Multiple resistant Amaranthus hybridus (syn: quitensis) from Argentina

INTERNATIONAL HERBICIDE-RESISTANT WEED DATABASE

MULTIPLE RESISTANT SMOOTH PIGWEED
(Amaranthus hybridus (syn: quitensis))

Multiple Resistance: 2 Sites of Action
Inhibition of Acetolactate Synthase HRAC Group 2 (Legacy B)
Inhibition of Enolpyruvyl Shikimate Phosphate Synthase HRAC Group 9 (Legacy G)

Argentina, Córdoba

INTRODUCTION		SMOOTH PIGWEED
Smooth Pigweed (Amaranthus hybridus (syn: quitensis)) is a dicot weed in the Amaranthaceae family. In Argentina this weed first evolved multiple resistance (to 2 herbicide sites of action) in 2014 and infests Corn (maize), and Soybean. Multiple resistance has evolved to herbicides in the Groups 2 (Legacy B), and Inhibition of Enolpyruvyl Shikimate Phosphate Synthase HRAC Group 9 (Legacy G). These particular biotypes are known to have resistance to glyphosate, and imazethapyr and they may be cross-resistant to other herbicides in the Groups 2 (Legacy B), and Inhibition of Enolpyruvyl Shikimate Phosphate Synthase HRAC Group 9 (Legacy G). The 'Group' letters/numbers that you see throughout this web site refer to the classification of herbicides by their site of action. To see a full list of herbicides and HRAC herbicide classifications click here.

QUIK STATS (last updated Jan 20, 2015 )
Common Name	Smooth Pigweed
Species	Amaranthus hybridus (syn: quitensis)
Group	Inhibition of Acetolactate Synthase HRAC Group 2 (Legacy B) Inhibition of Enolpyruvyl Shikimate Phosphate Synthase HRAC Group 9 (Legacy G)
Herbicides	glyphosate, and imazethapyr
Location	Argentina, Córdoba
Year	2014
Situation(s)	Corn (maize), and Soybean
Contributors - (Alphabetically)	Pablo Belluccini, and Diego Ustarroz
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NOTES ABOUT THIS BIOTYPE

MECHANISM

A triple target-site mutation confers high levels of resistance to glyphosate in an Amaranthus quitensis population from Argentina Sarah-Jane Hutchings^a, Eddie McIndoe^a, Ryan Carlin^b, Wenjin Yu^b, Anushka Howell^a, Weining Gu^b, Wenling Wang^b, Mike Langford^a, Jo Mattocks^a and Shiv-Shankar Kaundun^a ^a Syngenta, Jealott’s Hill International Research Centre, RG42 6EY Bracknell, UK ^b Syngenta, Research Triangle Park, NC USA E:mail: sarah-jane.hutchings@syngenta.com

Resistance to glyphosate has evolved and is quickly spreading in Amaranthus quitensis due to excessive use of the EPSPS-inhibiting herbicide in Argentinian soybean production systems. Here, we confirmed resistance to glyphosate and determined the mechanism involved in an A. quitensis population (AMAQU-R) from Santa Fe Province, Argentina. AMAQU-R plants survived glyphosate rates as high as 48 kg ai/ha, whereas individuals from the sensitive populations (AMAQU-S1 and AMAQU-S2) were killed at 750 g ai/ha or below. Differential glyphosate uptake, movement or metabolism was not associated with resistance in AMAQU-R and only a small average relative increase (1.94) in EPSPS gene copy number/expression was detected in AMAQU-R. Three linked EPSPS mutations were identified around the binding site of glyphosate in AMAQU-R. These comprised T102I and P106S amino acid substitutions documented to confer high levels of glyphosate resistance, as well as a novel A103V target-site mutation. A 3.5-fold more tolerance to glyphosate was observed for the TIAVPS mutant compared to the double TIPS strain following heterologous gene expression and enzyme analysis. The triple glyphosate resistance mutations may explain the rapid spread of A. quitensis in Argentina and could be a real threat for neighbouring countries under similar glyphosate selection pressure.

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ACADEMIC ASPECTS

Confirmation Tests

Greenhouse trials comparing a known susceptible Smooth Pigweed biotype with this Smooth Pigweed biotype have been used to confirm resistance. For further information on the tests conducted please contact the local weed scientists that provided this information.

Genetics

Genetic studies on HRAC Group 2, 9 resistant Smooth Pigweed have not been reported to the site. There may be a note below or an article discussing the genetics of this biotype in the Fact Sheets and Other Literature

Mechanism of Resistance

The mechanism of resistance for this biotype is either unknown or has not been entered in the database. If you know anything about the mechanism of resistance for this biotype then please update the database.

Relative Fitness

There is no record of differences in fitness or competitiveness of these resistant biotypes when compared to that of normal susceptible biotypes. If you have any information pertaining to the fitness of multiple resistant Smooth Pigweed from Argentina please update the database.

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CONTRIBUTING WEED SCIENTISTS

PABLO BELLUCCINI

Weed Scientist INTA Marcos Juarez Weeds Route 12 km. 3 (2580) Cordoba, Cordoba Argentina Email Pablo Belluccini

DIEGO USTARROZ

Research Associate Inta Sección Malezas Ruta 9 Km 636 Manfredi Córdoba Argentina. Manfredi, 5688, Córdoba Argentina Email Diego Ustarroz

ACKNOWLEDGEMENTS
The Herbicide Resistance Action Committee, The Weed Science Society of America, and weed scientists in Argentina have been instrumental in providing you this information. Particular thanks is given to Pablo Belluccini, and Diego Ustarroz for providing detailed information.

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Herbicide Resistant Smooth Pigweed Globally
(Amaranthus hybridus (syn: quitensis))

Country

FirstYear

Situation

Active Ingredients

Site of Action

Argentina

1996

Soybean

chlorimuron-ethyl, and imazethapyr

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

Argentina

2013

Soybean

glyphosate

Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)

Argentina

2014

Corn (maize), and Soybean

glyphosate, and imazethapyr

Multiple Resistance: 2 Sites of Action
Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)
Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)

Argentina

2016

Soybean

2,4-D, dicamba, and glyphosate

Multiple Resistance: 2 Sites of Action
Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)
Auxin Mimics ( HRAC Group 4 (Legacy O)

Argentina

2016

Soybean

2,4-D, and dicamba

Auxin Mimics ( HRAC Group 4 (Legacy O)

Argentina

2021

Soybean

fomesafen

Inhibition of Protoporphyrinogen Oxidase ( HRAC Group 14 (Legacy E)

Bolivia

2002

Soybean

chlorimuron-ethyl, imazamox, imazethapyr, and oxasulfuron

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

Bolivia

2005

Soybean

fomesafen, lactofen, and sulfentrazone

Inhibition of Protoporphyrinogen Oxidase ( HRAC Group 14 (Legacy E)

Brazil

2018

Soybean

chlorimuron-ethyl, and glyphosate

Multiple Resistance: 2 Sites of Action
Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)
Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)

Canada (Ontario)

2004

Corn (maize)

bentazon, and bromoxynil

PSII inhibitors - Histidine 215 Binders ( HRAC Group 6 (Legacy C3)

France

1980

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

Israel

1986

Cropland

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

Italy

1978

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

Italy

2018

Soybean

imazamox, and thifensulfuron-methyl

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

Paraguay

2022

Corn (maize), and Soybean

chlorimuron-ethyl, and glyphosate

Multiple Resistance: 2 Sites of Action
Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)
Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)

South Africa

1993

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

South Africa

2024

Corn (maize), and Soybean

glyphosate

Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)

Spain

1985

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

Switzerland

1982

Vegetables

simazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Maryland)

1972

Corn (maize), and Cropland

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Virginia)

1976

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Delaware)

1977

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (North Carolina)

1980

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Pennsylvania)

1980

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (New Jersey)

1980

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (New York)

1980

Corn (maize)

atrazine, metribuzin, and simazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Wisconsin)

1985

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Kentucky)

1987

Corn (maize)

atrazine, and simazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Kentucky)

1992

Soybean

chlorimuron-ethyl, flumetsulam, imazaquin, imazethapyr, nicosulfuron, primisulfuron-methyl, and thifensulfuron-methyl

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

United States (Illinois)

1993

Corn (maize)

atrazine

PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Virginia)

1994

Corn (maize), and Soybean

imazaquin, and imazethapyr

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

United States (Illinois)

1998

Soybean

imazethapyr, and primisulfuron-methyl

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

United States (Delaware)

2000

Vegetables

imazethapyr

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

United States (Illinois)

2000

Corn (maize)

atrazine, imazethapyr, and primisulfuron-methyl

Multiple Resistance: 2 Sites of Action
Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)
PSII inhibitors - Serine 264 Binders ( HRAC Group 5 (Legacy C1 C2)

United States (Ohio)

2001

Soybean

flumetsulam, and thifensulfuron-methyl

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

United States (Michigan)

2002

Soybean

chlorimuron-ethyl, imazamox, and thifensulfuron-methyl

Inhibition of Acetolactate Synthase ( HRAC Group 2 (Legacy B)

Uruguay

2022

Corn (maize), and Soybean

glyphosate

Inhibition of Enolpyruvyl Shikimate Phosphate Synthase ( HRAC Group 9 (Legacy G)

Literature about Similar Cases

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Perotti, V.E., Larran, A.S., Palmieri, V.E., Martinatto, A.K., Alvarez, C.E., Tuesca, D. and Permingeat, H.R.. 2019. A novel triple amino acid substitution in the EPSPS found in a high‐level glyphosate‐resistant Amaranthus hybridus population from Argentina. Pest Management Science 75 : 1242 - 1251.

Background

The evolution of herbicide‐resistant weeds is one of the most important concerns of global agriculture. Amaranthus hybridus L. is a competitive weed for summer crops in South America. In this article, we intend to unravel the molecular mechanisms by which an A. hybridus population from Argentina has become resistant to extraordinarily high levels of glyphosate.

Results

The glyphosate‐resistant population (A) exhibited particularly high parameters of resistance (GR50 = 20 900 g ai ha−1, Rf = 314), with all plants completing a normal life cycle even after 32X dose application. No shikimic acid accumulation was detected in the resistant plants at any of the glyphosate concentrations tested. Molecular and genetic analyses revealed a novel triple substitution (TAP‐IVS: T102I, A103V, and P106S) in the 5‐enol‐pyruvylshikimate‐3‐phosphate synthase (EPSPS) enzyme of population A and an incipient increase on the epsps relative copy number but without effects on the epspstranscription levels. The novel mechanism was prevalent, with 48% and 52% of the individuals being homozygous and heterozygous for the triple substitution, respectively. In silico conformational studies revealed that TAP‐IVS triple substitution would generate an EPSPS with a functional active site but with an increased restriction to glyphosate binding.

Conclusion

The prevalence of the TAP‐IVS triple substitution as the sole mechanism detected in the highly glyphosate resistant population suggests the evolution of a new glyphosate resistance mechanism arising in A. hybridus. This is the first report of a naturally occurring EPSPS triple substitution and the first glyphosate target‐site resistance mechanism described in A. hybridus.

García, M.J., Palma-Bautista, C., Rojano-Delgado, A.M., Bracamonte, E., Portugal, J., Alcántara-de la Cruz, R. and De Prado, R.. 2019. he Triple Amino Acid Substitution TAP-IVS in the EPSPS Gene Confers High Glyphosate Resistance to the Superweed Amaranthus hybridus. International Journal of Molecular Sciences 20 : 2396 - .

The introduction of glyphosate-resistant (GR) crops revolutionized weed management; however, the improper use of this technology has selected for a wide range of weeds resistant to glyphosate, referred to as superweeds. We characterized the high glyphosate resistance level of an Amaranthus hybridus population (GRH)—a superweed collected in a GR-soybean field from Cordoba, Argentina—as well as the resistance mechanisms that govern it in comparison to a susceptible population (GSH). The GRH population was 100.6 times more resistant than the GSH population. Reduced absorption and metabolism of glyphosate, as well as gene duplication of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) or its overexpression did not contribute to this resistance. However, GSH plants translocated at least 10% more ¹⁴C-glyphosate to the rest of the plant and roots than GRH plants at 9 h after treatment. In addition, a novel triple amino acid substitution from TAP (wild type, GSH) to IVS (triple mutant, GRH) was identified in the EPSPS gene of the GRH. The nucleotide substitutions consisted of ATA¹⁰², GTC¹⁰³ and TCA¹⁰⁶ instead of ACA¹⁰², GCG¹⁰³, and CCA¹⁰⁶, respectively. The hydrogen bond distances between Gly-101 and Arg-105 positions increased from 2.89 Å (wild type) to 2.93 Å (triple-mutant) according to the EPSPS structural modeling. These results support that the high level of glyphosate resistance of the GRH A. hybridus population was mainly governed by the triple mutation TAP-IVS found of the EPSPS target site, but the impaired translocation of herbicide also contributed in this resistance..

CARVALHO, S.J.P., GONÇALVES NETTO, A., NICOLAI, M., CAVENAGHI, A.L., LÓPEZ-OVEJERO, R.F., and CHRISTOFFOLETI, P.J.. 2015. DETECTION OF GLYPHOSATE-RESISTANT PALMER AMARANTH (Amaranthus palmeri) IN AGRICULTURAL AREAS OF MATO GROSSO, BRAZIL. Planta Daninha 33 : 579 - 586.

ABSTRACT - The recent introduction of Palmer amaranth (Amaranthus palmeri) in Brazilian agricultural areas may promote several changes on weed management, especially in no-till systems and in glyphosate-resistant crops, since glyphosate-resistant biotypes of A. palmeri have been frequently selected in other countries. Therefore, this research was developed in order to evaluate the glyphosate susceptibility of a Palmer amaranth biotype recently identified in the State of Mato Grosso, Brazil. For this purpose, glyphosate susceptibility of three Amaranthus biotypes was compared: A. hybridus var. patulus, collected in the State of Rio Grande do Sul - Brazil; A. hybridus var. patulus, collected in the State of São Paulo - Brazil; and A. palmeri, collected in the State of Mato Grosso - Brazil. Dose-response curves were generated for all biotypes, considering eight rates of glyphosate and six replicates. All the experiments were repeated twice. Both A. hybridus biotypes were satisfactorily controlled by glyphosate, demanding rates equal to or lower than 541.15 g a.e. ha-1 for 80% control (LD80). The A. palmeri biotype was not controlled by glyphosate in any of the assessments and required rates greater than 4,500 g a.e. ha-1 to reach LD80, which are economically and environmentally unacceptable. Comparison of the Brazilian A. palmeri biotype to the A. hybridus biotypes, as well as, to the results available in scientific international literature, led to the conclusion that the Brazilian Palmer amaranth biotype is resistant to glyphosate..

Gaines, T. A. ; Ward, S. M. ; Bukun, B. ; Preston, C. ; Leach, J. E. ; Westra, P.. 2012. Interspecific hybridization transfers a previously unknown glyphosate resistance mechanism in Amaranthus species. Evolutionary Applications 5 : 29 - 38.

A previously unknown glyphosate resistance mechanism, amplification of the 5-enolpyruvyl shikimate-3-phosphate synthase gene, was recently reported in Amaranthus palmeri. This evolved mechanism could introgress to other weedy Amaranthus species through interspecific hybridization, representing an avenue for acquisition of a novel adaptive trait. The objective of this study was to evaluate the potential for this glyphosate resistance trait to transfer via pollen from A. palmeri to five other weedy Amaranthus species (Amaranthus hybridus, Amaranthus powellii, Amaranthus retroflexus, Amaranthus spinosus, and Amaranthus tuberculatus). Field and greenhouse crosses were conducted using glyphosate-resistant male A. palmeri as pollen donors and the other Amaranthus species as pollen recipients. Hybridization between A. palmeri and A. spinosus occurred with frequencies in the field studies ranging from <0.01% to 0.4%, and 1.4% in greenhouse crosses. A majority of the A. spinosus × A. palmeri hybrids grown to flowering were monoecious and produced viable seed. Hybridization occurred in the field study between A. palmeri and A. tuberculatus (<0.2%), and between A. palmeri and A. hybridus (<0.01%). This is the first documentation of hybridization between A. palmeri and both A. spinosus and A. hybridus..

Bhowmik, P. C.. 2010. Current status of herbicide resistant weeds around the Globe. Journal of Crop and Weed 6 : 33 - 43.

The incidence and wide spread of herbicide resistant weeds is a global problem. Over the past 65 years, repeated use of herbicides has resulted in the evolution of resistant weed species. The first resistant species to triazine was discovered in 1970 in the United States. Since then, a large number of weed species has evolved resistance to several classes of herbicide. Currently, there are 334 resistant biotypes, including 190 weed species (113 dicots and 77 monocots) in over 310, 000 fields around the world Common resistant species are Chenopodium album and Amaranthus retroflexus resistant to triazine, Phalaris minor resistant to isoproturon, P. minor and P. paradoxa resistant to diclofop, Echinochloa colona resistant to propanil, Echinochloa crusgalli resistant to butachlor, Eleusine indica resistant to trifluralin, Lolium rigidum resistant to diclofop, Lactuca serriola resistant to metsuljuron, glyphosate resistance to Eleusine indica, Conyza canadensis, Lolium rigidum, and Lolium multiflorum. Multiple weed resistance to more than one class of herbicides with different modes of action has also been documented with many species. Currently there has been increased herbicide resistance to various weed species around the globe. Most common species are Lolium rigidum, Avena fatua, Amaranthus retroflexus, Chenopodium album, Setaria viridis, Echinochloa crusgalli, Eleusine indica, Kochia scoparia, Conyza canadensis, and Amaranthus hybridus..

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