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Molecular mechanism of resistance to mesosulfuron-methyl in shortawn foxtail (Alopecurus aequalis) from China

Published online by Cambridge University Press:  20 April 2023

Zhi Tang ,
Zilu Wang ,
Mali Wang ,
Fan Yin Open the ORCID record for Fan Yin [Opens in a new window] ,
Min Liao ,
Haiqun Cao Open the ORCID record for Haiqun Cao [Opens in a new window]  and
Ning Zhao Open the ORCID record for Ning Zhao [Opens in a new window]
Zhi Tang
Affiliation:
Graduate Student, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
Zilu Wang
Affiliation:
Graduate Student, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
Mali Wang
Affiliation:
Graduate Student, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
Fan Yin
Affiliation:
Graduate Student, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
Min Liao
Affiliation:
Associate Professor, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
Haiqun Cao
Affiliation:
Professor, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
Ning Zhao*
Affiliation:
Associate Professor, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China
*
Corresponding author: Ning Zhao, Anhui Province Key Laboratory of Crop Integrated Pest Management, School of Plant Protection, Anhui Agricultural University, Hefei, China. (Email: zhaon@ahau.edu.cn)
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Abstract

Shortawn foxtail (Alopecurus aequalis Sobol.) is an obligate wetland plant that is widely distributed throughout Europe, temperate Asia, and North America. In China, it is widespread in the middle and lower reaches of the Yangtze River as a noxious weed in winter cropping fields with a rice (Oryza sativa L.) rotation. The acetolactate synthase (ALS)-inhibiting herbicide mesosulfuron-methyl has been widely used to control annual grass and broadleaf weeds, including A. aequalis, in wheat (Triticum aestivum L.) fields, leading to the selection of herbicide-resistant weeds. In this study, an A. aequalis population, AHFT-4, that survived mesosulfuron-methyl at the field-recommended rate (9 g ai ha−1) was collected in Anhui Province. Single-dose testing confirmed that the suspected resistant AHFT-4 had evolved resistance to mesosulfuron-methyl. Target gene sequencing revealed a resistance mutation of Pro-197-Ala in ALS1 of the resistant plants, and a derived cleaved amplified polymorphic sequence marker was developed to specifically detect the mutation. A relative expression assay showed no significant difference in ALS expression between AHFT-4 and a susceptible population without or with mesosulfuron-methyl treatment. Whole-plant dose–response bioassays indicated that AHFT-4 had evolved broad-spectrum cross-resistance to ALS-inhibiting herbicides of all five chemical families tested, with GR50 resistance index (RI) values ranging from 21 to 206. However, it remained susceptible to the photosystem II inhibitor isoproturon. Pretreatment with the cytochrome P450 inhibitor malathion or the glutathione S-transferase inhibitor 4-chloro-7-nitrobenzoxadiazole had no significant effects on the resistance of AHFT-4 to mesosulfuron-methyl. To our knowledge, this study reports for the first time the ALS gene Pro-197-Ala substitution conferring broad-spectrum cross-resistance to ALS-inhibiting herbicides in A. aequalis.

Keywords

Acetolactate synthetase (ALS)cross-resistancegrass weedherbicide resistancetarget-site mutation
Type
Research Article
Information
Weed Science , Volume 71 , Issue 3 , May 2023 , pp. 224 - 232
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Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of the Weed Science Society of America

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Footnotes

Associate Editor: Vipan Kumar, Cornell University

*

These authors contributed equally to this work.

References

Beckie, HJ, Tardif, FJ (2012) Herbicide cross resistance in weeds. Crop Prot 35:15–28 CrossRefGoogle Scholar
Bobadilla, LK, Hulting, AG, Berry, PA, Moretti, ML, Mallory-Smith, C (2021) Frequency, distribution, and ploidy diversity of herbicide-resistant Italian ryegrass (Lolium perenne spp. multiflorum) populations of western Oregon. Weed Sci 69:177–185 CrossRefGoogle Scholar
Christopher, JT, Preston, C, Powles, SB (1994) Malathion antagonizes metabolism-based chlorsulfuron resistance in Lolium rigidum . Pestic Biochem Physiol 49:172–182 CrossRefGoogle Scholar
Cope, TA (1982) Poaceae. Page 678 in Nasir, E, Ali, SI, eds. Flora of Pakistan. Fascicle No. 143. Islamabad, Pakistan: National Herbarium Google Scholar
Cummins, I, Wortley, DJ, Sabbadin, F, He, ZS, Coxon, CR, Straker, HE, Sellars, JD, Knight, K, Edwards, L, Hughes, D (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110:5812–5817 CrossRefGoogle ScholarPubMed
Gaines, TA, Duke, SO, Morran, S, Rigon, CAG, Tranel, PJ, Küpper, A, Dayan, FE (2020) Mechanisms of evolved herbicide resistance. J Biol Chem 295:10307–10330 CrossRefGoogle ScholarPubMed
Garcia, MD, Nouwens, A, Lonhienne, TG, Guddat, LW (2017) Comprehensive understanding of acetohydroxyacid synthase inhibition by different herbicide families. Proc Natl Acad Sci USA 114:E1091–E1100 CrossRefGoogle ScholarPubMed
Guo, W, Chi, Y, Feng, L, Tian, X, Liu, W, Wang, J (2018) Fenoxaprop-P-ethyl and mesosulfuron-methyl resistance status of shortawn foxtail (Alopecurus aequalis Sobol.) in eastern China. Pestic Biochem Physiol 148:126–132 CrossRefGoogle ScholarPubMed
Guo, W, Yuan, G, Liu, W, Bi, Y, Du, L, Zhang, C, Li, Q, Wang, J (2015) Multiple resistance to ACCase and AHAS-inhibiting herbicides in shortawn foxtail (Alopecurus aequalis Sobol.) from China. Pestic Biochem Physiol 124:66–72 CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98 Google Scholar
Hashim, S, Hachinohe, M, Matsumoto, H (2010) Cloning and expression analysis of alpha-tubulin genes in water foxtail (Alopecurus aequalis). Weed Sci 58:89–95 Google Scholar
Heap, IM (2023) The International Herbicide-Resistant Weed Database. http://www.weedscience.org. Accessed: February 13, 2023Google Scholar
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
Jugulam, M, Shyam, C (2019) Non-target-site resistance to herbicides: recent developments. Plants 8:417 CrossRefGoogle ScholarPubMed
Kaloumenos, NS, Tsioni, VC, Daliani, EG, Papavassileiou, SE, Vassileiou, AG, Laoutidou, PN, Eleftherohorinos, IG (2012) Multiple Pro-197 substitutions in the acetolactate synthase of rigid ryegrass (Lolium rigidum) and their impact on chlorsulfuron activity and plant growth. Crop Prot 38:35–43 CrossRefGoogle Scholar
Kumar, V, Jha, P (2017) First report of Ser653Asn mutation endowing high-level resistance to imazamox in downy brome (Bromus tectorum L.). Pest Manag Sci 73:2585–2591 CrossRefGoogle ScholarPubMed
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 67:380–388 Google Scholar
Liu, K, Luo, K, Mao, A, Pan, L, Yan, B, Wu, J, Hu, L, Liu, M, Liu, X, Bai, L (2020) Endophytes enhance Asia minor bluegrass (Polypogon fugax) resistance to quizalofop-p-ethyl. Plant Soil 450:373–384 CrossRefGoogle Scholar
Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408 CrossRefGoogle Scholar
Lonhienne, T, Garcia, MD, Pierens, G, Mobli, M, Nouwens, A, Guddat, LW (2018) Structural insights into the mechanism of inhibition of AHAS by herbicides. Proc Natl Acad Sci USA 115:E1945–E1954 CrossRefGoogle ScholarPubMed
Matzrafi, M, Peleg, Z, Lati, R (2021) Herbicide resistance in weed management. Agronomy 11:280 CrossRefGoogle Scholar
McCourt, JA, Pang, SS, King-Scott, J, Guddat, LW, Duggleby, RG (2006) Herbicide-binding sites revealed in the structure of plant acetohydroxyacid synthase. Proc Natl Acad Sci USA 103:569–573 CrossRefGoogle ScholarPubMed
Mora, DA, Cheimona, N, Palma-Bautista, C, Rojano-Delgado, AM, Osuna-Ruiz, MD, de la Cruz, RA, De Prado, R (2019) Physiological, biochemical and molecular bases of resistance to tribenuron-methyl and glyphosate in Conyza canadensis from olive groves in southern Spain. Plant Physiol Biochem 144:14–21 CrossRefGoogle ScholarPubMed
Morishima, H, Oka, HI (1980) The impact of copper pollution on water foxtail (Alopecurus aequalis Sobol.) populations and winter weed communities in rice fields. Agro-Ecosystems 6:33–49 CrossRefGoogle Scholar
Murphy, BP, Tranel, PJ (2019) Target-site mutations conferring herbicide resistance. Plants 8:382 CrossRefGoogle ScholarPubMed
Nandula, VK, Riechers, DE, Ferhatoglu, Y, Barrett, M, Duke, SO, Dayan, FE, Goldberg-Cavalleri, A, Tétard-Jones, C, Wortley, DJ, Onkokesung, N, Brazier-Hicks, M, Edwards, R, Gaines, T, Iwakami, S, Jugulam, M, Ma, R (2019) Herbicide metabolism: crop selectivity, bioactivation, weed resistance, and regulation. Weed Sci 67:149–175 CrossRefGoogle Scholar
Neff, MM, Turk, E, Kalishman, M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615 CrossRefGoogle ScholarPubMed
Norsworthy, JK, Ward, SM, Shaw, DR, Llewellyn, RS, Nichols, RL, Webster, TM, Bradley, KW, Frisvold, G, Powles, SB, Burgos, NR (2012) Reducing the risks of herbicide resistance: best management practices and recommendations. Weed Sci 60:31–62 CrossRefGoogle Scholar
Ntoanidou, S, Kaloumenos, N, Diamantidis, G, Madesis, P, Eleftherohorinos, I (2016) Molecular basis of cyperus difformis cross-resistance to ALS-inhibiting herbicides. Pestic Biochem Physiol 127:38–45 CrossRefGoogle ScholarPubMed
Porebski, S, Bailey, LG, Baum, BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15 CrossRefGoogle Scholar
Rigon, CA, Gaines, TA, Küpper, A, Dayan, FE (2020) Metabolism-based herbicide resistance, the major threat among the non-target site resistance mechanisms. Outlooks Pest Manag 31:162–168 CrossRefGoogle Scholar
Rodriguez, J, Hauvermale, A, Carter, A, Zuger, R, Burke, IC (2021) An ALA122THR substitution in the AHAS/ALS gene confers imazamox-resistance in Aegilops cylindrica . Pest Manag Sci 77:4583–4592 CrossRefGoogle Scholar
Sada, Y, Uchino, A (2017) Biology and mechanisms of sulfonylurea resistance in Schoenoplectiella juncoides, a noxious sedge in the rice paddy fields of Japan. Weed Biol Manag 17:125–135 CrossRefGoogle Scholar
Schloss, JV (1990) Acetolactate synthase, mechanism of action and its herbicide binding site. Pestic Sci 29:283–292 CrossRefGoogle Scholar
Sen, MK, Hamouzová, K, Mikulka, J, Bharati, R, Košnarová, P, Hamouz, P, Roy, A, Soukup, J (2021) Enhanced metabolism and target gene overexpression confer resistance against acetolactate synthase-inhibiting herbicides in Bromus sterilis . Pest Manag Sci 77:2122–2128 CrossRefGoogle ScholarPubMed
Sibony, M, Michel, A, Haas, HU, Rubin, B, Hurle, K (2001) Sulfometuron-resistant amaranthus retroflexus: cross-resistance and molecular basis for resistance to acetolactate synthase-inhibiting herbicides. Weed Res 41:509–522 CrossRefGoogle Scholar
Tehranchian, P, Nandula, VK, Matzrafi, M, Jasieniuk, M (2019) Multiple herbicide resistance in California Italian ryegrass (Lolium perenne ssp. multiflorum): characterization of ALS-inhibiting herbicide resistance. Weed Sci 67:273–280 CrossRefGoogle Scholar
Tranel, PJ, Wright, TR, Heap, IM (2022) Mutations in Herbicide-Resistant Weeds to ALS Inhibitors. http://www.weedscience.com/Pages/MutationDisplayAll.aspx. Accessed: December 26, 2022Google Scholar
Wang, M, Tang, Z, Liao, M, Cao, H, Zhao, N (2023) Loop-mediated isothermal amplification for detecting the Ile-2041-Asn mutation in fenoxaprop-P-ethyl-resistant Alopecurus aequalis . Pest Manag Sci 79:711–718 CrossRefGoogle ScholarPubMed
Xia, W, Pan, L, Li, J, Wang, Q, Feng, Y, Dong, L (2015) Molecular basis of ALS-and/or ACCase-inhibitor resistance in shortawn foxtail (Alopecurus aequalis Sobol.). Pestic Biochem Physiol 122:76–80 CrossRefGoogle ScholarPubMed
Yu, Q, Han, HP, Powles, SB (2008) Mutations of the ALS gene endowing resistance to ALS-inhibiting herbicides in Lolium rigidum populations. Pest Manag Sci 64:1229–1236 CrossRefGoogle ScholarPubMed
Yu, Q, Powles, SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350 CrossRefGoogle ScholarPubMed
Yuan, JS, Tranel, PJ, Stewart, CN (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13 CrossRefGoogle ScholarPubMed
Zhang, F, Bai, S, Wang, H, Liu, W, Wang, J (2019) Greenhouse and field evaluation of a novel HPPD-inhibiting herbicide, QYM201, for weed control in wheat. Sci Rep 9:1625 CrossRefGoogle ScholarPubMed
Zhao, N, Yan, Y, Du, L, Zhang, X, Liu, W, Wang, J (2020) Unravelling the effect of two herbicide resistance mutations on acetolactate synthase kinetics and growth traits. J Exp Bot 71:3535–3542 CrossRefGoogle ScholarPubMed
Zhao, N, Yan, Y, Ge, L, Zhu, B, Liu, W, Wang, J (2019) Target site mutations and cytochrome P450s confer resistance to fenoxaprop-P-ethyl and mesosulfuron-methyl in Alopecurus aequalis . Pest Manag Sci 75:204–214 CrossRefGoogle ScholarPubMed
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
Zhao, N, Yan, Y, Wang, H, Bai, S, Wang, Q, Liu, W, Wang, J (2018) Acetolactate synthase overexpression in mesosulfuron-methyl-resistant shortawn foxtail (Alopecurus aequalis Sobol.): reference gene selection and herbicide target gene expression analysis. J Agric Food Chem 66:9624–9634 CrossRefGoogle ScholarPubMed
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