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Target and Nontarget Resistance Mechanisms Induce Annual Bluegrass (Poa annua) Resistance to Atrazine, Amicarbazone, and Diuron

  • Andrej W. Svyantek (a1), Phillipe Aldahir (a2), Shu Chen (a3), Michael L. Flessner (a4), Patrick E. McCullough (a5), Sudeep S. Sidhu (a5) and J. Scott McElroy (a2)...


Annual bluegrass is a weed species in turfgrass environments known for exhibiting resistance to multiple herbicide modes of action, including photosystem II (PSII) inhibitors. To evaluate populations of annual bluegrass for susceptibility to PSII inhibitors of varied chemistries, populations were treated with herbicides from triazolinone, triazine, and substituted urea families: amicarbazone, atrazine, and diuron, respectively. Sequencing of the psbA gene confirmed the presence of a Ser264 to Gly amino acid substitution within populations that exhibited resistance to both atrazine and amicarbazone. A single biotype, DR3, which lacked any previously reported psbA gene point mutation, exhibited resistance to diuron, atrazine, and amicarbazone. DR3 had a significantly lower rate of absorption and translocation of atrazine and had enhanced atrazine metabolism when compared with both the Ser264 to Gly resistant mutant and susceptible biotypes. We thus report possible nontarget mechanisms of resistance to PSII-inhibiting herbicides in annual bluegrass.

Poa annua es una especie de maleza en ambientes de céspedes conocida por presentar resistencia a múltiples modos de acción de herbicidas, incluyendo inhibidores del fotosistema II (PSII). Para evaluar la susceptibilidad de poblaciones de P. annua a inhibidores PSII de diferentes características químicas, varias poblaciones fueron tratadas con herbicidas de las familias triazolinone, triazine, y urea sustituidas: amicarbazone, atrazine, y diuron, respectivamente. La secuenciación del gen psbA confirmó la presencia de una sustitución de amino ácidos de Ser264 a Gly en poblaciones que presentaron resistencia a atrazine y amicarbazone. Un solo biotipo, DR3, el cual carecía de cualquier reporte previo de mutaciones puntuales en el gen psbA, presentó resistencia a diuron, atrazine, y amicarbazone. DR3 tuvo una tasa de absorción y translocación significativamente menor de atrazine y un mayor metabolismo de atrazine cuando se comparó con biotipos resistentes con la mutación Ser264 a Gly y con biotipos susceptibles. De esta forma, reportamos posibles mecanismos de resistencia a herbicidas inhibidores de PSII en P. annua que no involucran el sitio activo.


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Associate editor for this paper: Andrew Kniss, University of Wyoming.



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Arias, R.S, Netherland, MD, Scheffler, BE, Puri, A, Dayan, FE (2005) Molecular evolution of herbicide resistance to phytoene desaturase inhibitors in Hydrilla verticillata and its potential use to generate herbicide-resistant crops. Pest Manag Sci 61: 258268
Brosnan, JT, Breeden, GK, Mueller, TC (2012) A glyphosate-resistant biotype of annual bluegrass in Tennessee. Weed Sci 60: 97100
Brosnan, JT, Breeden, GK, Vargas, JJ, Grier, L (2015) A biotype of annual bluegrass (Poa annua) in Tennessee is resistant to inhibitors of ALS and photosystem II. Weed Sci 63: 321328
Burgos, NR, Tranel, PJ, Streibig, JC, Davis, VM, Shaner, D, Norsworthy, JK, Ritz, C (2013) Review: confirmation of resistance to herbicides and evaluation of resistance levels. Weed Sci 61: 420.
Burnet, MWM, Loveys, BR, Holtum, JAM, Powles, SB (1993a) A mechanism of chlorotoluron resistance in Lolium rigidum . Planta 190: 182189
Burnet, MWM, Loveys, BR, Holtum, JAM, Powles, SB (1993b) Increased detoxification is a mechanism of simazine resistance in Lolium rigidum . Pestic Biochem Physiol 46: 207218
Casler, MD, Duncan, RR (2003) Turfgrass Biology, Genetics, and Breeding. Hoboken, NJ: J. Wiley
Chodová, D, Mikulka, J, Koèová, M, Janáèek, J (1994) Different growth and photosynthetic efficiency of triazine resistant and susceptible biotypes of Poa annua L. Biol Plant (Prague) 36: 341
Cutulle, MA, McElroy, JS, Millwood, RW, Sorochan, JC, Stewart, CN (2009) Selection of bioassay method influences detection of annual bluegrass resistance to mitotic-inhibiting herbicides. Crop Sci 49: 1088
Darmency, H, Gasquez, J (1981) Inheritance of triazine resistance in Poa annua: Consequences for population dynamics. New Phytol 89: 487493
Dayan, FE, Trindade, MLB, Velini, ED (2009) Amicarbazone, a new photosystem II inhibitor. Weed Sci 57: 579583
Davis, DE, Gramlich, JV, Funderburk, HH Jr. (1965) Atrazine absorption and degradation by corn, cotton, and soybeans. Weeds 13: 252255
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: 176187
Délye, C, Jasieniuk, M, Le Corre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29: 649658
De Prado, R., De Prado, JL, Menendez, J (1997) Resistance to substituted urea herbicides in Lolium rigidum biotypes. Pestic Biochem Physiol 57: 126136
De Prado, R, Menendez, J (1996) Management of herbicide-resistant grass weeds in Europe. Pages 393398 in Brown, H, ed. Proceedings of the Second International Weed Control Congress. Copenhagen, Denmark: Department of Weed Control & Pesticide Ecology
Devine, MD, Shukla, A (2000) Altered target sites as a mechanism of herbicide resistance. Crop Prot 19: 881889
Gronwald, JW (1997) Resistance to PS II inhibitor herbicides. Pages 5359 in de Prado, R, Jorrin, J, Garcia-Torres, L, eds. Weed and Crop Resistance to Herbicides. Dordrecht, Netherlands: Springer
Gronwald, JW, Andersen, RN, Yee, C (1989) Atrazine resistance in velvetleaf (Abutilon theophrasti) due to enhanced atrazine detoxification. Pestic Biochem Physiol 34: 149163
Hall, LM, Moss, SR, Powles, SB (1995) Mechanism of resistance to chlorotoluron in two biotypes of the grass weed Alopecurus myosuroides . Pestic Biochem Physiol 53: 180192.
Hanson, BD, Mallory-Smith, CA (2000). Diuron-resistant Poa annua is resistant to norflurazon. Weed Sci 48: 666668
Heap, I (2015) The International Survey of Herbicide Resistant Weeds. Accessed February 17, 2015
Hoagload, DR, Arnon, DI (1950) The Water-Culture Method for Growing Plants without Soil. 2nd edn. Berkeley, CA: College of Agriculture, University of California Circ 347. 32 p
Hutto, KC, Coats, GE, Taylor, JM (2004) Annual bluegrass (Poa annua) resistance to simazine in Mississippi. Weed Technol 18: 846849
Kelly, ST, Coats, GE, Luthe, DS (1999) Mode of resistance of triazine-resistant annual bluegrass (Poa annua). Weed Technol 13: 747752
Matzrafi, M, Gadri, Y, Frenkel, E, Rubin, B, Peleg, Z (2014) Evolution of herbicide resistance mechanisms in grass weeds. Plant Sci 229: 4352
Mao, Q, Huff, DR (2012). The evolutionary origin of Poa annua L. Crop Sci 52: 19101922
McElroy, JS, Flessner, ML, Wang, Z, Dane, F, Walker, RH, Wehtje, GR (2013) A Trp 574 to Leu amino acid substitution in the ALS gene of annual bluegrass (Poa annua) is associated with resistance to ALS-inhibiting herbicides. Weed Sci 61: 2125
Menendez, J, Jorrin, J, Romera, E, Prado, RD (1994) Resistance to chlorotoluron of a slender foxtail (Alopecurus myosuroides) biotype. Weed Sci 42: 340344
Mengistu, LW, Mueller-Warrant, GW, Liston, A, Barker, RE (2000) psbA mutation (valine219 to isoleucine) in Poa annua resistant to metribuzin and diuron. Pest Manag Sci 56: 209217
Menne, H (2005) Classification of Herbicide Site of Action. HRAC Herbicide Resistance Action Committee. Accessed July 17, 2015
Netland, J (1996) Weed species and frequency of simazine-resistant populations of Poa annua and Senecio vulgaris in nursery stocks imported to Norway or inland-raised. Pages 461468 in Brown, H, ed. Proceedings of the Second International Weed Control Congress. Copenhagen, Denmark: Department of Weed Control & Pesticide Ecology
Pan, G, Si, P, Yu, Q, Tu, J, Powles, S (2012) Non-target site mechanism of metribuzin tolerance in induced tolerant mutants of narrow-leafed lupin (Lupinus angustifolius L.). Crop Pasture Sci 63: 452458
Patzoldt, WL, Dixon, BS, Tranel, PJ (2003) Triazine resistance in Amaranthus tuberculatus (Moq) Sauer that is not site-of-action mediated. Pest Manag Sci 59: 11341142
Patzoldt, WL, Hager, AG, McCormick, JS, Tranel, PJ (2006) A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc Natl Acad Sci USA 103: 1232912334
Perry, DH, McElroy, JS, Dane, F, van Santen, E, Walker, RH (2012) Triazine-resistant annual bluegrass (Poa annua) populations with Ser264 mutation are resistant to amicarbazone. Weed Sci 60: 355359
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol. 61: 317347
Preston, C (2003) Inheritance and linkage of metabolism-based herbicide cross-resistance in rigid ryegrass (Lolium rigidum). Weed Sci 51: 412
Preston, C, Powles, SB (1997) Light-dependent enhanced metabolism of chlorotoluron in a substituted urea herbicide-resistant biotype of Lolium rigidum Gaud. Planta 201: 202208
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: 123134
Putwain, PD (1982). Herbicide resistance in weeds—an inevitable consequence of herbicide use. Pages 719728 in Proceedings of the 1982 British Crop Protection Conference—Weeds. Farnham, UK: British Crop Protection Council.
Roeth, FW, Lavy, TL (1971) Atrazine uptake by sudangrass, sorghum and corn. Weed Sci 19: 9397
Singh, R, Sidhu, SS, McCullough, PE (2015) Physiological basis for triazine herbicide tolerance in bermudagrass, seashore paspalum, and zoysiagrass. Crop Sci 55: 23342341
Smith, AE (1983) Differential bahiagrass (Paspalum notatum) cultivar response to atrazine. Weed Sci 31: 8892
Tian, X, Darmency, H (2006) Rapid bidirectional allele-specific PCR identification for triazine resistance in higher plants. Pest Manag Sci 62: 531536
Vargas, JM, Turgeon, AJ (2003) Poa annua: Physiology, Culture, and Control of Annual Bluegrass. Hoboken, NJ: J. Wiley
Yelverton, F, Isgrigg, J (1998) Herbicide-resistant weeds in turfgrass. Golf Course Manag 66: 5661
Yuan, JS, Tranel, PJ, Stewart, CN (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12: 613
Yu, J, McCullough, PE, Vencill, WK (2013) Absorption, translocation, and metabolism of amicarbazone in annual bluegrass (Poa annua), creeping bentgrass (Agrostis stolonifera), and tall fescue (Festuca arundinacea). Weed Sci 61: 217221



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