Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T06:28:43.520Z Has data issue: false hasContentIssue false

Proline-106 EPSPS Mutation Imparting Glyphosate Resistance in Goosegrass (Eleusine indica) Emerges in South America

Published online by Cambridge University Press:  18 December 2018

Hudson K. Takano*
Affiliation:
Graduate Student, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Rafael R. Mendes
Affiliation:
Graduate Student, Agronomy Department, State University of Maringá, Paraná, Brazil
Leonardo B. Scoz
Affiliation:
Molecular Biology Researcher, Mato Grosso Cotton Institute, Rondonópolis, Mato Grosso, Brazil
Ramiro F. Lopez Ovejero
Affiliation:
Weed Resistance Management Leader, Monsanto Brazil, São Paulo, Brazil
Jamil Constantin
Affiliation:
Professor, Agronomy Department, State University of Maringá, Paraná, Brazil
Todd A. Gaines
Affiliation:
Assistant Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Philip Westra
Affiliation:
Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Franck E. Dayan
Affiliation:
Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Rubem S. Oliveira Jr
Affiliation:
Professor, Agronomy Department, State University of Maringá, Paraná, Brazil
*
Author for correspondence: Hudson K. Takano, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO 80523. (Email: hudsontakano@gmail.com)

Abstract

Glyphosate-resistant (GR) goosegrass [Eleusine indica (L.) Gaertn.] was recently identified in Brazil, but its resistance mechanism was unknown. This study elucidated the resistance mechanism in this species and developed a molecular marker for rapid detection of this target-site resistance trait. The resistance factor for the resistant biotype was 4.4-fold compared with the glyphosate-susceptible (GS) in greenhouse dose–response experiments. This was accompanied by a similar (4-fold) difference in the levels of in vitro and in planta shikimate accumulation in these biotypes. However, there was no difference in uptake, translocation, or metabolism of glyphosate between the GS and GR biotypes. Moreover, both biotypes showed similar values for 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) copy number and transcription. Sequencing of a 330-bp fragment of the EPSPS gene identified a single-nucleotide polymorphism that led to a Pro-106-Ser amino acid substitution in the enzyme from the GR biotype. This mutation imparted a 3.8-fold increase in the amount of glyphosate required to inhibit 50% of EPSPS activity, confirming the role of this amino acid substitution in resistance to glyphosate. A quantitative PCR–based genotyping assay was developed for the rapid detection of resistant plants containing this Pro-106-Ser mutation.

Type
Research Article
Copyright
© Weed Science Society of America 2018. 

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.)

References

Alarcón-Reverte, R, García, A, Watson, SB, Abdallah, I, Sabaté, S, Hernández, MJ, Dayan, FE, Fischer, AJ (2015) Concerted action of target-site mutations and high EPSPS activity in glyphosate-resistant junglerice (Echinochloa colona) from California. Pest Manag Sci 71:9961007Google Scholar
Baerson, SR, Rodriguez, DJ, Tran, M, Feng, Y, Biest, NA, Dill, GM (2002) Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol 129:12651275Google Scholar
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 61:420Google Scholar
Carvalho, LB, Alves, PLDCA, González-Torralva, F, Cruz-Hipolito, HE, Rojano-Delgado, AM, De Prado, R, Gil-Humanes, J, Barro, F, Luque de Castro, MD (2012) Pool of resistance mechanisms to glyphosate in Digitaria insularis. J Agric Food Chem 60:615622Google Scholar
Chen, J, Huang, H, Zhang, C, Wei, S, Huang, Z, Chen, J, Wang, X (2015) Mutations and amplification of EPSPS gene confer resistance to glyphosate in goosegrass (Eleusine indica). Planta 242:859868Google Scholar
Chen, J, Huang, H, Wei, S, Huang, Z, Wang, X, Zhang, C (2017a)Investigating the mechanisms of glyphosate resistance in goosegrass (Eleusine indica (L.) Gaertn.) by RNA sequencing technology. Plant J 89:407415Google Scholar
Chen, J, Jiang, C, Huang, H, Wei, S, Huang, Z, Wang, H, Zhang, C (2017b) Characterization of Eleusine indica with gene mutation or amplification in EPSPS to glyphosate. Pestic Biochem Physiol 143:201206Google Scholar
Corbett, CL, Tardif, FJ (2006) Detection of resistance to acetolactate synthase inhibitors in weeds with emphasis on DNA-based techniques: a review. Pest Manag Sci 62:584597Google Scholar
Dayan, FE, Owens, DK, Corniani, N, Silva, FML, WatsonSB, , Howell, JL, Shaner, DL (2015) Biochemical markers and enzyme assays for herbicide mode of action and resistance studies. Weed Sci 63(SP1):2363Google Scholar
Délye, C, Duhoux, A, Pernin, F, Riggins, CW, Tranel, PJ (2015) Molecular mechanisms of herbicide resistance. Weed Sci 63:91115Google Scholar
Délye, C, Michel, S, Berard, A, Chauvel, B, Brunel, D, Guillemin, JP, Dessaint, F, Le Corre, V (2010) Geographical variation in resistance to acetyl-coenzyme A carboxylase-inhibiting herbicides across the range of the arable weed Alopecurus myosuroides (blackgrass). New Phytol 186:10051017Google Scholar
Duke, SO, Powles, SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319325Google Scholar
Figueiredo, MR, Leibhart, LJ, Reicher, ZJ, Tranel, PJ, Nissen, SJ, Westra, P, Jugulam, M (2017) Metabolism of 2, 4-dichlorophenoxyacetic acid contributes to resistance in a common waterhemp (Amaranthus tuberculatus) population. Pest Manag Sci 73:213221Google Scholar
Gaines, TA, Heap, IM (2018) Mutations in herbicide-resistant weeds to EPSP synthase inhibitors. http://www.weedscience.com. Accessed: May 23, 2018Google Scholar
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 107:10291034Google Scholar
Giancola, S, McKhann, HI, Berard, A, Camilleri, C, Durand, S, Libeau, P, Roux, F, Reboud, X, Gut, IG, Brunel, D (2006) Utilization of the three high-throughput SNP genotyping methods, the GOOD assay, Amplifuor and TaqMan, in diploid and polyploid plants. Theoret Appl Gen 112:11151124Google Scholar
Han, H, Vila-Aiub, MM, Jalaludin, A, Yu, Q, Powles, SB (2017) A double EPSPS gene mutation endowing glyphosate resistance shows a remarkably high resistance cost. Plant Cell Environ 40:30313042Google Scholar
Han, H, Yu, Q, Widderick, MJ, Powles, SB (2016) Target-site EPSPS Pro-106 mutations: sufficient to endow glyphosate resistance in polyploid Echinochloa colona? Pest Manag Sci 72:264271Google Scholar
Heap, I (2018) The International Survey of Herbicide-Resistant Weeds. http://www.weedscience.org. Accessed: May 7, 2018Google Scholar
Jugulam, M, Niehues, K, Godar, AS, Koo, DH, Danilova, T, Friebe, B, Sehgal, S, Varanasi, VK, Wiersma, A, Westra, P, Stahlman, PW (2014) Tandem amplification of a chromosomal segment harboring 5-enolpyruvylshikimate-3-phosphate synthase locus confers glyphosate resistance in Kochia scoparia. Plant Physiol 166:12001207Google Scholar
Kaundun, SS, Zelaya, IA, Dale, RP, Lycett, AJ, Carter, P, Sharples, KR, Mcindoe, E (2008) Importance of the P106S target-site mutation in conferring resistance to glyphosate in a goosegrass (Eleusine indica) population from the Philippines. Weed Sci 56:637646Google Scholar
Kniss, AR, Vassios, JD, Nissen, SJ, Ritz, C (2011) Nonlinear regression analysis of herbicide absorption studies. Weed Sci 59:601610Google Scholar
Küpper, A, Borgato, EA, Patterson, EL, Netto, AG, Nicolai, M, Carvalho, SJD, Nissen, SJ, Gaines, TA, Christoffoleti, PJ (2017) Multiple resistance to glyphosate and acetolactate synthase inhibitors in palmer amaranth (Amaranthus palmeri) identified in Brazil. Weed Sci 65:317326Google Scholar
Lee, LJ, Ngim, JA (2000) First report of glyphosate-resistant goosegrass (Eleusine indica (L) Gaertn) in Malaysia. Pest Manag Sci 56:336339Google Scholar
Lopez Ovejero, RF, Takano, HK, Nicolai, M, Ferreira, A, Melo, MS, Cavenaghi, AL, Christoffoleti, PJ, Oliveira, RS Jr (2017) Frequency and dispersal of glyphosate-resistant sourgrass (Digitaria insularis) populations across Brazilian agricultural production areas. Weed Sci 65:285294Google Scholar
Lorentz, L, Gaines, TA, Nissen, SJ, Westra, P, Strek, HJ, Dehne, HW, Beffa, R (2014) Characterization of glyphosate resistance in Amaranthus tuberculatus populations. J Agric Food Chem 62:81348142Google Scholar
Ma, XY, Wu, HW, Jiang, WL, Yan, MA (2015) Goosegrass (Eleusine indica) density effects on cotton (Gossypium hirsutum). J Integrat Agric 14:17781785Google Scholar
Malone, JM, Morran, S, Shirley, N, Boutsalis, P, Preston, C. (2016) EPSPS gene amplification in glyphosate-resistant Bromus diandrus. Pest Manag Sci 72:8188Google Scholar
Malpassi, RN (2006) Herbicide effects on cuticle ultrastructure in Eleusine indica and Portulaca oleracea. Biocell 30:5156Google Scholar
Matallo, MB, Almeida, SDB, Cerdeira, AL, Franco, DA, Blanco, FMG, Menezes, PTC, Luchini, LC, Moura, MAM, Duke, SO (2009) Microwave-assisted solvent extraction and analysis of shikimic acid from plant tissues. Planta Daninha 27:987994Google Scholar
Molin, WT, Wright, AA, Nandula, VK (2013) Glyphosate-resistant goosegrass from Mississippi. Agronomy 3:474487Google Scholar
Mueller, TC, Barnett, KA, Brosnan, JT, Steckel, LE (2011) Glyphosate-resistant goosegrass (Eleusine indica) confirmed in Tennessee. Weed Sci 59:562566Google Scholar
Nandula, VK, Wright, AA, Bond, JA, Ray, JD, Eubank, TW, Molin, WT (2014) EPSPS amplification in glyphosate-resistant spiny amaranth (Amaranthus spinosus): a case of gene transfer via interspecific hybridization from glyphosate-resistant Palmer amaranth (Amaranthus palmeri). Pest Manag Sci 70:19021909Google Scholar
Ng, CH, Ratnam, W, Surif, S, Ismail, BS (2004a) Inheritance of glyphosate resistance in goosegrass (Eleusine indica). Weed Sci 52:564570Google Scholar
Ng, CH, Wickneswari, R, Salmijah, S, Teng, YT, Ismail, BS (2003) Gene polymorphisms in glyphosate-resistant and -susceptible biotypes of Eleusine indica from Malaysia. Weed Res 43:108115Google Scholar
Ng, CH, Wickneswari, R, Salmijah, S, Teng, YT, Ismail, BS (2004b) Glyphosate resistance in Eleusine indica (L.) Gaertn from different origins and polymerase chain reaction amplification of specific alleles. Austral J Agric Res 55:407414Google Scholar
Ngo, TD, Malone, JM, Boutsalis, P, Gill, G, Preston, C (2018) EPSPS gene amplification conferring resistance to glyphosate in windmill grass (Chloris truncata) in Australia. Pest Manag Sci 74:11011108Google Scholar
Osuna, MD, Goulart, ICGDR, Vidal, RA, Kalsing, A, Ruiz Santaella, JP, De Prado, R (2012) Resistance to ACCase inhibitors in Eleusine indica from Brazil involves a target site mutation. Planta Daninha 30:675681Google Scholar
Patterson, EL, Fleming, MB, Kessler, KC, Nissen, SJ, Gaines, TA (2017) A KASP genotyping method to identify Northern watermilfoil, Eurasian watermilfoil, and their interspecific hybrids. Front Plant Sci 8:752Google Scholar
Peterson, MA, Collavo, A, Ovejero, R, Shivrain, V, Walsh, MJ (2018) The challenge of herbicide resistance around the world: a current summary. Pest Manag Sci 75:112121Google Scholar
Ranade, K, Chang, MS, Ting, CT, Pei, D, Hsiao, CF, Olivier, M, Pesich, R, Hebert, J, Chen, YD, Dzau, VJ, Curb, D, Olshen, R, Risch, N, Cox, DR, Botstein, D (2001) High-throughput genotyping with single nucleotide polymorphisms. Genome Res 11:12621268Google Scholar
Ritz, C, Baty, F, Streibig, JC, Gerhard, D (2015) Dose-response analysis using R. PLoS ONE 10:e0146021Google Scholar
Salas, RA, Dayan, FE, Pan, Z, Watson, SB, Dickson, JW, Scott, RC, Burgos, NR (2012) EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp. multiflorum) from Arkansas. Pest Manag Sci 68:12231230Google Scholar
Sammons, RD, Gaines, TA (2014) Glyphosate resistance: state of knowledge. Pest Manag Sci 70:13671377Google Scholar
Shaner, DL, Nadler-Hassar, T, Henry, WB, Koger, CH (2005) A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci 53:769774Google Scholar
Streibig, JC (1988) Herbicide bioassay. Weed Res 28:479484Google Scholar
Takano, HK, Oliveira, RS Jr, Constantin, J, Braz, GBP, Padovese, JC (2016) Growth, development and seed production of goosegrass. Planta Daninha 34:249258Google Scholar
Takano, HK, Oliveira, RS Jr, Constantin, J, Braz, GBP, Gheno, EA (2017) Goosegrass resistant to glyphosate in Brazil. Planta Daninha 36:e017163071Google Scholar
Warwick, SI, Xu, R, Sauder, C, Beckie, HJ (2008) Acetolactate synthase target-site mutations and single nucleotide polymorphism genotyping in ALS-resistant kochia (Kochia scoparia). Weed Sci 56:797806Google Scholar
Wiersma, AT, Gaines, TA, Preston, C, Hamilton, JP, Giacomini, D, Buell, CR, Leach, JE, Westra, P (2015) Gene amplification of 5-enol-pyruvylshikimate-3-phosphate synthase in glyphosate-resistant Kochia scoparia. Planta 241:463474Google Scholar
Yu, Q, Jalaludin, A, Han, H, Chen, M, Sammons, RD, Powles, SB (2015) Evolution of a double amino acid substitution in the 5-enolpyruvylshikimate-3-phosphate synthase in Eleusine indica conferring high-level glyphosate resistance. Plant Physiol 167:14401447Google Scholar