Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-25T19:39:54.537Z Has data issue: false hasContentIssue false
  • English
  • Français

Multiple resistance to PPO and ALS inhibitors in redroot pigweed (Amaranthus retroflexus)

Published online by Cambridge University Press:  25 October 2019

Hao Wang ,
Hengzhi Wang ,
Ning Zhao ,
Baolin Zhu ,
Penglei Sun ,
Weitang Liu  and
Jinxin Wang Open the ORCID record for Jinxin Wang [Opens in a new window]
Hao Wang
Affiliation:
Graduate Student, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
Hengzhi Wang
Affiliation:
Graduate Student, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
Ning Zhao
Affiliation:
Graduate Student, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
Baolin Zhu
Affiliation:
Graduate Student, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
Penglei Sun
Affiliation:
Graduate Student, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
Weitang Liu*
Affiliation:
Associate Professor, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
Jinxin Wang*
Affiliation:
Professor, College of Plant Protection and Key Laboratory of Pesticide Toxicology and Application Technology, Shandong Agricultural University, Tai’an, Shandong, China
*
Weitang Liu, College of Plant Protection, Shandong Agricultural University, Tai’an 271018, Shandong, China. (Email: [email protected])
Authors for correspondence: Jinxin Wang, College of Plant Protection, Shandong Agricultural University, Tai’an 271018, Shandong, China. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

A redroot pigweed (Amaranthus retroflexus L.) population (HN-02) collected from Nenjiang County, Heilongjiang Province, exhibited multiple resistance to fomesafen and nicosulfuron. The purposes of this study were to characterize the herbicide resistance status of an HN-02 population for both acetolactate synthase (ALS) and protoporphyrinogen oxidase (PPO) inhibitors and the response to other herbicides and to investigate the target site-based mechanism governing fomesafen and nicosulfuron resistance. Three mutations, Ala-205-Val and Trp-574-Leu mutations in the ALS gene and an Arg-128-Gly mutation in the PPX2 gene, were identified in individual resistant plants. An HN-02F1-1 subpopulation homozygous for the Ala-205-Val and Arg-128-Gly mutations was generated, and whole-plant experiments confirmed multiple resistance to PPO inhibitors (fomesafen, fluoroglycofen-ethyl, and acifluorfen) and ALS inhibitors (imidazolinones [IMI], sulfonylureas [SU], and triazolopyrimidines [TP]) in the HN-02F1-1 plants, which presented resistance index values ranging from 8.3 to 110; however, these plants were sensitive to flumioxazin, fluroxypyr-meptyl, and 2,4-D butylate. In vitro ALS enzyme activity assays revealed that, compared with ALS from susceptible plants, ALS from the HN-02F1-1 plants was 15-, 28- and 320-fold resistant to flumetsulam, nicosulfuron, and imazethapyr, respectively. This study confirms the first case of multiple resistance to PPO and ALS inhibitors in A. retroflexus and determines that the target-site resistance mechanism was produced by Ala-205-Val and Arg-128-Gly mutations in the ALS gene and PPX2 gene, respectively. In particular, the Ala-205-Val mutation was found to endow resistance to three classes of ALS inhibitors: TP, SU, and IMI.

Keywords

In vitro ALSmultiple resistance
Type
Research Article
Information
Weed Science , Volume 68 , Issue 1 , January 2020 , pp. 19 - 26
Copyright
© Weed Science Society of America, 2019

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.)

Footnotes

Associate Editor: Patrick J. Tranel, University of Illinois

References

Ashigh, J, Tardif, F (2006) ALS-inhibitor resistance in populations of eastern black nightshade (Solanum ptychanthum) from Ontario. Weed Technol 20:308–314CrossRefGoogle Scholar
Ashigh, J, Tardif, FJ (2007) An Ala 205 Val substitution in acetohydroxyacid synthase of Eastern black nightshade (Solanum ptychanthum) reduces sensitivity to herbicides and feedback inhibition. Weed Sci 55:558–565CrossRefGoogle Scholar
Ashigh, J, Tardif, F (2009) An amino acid substitution at position 205 of acetohydroxyacid synthase reduces fitness under optimal light in resistant populations of Solanum ptychanthum. Weed Res 49:479–489CrossRefGoogle Scholar
Beale, SI, Weinstein, JD (1990) Tetrapyrrole metabolism in photosynthetic organisms. Pages 287–391in Dailey, HA, ed. Biosynthesis of Heme and Chlorophyll. New York: McGraw-HillGoogle Scholar
Beckie, HJ, Tardif, FJ (2012) Herbicide cross resistance in weeds. Crop Prot 35:15–28CrossRefGoogle Scholar
Bensch, CN, Horak, MJ, Peterson, D (2003) Interference of redroot pigweed (Amaranthus retroflexus L.), Palmer amaranth (A. palmeri), and common waterhemp (A. rudis) in soybean. Weed Sci 51:37–43CrossRefGoogle Scholar
Brosnan, JT, Vargas, JJ, Breeden, GK, Grier, L, Aponte, RA, Tresch, S, Laforest, M (2016) A new amino acid substitution (Ala-205-Phe) in acetolactate synthase (ALS) confers broad spectrum resistance to ALS-inhibiting herbicides. Planta 243:149–159CrossRefGoogle ScholarPubMed
Chaleff, RS, Mauvais, C (1984) Acetolactate synthase is the site of action of two sulfonylurea herbicides in higher plants. Science 224:1443–1445CrossRefGoogle ScholarPubMed
Chen, J, Huang, Z, Zhang, C, Huang, H, Wei, S, Chen, J, Wang, X (2015) Molecular basis of resistance to imazethapyr in redroot pigweed (Amaranthus retroflexus L.) populations from China. Pestic Biochem Physiol 124:43–47CrossRefGoogle ScholarPubMed
Dayan, FE, Barker, A, Tranel, PJ (2018) Origins and structure of chloroplastic and mitochondrial plant protoporphyrinogen oxidases: implications for the evolution of herbicide resistance. Pest Manag Sci 74:2226–2234CrossRefGoogle ScholarPubMed
Délye, C, Jasieniuk, M, Le Corre, V (2013) Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29:649–658CrossRefGoogle ScholarPubMed
Délye, C, Michel, S, Bérard, 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 (black-grass). New Phytol 186:1005–1017CrossRefGoogle Scholar
Délye, C, Pernin, F, Scarabel, L (2011) Evolution and diversity of the mechanisms endowing resistance to herbicides inhibiting acetolactate-synthase (ALS) in corn poppy (Papaver rhoeas L.). Plant Sci 180:333–342CrossRefGoogle Scholar
Duggleby, RG, McCourt, JA, Guddat, LW (2008) Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Plant Physiol Biochem 46:309–324CrossRefGoogle ScholarPubMed
Duke, SO, Lydon, J, Becerril, JM, Sherman, TD, Lehnen, LP, Matsumoto, H (1991) Protoporphyrinogen oxidase-inhibiting herbicides. Weed Sci 39:465–473CrossRefGoogle Scholar
Francischini, A, Constantin, J, Oliveira, R Jr, Santos, G, Franchini, L, Biffe, D (2014) Resistance of Amaranthus retroflexus L. to acetolactate synthase inhibitor herbicides in Brazil. Planta Daninha 32:437–446CrossRefGoogle Scholar
Gerwick, BC, Subramanian, MV, Loney-Gallant, VI, Chandler, DP (1990) Mechanism of action of the 1, 2, 4-triazolo [1, 5-a] pyrimidines. Pest Manag Sci 29:357–364CrossRefGoogle Scholar
Ghanizadeh, H, Lorzadeh, S, Aryannia, N (2014) Effect of weed interference on Zea mays: growth analysis. Weed Biol Manag 14:133–137CrossRefGoogle 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 L. Pest Manag Sci 73:1559–1563CrossRefGoogle Scholar
Han, H, Yu, Q, Purba, E, Li, M, Walsh, M, Friesen, S, Powles, SB (2012) A novel amino acid substitution Ala-122-Tyr in ALS confers high-level and broad resistance across ALS-inhibiting herbicides. Pest Manag Sci 68:1164–1170CrossRefGoogle ScholarPubMed
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: September 1, 2019Google Scholar
Jacobs, JM, Jacobs, NJ (1993) Porphyrin accumulation and export by isolated barley (Hordeum vulgare) plastids (effect of diphenyl ether herbicides). Plant Physiol 101:1181–1187CrossRefGoogle Scholar
Lee, HJ, Lee, SB, Chung, JS, Han, SU, Han, O, Guh, JO, Jeon, JS, An, G, Back, K (2000) Transgenic rice plants expressing a Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. Plant Cell Physiol 41:743–749CrossRefGoogle ScholarPubMed
Lermontova, I, Kruse, E, Mock, H-P, Grimm, B (1997) Cloning and characterization of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen IX oxidase. Proc Natl Acad Sci USA 94:8895–8900CrossRefGoogle Scholar
Li, D, Li, X, Yu, H, Wang, J, Cui, H (2017) Cross-resistance of eclipta (Eclipta prostrata) in China to ALS inhibitors due to a Pro-197-Ser point mutation. Weed Sci 65:547–556CrossRefGoogle Scholar
Li, W, Fan, D, Luan, Y (2008) Current situation, problems and solutions of ethametsulfuron, chlorimuron-ethyl and imazethapyr. Agrochemicals 47:781–789Google Scholar
Liu, W, Yuan, G, Du, L, Guo, W, Li, L, Bi, Y, Wang, J (2015) A novel Pro197Glu substitution in acetolactate synthase (ALS) confers broad-spectrum resistance across ALS inhibitors. Plant Physiol Biochem 117:31–38Google ScholarPubMed
Mandák, B, Zákravský, P, Dostál, P, Plačková, I (2011) Population genetic structure of the noxious weed Amaranthus retroflexus L. in Central Europe. Flora 206:697–703CrossRefGoogle Scholar
Matzrafi, M, Lazar, TW, Sibony, M, Rubin, B (2015) Conyza species: distribution and evolution of multiple target-site herbicide resistances. Planta 242:259–267CrossRefGoogle ScholarPubMed
McNaughton, KE, Letarte, J, Lee, EA, Tardif, FJ (2005) Mutations in ALS confer herbicide resistance in redroot pigweed (Amaranthus retroflexus L.) and Powell amaranth (Amaranthus powellii L.). Weed Sci 53:17–22Google Scholar
Patzoldt, WL, Hager, AG, McCormick, JS, Tranel, PJ (2006) A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc Natl Acad Sci USA 103:12329–12334CrossRefGoogle ScholarPubMed
Petit, C, Duhieu, B, Boucansaud, K, Délye, C (2010) Complex genetic control of non-target-site-based resistance to herbicides inhibiting acetyl-coenzyme A carboxylase and acetolactate-synthase in Alopecurus myosuroides Huds. Plant Sci 178:501–509CrossRefGoogle Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317–347.CrossRefGoogle ScholarPubMed
Rangani, G, Salas-Perez, RA, Aponte, RA, Knapp, M, Craig, IR, Meitzner, T, Burgos, NR (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
Rousonelos, SL, Lee, RM, Moreira, MS, VanGessel, MJ, Tranel, PJ (2012) Characterization of a common ragweed (Ambrosia artemisiifolia) population resistant to ALS- and PPO-inhibiting herbicides. Weed Sci 60:335–344CrossRefGoogle Scholar
Santel, H, Bowden, B, Sorensen, V, Mueller, K (1999) Flucarbazone-sodium-a new herbicide for the selective control of wild oat and green foxtail in wheat. Pages 23–28 in Proceedings of British Crop Protection Council. Brighton, UK: British Crop Protection CouncilGoogle Scholar
Scarabel, L, Varotto, S, Sattin, M (2007) A European biotype of Amaranthus retroflexus L. cross-resistant to ALS inhibitors and response to alternative herbicides. Weed Res 47:527–533CrossRefGoogle Scholar
Shaner, DL (1999) Resistance to acetolactate synthase (ALS) inhibitors in the United States: history, occurrence, detection, and management. Weed Sci 44:405–411CrossRefGoogle Scholar
Shaner, DL, Anderson, PC, Stidham, MA (1984) Imidazolinones: potent inhibitors of acetohydroxyacid synthase. Plant Physiol 76:545–546CrossRefGoogle ScholarPubMed
Sheibany, K, Baghestani Meybodi, MA, Atri, A (2009) Competitive effects of redroot pigweed (Amaranthus retroflexus L.) on the growth indices and yield of corn. Weed Biol Manag 9:152–159CrossRefGoogle Scholar
Stidham, MA (1991) Herbicides that inhibit acetohydroxyacid synthase. Weed Sci 39:428–434CrossRefGoogle Scholar
Tranel, P, Wright, T, Heap, I (2019) Mutations in Herbicide-Resistant Weeds to ALS Inhibitors. http://www.weedscience.org. Accessed: July 15, 2019Google Scholar
Tranel, PJ, Riggins, CW, Bell, MS, Hager, AG (2010) Herbicide resistances in Amaranthus tuberculatus: a call for new options. J Agric Food Chem 59:5808–5812CrossRefGoogle Scholar
Varanasi, VK, Brabham, C, Norsworthy, JK (2018) Confirmation and characterization of non–target site resistance to fomesafen in Palmer amaranth (Amaranthus palmeri L.). Weed Sci 66:702–709Google Scholar
Wang, H, Guo, W, Zhang, L, Zhao, K, Ge, L, Lv, X, Liu, W, Wang, J (2017) Multiple resistance to thifensulfuron-methyl and fomesafen in redroot pigweed (Amaranthus retroflexus L.) from China. Chil J Agric Res 77:311–317CrossRefGoogle Scholar
Wuerffel, RJ, Young, JM, Matthews, JL, Young, BG (2015) Characterization of PPO-inhibitor–resistant waterhemp (Amaranthus tuberculatus L.) response to soil-applied PPO-inhibiting herbicides. Weed Sci 63:511–521CrossRefGoogle Scholar
Yu, Q, Han, H, Vila-Aiub, MM, Powles, SB (2010) AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth. J Exp Bot 61:3925–3934CrossRefGoogle ScholarPubMed
Yu, Q, Powles, S (2014a) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:1106–1118CrossRefGoogle ScholarPubMed
Yu, Q, Powles, SB (2014b) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350CrossRefGoogle ScholarPubMed
Yuan, JS, Tranel, PJ, Stewart, CN Jr (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13CrossRefGoogle ScholarPubMed
Zhao, N, Li, W, Bai, S, Guo, W, Yuan, G, Wang, F, Liu, W, Wang, J (2017) Transcriptome profiling to identify genes involved in mesosulfuron-methyl resistance in Alopecurus aequalis. Fron Plant Sci 8:1391CrossRefGoogle ScholarPubMed