Hostname: page-component-6766d58669-tq7bh Total loading time: 0 Render date: 2026-05-15T07:13:33.776Z Has data issue: false hasContentIssue false
  • English
  • Français

A Trp-574-Leu mutation in acetolactate synthase confers imazamox resistance in barnyardgrass (Echinochloa crus-galli) from China

Published online by Cambridge University Press:  29 October 2024

Yu Liu ,
Kerong Shi ,
Haitao Gao ,
Shaojing Yin ,
Liyao Dong  and
Zhike Feng Open the ORCID record for Zhike Feng [Opens in a new window]
Yu Liu
Affiliation:
Master Student, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
Kerong Shi
Affiliation:
Master Student, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
Haitao Gao
Affiliation:
Doctoral Student, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
Shaojing Yin
Affiliation:
Doctoral Student, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
Liyao Dong
Affiliation:
Professor, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
Zhike Feng*
Affiliation:
Professor, College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
*
Corresponding author: Zhike Feng; Email: fengzk2011@njau.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Barnyardgrass [Echinochloa crus-galli (L.) P. Beauv.] is increasingly infesting imidazolinone-tolerant (IMI-T) rice (Oryza sativa L.) fields in China, and E. crus-galli imazamox resistance has become the major concern for weed management in IMI-T rice fields. In this study, the susceptible population JLGY-3 (S) and the suspected resistant population JHXY-2 (R) collected from IMI-T rice fields were used as research subjects. When treated with imazamox, the JHXY-2 (R) population showed a high level of herbicide resistance with a resistance index of 31.2. JHXY-2 (R) was cross-resistant to all five acetolactate synthase (ALS) inhibitors from different chemical families, but sensitive to herbicides inhibiting acetyl-CoA carboxylase. To understand the reason why JHXY-2 (R) was resistant to imazamox, we performed experiments to characterize potential target-site resistance (TSR) and non–target site resistance (NTSR) mechanisms. A Trp-574-Leu amino acid mutation in ALS and low imazamox ALS sensitivity were the main mechanisms underlying imazamox resistance in this JHXY-2 (R) population. There was no significant difference in ALS gene expression and ALS protein abundance between R and S populations. High-performance liquid chromatography–tandem mass spectrometry analysis showed enhanced metabolism of imazamox in JHXY-2 (R), which was in contrast to the results of pretreatment with a metabolic enzyme inhibitor. Treatments with cytochrome P450 monooxygenase/glutathione S-transferase (P450/GST) inhibitors did not alter the resistance level of JHXY-2 (R) against imazamox. Transcriptome sequencing showed that there was almost no significant difference in the expression of P450 and GST metabolic enzyme genes between R and S populations, and only GSTU1 showed a significant upregulation in the R population, further clarifying the NTSR mechanism of JHXY-2 (R). In conclusion, amino acid mutation and higher enzyme activity of ALS are the main causes of imazamox resistance in JHXY-2 (R). However, given the differences in imazamox residues in the leaves of E. crus-galli, there may still be undetectable NTSR mechanisms that are causing imazamox resistance in the R population.

Keywords

ALS protein abundanceIMI-T rice fieldstarget-site resistance

Information

Type
Research Article
Information
Weed Science , Volume 72 , Issue 6 , November 2024 , pp. 683 - 692
Check for updates
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.)

Article purchase

Temporarily unavailable

Footnotes

Associate Editor: Vipan Kumar, Cornell University

References

Bai, S, Yin, M, Lyu, Q, Jiang, B, Li, L (2022) Cytochrome P450 BsCYP99A44 and BsCYP704A177 confer metabolic resistance to ALS herbicides in Beckmannia syzigachne . Int J Mol Sci 23:12175 CrossRefGoogle ScholarPubMed
Burgos, NR, Norsworthy, JK, Scott, RC, Smith, KL (2008) Red rice (Oryza sativa) status after 5 years of imidazolinone-resistant rice technology in Arkansas. Weed Technol 22:200–208 CrossRefGoogle Scholar
Burgos, NR, Singh, V, Tseng, TM, Black, H, Young, ND, Huang, Z, Hyma, KE, Gealy, DR, Caicedo, AL (2014) The impact of herbicide-resistant rice technology on phenotypic diversity and population structure of United States weedy rice. Plant Physiol 166:1208–1220 CrossRefGoogle ScholarPubMed
Chen, G, Wang, Q, Yao, Z, Zhu, L, Dong, L (2016) Penoxsulam-resistant barnyardgrass (Echinochloa crus-galli) in rice fields in China. Weed Biol Manag 16:16–23 CrossRefGoogle Scholar
Chen, J, Huang, H, Wei, S, Cui, H, Li, X, Zhang, C (2020) Glyphosate resistance in Eleusine indica: EPSPS overexpression and P106A mutation evolved in the same individuals. Pestic Biochem Physiol 164:203–208 CrossRefGoogle ScholarPubMed
Cummins, I, Wortley, DJ, Sabbadin, F, He, Z, Coxon, CR, Straker, HE, Sellars, JD, Knight, K, Edwards, L, Hughes, D, Kaundun, SS, Hutchings, S-J, Steel, PG, Edwards, R (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110:5812–5817 CrossRefGoogle ScholarPubMed
De Leon, TB, Karn, E, Al-Khatib, K, Espino, L, Blank, T, Andaya, CB, Andaya, VC, Brim-DeForest, W (2019) Genetic variation and possible origins of weedy rice found in California. Ecol Evol 9:5835–5848 CrossRefGoogle ScholarPubMed
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 69:176–187 CrossRefGoogle Scholar
Dimaano, NG, Iwakami, S (2021) Cytochrome P450-mediated herbicide metabolism in plants: current understanding and prospects. Pest Manag Sci 77:22–32 CrossRefGoogle Scholar
Duggleby, RG, McCourt, JA, Guddat, LW (2008) Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Plant Physiol Biochem 46:309–324 CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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 67:281–287 Google Scholar
Fang, J, Yang, D, Zhao, Z, Chen, J, Dong, L (2022) A novel Phe-206-Leu mutation in acetolactate synthase confers resistance to penoxsulam in barnyardgrass (Echinochloa crus-galli (L.) P. Beauv). Pest Manag Sci 78:2560–2570 CrossRefGoogle ScholarPubMed
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 67:8085–8095 CrossRefGoogle ScholarPubMed
Feng, Y, Gao, Y, Zhang, Y, Dong, L, Li, J (2016) Mechanisms of resistance to pyroxsulam and ACCase inhibitors in Japanese foxtail (Alopecurus japonicus). Weed Sci 64:695–704 Google Scholar
Gao, H, Yu, J, Chen, J, Wang, H, Liang, S, Feng, Z, Gu, Y, Dong, L (2023) Target-site and metabolic resistance mechanisms to penoxsulam in late watergrass (Echinochloa phyllopogon) in China. J Agric Food Chem 71:17742–17751 CrossRefGoogle ScholarPubMed
Gao, H, Yu, J, Pan, L, Wu, X, Dong, L (2017) Target-site resistance to fenoxaprop-p-ethyl in Keng stiffgrass (Sclerochloa kengiana) from China. Weed Sci 65:452–460 Google Scholar
Guo, L, Qiu, J, Ye, C, Jin, G, Mao, L, Zhang, H, Yang, X, Peng, Q, Wang, Y, Jia, L, Lin, Z, Li, G, Fu, F, Liu, C, Chen, L, et al. (2017) Echinochloa crus-galli genome analysis provides insight into its adaptation and invasiveness as a weed. Nat Commun 8:1031 CrossRefGoogle ScholarPubMed
Heap, I (2024) The International Herbicide-Resistant Weed Database. www.weedscience.org. Accessed: June 8, 2024Google Scholar
Iwakami, S, Endo, M, Saika, H, Okuno, J, Nakamura, N, Yokoyama, M, Watanabe, H, Toki, S, Uchino, A, Inamura, T (2014) Cytochrome P450 CYP81A12 and CYP81A21 are associated with resistance to two acetolactate synthase inhibitors in Echinochloa phyllopogon . Plant Physiol 165:618–629 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 119:1–8. doi: 10.1016/j.pestbp.2015.02.007 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. doi: 10.3389/fpls.2017.00254 CrossRefGoogle ScholarPubMed
Laforest, M, Soufiane, B, Simard, M, Obeid, K, Page, E, Nurse, RE (2017) Acetyl-CoA carboxylase overexpression in herbicide-resistant large crabgrass (Digitaria sanguinalis). Pest Manag Sci 73:2227–2235 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 73:2538–2543 CrossRefGoogle ScholarPubMed
Liu, H, Yang, X, Liao, X, Zuo, T, Qin, C, Cao, S, Dong, L, Zhou, H, Zhang, Y, Liu, S, Shen, Y, Lin, H, Lübberstedt, T, Zhang, Z, Pan, G (2015) Genome-wide comparative analysis of digital gene expression tag profiles during maize ear development. Genomics 106:52–60 CrossRefGoogle ScholarPubMed
Liu, L, Wu, L, Li, Z, Fang, Y, Ju, B, Zhang, S, Bai, L, Pan, L (2024a) The Pro-197-Thr mutation in the ALS gene confers novel resistance patterns to ALS-inhibiting herbicides in Bromus japonicus in China. Front Plant Sci 15:1348815 CrossRefGoogle ScholarPubMed
Liu, X, Merchant, A, Xiang, S, Zong, T, Zhou, X, Bai, L (2021) Managing herbicide resistance in China. Weed Sci 69:4–17 Google Scholar
Liu, Y, Gao, H, Dong, L, Feng, Z (2024b) Preparation of polyclonal antibodies against acetolactate synthase of Lolium multiflorum Lamk and its application in the detection of various weeds. Plant Prot 50:266–274. doi: 10.16688/j.zwbh.2023641 Google Scholar
Liu, Y, Wang, H, Gao, H, Zhu, G, Peng, Z, Li, J, Dong, L (2022) Two mechanisms provide tolerance to cyhalofop-butyl in pond lovegrass [Eragrostis japonica (Thunb.) Trin.]. Pestic Biochem Physiol 188:105247 CrossRefGoogle ScholarPubMed
Lowe, C, Onkokesung, N, Goldberg, A, Beffa, R, Neve, P, Edwards, R, Comont, D (2024) RNA and protein biomarkers for detecting enhanced metabolic resistance to herbicides mesosulfuron-methyl and fenoxaprop-ethyl in black-grass (Alopecurus myosuroides). Pest Manag Sci 80:2539–2551 CrossRefGoogle ScholarPubMed
Ngo, TD, Malone, JM, Boutsalis, P, Gill, G, Preston, C (2018) EPSPS gene amplification conferring resistance to glyphosate in windmill grass (Chloris truncata) in Australia. Pest Manag Sci 74:1101–1108 CrossRefGoogle ScholarPubMed
Palma-Bautista, C, Rojano-Delgado, AM, Vázquez-García, JG, Yanniccari, M, Prado, RD (2020) Resistance to fomesafen, imazamox and glyphosate in Euphorbia heterophylla from Brazil. Agronomy 10:1573 CrossRefGoogle Scholar
Pan, L, Gao, H, Xia, W, Zhang, T, Dong, L (2016) Establishing a herbicide-metabolizing enzyme library in Beckmannia syzigachne to identify genes associated with metabolic resistance. J Exp Bot 67:1745–1757 CrossRefGoogle ScholarPubMed
Pan, L, Guo, Q, Wang, J, Shi, L, Yang, X, Zhou, Y, Yu, Q, Bai, L (2022) CYP81A68 confers metabolic resistance to ALS and ACCase-inhibiting herbicides and its epigenetic regulation in Echinochloa crus-galli . J Haz Mat 428:128225 CrossRefGoogle ScholarPubMed
Pan, L, Yu, Q, Han, H, Mao, L, Nyporko, A, Fan, L, Bai, L, Powles, S (2019) Aldo-keto reductase metabolizes glyphosate and confers glyphosate resistance in Echinochloa colona . Plant Physiol 181:1519–1534 CrossRefGoogle ScholarPubMed
Pan, L, Yu, Q, Wang, J, Han, H, Mao, L, Nyporko, A, Maguza, A, Fan, L, Bai, L, Powles, S (2021) An ABCC-type transporter endowing glyphosate resistance in plants. Proc Natl Acad Sci USA 118:e2100136118 CrossRefGoogle ScholarPubMed
Panozzo, S, Mascanzoni, E, Scarabel, L, Milani, A, Dalazen, G, Merotto, AJ, Tranel, PJ, Sattin, M (2021) Target-site mutations and expression of ALS gene copies vary according to Echinochloa species. Genes 12:1841 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 105:93–101 CrossRefGoogle Scholar
Riar, DS, Norsworthy, JK, Srivastava, V, Nandula, V, Bond, JA, Scott, RC (2013) Physiological and molecular basis of acetolactate synthase-inhibiting herbicide resistance in barnyardgrass (Echinochloa crus-galli). J Agric Food Chem 61:278–289 CrossRefGoogle ScholarPubMed
Singh, M, Bhullar, MS, Chauhan, BS (2015) Seed bank dynamics and emergence pattern of weeds as affected by tillage systems in dry direct-seeded rice. Crop Prot 67:168–177 CrossRefGoogle Scholar
Trapnell, C, Hendrickson, DG, Sauvageau, M, Goff, L, Rinn, JL, Pachter, L (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31:46–53 CrossRefGoogle ScholarPubMed
Trapnell, C, Williams, BA, Pertea, G, Mortazavi, A, Kwan, G, Van Baren, MJ, Salzberg, SL, Wold, BJ, Pachter, L (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515 CrossRefGoogle ScholarPubMed
Wang, J, Lian, L, Qi, J, Fang, Y, Nyporko, A, Yu, Q, Bai, L, Pan, L (2023) Metabolic resistance to acetolactate synthase inhibitors in Beckmannia syzigachne: identification of CYP81Q32 and its transcription regulation. Plant J 115:317–334 CrossRefGoogle ScholarPubMed
Wu, D, Shen, E, Jiang, B, Feng, Y, Tang, W, Lao, S, Jia, L, Lin, H-Y, Xie, L, Weng, X, Dong, C, Qian, Q, Lin, F, Xu, H, Lu, H, et al. (2022) Genomic insights into the evolution of Echinochloa species as weed and orphan crop. Nat Commun 13:689 CrossRefGoogle Scholar
Yasuor, H, Osuna, MD, Ortiz, A, Saldaín, NE, Eckert, JW, Fischer, AJ (2009) Mechanism of resistance to penoxsulam in late watergrass [Echinochloa phyllopogon (Stapf) Koss.]. J Agric Food Chem 57:3653–3660 CrossRefGoogle ScholarPubMed
Yu, Q, Han, H, Cawthray, GR, Wang, SF, Powles, SB (2013) Enhanced rates of herbicide metabolism in low herbicide-dose selected resistant Lolium rigidum . Plant Cell Environ 36:818–827 CrossRefGoogle ScholarPubMed
Yu, Q, Powles, S (2014a) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:1106–1118 CrossRefGoogle Scholar
Yu, Q, Powles, SB (2014b) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350 CrossRefGoogle ScholarPubMed
Yu, Q, Shane Friesen, LJ, Zhang, XQ, Powles, SB (2004) Tolerance to acetolactate synthase and acetyl-coenzyme A carboxylase inhibiting herbicides in Vulpia bromoides is conferred by two co-existing resistance mechanisms. Pestic Biochem Physiol 78:21–30 CrossRefGoogle Scholar
Zhao, N, Yan, Y, Liu, W, Wang, J (2022) Cytochrome P450 CYP709C56 metabolizing mesosulfuron-methyl confers herbicide resistance in Alopecurus aequalis . Cell Mol Life Sci 79:205 CrossRefGoogle ScholarPubMed
Zhong, S, Joung, J-G, Zheng, Y, Chen, Y, Liu, B, Shao, Y, Xiang, JZ, Fei, Z, Giovannoni, JJ (2011) High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc 2011:pdb.prot5652 CrossRefGoogle ScholarPubMed
Supplementary material: File

Liu et al. supplementary material

Liu et al. supplementary material
Download Liu et al. supplementary material(File)
File 350.9 KB