Skip to main content Accessibility help

Article contents

Variation in tolerance mechanisms to fluazifop-P-butyl among selected zoysiagrass lines

Published online by Cambridge University Press:  05 April 2019

Wenwen Liu
Graduate Research Assistant, Department of Agronomy, University of Florida, Gainesville, FL, USA
Gregory E. MacDonald
Professor, Department of Agronomy, University of Florida, Gainesville, FL, USA
J. Bryan Unruh
Professor, West Florida Research and Education Center, University of Florida, Jay, FL, USA
Kevin E. Kenworthy
Professor, Department of Agronomy, University of Florida, Gainesville, FL, USA
Laurie E. Trenholm
Professor, Department of Environmental Horticulture, University of Florida, Gainesville, FL, USA
Ramon G. Leon
Assistant Professor, Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC, USA
E-mail address:


Breeding herbicide tolerance into new cultivars can improve safety and weed control in turfgrass systems. The sensitivity to fluazifop-P-butyl of 27 zoysiagrass (Zoysia spp.) lines was screened under greenhouse conditions to identify potential tolerant germplasm for breeding programs. The herbicide rate that caused 50% biomass reduction (GR50) and the rate that caused 50% injury (ID50) were calculated to select the three most-tolerant and the five most-susceptible lines for studying the physiological mechanisms responsible for fluazifop-P-butyl tolerance. The differences in GR50 and ID50 between susceptible and tolerant lines ranged from 4-fold to more than 10-fold. Cytochrome P450–mediated metabolism was not detected in fluazifop-P-butyl–tolerant lines. Sequencing of the ACCase gene confirmed that none of the seven previously reported mutations conferring resistance to acetyl-CoA carboxylase (ACCase)-inhibiting herbicides in other species were present in any of the tolerant or susceptible zoysiagrass lines studied. An Ala-2073-Thr substitution was identified in two tolerant lines, but this mutation did not completely explain the tolerant phenotype. No clear differences in absorption and translocation rates of 14C-radiolabeled fluazifop-P-butyl were observed among most lines, with the exception of a susceptible line that exhibited greater translocation than two of the tolerant lines. Metabolite profiles did not differ between tolerant and susceptible lines. Our results suggest that the diversity in tolerance to fluazifop-P-butyl in zoysiagrass germplasm is most likely the result of a combination of different, minor, additive non–target site mechanisms such as translocation rate and compartmentation after absorption.

Research Article
© 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.


Anonymous (2009) Fusilade® II product label. Syngenta Crop Protection. Greensboro, NC: Syngenta. 37 p.Google Scholar
Baerg, RJ, Barrett, M, Polge, ND (1996) Insecticide and insecticide metabolite interactions with cytochrome P450 mediated activities in maize. Pestic Biochem Physiol 55:1020CrossRefGoogle ScholarPubMed
Boydston, RA (1992) Drought stress reduces fluazifop-P activity on green foxtail (Setaria viridis). Weed Sci 40:2024Google Scholar
Carr, JE, Davies, LG, Cobb, AH, Pallet, KE (1985) The metabolic activity of fluazifop acid in excised apical meristem sections. Pages 155162 in Proceedings of the British Crop Protection Conference, Weeds. Volume 1. Brighton, UK: British Crop Protection CouncilGoogle Scholar
Délye, C, Matejicek, A, Gasquez, J (2002) PCR-based detection of resistance to acetyl-CoA carboxylase-inhibiting herbicides in black-grass (Alopecurus myosuroides Huds) and ryegrass (Lolium rigidum Gaud). Pest Manag Sci 58:474478CrossRefGoogle Scholar
Délye, C, Zhang, XQ, Michel, S, Matejicek, A, Powles, SB (2005) Molecular bases for sensitivity to acetyl-coenzyme a carboxylase inhibitors in black-grass. Plant Physiol 137:794806CrossRefGoogle ScholarPubMed
Devine, MD (1997) Mechanisms of resistance to acetyl-coenzyme A carboxylase inhibitors: a review. Pestic Sci 51:2592643.0.CO;2-S>CrossRefGoogle Scholar
Devine, MD, Hall, LM (1990) Implications of sucrose transport mechanisms for the translocation of herbicides. Weed Sci 38:299304Google Scholar
Ferhatoglu, Y, Avdiushko, S, Barrett, M (2005) The basis for the safening of clomazone by phorate insecticide in cotton and inhibitors of cytochrome P450s. Pestic Biochem Physiol 81:5970CrossRefGoogle Scholar
Goggin, DE, Kaur, P, Owen, MJ,Powles, SB (2018) 2,4-D and dicamba resistance mechanisms in wild radish: subtle, complex and population specific? Ann Bot 122:627640CrossRefGoogle ScholarPubMed
Haughn, GW, Somerville, C (1986) Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol Gen Genet 204:430434CrossRefGoogle Scholar
Heap, IM (2018) The International Survey of Herbicide-Resistant Weeds. Accessed: August 23, 2018CrossRefGoogle Scholar
Hendley, P, Dicks, JW, Monaco, TJ, Slyfield, SM, Tummon, OJ, Barrett, JC (1985) Translocation and metabolism of pyrin-dinyloxy-p henoxypropionate herbicides in rhizomatous quackgrass (Agropyron repens). Weed Sci 33:1124Google Scholar
Hidayat, I, Preston, C (2001) Cross-resistance to imazethapyr in a fluazifop-P-butyl-resistant population of Digitaria sanguinalis. Pestic Biochem Physiol 71:190195CrossRefGoogle Scholar
Hunter, JH (1995) Effect of bud vs rosette growth stage on translocation of 14C-glyphosate in Canada thistle (Cirsium arvense). Weed Sci 43:347351Google Scholar
Jander, G, Baerson, SR, Hudak, JA, Gonzalez, KA, Gruys, KJ, Last, RL (2003) Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol 131:139146CrossRefGoogle ScholarPubMed
Johnson, BJ (1992) Common bermudagrass (Cynodon dactylon) suppression in Zoysia spp. with herbicides. Weed Technol 6:813819CrossRefGoogle Scholar
Kimball, JA, Zuleta, MC, Kenworthy, KE, Lehman, VG, Milla-Lewis, S (2012) Assessment of genetic diversity in Zoysia species using amplified fragment length polymorphism. Crop Sci 52:360370CrossRefGoogle Scholar
Leon, RG, Unruh, JB, Brecke, BJ, Kenworthy, KE (2014) Characterization of fluazifop-P-butyl tolerance in zoysiagrass cultivars. Weed Technol 28:385394CrossRefGoogle Scholar
Liu, WJ, Harrison, DK, Chalupska, D, Gornicki, P, O’Donnell, CC, Adkins, SW, Haselkorn, R, Williams, RR (2007) Single-site mutations in the carboxyltransferase domain of plastid acetyl-CoA carboxylase confer resistance to grass-specific herbicides. Proc Natl Acad Sci USA 104:36273632CrossRefGoogle ScholarPubMed
Liu, W, MacDonald, GE, Unruh, JB, Kenworthy, KE, Trenholm, LE, Leon, RG (2017) Application timing affects tolerance of zoysiagrass to fluazifop-P-butyl and safening effect of triclopyr. Abstract 271-11 in ASA-CSSA-SSSA Annual Meeting Abstracts. Tampa, FL, October 2017.Google Scholar
McElroy, JS, Breeden, GK (2006) Triclopyr safens the use of fluazifop and fenoxaprop on zoysiagrass while maintaining bermudagrass suppression. Appl Turfgrass Sci 3, 10.1094/ATS-2006-0502-01-RSCrossRefGoogle Scholar
Moore, KA, Zuleta, MC, Patton, AJ, Schwartz, BM, Aranaz, G, Milla-Lewis, SR (2017) SSR allelic diversity shifts in zoysiagrass (Zoysia spp.) cultivar released from 1910 to 2016. Crop Sci 57:S1S12CrossRefGoogle Scholar
Patton, A, Schwartz, BM, Kenworthy, KE (2017a) Zoysiagrass (Zoysia spp.) history, utilization, and improvement in the United States: a review. Crop Sci 57:S37S72CrossRefGoogle Scholar
Patton, AJ, Trappe, JM, Doroh, MC, McElroy, JS (2017b) Evaluation of herbicides and their tank-mixes for suppression of bermudagrass in zoysiagrass. Int Turf Soc Res J 13:716722Google Scholar
Petit, C, Duhieu, B, Boucansaud, K, Délye, C (2010) Complex genetic control of non-target-site-based resistance to herbicides inhibiting acetyl-coenzyme A carboxylase and acetolactate-synthase in Alopecurus myosuroides Huds. Plant Sci 178:501509CrossRefGoogle Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347CrossRefGoogle ScholarPubMed
Preston, C, Tardif, FJ, Christopher, JT, Powles, SB (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 54:123134CrossRefGoogle Scholar
San Cha, T, Najihah, MG, Sahid, IB, Chuah, TS (2014) Molecular basis for resistance to ACCase-inhibiting fluazifop in Eleusine indica from Malaysia. Pestic Biochem Physiol 111:713Google Scholar
Shah, DM, Horsch, RB, Klee, KJ, Kishore, GM, Winter, JA, Tumer, NE, Hironaka, CM, Sander, PR, Gasser, CS, Aykent, S, Siegel, NR, Roger, SG, Fraley, RT (1986) Engineering herbicide tolerance in transgenic plants. Science 233:748–481CrossRefGoogle ScholarPubMed
Souza Machado, V, Bandeen, JD, Stephenson, GR, Lavigne, P (1978) Uniparental inheritance of chloroplast atrazine tolerance in Brassica campestris. Can J Plant Sci 58:977981CrossRefGoogle Scholar
Sun, Y, Zhang, X, Wu, C, He, Y, Ma, Y, Hou, H, Guo, X, Du, W, Zhao, Y, Xia, L (2016) Engineering herbicide-resistant plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9:628631CrossRefGoogle ScholarPubMed
Tang, W, Zhou, F, Chen, J, Zhou, X (2014) Resistance to ACCase-inhibiting herbicides in an Asia minor bluegrass (Polypogon fugax) population in China. Pestic Biochem Physiol 108:1620CrossRefGoogle Scholar
Tardif, FJ, Hokum, JAM, Powles, SB (1993) Occurrence of a herbicide-resistant acetyl-coenzyme A carboxylase mutant in annual ryegrass (Lolium rigidum) selected by sethoxydim. Planta 190:176181CrossRefGoogle Scholar
Tate, TM (2012) Characterization of Acetyl Coenzyme A Inhibitor Resistance in Turfgrass and Grassy Weeds. Ph.D dissertation. University of Georgia, Griffin. 56 pGoogle Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2005) Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol 167:787796CrossRefGoogle ScholarPubMed
Werck-Reichhart, D, Hehn, A, Didierjean, L (2000) Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci 5:116123CrossRefGoogle ScholarPubMed
Yu, Q, Collavo, A, Zheng, MQ, Owen, M, Sattin, M, Powles, SB (2007) Diversity of acetyl-coenzyme a carboxylase mutation in resistant Lolium populations: evaluation using clethodim. Plant Physiol 145:547558CrossRefGoogle ScholarPubMed

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 6
Total number of PDF views: 58 *
View data table for this chart

* Views captured on Cambridge Core between 05th April 2019 - 15th January 2021. This data will be updated every 24 hours.

Hostname: page-component-77fc7d77f9-6mlss Total loading time: 0.701 Render date: 2021-01-15T22:06:27.084Z Query parameters: { "hasAccess": "0", "openAccess": "0", "isLogged": "0", "lang": "en" } Feature Flags last update: Fri Jan 15 2021 21:51:19 GMT+0000 (Coordinated Universal Time) Feature Flags: { "metrics": true, "metricsAbstractViews": false, "peerReview": true, "crossMark": true, "comments": true, "relatedCommentaries": true, "subject": true, "clr": true, "languageSwitch": true, "figures": false, "newCiteModal": false, "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true }

Send article to Kindle

To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Variation in tolerance mechanisms to fluazifop-P-butyl among selected zoysiagrass lines
Available formats

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Variation in tolerance mechanisms to fluazifop-P-butyl among selected zoysiagrass lines
Available formats

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Variation in tolerance mechanisms to fluazifop-P-butyl among selected zoysiagrass lines
Available formats

Reply to: Submit a response

Your details

Conflicting interests

Do you have any conflicting interests? *