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Phytoprotection

Green foxtail (Setaria viridis) resistance to acetolactate synthase inhibitors Résistance de la sétaire verte (Setaria viridis) aux inhibiteurs de l'acétolactate synthase D.S. Volenberg, D.E. Stoltenberg et C.M. Boerboom

Volume 83, numéro 2, 2002 Résumé de l'article Des sétaires vertes (Setaria viridis) présumées résistantes aux inhibiteurs de URI : https://id.erudit.org/iderudit/706232ar l'acétolactate synthase (ALS) ont été identifiées en 1999 au Wisconsin, É.-U., DOI : https://doi.org/10.7202/706232ar dans un champ de soja (Glycine max) issu d'un semis direct. La résistance aux herbicides imidazolinone et sulfonylurée a été caractérisée au niveau de la Aller au sommaire du numéro plante entière et de celui des enzymes. Ces sétaires vertes au stade trois à quatre feuilles étaient respectivement 1020, 53 et 6,5 fois plus résistantes à l'imazethapyr, à l'imazamox et au nicosulfuron que les sétaires sensibles. L'ALS Éditeur(s) in vivo était respectivement 1300 et 1,7 fois plus résistante à l'imazethapyr et au nicosulfuron. Ces résultats laissent supposer que ce groupe de sétaires Société de protection des plantes du Québec (SPPQ)l vertes était très résistant à l'imazethapyr et à l'imazamox, et que la résistance est associée à un enzyme ALS insensible. ISSN 0031-9511 (imprimé) 1710-1603 (numérique)

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Citer cet article Volenberg, D., Stoltenberg, D. & Boerboom, C. (2002). Green foxtail (Setaria viridis) resistance to acetolactate synthase inhibitors. Phytoprotection, 83(2), 99–109. https://doi.org/10.7202/706232ar

La société de protection des plantes du Québec, 2002 Ce document est protégé par la loi sur le droit d’auteur. L’utilisation des services d’Érudit (y compris la reproduction) est assujettie à sa politique d’utilisation que vous pouvez consulter en ligne. https://apropos.erudit.org/fr/usagers/politique-dutilisation/

Cet article est diffusé et préservé par Érudit. Érudit est un consortium interuniversitaire sans but lucratif composé de l’Université de Montréal, l’Université Laval et l’Université du Québec à Montréal. Il a pour mission la promotion et la valorisation de la recherche. https://www.erudit.org/fr/ Green foxtail (Setaria viridis) résistance to acetolactate synthase inhibitors

Dean S. Volenberg, David E. Stoltenberg, and Chris M. Boerboom1

Received 2001-12-07; accepted 2002-07-19

PHYTOPROTECTION 83 : 99-109

Green foxtail {Setaria viridis) plants putatively résistant to acetolactate synthase (ALS) inhibitors were identified in a Wisconsîn USA no-tillage soybean {Glycine max) field in 1999. Résistance to imidazolinone and sulfonylurea herbicides was characterized at the whole-plant level and enzyme level. Three- to four-leaf stage green foxtail plants were 1020, 53, and 6.5-fold résistant to imazethapyr, imazamox, and nicosulfuron, respec- tively, compared to susceptible plants. In vivo ALS was 1300 and 1.7-fold résistant to imazethapyr and nicosulfuron, respectively. Thèse results suggested that this green foxtail accession was highiy résistant to imazethapyr and imazamox, and that résistance was associated with an insensitive ALS enzyme. [Résistance de la sétaire verte [Setaria viridis) aux inhibiteurs de ï'acétolactate synthase] Des sétaires vertes {Setaria viridis) présumées résistantes aux inhibiteurs de ï'acétolactate synthase (ALS) ont été identifiées en 1999 au Wisconsin, E.-U., dans un champ de soja {Glycine max) issu d'un semis direct. La résistance aux herbicides imidazolinone et sulfonylurée a été caractérisée au niveau de la plante entière et de celui des enzymes. Ces sétaires vertes au stade trois à quatre feuilles étaient respectivement 1020, 53 et 6,5 fois plus résistantes à l'imazethapyr, à l'imazamox et au nicosulfuron que les sétaires sensibles. L'ALS in vivo était respectivement 1300 et 1,7 fois plus résistante à l'imazethapyr et au nicosulfuron. Ces résultats laissent sup­ poser que ce groupe de sétaires vertes était très résistant à l'imazethapyr et à l'imazamox, et que la résistance est associée à un enzyme ALS insen­ sible.

1. Department of Agronomy, University of Wisconsin, Madison, Wl USA 53706; e-mail: [email protected]

99 INTRODUCTION Mechanisms of green foxtail résis­ tance to herbicides hâve been associa- Green foxtail (Setaria viridis var. viridis ted with changes at the herbicide site (L.) Beauv.) is native to Eurasia (Li et al. of action in most cases. Dinitroanilines 1942; Li et al. 1945) and is found within inhibit cell division in susceptible species each state of the continental United by binding to p-tubulin, and therefore States (Lorenzi and Jeffery 1987) and in interfère with tubulin polymerization ail provinces of Canada (Douglas et al. (Devine et al. 1993). The mechanism of 1985; Hunter étal. 1990). Green foxtail green foxtail résistance to dinitroa­ is a major weed problem in temperate nilines has been linked to an altération régions and is part of the S. viridis of a microtubule-associated protein complex comprised of var. weinmanni (Smeda et al. 1992). In contrast, goose- (R. & S.) Brand. (Hubbard 1915), giant grass {Eleusine indica (L.) Gaertn.) ré­ green foxtail var. major (Gaud.) Posp. sistance to dinitroanilines is conferred (Slife 1954), robust white foxtail var. by a modified (3-tubulin (Vaughn and robusta-alba Schreiber (Schreiber and Vaughan 1990), butthis mechanism was Oliver 1971), and robust purple foxtail not associated with gène modifications var. robusta-purpurea Schreiber of a, (3 or 7 tubulin (Mysore and Baird (Schreiber and Oliver 1971), represent- 1995). However, subséquent research ing some of the world's worst weeds (Anthony et al. 1998) has shown that a (Holm et al. 1977). Although phenology base change in the a tubulin gène of and growth characteristics may differ goosegrass results in an amino acid among varieties, no genetic differenti- change from threonine to isoleucine that ation appears to occur among them confers résistance to dinitroanilines. (Wang et al. 1995). Green foxtail can The mechanism of green foxtail résis­ substantially reduce crop yields in small tance to ACCase inhibitors is due to an grains (Blackshaw et al. 1981) and row insensitive ACCase (Maries et al. 1993). crops such as maize (Zea mays L.) The green foxtail accession from Spain (Sibuga and Bandeen 1980). Green has two mechanisms of résistance with­ foxtail also serves as an alternative host in the plant to triazines, an altération in for several pathogenic organisms that the target site of photosystem II and are detrimental to small grain produc­ enhanced metabolism (De Prado et al. tion (Haber and Harder 1992; Krupinsky 2000). 1992). Weed résistance to herbicides that Although green foxtail has been typ- inhibit acetolactate synthase (ALS) (EC ically managed effectively with herbi­ 4.1.3.18) activity has increased dramat- cides, the persistent use of herbicides ically since their introduction in 1982. has created a high level of sélection In 2001, 69 weed species were reported intensity for résistant plants. Green to be résistant to at least one of the five foxtail résistance has been confirmed commercialized classes of ALS-inhibit- to three chemical classes of herbicides. ing herbicides (Heap 2001). The résis­ In Canada, green foxtail has evolved tance mechanism is typically associa­ résistance to dinitroaniline herbicides ted with an insensitive ALS enzyme, g (Morrison et al. 1989) and acetyl-coen- although non-target site résistance has © zyme A carboxylase (ACCase; EC 6.4.1.2) been reported (Christopher et al. 1994; 2^ inhibitors (Heap and Morrison 1996; Mallory-Smith et al. 1999; Veldhuis et ~ Maries et al. 1993). Furthermore, sev- al. 2000). Imazethapyr [2-[4,5-dihydro- * eral populations hâve developed multi- 4-methyl-4-(1-methylethyl)-5-oxo-1 H- O pie résistance to thèse herbicide class- imidazol-2-yl]-5-ethyl-3-pyridinecarbox- H es (Morrison and Devine 1994). In the ylic acid] and imazamox [2-[4,5-dihy- UJ USA, green foxtail has evolved resis- dro-4-methyl-4-(1-methylethyl)-5-oxo- O tancetodinitroanilinesonly (Heap 2001). 1H-imidazol-2-yl]-5-(methoxymethyl)-3- £ In France (De Prado and Menendez pyridinecarboxylic acid] are herbicides g 1996), Spain (De Prado et al. 2000), and commonly used throughout the Cana- > Yugoslavia (Heap 2001), populations of dian prairies and the Midwestern USA °- green foxtail hâve evolved résistance grain belt for management of monoco- to triazine herbicides. tyledonous and dicotyledonous weed

100 VOLENBERG ET AL. : GREEN FOXTAIL RESISTANCE

species (Anonymous 2001; Boerboom western USA. Nicosulfuron is used in et al. 2000). The herbicide nicosulfuron Canada and the Midwestern USA in [2-[[[[4,6-dimethoxy-2-pyrimidinyl)ami- maize. no]carbonyl]amino]sulfonyl]-A/,A/-dime- thyl-3-pyridinecarboxamide] is also In August 1999, a farmer in north- commonly used to manage monocoty- western Wisconsin reported lack of ledonous and dicotyledonous weed green foxtail control in a no-tillage soy­ species in the Midwestern USA grain bean field in which imazethapyr and belt, but has limited use in the Canadi- thifensulfuron [3-[[[[(4-methoxy-6-me- an prairies (Anonymous 2001; Boer­ thyl-1,3-5-triazin-2-yl)amino] boom et al. 2000). Imazethapyr and carbonyl]amino]sulfonyl]-2-thiophene­ imazamox are classified as imidazoli- carboxylic acid] had been applied post- none herbicides, whereas nicosulfuron emergence at 53 g a.i. ha_1 and 2.2 g a.i. is classified as a sulfonylurea herbicide; ha \ respectively. The field had been in each of thèse herbicides inhibits ALS. a maize-soybean rotation since 1994. In Canada, imazethapyr is used in var- Sulfonylurea and imidazolinone herbi­ ious dicotyledonous crops including cides were applied for the first time in field pea {Pisum sativum L.), dry bean this field in 1995, but were applied for (Phaseolus vulgaris L.), herbicide-résis­ 3 consécutive yr, starting in 1997 (Table tant canola {Brassica napus L.) variet- 1). The objectives of our experiments ies, and seedling alfalfa {Medicago sa- were to confirm and quantify résistance tiva L.), whereas in the Midwestern USA, of green foxtail based on whole-plant imazethapyr is used primarily in soy- response to imazethapyr, imazamox, bean {Glycine max (L.) Merr.). Imaza­ and nicosulfuron, and to détermine ALS mox is used in herbicide- résistant cano­ sensitivity to imazethapyr and nicosul­ la varieties and field pea in Canada and furon. primarily in soybean within the Mid­

Table 1. Crop and herbicide use in a Wisconsin USA field from which a putative acetolactate synthase (ALS) inhibitor-resistant accession of green foxtail was identified

Year Crop8 Herbicide6

1991 Alfalfa 1992 Alfalfa none 1993 Alfalfa glyphosate, 2,4-D 1994 Maize 2,4-D, pendimethalin, dicamba 1995 Soybean glyphosate, 2,4-D, imazethapyr, thifensulfuron 1996 Maize glyphosate, 2,4-D, pendimethalin, dicamba 1997 Soybean glyphosate, 2,4-D, imazethapyr, thifensulfuron 1998 Maize glyphosate, 2,4-D, metolachlor, nicosulfuron 1999 Soybean glyphosate, 2,4-D, imazethapyr, thifensulfuron, sethoxydim

Alfalfa {Medicago sativa L.); maize {Zea mays L.); soybean {Glycine max (L.) Merr.). Glyphosate [AMphosphonomethyDglycine]; 2,4-D [(2,4-dichlorophenoxy)acetic acid]; pendimethalin [A/-(1-ethylpropyl)-3,4-dimethyl-2,6-dinitrobenzenamine]; dicamba [3,6- dichloro-2-methoxybenzoic acid]; imazethapyr [2-[4,5-dihydro-4-methyl-4-(1- methylethyl)- 5-oxo-l f/-imidazol-2-yl]-5-ethyl-3-pyridinecarboxylic acid];thifensulfuron [3-[[[[(4-methoxy- 6-methyl-1,3-5-triazin-2-yl)amino]carbonyl]amino]sulfonyl]-2- thiophenecarboxylic acid]; metolachlor [2-chloro-A/-(2-ethyl-6-methylphenyl)-A/-(2-methoxy-1-methylethyl)acetamide]; nicosulfuron [2-[[[[(4,6-dimethoxy-2-pyrimidinyl)amino]carbonyl]amino]sulfonyl]-A/,A/- dimethyl-3-pyridinecarboxamide]; sethoxydim [2-[1-(ethoxyimino)butyl]-5-[2- (ethylthio)propyl]-3-hydroxy-2-cyclohexen-1- one].

101 MATERIALS AND METHODS 28% nitrogen (N) as urea-ammonium nitrate [(CO(NH2)2)-NH4N03] at 1.25% Seed sources (v:v). Astationary pot sprayer with one In August 1999, three putative herbi­ 8002E nozzle calibrated to deliver 187 L cide-résistant green foxtail plants were ha 1 at 275 kPa was used for each her­ transplanted from a soybean field in bicide application. Chippewa County, Wisconsin, to a greenhouse at the University of Wis- Shoot biomass was harvested 14 d consin-Madison. Plants were grown to after treatment (DAT), dried at 70°C for maturity and seeds were collected for 72 h, and weighed. The expérimental experiments. Seeds from putative her­ design was completely randomized for bicide-susceptible green foxtail plants each experiment with four replicates were collected in September 1999 in a per treatment. The expérimental unit maize field in Dane County, Wisconsin, was one plant. Experiments were re- in which no ALS-inhibiting herbicides peated at least once. Each herbicide was had been applied. Ail plants were iden- evaluated as a separate experiment. tified as green foxtail Setaria viridis var. Analysis of variance was performed on viridis based on morphological charac- ail data. For each herbicide, the exper­ teristics described by Douglas et al. iment by treatment interaction was not (1985). significant and the data from repeated experiments were pooled. A non-linear Whole-plant dose-response logistic four-parameter model was si- Experiments were conducted in a green­ multaneously fit to the dose-response house at the University of Wisconsin- data for the résistant and susceptible Madison using three- to four-leaf stage accessions of each replication (Stolten- green foxtail plants. Approximately 10 berg and Wiederholt 1995; Volenberg seeds of résistant or susceptible green et al. 2000a; Volenberg et al. 2001). To foxtail accessions were placed on the obtain dose-response curves, data for surface of an autoclaved soil mixture of each replication were regressed using silt loam and sand (3:2 v:v) in a 325 ml_ the following model: y = C + (D-C)/(1 + container and covered with 1 cm of the exp((logl5o - logX) b)). The model esti- soil mixture. Four d after émergence, mated the dosage of ALS inhibitor that plants were thinned to one plant per reduced shoot dry biomass by 50% container. Plants were grown under (ED50) relative to non-treated plants and natural light supplemented with artifi- included the following parameters: y, cial light from métal halide lamps to shoot dry biomass; C, the lower limit of extend the photoperiod to 16 h at 25/ the ALS inhibitor dose-response curve 20°C (day/night) températures. at the highest herbicide concentration; D, the upper limit of the ALS inhibitor Commercially formulated herbicides dose-response curve at the lowest her­ were used in ail dose-response experi­ bicide concentration; b, the slope of the ments. Each experiment consisted of a ALS inhibitor dose-response curve single herbicide. Herbicide doses were around the ED5o; and X, the ALS inhib­ determined from preliminary experi- itor concentration. Nonlinear régres­ g ments. Imazethapyr was applied at 0, sion équations were calculated using © 0.70, 1.4, 2.8, 5.6, and 11 g a.i. ha1 to GraphPad Prism version 3.02 (Graph- ^ susceptible plants and at 0, 70, 140, Pad Software, San Diego, CA) curve fit- ~ 280, 560, and 1120 g a.i. ha 1to résistant ting software. A Runs Test determined SJ plants. Imazamox was applied at 0,0.3, if sigmoidal équations adequately des­ O 0.6,1.1,2.2, and 4.4 g a.i. ha1 tosuscep- cribed the data (P= 0.05) (Bradley 1968). K tible plants and at 0, 44, 88, 176, 352, The ratio of résistant to susceptible ED5o UJ and 704 g a.i. ha"1 to résistant plants. values was calculated to détermine the O Nicosulfuron was applied at 0,0.11,0.22, level of résistance to each herbicide. £ 0.44, 0.88, and 1.75 g a.i. ha1to suscep- g tible plants and at 0, 0.88, 1.75, 3.5, 7.0, In vivo ALS assay ^ and 14 g a.i. ha1 to résistant plants. Experiments were conducted in a green­ Û- Each herbicide treatment included non- house and laboratory at the University ionic surfactant (NIS) at 0.25% (v:v) and of Wisconsin-Madison following proce-

102 VOLENBERG ETAL. : GREEN FOXTAIL RESISTANCE

dures described by Lovell et al. (1996). for 30 min to decarboxylate acetolac­ Green foxtail plants were grown as tate to acetoin. One mL of a creatine (9 described above. Résistant or suscep­ g L1) and napthol (90 g L1) solution in tible three- to four- leaf stage plants 2.5 N NaOH was added to each sample, were treated with 0, 0.007, 0.07, 0.70, which was mixed and incubated at 60°C 7.0, 70, 700, and 1120 g a.i. ha1 for 30 min. Samples were cooled to imazethapyr or nicosulfuron. Herbicides ambient room température and centri- were applied with a stationary pot spray- fuged at 10 000 g for 10 min. Absor- er as described above. AH herbicide bance of acetoin was measured at 530 treatments included NIS at 0.25% (v:v) nm. Extracts from plant leaves not treat­ and 28% N at 1.25% (v:v). Plants were ed with herbicide or CPCA were used as treated with 1,1-cyclopropanedicarbox- background for spectrophotometric ylic acid (CPCA) at 766 g ha1 containing measurements. Absorbance measure- NIS at 0.25% (v:v) 21 h after herbicide ments were converted to |mg acetoin application (Gerwick et al. 1993; Simp­ using a standard curve. Enzyme acti­ son et al. 1995). Résistant or suscepti­ vity was expressed as |xg acetoin g1 (fresh ble négative control plants were not biomass) h"1. treated with herbicide or CPCA. The expérimental design was com- Acetolactate synthase activity was pletely randomized with four replica- measured by the accumulation of ace­ tions per treatment. The expérimental tolactate in leaf tissue 24 h after herbi­ unit was one plant. Experiments were cide treatment. The third and fourth repeated once. Analysis of variance leaf were removed from each plant and was performed on ail data. For each eut into 1 to 2 mm wide sections. A herbicide, the experiment by treatment total of 0.2 g of leaf tissue was harvest- interaction was not significant and the ed per plant and stored at -20°C for 24 data from repeated experiments were h to rupture cell walls. Three mL of pooled. Non-linear dose-response ana­ purified water was added to each sam- lysis was conducted as described above, ple, which was incubated at 60°C for and the dose that inhibited ALS activity 30 min and at 20°C for 45 min. Each by 50% (l5o) relative to non-treated plants sample was mixed every 15 min: twice was calculated. The ratio of résistant to at 60°C and three times at 20°C. A 2 susceptible l50 values was calculated to mL aliquot was removed from each détermine the level of résistance to each

sample and 50 |JLL 6 N H2S04 were add­ herbicide. ed. Aliquots were incubated at 60°C

Table 2. Parameter values of whole-plant dose-response curves (shown in Figure 1) for résistant and susceptible accessions of green foxtail as influenced by imazethapyr, imazamox, and nicosulfuron

Parameter value3 Accession Résistant Susceptible

Herbicide C D b R2 C D b R2 mg plant1 mg plant1 mg plant1 mg plant1

Imazethapyr 450 + 24b 980 ± 21 -2.42 ± 0.51 0.98 68 ± 18 1590 ± 59 -1.08 ± 0.27 0.97 Imazamox 150 ± 46 885 + 59 -2.32 ± 0.75 0.98 16 ± 14 830 ± 63 -1.88 ± 0.70 0.98 Nicosulfuron 207 ± 37 690 ± 15 -1.99 ± 0.37 0.97 158 ± 19 1128 ± 35 -0.70 + 0.31 0.96

y = C + (D-C)/(1 + exp((logl50 - logX) b)); y, shoot dry biomass; C, the lower limit of the dose- response curve at the highest herbicide concentration; D, the upper limit of the dose- response curve at the lowest herbicide concentration; b, the slope of the dose-response curve around the ED50; and X, the herbicide concentration. b Fitted value ± standard error.

103 1200

10000

Imazamox (g ha'1)

lUUU" (A C (A <0 800J

O 'J-I s S' 600^ > â ^Nx ^^L ^ O) N. "N. o £ 400- o JZ X^N . N" (/) 200^

J 0 1 1 —] 0.1 1 10 100 Nicosulfuron (g ha"1)

Figure 1. Whole-plant dose response of résistant (•) and susceptible (°) accessions of green foxtail to imazethapyr (A), imazamox (B), and nicosulfuron (C). Parameter values for dose- response curves are shown in Table 2. Each point represents the mean of eight replicates ± SE.

104 VOLENBERG ET AL. : GREEN FOXTAIL RESISTANCE

Table 3. Whole-plant dose-response (ED50) of résistant (R) and susceptible (S) green foxtail to imazethapyr, imazamox, and nicosulfuron

9 1 ED50 value (g ha ) Accession

Herbicide R/S

Imazethapyr 175 ± 11 0.2 ±<0.1 1020 ± 99 Imazamox 59 ± 8 1.2 ±0.2 53 ± 10 Nicosulfuron 4.6 ± 1.4 1.0 ±0.6 6.5 ± 1.7 a ED50 value indicates effective herbicide dose that reduced shoot dry biomass by 50% relative to non-treated plants. Each value represents the mean of eight replicates ± 95% confidence interval.

RESULTS sion. Furthermore, the imidazolinone- resistant green foxtail accession was The non-linear model fit ail shoot dry also résistant to the sulfonylurea herbi­ biomass data (Table 2; Fig. 1). Résis­ cide nicosulfuron at the whole-plant tance to imazethapyr and imazamox was level. The nicosulfuron ED50 value was confirmed by the high ratios of R to S 4.6 g ha-1 forthe résistant accession and -1 whole-plant ED50 values (Table 3). The 1.0 g ha for the susceptible accession. 1 imazethapyr ED50 value was 175 g ha Based on thèse values, the résistant for the résistant accession and 0.2 g ha1 accession was 6.5-fold résistant to nico­ for the susceptible accession. The sulfuron. The résistant accession was 1 imazamox ED50 value was 59 g ha for susceptible to the ACCase inhibitors the résistant accession and 1.2 g ha1 for sethoxydim [2-[1-(ethoxyimino)butyl]-5- the susceptible accession. Based on [2-(ethylthio)propyl]-3-hydroxy-2-cyclo- 1 ED50 values, the résistant accession was hex-1- one] at 315 g a.i. ha in the field 1020 and 53-fold less sensitive to and fluazifop-P [(fl)-2-[4-[[5-(trifluorome- imazethapyr and imazamox, respective- thyl)-2-pyridinyl]oxy]phenoxy]propionic ly, compared to the susceptible acces­ acid] at 210 g a.i. ha1 in the greenhouse

Table 4. Parameter values of acetolactate synthase (ALS) dose-response curves (shown in Figure 2) for résistant and susceptible accessions of green foxtail as influenced by imazethapyr and nicosulfuron

Parameter value3 Accession Résistant Susceptible

C D C D Herbicide (|ig acetoin g FW^h1) (|xg acetoin g FW"1hr1)

Imazethapyr 0.95 ± 0.02b 1.86 + 0.02 -0.89 + 0.09 0.95 0.33 + 0.13 2.37 ± 0.40 -0.38 + 0.12 0.92 Nicosulfuron 0.84 ±0.03 1.63 + 0.03 -1.50 ± 0.65 0.96 0.30 + 0.05 1.56 ± 0.07 -0.95 ± 0.29 0.94 a y = C + (D-Q/O + exp((logl5o - logX) b)); y, acetoin concentration; C, the lower limit of the dose-response curve at the highest herbicide concentration; D, the upper limit of the dose- response curve at the lowest herbicide concentration; b, the slope of the dose-response curve around the l50; and X, the herbicide concentration. b Fitted value ± standard error.

105 i 5 Li- c "5 o (0 O)

•>

co (O <

10000 Inhibitor (g ha )

Figure 2. In vivo inhibition of acetolactate synthase (ALS) from résistant (•) and susceptible (°) accessions of green foxtail by imazethapyr (A) and nicosulfuron (B). Parameter values for dose-response curves are shown in Table 4. Each point represents the mean of eight replicates ± SE.

Table 5. Acetolactate synthase (ALS) enzyme response (Uo) of résistant (R) and susceptible (S) green foxtail to imazethapyr and nicosulfuron

8 1 l5o value (g ha ) Accession

Herbicide R/S

Imazethapyr 3.2 ±0.3 2.4 x 103 ± 1.6 x 104 1300 ± 100 Nicosulfuron 0.74 ± 0.07 0.42 ± 0.04 1.7 ± 0.7

Uo value indicates effective herbicide dose that inhibited ALS activity by 50% relative to non- treated plants. Each value represents the mean of eight replicates ± 95% confidence interval.

106 VOLENBERG ET AL. : GREEN FOXTAIL RESISTANCE

(data not shown), suggesting no cross- none and sulfonylurea herbicides (Vo­ resistance to ACCase-inhibiting herbi­ lenberg et al. 2001). cides. The sélection of résistant green fox­ The non-linear model fit ail data from tail occurred in a Wisconsin field where the ALS in vivo assay (Table 4; Fig. 2). imidazolinone or sulfonylurea herbi­ Imazethapyr and nicosulfuron l50 values cides were applied annually for three were greater for the ALS-inhibitor ré­ consécutive yr. Other ALS-inhibitor sistant accession than for the suscepti­ résistant weed species hâve evolved ble accession (Table 5). The imazetha­ under similar herbicide sélection intensi­ pyr Uo value was 3.2 g ha 1 for the résis­ ves. Eastern black nightshade (Solanum tant accession and 0.0024 g ha1 for the ptycanthum L.) evolved ALS-inhibitor susceptible accession. The nicosulfu­ résistance after only four applications ron Uo value was 0.7 g ha 1 for the résis­ of imazethapyr over a 5-yr period (Vo­ tant accession and 0.4 g ha1 for the lenberg et al. 2000a). However, sélec­ susceptible accession. Based on I50 tion for résistance to ALS inhibitors can values, the ALS-inhibitor résistant green occur over a longer period. A giant foxtail accession was 1300- and 1.7-fold foxtail accession résistant to ALS inhib­ résistant to imazthapyr and nicosulfu­ itors was selected in a Wisconsin maize ron, respectively, compared to the sus­ field where nicosulfuron was applied ceptible accession. annually for 9 yr (Volenberg ef a/. 2000b). Multiple herbicide résistance has DISCUSSION evolved in green foxtail populations to dinitroaniline and ACCase-inhibiting Thèse results indicated that green fox­ herbicides in Canada (Morrison and tail from Wisconsin is highly résistant Devine 1994). However, it is not known to imazethapyr and imazamox, but whether thèse populations were select­ much less résistant to nicosulfuron. The ed for by herbicide use or by interbreed- mechanism of résistance is due to an ing between dinitroaniline- and ACCa- insensitive ALS enzyme. Relatively few se-resistant populations. Although grass species hâve evolved résistance green foxtail is considered self-pollinat- to imidazolinone and sulfonylurea her­ ing, outcrossing has been quantified in bicides. Rigid ryegrass (Lolium rigi- the field at levels as high as 2.2% (Bot- dum Gaud.) in Australia (Heap and traud et al. 1992). However, it is unlike- Knight 1986) and blackgrass {Alopecu- ly that multiple herbicide résistant green rus myosuroides Huds.) in England foxtail evolved through interbreeding (Moss and Cussans 1991) hâve evolved since résistance to the dinitroaniline cross-resistance to sulfonylureas, but trifluralin (2,6-dinitro-/V,/V-dipropyl-4- were selected with non-ALS inhibiting (trifluoromethyl)benzenamine) is inher- herbicides. Goosegrass and Honduras ited as a récessive trait (Jasieniuk et al. grass (Ixophorus unisetus (Presl) 1994). Therefore, management of ré­ Schlecht.) in Costa Rica selected with sistant green foxtail should address the imazapyr were cross-resistant to both spread of résistance traits via seed imidazolinone and sulfonylurea herbi­ immigration. cides (Valverde et al. 1993). Within the Populations résistant to herbicides USA, few grass species hâve developed can become widespread in a short pe­ résistance to ALS-inhibiting herbicides, riod of time as evidenced by dinitroa- including shattercane {Sorghum bicol- niline-resistant green foxtail in Canada. or{L.) Moench) (Anderson et al. 1998), Five yr after the confirmation of résis­ Italian ryegrass {Lolium multiflorum L.) tance (Morrison et al. 1989), the num- (Taylor and Coats 1996), wild oat (Ave- ber of fields infested with dinitroaniline- na fatua L.) (Nandula and Messersmith resistant green foxtail across the prai­ 2000) and giant foxtail (Setaria faberi ries was so large that it was difficult to Herrm.) (Volenberg et al. 2001). ALS estimate the number of fields infested inhibitor-resistant giant foxtail acces­ (Morrison and Devine 1994). Further- sions from Wisconsin, Illinois, and Min­ more, increased availability and adop­ nesota are cross-resistant to imidazoli­ tion of transgenic herbicide-résistant

107 crop species may be associated with De Prado, R., N. Lopez-Martînez, and J. even greater reliance on single herbi­ Gonzalez-Gutierrez. 2000. Identification cide chemistries (e.g. ALS inhibitors) oftwo mechanismsof atrazine résistance for weed management (Warwick et al. in Setaria faberi and Setaria viridis bio­ types. Pestic. Biochem. Physiol. 67 : 114- 1999). As such, management practices 124. that integrate cultural, mechanical, and Devine, M.D., S.O. Duke, and C. Fedtke. 1993. alternative chemical approaches should Physiology of herbicide action. Prentice be implemented for management of Hall, Englewood Cliffs, NJ. Pages 189-224. ALS inhibitor-resistant green foxtail Douglas, B.J., A.G. Thomas, I.N. Morrison, populations, as well as other herbicide- and M.G. Maw. 1985. The biology of résistant weed species, and to help delay Canadian weeds. 70. Setaria viridis (L.) development of additional résistance Beauv. Can J. Plant Sci. 65 : 669-690. problems. Gerwick, B.C., L.C. Mireles, and R.J. Eilers. 1993. Rapid diagnosis of ALS/AHAS- ré­ sistant weeds. Weed Technol. 7 : 519- REFERENCES 524. Haber, S., and D.E. Harder. 1992. Green fox­ Anderson, D.D., F.W. Roeth, and A.R. Mar­ tail (Setaria viridis) and barnyard grass tin. 1998. Discovery of a primisulfuron- (Echinochloa crusgalli), new hosts of the resistant shattercane (Sorghum bicolor) virus-like agent causing flame chlorosis biotype. Weed Technol. 12 : 74-77. in cereals. J. Plant Pathol. 14 : 278-280. Anonymous. 2001. Guide to crop protection Heap, I. 2001. International survey of 2001. Saskatchewan Agriculture and herbicide-résistant weeds. Herbicide Ré­ Food. Internet: www.agr.gov.sk.ca/docs/ sistance Action Committee and Weed cropguide01.pdf (May 2001). Sci. Soc. Am. Internet: Anthony, R.G., T.R. Waldin, J.A. Ray, S.W. www.weedscience.com (May 2001). Bright-Simon, and P.J. Hussey. 1998. Heap, I., and R. Knight. 1986. The occur­ Herbicide résistance caused by sponta- rence of herbicide cross-resistance in a neous mutation of cytoskeletal protein population of annual ryegrass, Lolium tubulin. Nature 393 : 260-262. rigidum, résistant to diclofop-methyl. Blackshaw, R.E., E.H. Stobbe, and A.R.W. Aust. J. Agric. Res. 37 : 149-156. Sturko. 1.981. Effect of seeding dates and Heap, I., and I.N. Morrison. 1996. Résistance densities of green foxtail (Setaria viridis) to aryloxyphenoxypropionate and cyclo- on growth and productivity of spring hexanedione herbicides in green foxtail wheat (Triticum aestivum). Weed Sci. (Setaria viridis). Weed Sci. 44 : 25- 30. 29 : 212-217. Holm, L.G., D.L. Plucknett, J.V. Pancho, and Boerboom, CM., J.D. Doll, R.A. Flashinski, J.P. Herberger. 1977. The world's worst C.R. Grau, and J.L. Wedberg. 2000. Pest weeds-distribution and biology. The East- management in Wisconsin field crops. West Food Institute, Honolulu Hl. Pages Univ. Wisc. Ext. Madison, Wl. 196 pp. 420-425. Bottraud, T., X. Reboud, P. Brabant, M. Hubbard, F.T. 1915. A taxonomic study of Lefranc, B. Rherissi, F. Vedal, and H. Setaria and its immédiate allies. Am. J. Darmency. 1992. Outcrossing and hybrid- Bot. 2 : 169-198. ization in wild and cultivated foxtail mil­ Hunter, J.H., I.N. Morrison, and D.S.R. lets: conséquences for release of trans- Rourke. 1990. The Canadian prairie prov­ genic crops. Theor. Appl. Genêt. 83 : 940- inces. Pages 51-89 in W.W. Donald (éd.), 946. Systems of weed control in wheat in North Bradley, J. 1968. Distribution-free statistical America. Weed Sci. Soc. Am, Champaign, tests. Prentice-Hall, Englewood Cliffs, NJ. IL Pages 250-270. Jasieniuk, M., A.L. Brule-Babel, and I.N. Christopher, J.T., C. Preston, and S.B. Morrison. 1994. Inheritance of trifluralin Powles. 1994. Malathion antagonizes résistance in green foxtail (Setaria viri­ metabolism-based chlorsulfuron résis­ dis). Weed Sci. 42 : 123-127. tance in Lolium rigidum. Pestic. Biochem. Krupinsky, J.M. 1992. Grass host of Pyreno- Physiol. 49 : 172-182. phora tritici repentis. Plant Dis. 76 : 92-95. De Prado, R., and J. Menendez. 1996. Man­ Li, C.H., W.K. Pao, and H.W. Li. 1942. Inter- agement of herbicide-résistant grass specific crosses in Setaria. J. Hered. 33 : weeds in Europe. Pages 393-398 in H. 351-355. Brown, G.W. Cussans, M.D. Devine, S.O. Duke, C. Fernandez-Quintanilla, A. Hel- weg, R.E. Labrada, M. Landes, P. Kudsk, and J.C. Streibig (eds). Proc. 2nd Int. Weed Cont. Cong. Copenhagen.

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