Hostname: page-component-669899f699-swprf Total loading time: 0 Render date: 2025-04-27T03:53:14.607Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular confirmation of resistance to PPO inhibitors in Amaranthus tuberculatus and Amaranthus palmeri, and isolation of the G399A PPO2 substitution in A. palmeri

Published online by Cambridge University Press:  18 August 2020

Jacob S. Montgomery ,
Darci A. Giacomini  and
Patrick J. Tranel Open the ORCID record for Patrick J. Tranel [Opens in a new window]
Jacob S. Montgomery
Affiliation:
Graduate Student, University of Illinois, Urbana, IL, USA
Darci A. Giacomini
Affiliation:
Research Assistant Professor, University of Illinois, Urbana, IL, USA
Patrick J. Tranel*
Affiliation:
Professor, University of Illinois, Urbana, IL, USA
*
Author for correspondence: Patrick J. Tranel, 1201 W Gregory Drive, University of Illinois, Urbana, IL61801. Email: tranel@illinois.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

During the 2017 to 2019 growing seasons, samples of waterhemp and Palmer amaranth that had reportedly survived field-rate applications of protoporphyrinogen oxidase (PPO)–inhibiting herbicides were collected from the American Midwest and tested for target-site mutations known at the time to confer resistance. Target-site resistance was identified in nearly all (135 of 145) tested common waterhemp populations but in only 8 of 13 Palmer amaranth populations. Follow-up research on one population of Palmer amaranth (W-8), which tested negative for all such mutations, confirmed it was resistant to lactofen, with a magnitude of resistance comparable to that conferred by the ΔG210 PPO2 mutation. Gene sequences from both isoforms of PPO (PPO1 and PPO2) were compared between W-8 and known PPO inhibitor–sensitive sequence. A glycine-to-alanine substitution at the 399th amino acid position (G399A) of PPO2, recently identified to reduce target-site herbicide sensitivity, was observed in a subset of resistant W-8 plants. Because no missense mutation completely delimited resistant and sensitive sequences, we initially suspected the presence of a secondary, non-target-site resistance mechanism in this population. To isolate G399A, a segregating F2 population was produced and screened with a delimiting rate of lactofen. χ2 goodness-of-fit analysis of dead/alive ratings indicated single-locus inheritance of resistance in the F2 population, and molecular markers for the W-8 parental PPO2 coding region co-segregated tightly, but not perfectly, with resistance. More research is needed to fully characterize Palmer amaranth PPO inhibitor–resistance mechanisms, which appear to be more diverse than those found in common waterhemp.

Keywords

Target-site resistancePPO1PPO-inhibiting herbicidesallele-specific markersLactofencommon waterhempAmaranthus tuberculatus (Moq.) J.D. SauerPalmer amaranthAmaranthus palmeri S. Watson
Type
Research Article
Information
Weed Technology , Volume 35 , Issue 1 , February 2021 , pp. 99 - 105
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of Weed Science Society of America

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.)

Article purchase

Temporarily unavailable

Footnotes

Associate Editor: R. Joseph Wuerffel, Syngenta

References

Becerril, JM, Duke, SO (1989) Protoporphyrin IX content correlates with activity of photobleaching herbicides. Plant Physiol 90:1175–1181 CrossRefGoogle ScholarPubMed
Bi, B, Wang, Q, Coleman, JJ, Porri, A, Peppers, JM, Patel, JD, Betz, M, Lerchl, J, McElroy, JS (2019) A novel mutation A212T in chloroplast protoporphyrinogen oxidase (PPO1) confers resistance to PPO inhibitor Oxadiazon in Eleusine indica. Pest Manag Sci 76:1786–1794 CrossRefGoogle Scholar
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 32:592–596 CrossRefGoogle 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 74:2226–2234 CrossRefGoogle ScholarPubMed
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 73:1559–1563 CrossRefGoogle ScholarPubMed
Guo, J, Riggins, CW, Hausman, NE, Hager, AG, Riechers, DE, Davis, AS, Tranel, PJ (2015) Nontarget-site resistance to ALS inhibitors in waterhemp (Amaranthus tuberculatus). Weed Sci 63:399–407 Google Scholar
Hao, GF, Zuo, Y, Yang, SH, Yang, GF (2011) Protoporphyrinogen oxidase inhibitor: an ideal target for herbicide discovery. Chimia 65:961–969 CrossRefGoogle ScholarPubMed
Heap, I (2020) International Herbicide-Resistant Weed Database. http://www.weedscience.com. Accessed: August 14, 2020Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Meintjes, P, Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649 10.1093/bioinformatics/bts199CrossRefGoogle ScholarPubMed
Korte, A, Farlow, A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29 10.1186/1746-4811-9-29CrossRefGoogle ScholarPubMed
Legleiter, TR, Bradley, KW, Massey, RE (2009) Glyphosate-resistant waterhemp (Amaranthus rudis) control and economic returns with herbicide programs in soybean. Weed Technol 23:54–61 CrossRefGoogle Scholar
Lillie, K, Giacomini, D, Green, J, Tranel, P (2019) Coevolution of resistance to PPO inhibitors in waterhemp (Amaranthus tuberculatus) and Palmer amaranth (Amaranthus palmeri). Weed Sci 67:521–526 10.1017/wsc.2019.41CrossRefGoogle Scholar
Lillie, K, Giacomini, D, Tranel, P (2020) Comparing responses of sensitive and resistant populations of Palmer amaranth (Amaranthus palmeri) and waterhemp (Amaranthus tuberculatus var. rudis) to PPO inhibitors. Weed Technol 34:140–146 CrossRefGoogle Scholar
Matringe, M, Camadro, J-M, Labbe, P, Scalla, R (1989a) Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem J 260:231–235 10.1042/bj2600231CrossRefGoogle ScholarPubMed
Matringe, M, Camadro, J-M, Labbe, P, Scalla, R (1989b) Protoporphyrinogen oxidase inhibition by three peroxidizing herbicides: oxadiazon, LS 82-556 and M&B 39279. FEBS Lett 245:35–38 CrossRefGoogle Scholar
Nicot, N, Hausman, JF, Hoffmann, L, Evers, D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914 CrossRefGoogle ScholarPubMed
Patzoldt, WL, Hager, AG, McCormick, JS, Tranel, PJ (2006) A codon deletion confers resistance to herbicides inhibiting protoporphyrinogen oxidase. Proc Natl Acad Sci USA 103:12329–12334 CrossRefGoogle ScholarPubMed
R Core Team (2018) R: a language and environment for statistical computing. https://www.R-project.org/. Vienna, Austria: R Foundation for Statistical ComputingGoogle 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 10:568 CrossRefGoogle ScholarPubMed
Rio, DC, Ares, M, Hannon, GJ, Nilsen, TW (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc, doi: 10.1101/pdb.prot5439 CrossRefGoogle Scholar
Ritz, C, Baty, F, Streibig, C, Gerhard, D (2015) Dose-response analysis using R. PLoS ONE 10:e0146021 CrossRefGoogle 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 72:864–869 10.1002/ps.4241CrossRefGoogle ScholarPubMed
Taylor, S, Scott, R, Kurtz, R, Fisher, C, Patel, V, Bizouarn, F (2010) A practical guide to high resolution melt analysis genotyping. Bio-Rad Bulletin Tech Note 6004. http://www.bio-rad.com/webroot/web/pdf/lsr/literature/Bulletin_6004.pdf. Accessed: August 24, 2020Google Scholar
[USDA-NASS] US Department of Agriculture, National Agricultural Statistics Service (2017) Agricultural Chemical Use Program. https://www.nass.usda.gov/Surveys/Guide_to_NASS_Surveys/Chemical_Use/. Accessed: May 15, 2020Google Scholar
Varanasi, VK, Brabham, C, Norsworthy, JK (2018) Confirmation and characterization of nontarget site resistance to fomesafen in Palmer amaranth (Amaranthus palmeri). Weed Sci 66:702–709 10.1017/wsc.2018.60CrossRefGoogle Scholar
Wu, C, Goldsmith, M-R, Pawlak, J, Feng, P, Smith, S, Navarro, S, Perez-Jones, A (2020) Differences in efficacy, resistance mechanism and target protein interaction between two PPO inhibitors in Palmer amaranth (Amaranthus palmeri). Weed Sci 68:105–115 CrossRefGoogle Scholar
Wuerffel, RJ, Young, JM, Lee, RM, Tranel, PJ, Lightfoot, DA, Young, BG (2015) Distribution of the ΔG210 protoporphyrinogen oxidase mutation in Illinois waterhemp (Amaranthus tuberculatus) and an improved molecular method for detection. Weed Sci 63:839–845 CrossRefGoogle Scholar
Xin, Z, Chen, J (2012) A high throughput DNA extraction method with high yield and quality. Plant Methods 8:26 CrossRefGoogle ScholarPubMed
Supplementary material: File

Montgomery et al. supplementary material

Montgomery et al. supplementary material 1

Download Montgomery et al. supplementary material(File)
File 48.3 KB
Supplementary material: File

Montgomery et al. supplementary material

Montgomery et al. supplementary material 2

Download Montgomery et al. supplementary material(File)
File 51.5 KB