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Distribution differences in the EPSPS gene in chromosomes between glyphosate-resistant and glyphosate-susceptible goosegrass (Eleusine indica)

Published online by Cambridge University Press:  25 November 2019

Jingchao Chen ,
Hailan Cui ,
Xiaoyan Ma ,
Yan Ma  and
Xiangju Li Open the ORCID record for Xiangju Li [Opens in a new window]
Jingchao Chen
Affiliation:
Associate Professor, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, P. R. China
Hailan Cui
Affiliation:
Associate Professor, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, P. R. China
Xiaoyan Ma*
Affiliation:
Professor, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, Henan, P. R. China
Yan Ma
Affiliation:
Professor, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, Henan, P. R. China
Xiangju Li
Affiliation:
Professor, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, P. R. China
*
Authors for correspondence: Xiangju Li, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, P. R. China. (Email: xjli@ippcaas.cn); and Yan Ma, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, Henan455000, P. R. China. (Email: aymayan@126.com).
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Abstract

Glyphosate is a popular herbicide used to control goosegrass [Eleusine indica (L.) Gaertn.], one of the most troublesome weeds in cotton (Gossypium hirsutum L.) fields. However, high selection pressure has led to some populations being difficult to control in cotton fields in China. In this study, levels of glyphosate resistance were quantified and 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) amplification was confirmed. In addition, distribution of the EPSPS gene among the chromosomes was also investigated using fluorescence in situ hybridization (FISH) methodology. One population (AHCZ) was confirmed to be glyphosate resistant with a resistance index of 3.4 and significantly reduced shikimate accumulation compared with the susceptible population. All examined AHCZ individuals exhibited no mutations in the EPSPS gene. Expression and copy numbers of EPSPS in the AHCZ population were 5.7 and 15.4 times higher, respectively, than in the susceptible population. A positive correlation was identified between signal intensities of primary anti-EPSPS antibody and copy numbers of the EPSPS protein, as indicated by immunoblot analysis. FISH results revealed that, in mitotic metaphase chromosomes, signals were observed dispersed across two sets of homologous chromosomes in a resistant individual (copy number = 31), while in susceptible individuals, signals were only partially detected in one set of homologous chromosomes. In interphase nuclei, EPSPS signals were brightest in resistant individuals compared with susceptible individuals. In conclusion, one E. indica population from a cotton field in the Anhui Province has evolved resistance to glyphosate, and EPSPS gene amplification was confirmed as the resistance mechanism.

Keywords

Amplified target sitegene overexpressionherbicide resistance
Type
Research Article
Information
Weed Science , Volume 68 , Issue 1 , January 2020 , pp. 33 - 40
Copyright
© Weed Science Society of America, 2019

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Footnotes

Associate Editor: Patrick J. Tranel, University of Illinois

References

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 129:1265–1275CrossRefGoogle ScholarPubMed
Bustin, SA, Benes, V, Garson, JA, Hellemans, J, Huggett, J, Kubista, M, Mueller, R, Nolan, T, Pfaffl, MW, Shipley, GL (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622CrossRefGoogle ScholarPubMed
Cahoon, CW, York, AC, Jordan, DL, Everman, WJ, Seagroves, RW, Braswell, LR, Jennings, KM (2015) Weed control in cotton by combinations of microencapsulated acetochlor and various residual herbicides applied preemergence. Weed Technol 29:740–750CrossRefGoogle Scholar
Chen, J, Huang, Z, Huang, H, Wei, S, Yan, L, Jiang, C, Jie, Z, Zhang, C (2017a) Selection of relatively exact reference genes for gene expression studies in goosegrass (Eleusine indica) under herbicide stress. Sci Rep UK 7:46494CrossRefGoogle ScholarPubMed
Chen, J, Huang, H, Wei, S, Zhang, C, Huang, Z (2015a) Characterization of glyphosate-resistant goosegrass (Eleusine indica) populations in China. J Integr Agric 14:919–925CrossRefGoogle Scholar
Chen, J, Huang, H, Zhang, C, Wei, S, Huang, Z, Chen, J, Wang, X (2015b) Mutations and amplification of EPSPS gene confer resistance to glyphosate in goosegrass (Eleusine indica). Planta 242:1–10CrossRefGoogle Scholar
Chen, J, Jiang, C, Huang, H, Wei, S, Huang, Z, Wang, H, Zhao, D, Zhang, C (2017b) Characterization of Eleusine indica with gene mutation or amplification in EPSPS to glyphosate. Pestic Biochem Physiol 143:201–206CrossRefGoogle ScholarPubMed
Dillon, AJ, Varanasi, VK, Danilova, T, Koo, D-H, Nakka, S, Peterson, D, Tranel, P, Friebe, B, Gill, BS, Jugulam, M (2017) Physical mapping of amplified 5-enolpyruvylshikimate-3-phosphate synthase gene copies in glyphosate-resistant Amaranthus tuberculatus. Plant Physiol 173:1226–1234CrossRefGoogle ScholarPubMed
Duke, SO, Powles, SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319–325CrossRefGoogle ScholarPubMed
Fedoroff, NV (2012) Transposable elements, epigenetics, and genome evolution. Science 338:758–767CrossRefGoogle ScholarPubMed
Gaines, TA, Wright, AA, Molin, WT, Lorentz, L, Riggins, CW, Tranel, PJ, Beffa, R, Westra, P, Powles, SB (2013) Identification of genetic elements associated with EPSPS gene amplification. PLoS ONE 8:e65819CrossRefGoogle ScholarPubMed
Gaines, TA, Zhang, W, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA 107:1029–1034CrossRefGoogle ScholarPubMed
Ganeshaiah, K, Shaanker, RU (1982) Evolution of reproductive behaviour in the genus Eleusine. Euphytica 31:397–404CrossRefGoogle Scholar
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed: December 18, 2019Google Scholar
Heap, I, Duke, SO (2018) Overview of glyphosate-resistant weeds worldwide. Pest Manag Sci 74:1040–1049CrossRefGoogle ScholarPubMed
Holm, LG, Plucknett, DL, Pancho, JV, Herberger, JP (1977) The World’s Worst Weeds: Distribution and Biology. Honolulu: University Press of Hawaii. Pp 47–53Google Scholar
Hu, F, Dong, H, Shen, X, Liu, J, Wei, J, Chen, Y (2018) Resistance level of Eleusine indica populations to paraquat, glyphosate and glufosinate. Southwest China J Agric Sci 31:335–341Google Scholar
Jugulam, M, Niehues, K, Godar, AS, Koo, D-H, Danilova, T, Friebe, B, Sehgal, S, Varanasi, VK, Wiersma, A, Westra, P (2014) Tandem amplification of a chromosomal segment harboring EPSPS locus confers glyphosate resistance in Kochia scoparia. Plant Physiol 166:1200–1207CrossRefGoogle ScholarPubMed
Kato, A, Kato, A, Albert, P, Vega, J, Kato, A, Albert, P, Vega, J, Birchler, J (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem 81:71–78CrossRefGoogle ScholarPubMed
Kato, A, Lamb, JC, Birchler, JA (2004) Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc Natl Acad Sci USA 101:13554–13559CrossRefGoogle ScholarPubMed
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
Li, J, Peng, Q, Han, H, Nyporko, A, Kulynych, T, Yu, Q, Powles, S (2018) Glyphosate resistance in Tridax procumbens via a novel EPSPS Thr-102-Ser substitution. J Agric Food Chem 66:7880–7888CrossRefGoogle Scholar
Lorentz, L, Gaines, TA, Nissen, SJ, Westra, P, Strek, HJ, Dehne, HW, Ruiz-Santaella, JP, Beffa, R (2014) Characterization of glyphosate resistance in Amaranthus tuberculatus populations. J Agric Food Chem 62:8134–8142CrossRefGoogle ScholarPubMed
Luo, S, Peng, J, Li, K, Wang, M, Kuang, H (2010) Contrasting evolutionary patterns of the Rp1 resistance gene family in different species of Poaceae. Mol Biol Evol 28:313–325CrossRefGoogle ScholarPubMed
Ma, X, Wu, H, Jiang, W, Ma, Y (2015) Goosegrass (Eleusine indica) density effects on cotton (Gossypium hirsutum). J Integr Agric 14:1778–1785CrossRefGoogle Scholar
Malone, JM, Morran, S, Shirley, N, Boutsalis, P, Preston, C (2015) EPSPS gene amplification in glyphosate-resistant Bromus diandrus. Pest Manag Sci 72:81–88CrossRefGoogle ScholarPubMed
Moretti, ML, Van Horn, CR, Robertson, R, Segobye, K, Weller, SC, Young, BG, Johnson, WG, Douglas Sammons, R, Wang, D, Ge, X (2018) Glyphosate resistance in Ambrosia trifida: Part 2. Rapid response physiology and non-target-site resistance. Pest Manag Sci 74:1079–1088CrossRefGoogle ScholarPubMed
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 70:1902–1909CrossRefGoogle 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 74:1101–1108CrossRefGoogle Scholar
Panchy, N, Lehti-Shiu, M, Shiu, S-H (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316Google ScholarPubMed
Perotti, VE, Larran, AS, Palmieri, VE, Martinatto, AK, Alvarez, CE, Tuesca, D, Permingeat, HR (2019) A novel triple amino acid substitution in the EPSPS found in a high-level glyphosate resistant Amaranthus hybridus population from Argentina. Pest Manag Sci 75:1242–1251CrossRefGoogle 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 68:1223–1230CrossRefGoogle ScholarPubMed
Seefeldt, SS, Fuerst, EP (1995) Log-logistic analysis of herbicide dose-response relationships. Weed Technol 9:218–227CrossRefGoogle Scholar
Steinrücken, H, Amrhein, N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochem Biophys Res Commun 94:1207–1212CrossRefGoogle Scholar
Takano, H, Oliveira, R, Jr, Constantin, J, Silva, V, Mendes, R (2018) Chemical control of glyphosate-resistant goosegrass. Planta Daninha 36:e018176124CrossRefGoogle Scholar
Takano, HK, Mendes, RR, Scoz, LB, Ovejero, RFL, Constantin, J, Gaines, TA, Westra, P, Dayan, FE, Oliveira, RS (2019) Proline-106 EPSPS mutation imparting glyphosate resistance in goosegrass (Eleusine indica) emerges in South America. Weed Sci 67:48–56CrossRefGoogle Scholar
Van Binsbergen, E (2011) Origins and breakpoint analyses of copy number variations: up close and personal. Cytogenet Genome Res 135:271–276CrossRefGoogle Scholar
Van Horn, CR, Moretti, ML, Robertson, RR, Segobye, K, Weller, SC, Young, BG, Johnson, WG, Schulz, B, Green, AC, Jeffery, T (2018) Glyphosate resistance in Ambrosia trifida: Part 1. Novel rapid cell death response to glyphosate. Pest Manag Sci 74:1071–1078CrossRefGoogle ScholarPubMed
Wang, J, LI, X, Li, D, Han, Y, Zheng, L, Yu, H, Cui, H (2018) Non-target-site and target-site resistance to AHAS inhibitors in American sloughgrass (Beckmannia syzigachne). J Integr Agric 17:2714–2723CrossRefGoogle Scholar
Wiersma, AT, Gaines, TA, Preston, C, Hamilton, JP, Giacomini, D, Buell, CR, Leach, JE, Westra, P (2014) Gene amplification of 5-enol-pyruvylshikimate-3-phosphate synthase in glyphosate-resistant Kochia scoparia. Planta 241:463–474CrossRefGoogle ScholarPubMed
Yang, C, Tian, X, Feng, L, Yue, M (2012) Resistance of Eleusine indica Gaertn to glyphosate. Scientia Agricultura Sinica 45:2093–2098Google Scholar
Yu, Q, Jalaludin, A, Han, H, Chen, M, Sammons, RD, Powles, SB (2015) Evolution of a double amino acid substitution in the EPSP synthase in Eleusine indica conferring high level glyphosate resistance. Plant Physiol 167:1440–1447CrossRefGoogle ScholarPubMed
Zhang, C, Feng, L, He, T-T, Yang, C-H, Chen, G-Q, Tian, X-S (2015) Investigating the mechanisms of glyphosate resistance in goosegrass (Eleusine indica) population from South China. J Integr Agric 14:909–918CrossRefGoogle Scholar
Zhang, Z (2003) Development of chemical weed control and integrated weed management in China. Weed Biol Manag 3:197–203CrossRefGoogle Scholar
Zhu, J, Wang, J, DiTommaso, A, Zhang, C, Zheng, G, Liang, W, Islam, F, Yang, C, Chen, X, Zhou, W (2018) Weed research status, challenges, and opportunities in China. Crop Prot, 10.1016/j.cropro.2018.02.001CrossRefGoogle Scholar