Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-30T16:17:50.511Z Has data issue: false hasContentIssue false

Plastidic ACCase Ile-1781-Leu is present in pinoxaden-resistant southern crabgrass (Digitaria ciliaris)

Published online by Cambridge University Press:  09 October 2019

Suma Basak*
Affiliation:
Graduate Research Assistant, Department of Crop, Soil, and Environmental Sciences, Auburn University, Auburn, AL, USA
J. Scott McElroy
Affiliation:
Professor, Department of Crop, Soil, and Environmental Sciences, Auburn University, Auburn, AL, USA
Austin M. Brown
Affiliation:
Graduate Research Assistant, Department of Crop, Soil, and Environmental Sciences, Auburn University, Auburn, AL, USA
Clebson G. Gonçalves
Affiliation:
Graduate Research Assistant, Department of Crop, Soil, and Environmental Sciences, Auburn University, Auburn, AL, USA
Jinesh D. Patel
Affiliation:
Research Associate, Department of Crop, Soil, and Environmental Sciences, Auburn University, Auburn, AL, USA
Patrick E. McCullough
Affiliation:
Associate Professor, Department of Crop and Soil Sciences, University of Georgia, Griffin, GA, USA
*
Author for correspondence: Suma Basak, Department of Crop, Soil, and Environmental Sciences, 201 Funchess Hall, Auburn University, Auburn, AL 36849. Email: szb0099@auburn.edu

Abstract

Southern crabgrass [Digitaria ciliaris (Retz.) Koeler] is an annual grass weed that commonly infests turfgrass, roadsides, wastelands, and cropping systems throughout the southeastern United States. Two biotypes of D. ciliaris (R1 and R2) with known resistance to cyclohexanediones (DIMs) and aryloxyphenoxypropionates (FOPs) previously collected from sod production fields in Georgia were compared with a separate susceptible biotype (S) collected from Alabama for the responses to pinoxaden and to explore the possible mechanisms of resistance. Increasing rates of pinoxaden (0.1 to 23.5 kg ha−1) were evaluated for control of R1, R2, and S. The resistant biotypes, R1 and R2, were resistant to pinoxaden relative to S. The S biotype was completely controlled at rates of 11.8 and 23.5 kg ha−1, resulting in no aboveground biomass at 14 d after treatment. Pinoxaden rates at which tiller length and aboveground biomass would be reduced 50% (I50) and 90% (I90) for R1, R2, and S ranged from 7.2 to 13.2 kg ha−1, 6.9 to 8.6 kg ha−1, and 0.7 to 2.1 kg ha−1, respectively, for tiller length, and 7.7 to 10.2 kg ha−1, 7.2 to 7.9 kg ha−1, and 1.6 to 2.3 kg ha−1, respectively, for aboveground biomass. Prior selection pressure from DIM and FOP herbicides could result in the evolution of D. ciliaris cross-resistance to pinoxaden herbicides. Amplification of the carboxyl-transferase domain of the plastidic ACCase by standard PCR identified a point mutation resulting in an Ile-1781-Leu amino acid substitution only for the resistant biotype, R1. Further cloning of PCR product surrounding the 1781 region yielded two distinct ACCase gene sequences, Ile-1781 and Leu-1781. The amino acid substitution, Ile-1781-Leu in both resistant biotypes (R1 and R2), however, was revealed by next-generation sequencing of RNA using Illumina platform. A point mutation in the Ile-1781 codon leading to herbicide insensitivity in the ACCase enzyme has been previously reported in other grass species. Our research confirms that the Ile-1781-Leu substitution is present in pinoxaden-resistant D. ciliaris.

Type
Research Article
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.)

Footnotes

Associate Editor: Dean Riechers, University of Illinois

References

Andrews, S (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc. Accessed: October 20, 2016Google Scholar
Bantilan, RT, Palada, MC, Harwood, RR (1974) Integrated weed management: 1. Ley factors affecting crop–weed balance. Philipp Weed Sci Bull 1:1436Google Scholar
Beckie, HJ, Tardif, FJ (2012) Herbicide cross resistance in weeds. Crop Prot 35:1528CrossRefGoogle Scholar
Bolger, AM, Lohse, M, Usadel, B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:21142120CrossRefGoogle ScholarPubMed
Bradley, KW, Wu, J, Hatzios, KK, Hagood, ES (2001) The mechanism of resistance to aryloxyphenoxypropionate and cyclohexanedione herbicides in a johnsongrass biotype. Weed Sci 49:477484CrossRefGoogle Scholar
Brown, AC, Moss, SR, Wilson, ZA, Field, LM (2002) An isoleucine to leucine substitution in the ACCase of Alopecurus myosuroides (black-grass) is associated with resistance to the herbicide sethoxydim. Pestic Biochem Physiol 72:160168CrossRefGoogle Scholar
Christoffers, MJ, Berg, ML, Messermith, CG (2002) An isoleucine to leucine mutation in acetyl-CoA carboxylase confers herbicide resistance in wild oat. Genome 45:10491056CrossRefGoogle ScholarPubMed
Cocker, KM, Coleman, JOD, Blair, AM, Clarke, JH, Moss, SR (2000) Biochemical mechanisms of cross-resistance to aryloxyphenoxypropionate and cyclohexanedione herbicides in populations of Avena spp. Weed Res 40:323334CrossRefGoogle Scholar
Collavo, A, Panozzo, S, Lucchesi, G, Scarabel, L, Sattin, M (2011) Characterisation and management of Phalaris paradoxa resistant to ACCase inhibitors. Crop Prot 30:293299CrossRefGoogle Scholar
Cummins, I, Moss, S, Cole, DJ, Edwards, R (1997) Glutathione transferases in herbicide-resistant and herbicide-susceptible black-grass (Alopecurus myosuroides). Pestic Sci 51:2442503.0.CO;2-2>CrossRefGoogle Scholar
Délye, C (2005) Weed resistance to acetyl coenzyme A carboxylase inhibitors: an update. Weed Sci 53:728746CrossRefGoogle Scholar
Délye, C, Calmès, E, Matéjicek, A (2002a) SNP markers for blackgrass (Alopecurus myosuroides Huds.) genotypes resistant to acetyl CoA-carboxylase inhibiting herbicides. Theor Appl Genet 104:11141120CrossRefGoogle Scholar
Délye, C, Jasieniuk, M, LeCorre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649658CrossRefGoogle ScholarPubMed
Délye, C, Matéjicek, A, Gasquez, J (2002b) 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, Pernin, F, Michel, S (2011) “Universal” PCR assays detecting mutations in acetyl coenzyme A carboxylase or acetolactate synthase that endow herbicide resistance in grass weeds. Weed Res 51:353362CrossRefGoogle Scholar
Délye, C, Wang, TY, Darmency, H (2002c) An isoleucine-leucine substitution in chloroplastic acetyl-CoA carboxylase from green foxtail (Setaria viridis L. Beauv.) is responsible for resistance to the cyclohexanedione herbicide sethoxydim. Planta 214:421427CrossRefGoogle ScholarPubMed
DePrado, JL, Osuna, MD, Heredia, A, DePrado, R (2005) Lolium rigidum, a pool of resistance mechanisms to ACCase inhibitor herbicides. J Agric Food Chem 53:21852191.CrossRefGoogle Scholar
Devine, MD (1997) Mechanisms of resistance to acetyl–coenzyme carboxylase inhibitors: a review. Pestic Sci 51:2593.0.CO;2-S>CrossRefGoogle Scholar
Gherekhloo, J, Osuna, MD, DePrado, R (2012) Biochemical and molecular basis of resistance to ACCase-inhibiting herbicides in Iranian Phalaris minor populations. Weed Res 52:367372CrossRefGoogle Scholar
Gleason, A, Cronquist, A (1991) Manual of Vascular Plants of Northeastern United States and Adjacent Canada. 2nd ed. New York: New York Botanical Garden. 910 pCrossRefGoogle Scholar
Götz, S, García-Gómez, JM, Terol, J, Williams, TD, Nagaraj, SH, Nueda, MJ, Dopazo, J, Talón, M, Robles, M, Conesa, A (2008). High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:34203435CrossRefGoogle ScholarPubMed
Grabherr, MG, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R, Zeng, Q, Chen, Z, Mauceli, E, Hacohen, N, Gnirke, A, Rhind, N, et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29:644CrossRefGoogle ScholarPubMed
Hidayat, I, Preston, C (1997) Enhanced metabolism of fluazifop acid in a biotype of Digitaria sanguinalis resistant to the herbicide fluazifop-p-butyl. Pestic Biochem Physiol 57:137146CrossRefGoogle Scholar
Hochberg, O, Sibony, M, Rubin, B (2009) The response of ACCase-resistant Phalaris paradoxa populations involves two different target site mutations. Weed Res 49:3746CrossRefGoogle Scholar
Hofer, U, Muehlebach, M, Hole, S, Zoschke, A (2006) Pinoxaden—for broad spectrum grass weed management in cereal crops. J Plant Dis Prot 20:989995Google Scholar
Ito, M, Ichikawa, E (1994) Nitrification inhibition by roots of Digitaria adscendens (H.B.K.) Henr. Weed Res (Tokyo) 39:125127.Google Scholar
Ito, M, Kobayashi, H, Ueki, K (1987) Allelopathic potential of Digitaria adscendens: inhibitory effects of previously grown soil on crop growth and weed emergence. Pages 607612In Proceedings of the 11th Asian Pacific Weed Science Society Conference. Vol. 2. Taipei, Taiwan: Asian Pacific Weed Science SocietyGoogle Scholar
Kaundun, SS (2010) An aspartate to glycine changes in the carboxyl transferase domain of acetyl CoA carboxylase and non-target-site mechanism(s) confer resistance to ACCase inhibitor herbicides in a Lolium multiflorum population. Pest Manag Sci 66:12491256CrossRefGoogle Scholar
Kaundun, SS, Bailly, GC, Dale, RP, Hutchings, SJ, McIndoe, E (2013) A novel W1999S mutation and non-target site resistance impact on acetyl-CoA carboxylase inhibiting herbicides to varying degrees in a UK Lolium multiflorum population. PLoS ONE 8:e58012CrossRefGoogle Scholar
Kuk, Y, Burgos, NR, Scott, RC (2008) Resistance profile of diclofop resistant Italian ryegrass (Lolium multiflorum) to ACCase- and ALS-inhibiting herbicides in Arkansas, USA. Weed Sci 56:614623CrossRefGoogle Scholar
Lepschi, BJ, Macfarlane, TD (1997) Digitaria aequiglumis (Poaceae), a new weed for Western Australia. Nuytsia 11:425427.Google Scholar
Letouzé, A, Gasquez, J (2003) Enhanced activity of several herbicide degrading enzymes: a suggested mechanism responsible for multiple resistance in blackgrass (Alopecurus myosuroides Hud.). Agronomie 23:601608CrossRefGoogle Scholar
Li, H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997Google Scholar
Liu, W, 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
Locke, MA, Reddy, KN, Zablotowicz, RM (2002) Weed management in conservation crop production systems. Weed Biol Manag 2:123132CrossRefGoogle Scholar
Maneechote, C, Preston, C, Powles, SB (1999) A diclofop-methyl-resistant Avena sterilis biotype with a herbicide-resistant acetyl-coenzyme A carboxylase and enhanced metabolism of diclofop-methyl. Pest Manag. Sci. 49:1051143.0.CO;2-3>CrossRefGoogle Scholar
Martins, BA, Sánchez-Olguín, E, Perez-Jones, A, Hulting, AG, Mallory-Smith, C (2014) Alleles contributing to ACCase-resistance in an Italian ryegrass (Lolium perenne ssp. multiflorum) population from Oregon. Weed Sci 62:468473CrossRefGoogle Scholar
Mendez, J, DePrado, R (1996) Diclofop-methyl cross-resistance in a chlorotoluron-biotype of Alopecurus myosuroides. Pest Biochem Physiol 56:123133CrossRefGoogle Scholar
Mohamed, IA, Li, R, You, Z, Li, Z (2012) Japanese foxtail (Alopecurus japonicus) resistance to fenoxaprop and pinoxaden in China. Weed Sci 60:167171CrossRefGoogle Scholar
Muehlebach, M, Boeger, M, Cederbaum, F, Cornes, D, Friedmann, AA, Glock, J, Niderman, T, Stoller, A, Wagner, T (2009) Aryldiones incorporating a [1,4,5] oxadiazepane ring. Part I: Discovery of the novel cereal herbicide pinoxaden. Bioorg Med Chem 17:42414256CrossRefGoogle Scholar
Murphy, TR, Colvin, DL, Dickens, R, Everest, JW, Hall, D, McCarty, LB (2014) Weeds of Southern Turfgrasses. Athens, GA: University of Georgia Extension Special Bulletin 31. 208 pGoogle Scholar
Nikolskaya, T, Zagnitko, O, Tevzadze, G, Haselkorn, R, Gornicki, P (1999) Herbicide sensitivity determinant of wheat plastid acetyl-CoA carboxylase is located in a 400-amino acid fragment of the carboxyltransferase domain. Proc Natl Acad Sci USA 96:1464714651CrossRefGoogle Scholar
Petit, C, Bay, G, Pernin, F, Délye, C (2010) Prevalence of cross or multiple resistance to the acetylcoenzyme A carboxylase inhibitors fenoxaprop, clodinafop and pinoxaden in black-grass (Alopecurus myosuroides Huds.) in France. Pest Manag Sci 66:168177Google Scholar
Porter, DJ, Kopec, M, Hofer, U (2005) Pinoxaden: a new selective postemergence graminicide for wheat and barley. Proc Weed Sci Soc Am 45:95Google Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347CrossRefGoogle ScholarPubMed
Preston, C, Mallory-Smith, CA (2001) Biochemical mechanism, inheritance, and molecular genetics of herbicide resistance in weeds. Pages 2360in Powles, SB, Shaner, DL, eds. Herbicide Resistance and World Grains. Boca Raton, FL: CRCCrossRefGoogle Scholar
Preston, C, Powles, SB (1998) Amitrole inhibits diclofop metabolism and synergises diclofop-methyl in a diclofopmethyl resistant biotype of Lolium rigidum. Pestic Biochem Physiol 62:179189CrossRefGoogle Scholar
Senseman, SA (2007) Herbicide Handbook. 9th ed. Lawrence, KS: Weed Science Society of America. Pp 1148Google Scholar
Shetty, SVR, Sivakumar, MVK, Ram, SA (1982) Effect of shading on the growth of some common weeds of the semi-arid tropics. Agron J 74:10231029CrossRefGoogle Scholar
Tang, W, Zhou, F, Chen, J, Zhou, X (2014) Resistance to ACCase-inhibiting herbicides in an Asia minor bluegrass (Polypogon fugax) population in China. Pest Biochem Physiol 108:1621CrossRefGoogle Scholar
Torres-García, JR, Tafoya-Razo, JA, Velázquez-Márquez, S, Tiessen, A (2018) Double herbicide-resistant biotypes of wild oat (Avena fatua) display characteristic metabolic fingerprints before and after applying ACCase- and ALS-inhibitors. Acta Physiologiae Plantarum 40:119CrossRefGoogle Scholar
Watson, L, Dallwitz, MJ (1992) The Grass Genera of the World. Wallingford, UK: CABI. 1038 pGoogle Scholar
White, GM, Moss, SR, Karp, A (2005) Differences in the molecular basis of resistance to the cyclohexanedione herbicide sethoxydim in Lolium multiflorum. Weed Res 45:440448CrossRefGoogle Scholar
Yu, Q, Collavo, A, Zheng, MQ, Owen, M, Sattin, M, Powles, SB (2007) Diversity of acetyl-coenzyme A carboxylase mutations in resistant Lolium populations: evaluation using clethodim. Plant Physiol 145:547558CrossRefGoogle ScholarPubMed
Yu, LPC, Kim, YS, Tong, L (2010) Mechanism for the inhibition of the carboxyltransferase domain of acetyl-coenzyme A carboxylase by pinoxaden. Proc Natl Acad Sci USA 107:2207222077CrossRefGoogle ScholarPubMed
Yu, Q, Ahmad-Hamdani, MS, Han, H, Christoffers, MJ, Powles, SB (2013) Herbicide resistance-endowing ACCase mutations in hexaploidy wild oat (Avena fatua): insights into resistance evolution in a hexaploidy species. Heredity 110:220231CrossRefGoogle Scholar
Yu, J, McCullough, PE, Czarnota, MA (2017) First report of acetyl-CoA carboxylase resistant southern crabgrass (Digitaria ciliaris) in the United States. Weed Technol 31:252259CrossRefGoogle Scholar
Yuan, JS, Tranel, PJ, Stewart, CN (2006) Non-target site herbicide resistance: a family business. Trends Plant Sci 12:5266Google ScholarPubMed
Zagnitko, O, Jelenska, J, Tevzadze, G, Haselkorn, R, Gornicki, P (2001) An isoleucine/leucine residue in the carboxyltransferase domain of acetyl-CoA carboxylase is critical for interaction with aryloxyphenoxypropionate and cyclohexanedione inhibitors. Proc Natl Acad Sci USA 98:66176622CrossRefGoogle ScholarPubMed
Zerbino, DR, Birney, E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821829CrossRefGoogle Scholar
Zhang, XQ, Powles, SB (2006a) The molecular bases for resistance to acetyl coenzyme A carboxylase (ACCase) inhibiting herbicides in two target-based resistant biotypes of annual ryegrass (Lolium rigidum). Planta 223:550557CrossRefGoogle Scholar
Zhang, XQ, Powles, SB (2006b) Six amino acid substitutions in the carboxyl-transferase domain of the plastidic acetyl-CoA carboxylase gene are linked with resistance to herbicides in a Lolium rigidum population. New Phytol 172:636645CrossRefGoogle Scholar
Supplementary material: File

Basak et al. supplementary material

Basak et al. supplementary material

Download Basak et al. supplementary material(File)
File 53.3 KB