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Distribution and validation of genotypic and phenotypic glyphosate and PPO-inhibitor resistance in Palmer amaranth (Amaranthus palmeri) from southwestern Nebraska

Published online by Cambridge University Press:  09 July 2020

Maxwel C Oliveira Open the ORCID record for Maxwel C Oliveira [Opens in a new window] ,
Darci A Giacomini ,
Nikola Arsenijevic ,
Gustavo Vieira ,
Patrick J Tranel  and
Rodrigo Werle
Maxwel C Oliveira
Affiliation:
Assistant Professor, Department of Agronomy, Western São Paulo University, Presidente Prudente, São Paulo, Brazil Researcher, Department of Agronomy, University of Wisconsin-Madison, Madison, Wisconsin, USA Former University of Nebraska-Lincoln, Department of Agronomy and Horticulture, Lincoln, Nebraska, USA
Darci A Giacomini
Affiliation:
Research Assistant Professor, Department of Crop Sciences, University of Illinois Urbana-Champaign, Urbana, Illinois, USA
Nikola Arsenijevic
Affiliation:
Former Undergraduate Research Assistant, Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska, USA
Gustavo Vieira
Affiliation:
Former Undergraduate Research Assistant, Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska, USA
Patrick J Tranel
Affiliation:
Professor, Department of Crop Sciences, University of Illinois Urbana-Champaign, Urbana, Illinois, USA
Rodrigo Werle*
Affiliation:
Assistant Professor, Department of Agronomy, University of Wisconsin-Madison, Madison, Wisconsin, USA Former University of Nebraska-Lincoln, Department of Agronomy and Horticulture, Lincoln, Nebraska, USA
*
Author for correspondence: Rodrigo Werle, Assistant Professor, University of Wisconsin-Madison, Department of Agronomy, 1575 Linden Drive, Madison, WI53706 Email: [email protected]
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Abstract

Failure to control Palmer amaranth with glyphosate and protoporphyrinogen IX oxidase (PPO)-inhibitor herbicides was reported across southwestern Nebraska in 2017. The objectives of this study were to 1) confirm and 2) validate glyphosate and PPO-inhibitor (fomesafen and lactofen) resistance in 51 Palmer amaranth accessions from southwestern Nebraska using genotypic and whole-plant phenotypic assay correlations and cluster analysis, and 3) determine which agronomic practices might be influencing glyphosate resistance in Palmer amaranth accessions in that location. Based on genotypic assay, 88% of 51 accessions contained at least one individual with amplification (>2 copies) of the 5-enolypyruvyl-shikimate-3-phosphate synthase (EPSPS) gene, which confers glyphosate resistance; and/or a mutation in the PPX2 gene, either ΔG210 or R128G, which endows PPO-inhibitor resistance in Palmer amaranth. Cluster analysis and high correlation (0.83) between genotypic and phenotypic assays demonstrated that EPSPS gene amplification is the main glyphosate resistance mechanism in Palmer amaranth accessions from southwestern Nebraska. In contrast, there was poor association between genotypic and phenotypic responses for PPO-inhibitor resistance, which was attributed to segregation for PPO-inhibitor resistance within these accessions and/or the methodology that was adopted herein. Genotypic assays can expedite the process of confirming known glyphosate and PPO-inhibitor resistance mechanisms in Palmer amaranth from southwestern Nebraska and other locations. Phenotypic assays are also a robust method for confirming glyphosate resistance but not necessarily PPO-inhibitor resistance in Palmer amaranth. Moreover, random forest analysis of glyphosate resistance in Palmer amaranth indicated that EPSPS gene amplification, county, and current and previous crops are the main factors influencing glyphosate resistance within that geographic area. Most glyphosate-susceptible Palmer amaranth accessions were found in a few counties in areas with high crop diversity. Results presented here confirm the spread of glyphosate resistance and PPO-inhibitor resistance in Palmer amaranth accessions from southwestern Nebraska and demonstrate that less diverse cropping systems are an important driver of herbicide resistance evolution in Palmer amaranth.

Keywords

fomesafenglyphosatelactofenPalmer amaranth, Amaranthus palmeri S. WatsonEPSPSherbicidegene amplificationpigweedprotoporphyrinogen IX oxidaseweed resistance
Type
Research Article
Information
Weed Technology , Volume 35 , Issue 1 , February 2021 , pp. 65 - 76
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of Weed Science Society of America

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Footnotes

Associate Editor: R. Joseph Wuerffel, Syngenta

*This article has been updated since its original publication. See https://doi.org/10.1017/wet.2020.124.

References

Andrade, JF, Satorre, EH, Ermácora, CM, Poggio, SL (2017) Weed communities respond to changes in the diversity of crop sequence composition and double cropping. Weed Res 57:148–158CrossRefGoogle Scholar
Bass, C, Field, LM (2011) Gene amplification and insecticide resistance. Pest Manag Sci 67:886–890CrossRefGoogle ScholarPubMed
Beckie, HJ, Reboud, X (2009) Selecting for weed resistance: Herbicide rotation and mixture. Weed Technol 23:363–370CrossRefGoogle Scholar
Biau, G, Scornet, E (2016) A random forest guided tour. TEST 25:197–227CrossRefGoogle Scholar
Breiman, L (2001) Random Forests. Mach Learn 45:5–32CrossRefGoogle Scholar
Burgos, NR (2015) Whole-Plant and Seed Bioassays for Resistance Confirmation. Weed Sci 63(SP1):152–165Google Scholar
Chahal, PS, Varanasi, VK, Jugulam, M, Jhala, AJ (2017) Glyphosate-resistant Palmer amaranth (Amaranthus palmeri) in Nebraska: Confirmation, EPSPS gene amplification, and response to POST corn and soybean herbicides. Weed Technol 31:80–9310.1614/WT-D-16-00109.1CrossRefGoogle Scholar
Chatham, LA, Bradley, KW, Kruger, GR, Martin, JR, Owen, MD, Peterson, DE, Mithila, J, Tranel, PJ (2015) A multistate study of the association between glyphosate resistance and EPSPS gene amplification in waterhemp (Amaranthus tuberculatus). Weed Sci 63:569–57710.1614/WS-D-14-00149.1CrossRefGoogle Scholar
Coburn, C (2017) Influence of Experimental Methods on Herbicide Resistance Confirmation. Ph.D dissertation. Laramie: University of Wyoming. 145 pGoogle Scholar
Copeland, JD, Montgomery, GB, Steckel, LE (2019) Evaluation of the time-of-day effect of herbicides applied POST on protoporphyrinogen IX oxidase– resistant and –susceptible Palmer amaranth (Amaranthus palmeri). Weed Technol 33:651–657CrossRefGoogle Scholar
Culpepper, AS, Grey, TL, Vencill, WK, Kichler, JM, Webster, TM, Brown, SM, York, AC, Davis, JW, Hanna, WW (2006) Glyphosate-resistant Palmer amaranth (Amaranthus palmeri) confirmed in Georgia. Weed Sci 54:620–626CrossRefGoogle Scholar
Dayan, FE, Owens, DK, Corniani, N, Silva, FM, Watson, SB, Howell, J, Shaner, DL (2015) Biochemical markers and enzyme assays for herbicide mode of action and resistance studies. Weed Sci 63(SP1):23–63CrossRefGoogle Scholar
Délye, C, Duhoux, A, Pernin, F, Riggins, C, Tranel, P (2015) Molecular Mechanisms of Herbicide Resistance. Weed Sci 63(SP1):91–115Google Scholar
Dominguez-Valenzuela, JA, Gherekhloo, J, Fernández-Moreno, PT, Cruz-Hipolito, HE, Alcántara-de la Cruz, R, Sánchez-González, E, De Prado, R (2017) First confirmation and characterization of target and non-target site resistance to glyphosate in Palmer amaranth (Amaranthus palmeri) from Mexico. Plant Physiol Biochem 115:212–218CrossRefGoogle ScholarPubMed
Doyle, JJ, Doyle, JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
Evans, JA, Tranel, PJ, Hager, AG, Schutte, B, Wu, C, Chatham, LA, Davis, AS (2016) Managing the evolution of herbicide resistance: Managing the evolution of herbicide resistance. Pest Manag Sci 72:74–80CrossRefGoogle ScholarPubMed
Farmer, JA, Webb, EB, Pierce, RA, Bradley, KW (2017) Evaluating the potential for weed seed dispersal based on waterfowl consumption and seed viability. Pest Manag Sci 73:2592–2603CrossRefGoogle ScholarPubMed
Gaines, TA, Barker, AL, Patterson, EL, Westra, P, Westra, EP, Wilson, RG, Jha, P, Kumar, V, Kniss, AR (2016) EPSPS Gene Copy Number and Whole-Plant Glyphosate Resistance Level in Kochia scoparia. PLoS ONE 11(12):e0168295CrossRefGoogle ScholarPubMed
Gaines, TA, Patterson, EL, Neve, P (2019) Molecular mechanisms of adaptive evolution revealed by global selection for glyphosate resistance. New Phytol 223:1770–1775CrossRefGoogle ScholarPubMed
Gaines, TA, Shaner, DL, Ward, SM, Leach, JE, Preston, C, Westra, P (2011) Mechanism of Resistance of Evolved Glyphosate-Resistant Palmer Amaranth (Amaranthus palmeri). J Agric Food Chem 59:5886–5889CrossRefGoogle Scholar
Gaines, TA, Ward, SM, Bukun, B, Preston, C, Leach, JE, Westra, P (2012) Interspecific hybridization transfers a previously unknown glyphosate resistance mechanism in Amaranthus species. Evol Appl 5:29–38CrossRefGoogle ScholarPubMed
Gaines, TA, Zhang, W, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS, Grey, TL, Webster, TM, Vencill, WK, Sammons, RD, Jiang, J, Preston, C, Leach, JE, Westra, P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA 7:1029–1034CrossRefGoogle Scholar
Giacomini, DA, Umphres, AM, Nie, H, Mueller, TC, Steckel, LE, Young, BG, Scott, RC, Tranel, PJ (2017) Two new PPX2 mutations associated with resistance to PPO-inhibiting herbicides in Amaranthus palmeri. Pest Manag Sci 73:1559–156310.1002/ps.4581CrossRefGoogle ScholarPubMed
Giacomini, DA, Westra, P, Ward, SM (2019) Variable Inheritance of Amplified EPSPS Gene Copies in Glyphosate-Resistant Palmer Amaranth (Amaranthus palmeri). Weed Sci 67:176–182CrossRefGoogle Scholar
Gossett, BJ, Murdock, EC, Toler, JE (1992) Resistance of Palmer amaranth (Amaranthus palmeri) to the dinitroaniline herbicides. Weed Technol 6:587–59110.1017/S0890037X00035843CrossRefGoogle Scholar
Hamilton, KC, Arle, HF (1958) Weeds of crops in Southern Arizona. Tucson: College of Agriculture, University of Arizona. 66 pGoogle Scholar
Hartigan, JA, Wong, MA (1979) Algorithm AS: a K-means clustering algorithm. J R Stat Soc C-APPL 28:100–108Google Scholar
Heap, I (2020) List of Herbicide Resistant Weeds by Weed Species. http://www.weedscience.org/Summary/Species.aspx. Accessed: January 12, 2020Google Scholar
Hicks, HL, Comont, D, Coutts, SR, Crook, L, Hull, R, Norris, K, Neve, P, Childs, DZ, Freckleton, RP (2018) The factors driving evolved herbicide resistance at a national scale. Nat Ecol Evol 2:529–536CrossRefGoogle Scholar
Hiller, TL, Powell, LA, McCoy, TD, Lusk, JJ (2009) Long-term agricultural land-use trends in Nebraska. Great Plains Res 19:225–237Google Scholar
Horak, MJ, Peterson, DE (1995) Biotypes of Palmer amaranth (Amaranthus palmeri) and common waterhemp (Amaranthus rudis) are resistant to imazethapyr and thifensulfuron. Weed Technol 9:192–195CrossRefGoogle Scholar
Ghanizadeh, H, Harrington, KC (2017) Non-target Site Mechanisms of Resistance to Herbicides. Crit Rev Plant Sci 36:24–34CrossRefGoogle Scholar
Jhala, AJ, Sandell, LD, Rana, N, Kruger, GR, Knezevic, SZ (2014) Confirmation and control of triazine and 4-hydroxyphenylpyruvate dioxygenase-inhibiting herbicide-resistant Palmer amaranth (Amaranthus palmeri) in Nebraska. Weed Technol 28:28–38CrossRefGoogle Scholar
Jugulam, M, Niehues, K, Godar, AS, Koo, D-H, Danilova, T, Friebe, B, Sehgal, S, Varanasi, VK, Wiersma, A, Westra, P, Stahlman, PW, Gill, BS (2014) Tandem amplification of a chromosomal segment harboring 5-enolpyruvylshikimate-3-phosphate synthase locus confers glyphosate resistance in Kochia scoparia. Plant Physiol 166:1200–1207CrossRefGoogle ScholarPubMed
Kohrt, JR, Sprague, CL, Nadakuduti, SS, Douches, D (2017) Confirmation of a Three-Way (Glyphosate, ALS, and Atrazine) Herbicide-Resistant Population of Palmer Amaranth (Amaranthus palmeri) in Michigan. Weed Sci 65:327–338CrossRefGoogle Scholar
Koo, D-H, Molin, WT, Saski, CA, Jiang, J, Putta, K, Jugulam, M, Friebe, B, Gill, BS (2018) Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proc Natl Acad Sci USA 115:3332–3337CrossRefGoogle ScholarPubMed
Kuhn, M, Wickham, H (2020) Tidymodels: Easily Install and Load the ’Tidymodels’ Packages. R package version 0.1.0. https://CRAN.R-project.org/package=tidymodels. Accessed: May 27, 2020Google Scholar
Kumar, V, Jha, P, Giacomini, D, Westra, EP, Westra, P (2015) Molecular basis of evolved resistance to glyphosate and acetolactate synthase-inhibitor herbicides in Kochia (Kochia scoparia) accessions from Montana. Weed Sci 63:758–769CrossRefGoogle Scholar
Kumar, V, Liu, R, Boyer, G, Stahlman, PW (2019) Confirmation of 2,4-D resistance and identification of multiple resistance in a Kansas Palmer amaranth (Amaranthus palmeri) population. Pest Manag Sci 75:2925–2933CrossRefGoogle Scholar
Küpper, A, Manmathan, HK, Giacomini, D, Patterson, EL, McCloskey, WB, Gaines, TA (2018) Population genetic structure in glyphosate-resistant and -susceptible Palmer amaranth (Amaranthus palmeri) accessions using genotyping-by-sequencing (GBS). Front Plant Sci 9:29CrossRefGoogle Scholar
Langemeier, CB, Robertson, AE, Wang, D, Jackson-Ziems, TA, Kruger, GR (2016) Factors affecting the development and severity of goss’s bacterial wilt and leaf blight of corn, caused by Clavibacter michiganensis subsp. nebraskensis. Plant Dis 101:54–61CrossRefGoogle ScholarPubMed
Lillie, KJ, Giacomini, DA, Tranel, PJ (2020) Comparing responses of sensitive and resistant populations of Palmer amaranth (Amaranthus palmeri) and waterhemp (Amaranthus tuberculatus var. rudis) to PPO inhibitors. Weed Technol 34:140–146CrossRefGoogle Scholar
Malone, JM, Morran, S, Shirley, N, Boutsalis, P, Preston, C (2016) EPSPS gene amplification in glyphosate-resistant Bromus diandrus. Pest Manag Sci 72:81–88CrossRefGoogle ScholarPubMed
Massinga, RA, Currie, RS, Trooien, TP (2003) Water use and light interception under Palmer amaranth (Amaranthus palmeri) and corn competition. Weed Sci 51:523–531CrossRefGoogle Scholar
Morgan, GD, Baumann, PA, Chandler, JM (2001) Competitive impact of Palmer amaranth (Amaranthus palmeri) on cotton (Gossypium hirsutum) development and yield. Weed Technol 15:408–412CrossRefGoogle Scholar
Norsworthy, JK, Griffith, G, Griffin, T, Bagavathiannan, M, Gbur, EE (2014) In-field movement of glyphosate-resistant Palmer amaranth (Amaranthus palmeri) and its impact on cotton lint yield: Evidence supporting a zero-threshold strategy. Weed Sci 62:237–249CrossRefGoogle Scholar
Nakka, S, Godar, AS, Wani, PS, Thompson, CR, Peterson, DE, Roelofs, J, Jugulam, M (2017) Physiological and Molecular Characterization of Hydroxyphenylpyruvate Dioxygenase (HPPD)-inhibitor Resistance in Palmer Amaranth (Amaranthus palmeri S. Wats.). Front Plant Sci 8:555CrossRefGoogle Scholar
Oliveira, MC, Gaines, TA, Patterson, EL, Jhala, AJ, Irmak, S, Amundsen, K, Knezevic, SZ (2018) Interspecific and intraspecific transference of metabolism-based mesotrione resistance in dioecious weedy Amaranthus. Plant J 96:1051–1063CrossRefGoogle ScholarPubMed
Palma-Bautista, C, Torra, J, Garcia, MJ, Bracamonte, E, Rojano-Delgado, AM, Alcántara-de la Cruz, R, De Prado, R (2019) Reduced Absorption and Impaired Translocation Endows Glyphosate Resistance in Amaranthus palmeri Harvested in Glyphosate-Resistant Soybean from Argentina. J Agric Food Chem 67:1052–1060CrossRefGoogle ScholarPubMed
Patterson, EL, Pettinga, DJ, Ravet, K, Neve, P, Gaines, TA (2018) Glyphosate resistance and EPSPS gene duplication: Convergent evolution in multiple plant species. J Hered 109:117–125CrossRefGoogle ScholarPubMed
Powles, SB (2008) Evolved glyphosate-resistant weeds around the world: Lessons to be learnt. Pest Manag Sci 64:360–365CrossRefGoogle ScholarPubMed
Price, AJ, Balkcom, KS, Culpepper, SA, Kelton, JA, Nichols, RL, Schomberg, H (2011) Glyphosate-resistant Palmer amaranth: A threat to conservation tillage. J Soil Water Conserv 66:265–275CrossRefGoogle Scholar
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed: January 2, 2020Google Scholar
Rangani, G, Salas-Perez, RA, Aponte, RA, Knapp, M, Craig, IR, Mietzner, T, Langaro, AC, Noguera, MM, Porri, A, Roma-Burgos, N (2019) A Novel Single-Site Mutation in the Catalytic Domain of Protoporphyrinogen Oxidase IX (PPO) Confers Resistance to PPO-Inhibiting Herbicides. Front Plant Sci 10:568CrossRefGoogle ScholarPubMed
Remnant, EJ, Good, RT, Schmidt, JM, Lumb, C, Robin, C, Daborn, PJ, Batterham, P (2013) Gene duplication in the major insecticide target site, Rdl, in Drosophila melanogaster. Proc Natl Acad Sci USA 110:14705–1471010.1073/pnas.1311341110CrossRefGoogle ScholarPubMed
Salas, RA, Burgos, NR, Tranel, PJ, Singh, S, Glasgow, L, Scott, RC, Nichols, RL (2016) Resistance to PPO-inhibiting herbicide in Palmer amaranth from Arkansas. Pest Manag Sci 72:864–869CrossRefGoogle ScholarPubMed
Salas-Perez, RA, Burgos, NR, Rangani, G, Singh, S, Refatti, JP, Piveta, L, Tranel, PJ, Mauromoustakos, A, Scott, RC (2017) Frequency of gly-210 deletion mutation among protoporphyrinogen oxidase inhibitor–resistant Palmer amaranth (Amaranthus palmeri) populations. Weed Sci 65:718–731CrossRefGoogle Scholar
Sammons, RD, Gaines, TA (2014) Glyphosate resistance: State of knowledge. Pest Manag Sci 70:1367–1377CrossRefGoogle ScholarPubMed
Sarangi, D, Jhala, AJ (2018) A statewide survey of stakeholders to assess the problem weeds and weed management practices in Nebraska. Weed Technol 32:642–655CrossRefGoogle Scholar
Sauer, J (1955) Revision of the dioecious Amaranths. Madroño 13:5–46Google Scholar
Sauer, J (1957) Recent migration and evolution of the dioecious Amaranths. Evolution 11:11–31CrossRefGoogle Scholar
Sauer, JD (1972) The dioecious Amaranths: A new species name and major range extensions. Madroño 21:426–434Google Scholar
Schwartz-Lazaro, LM, Norsworthy, JK, Scott, RC, Barber, LT (2017) Resistance of two Arkansas Palmer amaranth populations to multiple herbicide sites of action. Crop Prot 96:158–163CrossRefGoogle Scholar
Smith, J (1900) Fodder and forage plants. Exclusive of the grasses. Washington, DC: U.S. Department of Agriculture. 65 pGoogle Scholar
Tibshirani, R, Walther, G, Hastie, T (2001) Estimating the number of clusters in a data set via the gap statistic. J Roy Stat Soc B 63:441–423CrossRefGoogle Scholar
Varanasi, VK, Brabham, C, Norsworthy, JK (2018a) Confirmation and characterization of non–target site resistance to fomesafen in Palmer amaranth (Amaranthus palmeri). Weed Sci 66:702–709CrossRefGoogle Scholar
Varanasi, VK, Brabham, C, Norsworthy, JK, Nie, H, Young, BG, Houston, M, Barber, T, Scott, RC (2018b) A statewide survey of PPO-inhibitor resistance and the prevalent target-site mechanisms in Palmer amaranth (Amaranthus palmeri) accessions from Arkansas. Weed Sci 66:149–158CrossRefGoogle Scholar
Vieira, BC, Samuelson, SL, Alves, GS, Gaines, TA, Werle, R, Kruger, GR (2018) Distribution of glyphosate-resistant Amaranthus spp. in Nebraska. Pest Manag Sci 74:2316–2324CrossRefGoogle ScholarPubMed
Ward, SM, Webster, TM, Steckel, LE (2013) Palmer amaranth (Amaranthus palmeri): A review. Weed Technol 27:12–27CrossRefGoogle Scholar
Wiersma, AT, Gaines, TA, Preston, C, Hamilton, JP, Giacomini, D, Robin Buell, C, Leach, JE, Westra, P (2015) Gene amplification of 5-enol-pyruvylshikimate-3-phosphate synthase in glyphosate-resistant Kochia scoparia. Planta 241:463–474CrossRefGoogle ScholarPubMed
Wuerffel, RJ, Young, JM, Lee, RM, Tranel, PJ, Lightfoot, DA, Young, BG (2015) Distribution of the G210 protoporphyrinogen oxidase mutation in Illinois waterhemp (Amaranthus tuberculatus) and an improved molecular method for detection. Weed Sci 63:839–845CrossRefGoogle Scholar