Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-19T07:41:29.758Z Has data issue: false hasContentIssue false
  • English
  • Français

Differences in efficacy, resistance mechanism and target protein interaction between two PPO inhibitors in Palmer amaranth (Amaranthus palmeri)

Published online by Cambridge University Press:  13 January 2020

Chenxi Wu Open the ORCID record for Chenxi Wu [Opens in a new window] ,
Michael-Rock Goldsmith ,
John Pawlak ,
Paul Feng ,
Stacie Smith ,
Santiago Navarro  and
Alejandro Perez-Jones
Chenxi Wu*
Affiliation:
Bayer CropScience, St Louis, MO, USA
Michael-Rock Goldsmith
Affiliation:
Bayer CropScience, St Louis, MO, USA
John Pawlak
Affiliation:
Valent USA, Walnut Creek, CA, USA
Paul Feng
Affiliation:
Bayer CropScience, St Louis, MO, USA
Stacie Smith
Affiliation:
Bayer CropScience, St Louis, MO, USA
Santiago Navarro
Affiliation:
Bayer CropScience, St Louis, MO, USA
Alejandro Perez-Jones
Affiliation:
Bayer CropScience, St Louis, MO, USA
*
Author for correspondence: Chenxi Wu, Bayer CropScience, 700 Chesterfield Parkway West, St Louis, MO63017. Email: chenxi.wu@bayer.com
Get access Rights & Permissions [Opens in a new window]

Abstract

A weed survey was conducted on 134 Palmer amaranth (Amaranthus palmeri S. Watson) populations from Mississippi and Arkansas in 2017 to investigate the spread of resistance to protoporphyrinogen oxidase (PPO) inhibitors using fomesafen as a proxy. Fomesafen resistance was found in 42% of the A. palmeri populations. To investigate the resistance basis of different PPO inhibitors, we further characterized 10 representative populations by in planta bioassay in a controlled environment and molecular characterizations (DNA sequencing and TaqMan® gene expression assay). A total of 160 plants were sprayed with a labeled field rate (1X) of fomesafen or salfufenacil and screened for the presence of three known resistance-endowing mutations in the mitochondrial PPX2 gene (ΔGly-210, Arg-128-Gly, Gly-399-Ala). To compare the potencies of fomesafen and saflufenacil, dose–response studies were conducted on two highly resistant and one sensitive populations. The interaction of the two herbicides with the target protein harboring known PPX2 mutations was also analyzed. Our results showed that: (1) 90% of the fomesafen- or saflufenacil-resistant plants have at least one of the three known PPX2 mutations, with ΔGly-210 being the most prevalent; (2) saflufenacil is more potent than fomesafen, with five to nine times lower resistance/susceptible (R/S) ratios; (3) fomesafen selects for more diverse mutations, and computational inhibitor/target modeling of fomesafen suggest a weaker binding affinity in addition to a smaller interaction volume and volume overlap with the substrate protoporphyrinogen IX than saflufenacil. As a result, saflufenacil shows reduced sensitivity to PPX2 target-site mutations. Results from current study can help pave the way for designing weed management strategies to delay resistance development and maintain the efficacy of PPO inhibitors.

Keywords

PPX2 mutationsprotoporphyrinogen oxidase (PPO) inhibitorstarget-site resistance
Type
Research Article
Information
Weed Science , Volume 68 , Issue 2 , March 2020 , pp. 105 - 115
Copyright
© Weed Science Society of America, 2020

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: Franck E. Dayan, Colorado State University

References

Alcántara-de la Cruz, R, Fernández-Moreno, PT, Ozuna, CV, Rojano-Delgado, AM, Cruz-Hipolito, HE, Domínguez-Valenzuela, JA, Barro, F, De Prado, R (2017) Target and non-target site mechanisms developed by glyphosate-resistant hairy beggarticks (Bidens pilosa L.). Front Plant Sci 7:1492Google Scholar
Ashigh, J, Hall, JC (2010) Bases for interactions between saflufenacil and glyphosate in plants. J Agric and Food Chem 58:7335–7343CrossRefGoogle ScholarPubMed
Beale, SI, Weinstein, JD (1990) Tetrapyrrole metabolism in photosynthetic organisms. Pages 287–391in Dailey, HA, ed. Biosynthesis of Heme and Chlorophylls. New York: McGraw-HillGoogle Scholar
Bi, B, Wang, Q, Coleman, J, McElroy, J, Peppers, J, Hall, N (2019) Single nucleotide polymorphism in plastid protoporphyrinogen oxidase gene (PPO1) confers resistance to oxidiazon in Eleusine indica. Abstract 254 in Proceedings of the 59th Annual Meeting of Weed Science Society of America. New Orleans, LA: Weed Science Society of AmericaGoogle Scholar
Choi, KW, Han, O, Lee, HJ, Yun, YC, Moon, YH, Kim, MK, Kuk, YI, Han, SU, Guh, JO (1998) Generation of resistance to the diphenyl ether herbicide, oxyfluorfen, via expression of the Bacillus subtilis protoporphyrinogen oxidase gene in transgenic tobacco plants. Biosci Biotechnol Biochem 62:558–560CrossRefGoogle ScholarPubMed
Copeland, JD, Giacomini, DA, Tranel, PJ, Montgomery, GB, Steckel, LE (2018) Distribution of PPX2 mutations conferring PPO-inhibitor resistance in Palmer amaranth populations of Tennessee. Weed Technol 32:592–596CrossRefGoogle Scholar
Cornell, WD, Cieplak, P, Bayly, CI, Gould, IR, Merz, KM Jr., Ferguson, DM, Spellmeyer, DC, Fox, T, Caldwell, JW, Kollman, PA (1995) A second generation force field for the simulation of proteins and nucleic acids. J Am Chem Soc 177:5179–5197CrossRefGoogle Scholar
Costea, M, Weaver, SE, Tardif, FJ (2004) Biology of Canadian weeds 130. Amaranthus retroflexus L., A. powellii S. Watson and A. hybridus L. Can J Plant Sci 84:631–668CrossRefGoogle Scholar
Dayan, FE, Barker, A, Tranel, PJ (2017) Origins and structure of chloroplastic and mitochondrial plant protoporphyrinogen oxidases: implications for the evolution of herbicide resistance. Pest Manag Sci 74:2226–2234CrossRefGoogle ScholarPubMed
Dayan, FE, Daga, PR, Duke, SO, Lee, RM, Tranel, PJ, Doerksen, RJ (2010) Biochemical and structural consequences of a glycine deletion in the α-8 helix of protoporphyrinogen oxidase. Biochim Biophys Acta 1804:1548–1556CrossRefGoogle ScholarPubMed
Duke, SO, Lydon, J, Becerril, JM, Sherman, TD, Lehnen, LP, Matsumoto, H (1991) Protoporphyrinogen oxidase-inhibiting herbicides. Weed Sci 39:465–473CrossRefGoogle Scholar
Evans, CM, Strom, SA, Riechers, DE, Davis, AS, Tranel, PJ, Hager, AG (2019) Characterization of a waterhemp (Amaranthus tuberculatus) population from Illinois resistant to herbicides from five site-of-action groups. Weed Technol 33:400–410CrossRefGoogle Scholar
Fang, J, Zhang, Y, Liu, T, Yan, B, Li, J, Dong, L (2019) Target-site and metabolic resistance mechanisms to penoxsulam in barnyardgrass (Echinochloa crus-galli (L.) P. Beauv). J Agric Food Chem 67:8085–8095CrossRefGoogle Scholar
Franssen, AS, Skinner, DZ, Al-Khatib, K, Horak, MJ, Kulakow, PA (2001) Interspecific hybridization and gene flow of ALS resistance in Amaranthus species. Weed Sci 49:598–606CrossRefGoogle 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
Giacomini, DA, Umphres, AM, Nie, H, Mueller, TC, Steckel, LE, Young, BG, Scott, RC, Tranel, PJ (2017) Two new PPX2 mutation associated with resistance to PPO inhibiting herbicides in Amaranthus palmeri. Pest Manag Sci 73:1559–1563CrossRefGoogle ScholarPubMed
Grimm, B (1998) Novel insights in the control of tetrapyrrole metabolism of higher plants. Curr Opin Plant Biol 1:245–250CrossRefGoogle ScholarPubMed
Grossmann, K, Niggeweg, R, Christiansen, N, Looser, R, Ehrhardt, T (2010) The herbicide saflufenacil (Kixor™) is a new inhibitor of protoporphyrinogen IX oxidase activity. Weed Sci 58:1–9CrossRefGoogle Scholar
Harder, DB, Nelson, KA, Smeda, RJ (2012) Management options and factors affecting control of a common waterhemp (Amaranthus rudis) biotype resistant to protoporphyrinogen oxidase-inhibiting herbicides. Int J Agron 2012:1–7CrossRefGoogle Scholar
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org. Accessed: November 2, 2019Google Scholar
Heinemann, IU, Jahn, M, Jahn, D (2008) The biochemistry of heme biosynthesis. Arch Biochem Biophys 474:238–251CrossRefGoogle ScholarPubMed
Jacobs, JM, Jacobs, NJ (1993) Porphyrin accumulation and export by lsolated barley (Hordeum vulgare) plastids. Plant Physiol 101:1181–1187CrossRefGoogle Scholar
Koch, M, Breithaupt, C, Kiefersauer, R, Freigang, J, Huber, R, Messerschmidt, A (2004) Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J 23:1720–1728CrossRefGoogle ScholarPubMed
Labute, P (2008) The generalized Born/volume integral implicit solvent model: estimation of the free energy of hydration using London dispersion instead of atomic surface area. J Comput Chem 29:1693–1698CrossRefGoogle ScholarPubMed
Labute, P (2009) Protonate3D: assignment of ionization states and hydrogen coordinates to macromolecular structures. Proteins 75:187–205CrossRefGoogle ScholarPubMed
Larue, CT, Ream, JE, Zhou, X, Moshiri, F, Howe, A, Goley, M, Sparks, OC, Voss, ST, Hall, E, Ellis, C, et al. (2019) Microbial HemG-type protoporphyrinogen IX oxidase enzymes for biotechnology applications in plant herbicide tolerance traits. Pest Manag Sci doi:10.1002/ps.5613Google ScholarPubMed
Lee, HJ, Duke, SO (1994) Protoporphyrinogen IX-oxidizing activities involved in the mode of action of peroxidizing herbicides. J Agric Food Chem 42:2610–2618CrossRefGoogle 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
Lee, R, Hager, A, Tranel, PJ (2008) Prevalence of a novel resistance mechanism to PPO-inhibiting herbicides in waterhemp (Amaranthus tuberculatus). Weed Sci 56:371–375CrossRefGoogle Scholar
Lermontova, I, Kruse, E, Mock, HP, Grimm, B (1997) Cloning and characterization of a plastidal and a mitochondria isoform of tobacco protoporphyrinogen IX oxidase. Proc Natl Acad Sci USA 94:8895–8900CrossRefGoogle Scholar
Lillie, KJ, Giacomini, DA, Green, JD, Tranel, PJ (2019) Coevolution of resistance to PPO inhibitors in waterhemp (Amaranthus tuberculatus) and Palmer amaranth (Amaranthus palmeri). Weed Sci 67:521–526CrossRefGoogle Scholar
Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
Matzenbacher, FO, Vidal, RA, Merotto, JA, Trezzi, MM (2014) Environmental and physiological factors that affect the efficacy of herbicides that inhibit the enzyme protoporphyrinogen oxidase: a literature review. Planta Daninha 32:457–463CrossRefGoogle Scholar
Mueller, TC, Boswell, BW, Mueller, SS, Steckel, LE (2014) Dissipation of fomesafen, saflufenacil, sulfentrazone, and flumioxazin from a Tennessee soil under field conditions. Weed Sci 62:664–671CrossRefGoogle 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 70:1902–1909CrossRefGoogle Scholar
Nie, HB, Mansfield, C, Harre, NT, Young, JM, Steppig, NR, Young, BG (2019) Investigating target-site resistance mechanism to the PPO-inhibiting herbicide fomesafen in waterhemp and interspecific hybridization of Amaranthus species using next generation sequencing. Pest Manag Sci 75:3235–3244CrossRefGoogle ScholarPubMed
Obenland, OA, Ma, R, O’Brien, SR, Lygin, AV, Riechers, DE (2019) Carfentrazone-ethyl resistance in an Amaranthus tuberculatus population is not mediated by amino acid alterations in the PPO2 protein. PLoS ONE 14:e0215431CrossRefGoogle 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
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
Ritz, C, Baty, F, Streibig, JC, Gerhard, D (2016) Dose-response analysis using R. PLoS ONE 10:e0146021CrossRefGoogle Scholar
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
Salas-Perez, RA, Burgos, NR, Rangani, G, Singh, S, Refatti, JP, Pivetam, 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
Schultz, JL, Chatham, LA, Riggins, CW, Tranel, PJ, Bradley, KW (2015) Distribution of herbicide resistances and molecular mechanisms conferring resistance in Missouri waterhemp (Amaranthus rudis Sauer) populations. Weed Sci 63:336–345CrossRefGoogle Scholar
Selby, TP, Ruggiero, M, Hong, W, Travis, DA, Satterfield, AD, Ding, AX (2015) Broad-spectrum PPO-inhibiting N-phenoxyphenyluracil acetal ester herbicides. ACS Symp Ser 1204:277–289CrossRefGoogle Scholar
Shauck, TC (2014) Identification of Nontarget-Site Mechanisms of Glyphosate Resistance in Roots and Pollen of Amaranthus and Ambrosia. Ph.D dissertation. Columbia: University of Missouri. 92 pGoogle Scholar
Shergill, LS, Barlow, BR, Bish, MD, Bradley, KW (2018) Investigations of 2,4-D and multiple herbicide resistance in a Missouri waterhemp (Amaranthus tuberculatus) population. Weed Sci 66:386–394CrossRefGoogle Scholar
Thinglum, KA, Riggins, CW, Davis, AS, Bradley, KW, Al-Khatib, K, Tranel, PJ (2011) Wide distribution of the waterhemp (Amaranthus tuberculatus) ΔG210 PPX2 mutation, which confers resistance to PPO-inhibiting herbicides. Weed Sci 59:22–27CrossRefGoogle Scholar
Trucco, F, Jeschke, MR, Rayburn, AL, Tranel, PJ (2005) Amaranthus hybridus can be pollinated frequently by A. tuberculatus under field conditions. Heredity 94:64–70CrossRefGoogle ScholarPubMed
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
Varanasi, VK, Brabham, C, Korres, NE, Norsworthy, JK (2019) Nontarget site resistance in Palmer amaranth [Amaranthus palmeri (S.) Wats.] confers cross-resistance to protoporphyrinogen oxidase-inhibiting herbicides. Weed Technol 33:349–354CrossRefGoogle Scholar
von Wettstein, D, Gough, S, Kannangara, CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1057CrossRefGoogle ScholarPubMed
Watanabe, N, Che, FS, Iwano, M, Takayama, S, Yoshida, S, Isogai, A (2001) Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem 276:20474–20481CrossRefGoogle ScholarPubMed
Watanabe, N, Takayama, S, Yoshida, S, Isogai, A, Che, FS (2002) Resistance to protoporphyrinogen oxidase-inhibiting compound S23142 from overproduction of mitochondrial protoporphyrinogen oxidase by gene amplification in photomixotrophic tobacco cells. Biosci Biotechnol Biochem 66:1799–1805CrossRefGoogle ScholarPubMed
Wuerffel, RJ, Young, JM, Lee, RM, Tranel, PJ, Lightfoot, DA, Young, BG (2015a) Distribution of the ΔG210 protoporphyrinogen oxidase mutation in Illinois waterhemp (Amaranthus tuberculatus) and an improved molecular method for detection. Weed Sci 63:839–845CrossRefGoogle Scholar
Wuerffel, RJ, Young, JM, Matthews, JL, Young, BG (2015b) Characterization of PPO-inhibitor–resistant waterhemp (Amaranthus tuberculatus) response to soil-applied PPO-inhibiting herbicides. Weed Sci 63:511–521CrossRefGoogle Scholar