different combinations of ALS isozymes with a Pro-197-Thr mutation or a novel Trp-574-Leu mutation. Pestic Biochem Physiol 136:4145 CrossRefGoogle ScholarPubMed
Dong, L, Gao, Y, Fang, J, Chen, G (2018) Research progress on the herbicide-resistance of weeds in rice fields in China. Plant Prot. 44:6976. ChineseGoogle Scholar
Fang, J, He, Z, Liu, T, Li, J, Dong, L (2020) A novel mutation Asp-2078-Glu in ACCase confers resistance to ACCase herbicides in barnyardgrass (Echinochloa crus-galli). Pestic Biochem Physiol 168:104634 CrossRefGoogle Scholar
Fang, J, Liu, T, Zhang, Y, Li, J, Dong, L (2019a) Target site-based penoxsulam resistance in barnyardgrass (Echinochloa crus-galli) from China. Weed Sci 67:281287 CrossRefGoogle Scholar
Fang, J, Zhang, Y, Liu, T, Yan, B, Li, J, Dong, L (2019b) Target-site and metabolic resistance mechanisms to penoxsulam in barnyardgrass (Echinochloa crus-galli (L.) P. Beauv). J Agric Food Chem 67:80858095 CrossRefGoogle Scholar
Feng, Y, Gao, Y, Zhang, Y, Dong, L, Li, J (2017) Mechanisms of resistance to pyroxsulam and ACCase inhibitors in Japanese foxtail (Alopecurus japonicus). Weed Sci 64:695704 CrossRefGoogle Scholar
Gao, Y, Pan, X, Sun, X, Li, J, Dong, L (2019) Is the protection of photosynthesis related to the mechanism of quinclorac resistance in Echinochloa crus-galli var. zelayensis? Gene 683:133148 CrossRefGoogle ScholarPubMed
Ghanizadeh, H, Harrington, KC (2017) Non-target site mechanisms of resistance to herbicides. Crit Rev Plant Sci 36:2434 CrossRefGoogle Scholar
Heap, I (2021) International Herbicide-Resistant Weed Database. http://www.weedscience.org. Accessed: February 5, 2021Google Scholar
Hernandez, MJ, Leon, R, Fischer, AJ, Gebauer, M, Galdames, R, Figueroa, R (2015) Target-Site resistance to nicosulfuron in johnsongrass (Sorghum halepense) from Chilean corn fields. Weed Sci 63:631640 CrossRefGoogle Scholar
Iwakami, S, Endo, M, Saika, H, Okuno, J, Nakamura, N, Yokoyama, M, Inamura, T (2014) Cytochrome P450 CYP81A12 and CYP81A21 are associated with resistance to two acetolactate synthase inhibitors in Echinochloa phyllopogon . Plant Physiol 165:618629 CrossRefGoogle ScholarPubMed
Iwakami, S, Hashimoto, M, Matsushima, K, Watanabe, H, Hamamura, K, Uchino, A (2015) Multiple-herbicide resistance in Echinochloa crus-galli var. formosensis, an allohexaploid weed species, in dry-seeded rice. Pestic Biochem Physiol 119:18 CrossRefGoogle ScholarPubMed
Iwakami, S, Shimono, Y, Manabe, Y, Endo, M, Shibaike, H, Uchino, A, Tominaga, T (2017) Copy number variation in acetolactate synthase genes of thifensulfuron-methyl resistant Alopecurus aequalis (shortawn foxtail) accessions in Japan. Front Plant Sci 8:254 CrossRefGoogle ScholarPubMed
Kaundun, SS (2014) Resistance to acetyl-CoA carboxylase-inhibiting herbicides. Pest Manag Sci 70:14051417 CrossRefGoogle ScholarPubMed
Kuenzer, C, Knauer, K (2013) Remote sensing of rice crop areas. Int J Remote Sens 34:21012139 CrossRefGoogle Scholar
Liu, J, Fang, J, He, Z, Li, J, Dong, L (2019) Target site-based resistance to penoxsulam in late watergrass (Echinochloa phyllopogon) from China. Weed Sci 67:380388 CrossRefGoogle Scholar
Matzenbacher, FO, Bortoly, ED, Kalsing, A, Merotto, A (2015) Distribution and analysis of the mechanisms of resistance of barnyardgrass (Echinochloa crus-galli) to imidazolinone and quinclorac herbicides. J Agric Sci 153:10441058 CrossRefGoogle Scholar
McElroy, JS, Flessner, ML, Wang, ZY, Dane, F, Walker, RH, Wehtje, GR (2013) A Trp574 to leu amino acid substitution in the ALS gene of annual bluegrass (Poa annua) is associated with resistance to ALS-inhibiting herbicides. Weed Sci 61:2125 CrossRefGoogle Scholar
Panozzo, S, Scarabel, L, Rosan, V, Sattin, M (2017) A new Ala-122-Asn amino acid change confers decreased fitness to ALS-resistant Echinochloa crus-galli . Front Plant Sci 8:13 CrossRefGoogle ScholarPubMed
Panozzo, S, Scarabel, L, Tranel, PJ, Sattin, M (2013) Target-site resistance to ALS inhibitors in the polyploid species Echinochloa crus-galli . Pestic Biochem Physiol 105:93101 CrossRefGoogle Scholar
Perotti, VE, Larran, AS, Palmieri, VE, Martinatto, AK, Permingeat, HR (2020) Herbicide resistant weeds: a call to integrate conventional agricultural practices, molecular biology knowledge and new technologies. Plant Sci 290:110255 CrossRefGoogle Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347 CrossRefGoogle ScholarPubMed
Sasaki, Y, Konishi, T, Nagano, Y (1995) The compartmentation of acetyl-coenzyme A carboxylase in plants. Plant Physiol 108:445449 CrossRefGoogle ScholarPubMed
Seefeldt, SS, Jensen, JE, Fuerst, EP (1995) Log-logistic analysis of herbicide dose-response relationships. Weed Technol 9:218227 CrossRefGoogle Scholar
Tranel, PJ, Wright, TR (2002) Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci 50:700712 CrossRefGoogle Scholar
Wang, Q, Ge, L, Zhang, L, You, L, Wang, D, Liu, W, Wang, J (2019) A Trp-574-Leu mutation in the acetolactate synthase (ALS) gene of Lithospermum arvense L. confers broad-spectrum resistance to ALS inhibitors. Pestic Biochem Physiol 158:1217 CrossRefGoogle ScholarPubMed
Xia, X, Tang, W, He, S, Kang, J, Ma, H, Li, J (2016) Mechanism of metamifop inhibition of the carboxyltransferase domain of acetyl-coenzyme A carboxylase in Echinochloa crus-galli . Sci Rep 6:34066 CrossRefGoogle ScholarPubMed
Yang, Q, Deng, W, Li, X., Yu, Q, Bai, L, Zheng, M (2016) Target-site and non-target-site based resistance to the herbicide tribenuron-methyl in flixweed (Descurainia sophia L.). BMC Genomics 17:551 CrossRefGoogle Scholar
Yang, X, Yu, X, Li, Y (2013) De novo assembly and characterization of the barnyardgrass (Echinochloa crus-galli) transcriptome using next-generation pyrosequencing. PLoS ONE 8:e69168 CrossRefGoogle ScholarPubMed
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 hexaploidy species. Heredity 110:220231 CrossRefGoogle Scholar
Yu, Q, Powles, S (2014) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:11061118 CrossRefGoogle ScholarPubMed
Zhang, L, Guo, W, Li, Q, Wu, C, Zhao, N, Liu, W, Wang, J (2017) Tribenuron-methyl resistance and mutation diversity of the AHAS gene in shepherd’s purse (Capsella bursa-pastoris (L.) Medik.) in Henan Province, China. Pestic Biochem Physiol 143:239245 CrossRefGoogle Scholar
Zhang, Z, Gu, T, Zhao, B, Yang, X, Peng, Q, Li, Y, Bai, L (2017) Effects of common Echinochloa varieties on grain yield and grain quality of rice. Field Crop Res 203:163172 CrossRefGoogle Scholar