Hostname: page-component-848d4c4894-p2v8j Total loading time: 0 Render date: 2024-06-09T19:36:30.293Z Has data issue: false hasContentIssue false
  • English
  • Français

Non–target site based resistance to the ALS-inhibiting herbicide mesosulfuron-methyl in American sloughgrass (Beckmannia syzigachne)

Published online by Cambridge University Press:  30 May 2019

Mingliang Wang ,
Bingqi Liu ,
Yihui Li ,
Xiaoyong Luo  and
Lingxu Li Open the ORCID record for Lingxu Li [Opens in a new window]
Mingliang Wang
Affiliation:
Master’s Student, College of Plant Health and Medicine, Qingdao Agricultural University, Shandong Qingdao, People’s Republic of China
Bingqi Liu
Affiliation:
Master’s Student, College of Plant Health and Medicine, Qingdao Agricultural University, Shandong Qingdao, People’s Republic of China
Yihui Li
Affiliation:
Master’s Student, College of Plant Health and Medicine, Qingdao Agricultural University, Shandong Qingdao, People’s Republic of China
Xiaoyong Luo
Affiliation:
Professor, College of Plant Health and Medicine, Qingdao Agricultural University, Shandong Qingdao, People’s Republic of China
Lingxu Li*
Affiliation:
Associate Professor, College of Plant Health and Medicine, Qingdao Agricultural University, Shandong Qingdao, People’s Republic of China
*
Author for correspondence: Lingxu Li, College of Plant Health and Medicine, Qingdao Agricultural University, Shandong Qingdao 266109, People’s Republic of China. Email: lingxulipvi@126.com
Get access Rights & Permissions [Opens in a new window]

Abstract

American sloughgrass [Beckmannia syzigachne (Steud.) Fernald] is one of the most predominant and troublesome weeds in wheat (Triticum aestivum L.) fields rotated with rice (Oryza sativa L.) in China. Mesosulfuron-methyl is one of the main herbicides used to selectively control B. syzigachne in winter wheat fields in China. After many years of application, mesosulfuron-methyl failed to control B. syzigachne in Yutai County. The objectives of this study were to determine the resistance level to mesosulfuron-methyl and other acetolactate synthase (ALS) inhibitors in the B. syzigachne population collected from Yutai County (R) and identify the mechanism of resistance. The results indicated that the R population was 4.1-fold resistant to mesosulfuron-methyl and was cross-resistant to pyroxsulam (600-fold), imazethapyr (4.1-fold), flucarbazone (12-fold), and bispyribac-sodium (12-fold). In vitro assays revealed that ALS in the R population was as sensitive as that in a susceptible (S) population. Gene sequence analysis identified no known resistant mutations in the ALS gene of the R population. Furthermore, real-time quantitative reverse transcriptase PCR experiments indicated that the expression level of the ALS gene in the R population was not different from that of the S population. However, the cytochrome P450 inhibitor malathion reversed the R population's resistance to mesosulfuron-methyl. The result of ultraperformance liquid chromatography–tandem mass spectrometry (UPLC-MS-MS) spectral analysis indicated that the metabolic rates of mesosulfuron-methyl in the R population were significantly faster than in the S population. Therefore, non-target resistance to mesosulfuron-methyl has been demonstrated in the R population. The resistance was very likely caused by enhanced herbicide metabolism.

Keywords

Steven S. Seefeldt, Washington State UniversityALS-inhibitor resistanceenzyme sensitivityexpression levelgene sequencemetabolic rate
Type
Research Article
Information
Weed Science , Volume 67 , Issue 5 , September 2019 , pp. 527 - 533
Copyright
© Weed Science Society of America, 2019 

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.)

References

Bai, S, Liu, W, Wang, H, Zhao, N, Jia, S, Zou, N, Guo, W, Wang, J (2018) Enhanced herbicide metabolism and metabolic resistance genes identified in tribenuron-methyl resistant Myosoton aquaticum L. J Agric Food Chem 66:9850–9857CrossRefGoogle ScholarPubMed
Beckie, H, Tardif, F (2012) Herbicide cross resistance in weeds. Crop Prot 35:15–28CrossRefGoogle Scholar
Bradford, M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle ScholarPubMed
Chatham, L, Wu, C, Riggins, C, Hager, A, Young, B, Roskamp, G, Tranel, P (2015) EPSPS gene amplification is present in the majority of glyphosate-resistant Illinois waterhemp (Amaranthus tuberculatus) populations. Weed Technol 29:48–55CrossRefGoogle Scholar
Chen, J, Huang, H, Zhang, C, Wei, S, Huang, Z, Chen, J, Wang, X (2015) Mutations and amplification of EPSPS gene confer resistance to glyphosate in goosegrass (Eleusine indica). Planta 242:859–868CrossRefGoogle Scholar
Christopher, J, Preston, C, Powles, S (1994) Malathion antagonizes metabolism-based chlorsulfuron resistance. Pestic Biochem Physiol 49:172–182CrossRefGoogle 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 69:176–187CrossRefGoogle Scholar
Didierjean, L, Gondet, L, Perkins, R, Lau, SM, Schaller, H, O’Keefe, DP, Werck-Reichhart, D (2002) Engineering herbicide metabolism in tobacco and Arabidopsis with CYP76B1, a cytochrome P450 enzyme from Jerusalem artichoke. Plant Physiol 130:179–189CrossRefGoogle ScholarPubMed
Doyle, J, Doyle, J (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus 12:13–15Google Scholar
Durner, J, Gailus, V, Boger, P (1991) New aspects on inhibition of plant acetolactate synthase by chlosulfuron and imaaquin. Plant Physiol 95:1144–1149CrossRefGoogle Scholar
Feng, Y, Gao, Y, Zhang, Y, Dong, L (2016) Mechanisms of resistance to pyroxsulam and ACCase inhibitors in Japanese foxtail (Alopecurus japonicus). Weed Sci 64:695–704CrossRefGoogle Scholar
Gaines, T, Shaner, D, Ward, S, Leach, J, Preston, C, Westra, P (2011) Mechanism of resistance of evolved glyphosate-resistant Palmer amaranth (Amaranthus palmeri). J Agric Food Chem 59:5886–5889CrossRefGoogle Scholar
Guo, J, Riggins, C, Hausman, N, Hager, A, Riechers, D, Davis, A, Tranel, P (2017) Nontarget-site resistance to ALS inhibitors in waterhemp (Amaranthus tuberculatus). Weed Sci 63:399–407CrossRefGoogle 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 8:254CrossRefGoogle Scholar
Kaiser, Y, Gerhards, R (2015) Degradation and metabolism of fenoxaprop and mesosulfuron + iodosulfuron in multiple resistant blackgrass (Alopecurus myosuroides). Gesunde Pflanzen 67:109–117CrossRefGoogle Scholar
Koo, D, Jugulam, M, Putta, K, Cuvaca, I, Peterson, D, Currie, R, Friebe, B, Gill, B (2018) Gene duplication and aneuploidy trigger rapid evolution of herbicide resistance in common waterhemp. Plant Physiol 176:1932–1938CrossRefGoogle ScholarPubMed
Kwon, C, Pennner, D (1995) Response of a chlorsulfuron-resistant biotype of Kochia scoparia to ALS inhibiting herbicides and piperonyl butoxide. Weed Sci 43:561–565CrossRefGoogle 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 73:2227–2235CrossRefGoogle Scholar
Li, L, Bi, Y, Liu, W, Yuan, G, Wang, J (2013) Molecular basis for resistance to fenoxaprop-p-ethyl in American sloughgrass (Beckmannia syzigachne Steud.). Pestic Biochem Physiol 105:118–121CrossRefGoogle Scholar
Li, L, Liu, W, Chi, Y, Guo, W, Luo, X, Wang, J (2015) Molecular mechanism of mesosulfuron-methyl resistance in multiply-resistant american sloughgrass (Beckmannia syzigachne). Weed Sci 63:781–787CrossRefGoogle Scholar
Li, W, Zhang, L, Zhao, N, Guo, W, Liu, W, Li, L, Wang, J (2017) Multiple resistance to ACCase and ALS-inhibiting herbicides in Beckmannia syzigachne (Steud.) Fernald without mutations in the target enzymes. Chil J Agric Res 77:257–265CrossRefGoogle Scholar
Liu, W, Bai, S, Zhao, N, Jia, S, Li, W, Zhang, L, Wang, J (2018) Non-target site-based resistance to tribenuron-methyl and essential involved genes in Myosoton aauaticum (L.). Plant Biol 18:225–238Google Scholar
Mei, Y, Si, C, Liu, M, Qiu, L, Zheng, M (2017) Investigation of resistance levels and mechanisms to nicosulfuron conferred by non-target-site mechanisms in large crabgrass (Digitaria sanguinalis L.) from China. Pestic Biochem Physiol 141:84–89CrossRefGoogle ScholarPubMed
Owen, M, Goggin, D, Powles, S (2011) Non-traget-site-based resistance to ALS-inhibiting herbicides in six Bromus rigidus populations from Western Australian cropping fields. Pest Manag Sci 68:1077–1082CrossRefGoogle Scholar
Powles, S, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347CrossRefGoogle ScholarPubMed
Preston, C, Tardif, F, Christopher, J, Powles, S (1996) Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide degrading enzymes. Pestic Biochem Physiol 54:123–134CrossRefGoogle Scholar
Ray, T (1986) Sulfonylurea herbicides as inhibitors of amino acid biosynthesis in plants. Trends Biochem Sci 11:180–183CrossRefGoogle Scholar
Sammons, R, Gaines, T (2014) Glyphosate resistance: state of knowledge. Pest Manage Sci 70:1367–1377CrossRefGoogle ScholarPubMed
Schmittgen, T, Livak, K (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108CrossRefGoogle Scholar
Seefeldt, S, Jensen, J, Fuerst, E (1995) Log-logistic analysis of herbicide dose response relationship. Weed Technol 9:218–227CrossRefGoogle Scholar
Wang, J, Li, X, Li, D, Han, Y, Li, Z, Yu, H, Cui, H (2018) Non-target-site and target-site resistance to AHAS inhibitors in american sloughgrass (Beckmannia syzigachne). J Integr Agric 17:30345–30347CrossRefGoogle Scholar
Wrzesińska, B, Kierzek, R, Obrępalska-Stęplowska, A (2016) Evaluation of six commonly used reference genes for gene expression studies in herbicide-resistant Avena fatua biotypes. Weed Res 56:284–292CrossRefGoogle Scholar
Xu, J, Wang, X-Y, Guo, W-Z (2015) The cytochrome P450 superfamily: key players in plant development and defense. J Integr Agric 14:1673–1686CrossRefGoogle Scholar
Yang, Q, Li, J, Shen, J, Xu, Y, Liu, H, Deng, W, Li, X, Zheng, M (2018) Metabolic resistance to acetolactate synthase inhibiting herbicide tribenuron-methyl in Descurainia sophia L. mediated by cytochrome P450 enzymes. J Agric Food Chem 66:4319–4327CrossRefGoogle ScholarPubMed
Yu, Q, Abdallah, I, Han, H, Owen, M, Powles, S (2009) Distinct non-target site mechanisms endow resistance to glyphosate, ACCase and ALS-inhibiing herbicides in multiple herbicide-resistant Lolium rigidum. Planta 230:713–723CrossRefGoogle ScholarPubMed
Yu, Q, Friesen, L, Zhang, X, Powles, S (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 78:21–30CrossRefGoogle Scholar
Yu, Q, Powles, S (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350CrossRefGoogle ScholarPubMed
Yuan, J, Tranel, P, Stewart, C J r (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13CrossRefGoogle ScholarPubMed
Zhao, B, Fu, D, Yu, Y, Huang, C, Yan, K, Li, P, Shafi, J, Zhu, H, Wei, S, Ji, M (2017) Non-target-site resistance to ALS-inhibiting herbicides in a Sagittaria trifolia L. population. Pestic Biochem Physiol 140:79–84CrossRefGoogle Scholar
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 66:9624–9634CrossRefGoogle ScholarPubMed