Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T10:51:05.221Z Has data issue: false hasContentIssue false
  • English
  • Français

Arg-128-Leu target-site mutation in PPO2 evolves in wild poinsettia (Euphorbia heterophylla) with cross-resistance to PPO-inhibiting herbicides

Published online by Cambridge University Press:  02 June 2020

Rafael R. Mendes Open the ORCID record for Rafael R. Mendes [Opens in a new window] ,
Hudson K. Takano Open the ORCID record for Hudson K. Takano [Opens in a new window] ,
Fernando S. Adegas Open the ORCID record for Fernando S. Adegas [Opens in a new window] ,
Rubem S. Oliveira Jr Open the ORCID record for Rubem S. Oliveira Jr [Opens in a new window] ,
Todd A. Gaines Open the ORCID record for Todd A. Gaines [Opens in a new window]  and
Franck E. Dayan Open the ORCID record for Franck E. Dayan [Opens in a new window]
Rafael R. Mendes
Affiliation:
Graduate Student, Agronomy Department, State University of Maringá, Maringá, PR, Brazil
Hudson K. Takano
Affiliation:
Postdoctoral Fellow, Agricultural Biology, Colorado State University, Fort Collins, CO, USA
Fernando S. Adegas
Affiliation:
Weed Scientist, Embrapa Soybean, Londrina, PR, Brazil
Rubem S. Oliveira Jr
Affiliation:
Professor, Agronomy Department, State University of Maringá, Maringá, PR, Brazil
Todd A. Gaines
Affiliation:
Associate Professor, Agricultural Biology, Colorado State University, Fort Collins, CO, USA
Franck E. Dayan*
Affiliation:
Professor, Agricultural Biology, Colorado State University, Fort Collins, CO, USA
*
Author for correspondence: Franck E. Dayan, Colorado State University, Agricultural Biology, 1177 Campus Delivery, Fort Collins, CO80523. Email: franck.dayan@colostate.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Wild poinsettia (Euphorbia heterophylla L.) is a troublesome broadleaf weed in grain production areas in South America. Herbicide resistance to multiple sites of action has been documented in this species, including protoporphyrinogen oxidase (PPO) inhibitors. We investigated the physiological and molecular bases for PPO-inhibitor resistance in a E. heterophylla population (RPPO) from Southern Brazil. Whole-plant dose–response experiments revealed a cross-resistance profile to three different chemical groups of PPO inhibitors. Based on dose–response parameters, RPPO was resistant to lactofen (47.7-fold), saflufenacil (8.6-fold), and pyraflufen-ethyl (3.5-fold). Twenty-four hours after lactofen treatment (120 g ha−1) POST, RPPO accumulated 27 times less protoporphyrin than the susceptible population (SPPO). In addition, RPPO generated 5 and 4.5 times less hydrogen peroxide and superoxide than SPPO, respectively. The chloroplast PPO (PPO1) sequences were identical between the two populations, whereas 35 single-nucleotide polymorphisms were found for the mitochondrial PPO (PPO2). Based on protein homology modeling, the Arg-128-Leu (homologous to Arg-98-Leu in common ragweed [Ambrosia artemisiifolia L.] was the only one located near the catalytic site, also in a conserved region of PPO2. The cytochrome P450 monooxygenase inhibitor malathion did not reverse resistance to lactofen in RPPO, and both populations showed similar levels of PPO1 and PPO2 expression, suggesting that metabolic resistance and PPO overexpression are unlikely. This is the first report of an Arg-128-Leu mutation in PPO2 conferring cross-resistance to PPO inhibitors in E. heterophylla.

Keywords

Cytochrome P450 monooxygenaseflumioxazinlactofenPPO1protoporphyrinpyraflufen-ethylreactive oxygen speciessaflufenacil
Type
Research Article
Information
Weed Science , Volume 68 , Issue 5 , September 2020 , pp. 437 - 444
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: Te-Ming Paul Tseng, Mississippi State University

References

Becerril, JM, Duke, SO (1989) Protoporphyrin IX content correlates with activity of photobleaching herbicides. Plant Physiol 90:1175–1181CrossRefGoogle ScholarPubMed
Bi, B, Wang, Q, Coleman, JJ, Porri, A, Peppers, JM, Patel, JD, Betz, M, Lerchl, J, McElroy, JS (2020) A novel mutation A212T in chloroplast protoporphyrinogen oxidase (PPO1) confers resistance to PPO inhibitor oxadiazon in Eleusine indica. Pest Manag Sci 76:1786–1794CrossRefGoogle ScholarPubMed
Brunharo, CACG, Takano, HK, Mallory-Smith, CA, Dayan, FE, Hanson, BD (2019) Role of glutamine synthetase isogenes and herbicide metabolism in the mechanism of resistance to glufosinate in Lolium perenne L. spp. multiflorum biotypes from Oregon. J Agric Food Chem 67:8431–8440CrossRefGoogle ScholarPubMed
Brusamarello, AP, Oliveira, PH, Trezzi, MM, Xavier, E, Dalosto, ED (2016) Inheritance of resistance to protoporphyrinogen oxidase inhibitor herbicides in wild poinsettia. Planta Daninha 34:575–580CrossRefGoogle Scholar
Busi, R, Gaines, TA, Powles, S (2017) Phorate can reverse P450 metabolism-based herbicide resistance in Lolium rigidum. Pest Manag Sci 73:410–417CrossRefGoogle ScholarPubMed
Chen, J, Huang, Z, Huang, H, Wei, S, Liu, Y, Jiang, C, Zhang, J, Zhang, C (2017) Selection of relatively exact reference genes for gene expression studies in goosegrass (Eleusine indica) under herbicide stress. Sci Rep 7:46494CrossRefGoogle ScholarPubMed
Dayan, FE, Armstrong, BM, Weete, JD (1998) Inhibitory activity of sulfentrazone and its metabolic derivatives on soybean (Glycine max) protoporphyrinogen oxidase. J Agric Food Chem 46:2024–2029CrossRefGoogle Scholar
Dayan, FE, Barker, A, Takano, H, Bough, R, Ortiz, M, Duke, SO (2020) Herbicide mechanisms of action and resistance. Pages 36–48in Grodzinski, B, ed. Comprehensive Biotechnology. Amsterdam: ElsevierGoogle Scholar
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
Dayan, FE, Duke, SO, Weete, JD, Hancock, HG (1997a) Selectivity and mode of action of carfentrazone-ethyl, a novel phenyl triazolinone herbicide. Pestic Sci 51:65–733.0.CO;2-9>CrossRefGoogle Scholar
Dayan, FE, Owens, DK, Corniani, N, Silva, FML, Watson, SB, Howell, JL, Shaner, DL (2015) Biochemical markers and enzyme assays for herbicide mode of action and resistance studies. Weed Sci 63:23–63CrossRefGoogle Scholar
Dayan, FE, Owens, DK, Tranel, PJ, Preston, C, Duke, SO (2014) Evolution of resistance to phytoene desaturase and protoporphyrinogen oxidase inhibitors—state of knowledge. Pest Manag Sci 70:1358–1366CrossRefGoogle ScholarPubMed
Dayan, FE, Weete, JD, Duke, SO, Hancock, HG (1997b) Soybean (Glycine max) cultivar differences in response to sulfentrazone. Weed Sci 45:634–641Google Scholar
Dayan, FE, Weete, JD, Hancock, HG (1996) Physiological basis for differential sensitivity to sulfentrazone by sicklepod (Senna obtusifolia) and coffee senna (Cassia occidentalis). Weed Sci 44:12–17CrossRefGoogle Scholar
de Oliveira, RSJ, Constantin, J, Toledo, R, Kajihara, LH, Stasieviski, Â, Pagliari, PH, de Arantes, JGZ, Cavalieri, SD, Alonso, DG, Roso, AC (2006) Aplicações seqüenciais de flumiclorac-pentil para o controle de Euphorbia heterophylla na cultura da soja. Act Scientiar Agron 28:1–8Google Scholar
Duke, SO (2018) The history and current status of glyphosate. Pest Manag Sci 74:1027–1034CrossRefGoogle ScholarPubMed
Duke, SO, Dayan, FE (2018) Herbicides. Page 9in Encyclopedia of Life Sciences—eLS. Chichester, UK: WileyGoogle Scholar
Frigo, MJ, Mangolin, CA, Oliveira, RS, Maria de Fátima, P (2009) Esterase polymorphism for analysis of genetic diversity and structure of wild poinsettia (Euphorbia heterophylla) populations. Weed Sci 57:54–60CrossRefGoogle 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, Jet al. (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci USA 107:1029–1034CrossRefGoogle ScholarPubMed
Gelmini, GA, Victória Filho, R, Soares, MdCdS, Adoryan, ML (2001) Resistência de biótipos de Euphorbia heterophylla L. aos herbicidas inibidores da enzima ALS utilizados na cultura de soja. Bragantia 60:93–99CrossRefGoogle 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. Pest Manag Sci 73:1559–1563CrossRefGoogle ScholarPubMed
Ha, SB, Lee, SB, Lee, Y, Yang, K, Lee, N, Jang, SM, Chung, JS, Jung, S, Kim, YS, Wi, SG, Back, K (2003) The plastidic Arabidopsis protoporphyrinogen IX oxidase gene, with or without the transit sequence, confers resistance to the diphenyl ether herbicide in rice. Plant Cell Environ 27:79–88CrossRefGoogle Scholar
Heap, IM (2020) International Herbicide-Resistant Weed Database. http://www.weedscience.org. Accessed: March 17, 2020Google Scholar
Heinemann, IU, Diekmann, N, Masoumi, A, Koch, M, Messerschmidt, A, Jahn, M, Jahn, D (2007) Functional definition of the tobacco protoporphyrinogen IX oxidase substrate-binding site. Biochem J 402:575–580CrossRefGoogle ScholarPubMed
Jung, S, Lee, Y, Yang, K, Lee, SB, Jang, SM, Ha, SB, Back, K (2004) Dual targeting of Myxococcus xanthus protoporphyrinogen oxidase into chloroplasts and mitochondria and high level oxyfluorfen resistance. Plant Cell Environ 27:1436–1446CrossRefGoogle Scholar
Keith, BK, Lehnhoff, EA, Burns, EE, Menalled, FD, Dyer, WB (2015) Characterisation of Avena fatua populations with resistance to multiple herbicides. Weed Res 55:621–630CrossRefGoogle 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
Lee, HJ, Duke, MV, Duke, SO (1993) Cellular localization of protoporphyrinogen-oxidizing activities of etiolated barley (Hordeum vulgare L.) leaves. Plant Physiol 102:881–889CrossRefGoogle ScholarPubMed
Lermontova, I, Grimm, B (2000) Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to the diphenyl-ether herbicide acifluorfen. Plant Physiol 122:75–84CrossRefGoogle ScholarPubMed
Machado, AB, Trezzi, MM, Vidal, RA, Patel, F, Cieslik, LF, Debastiani, F (2015) Rendimento de grãos de feijão e nível de dano econômico sob dois períodos de competição com Euphorbia heterophylla. Planta Daninha 33:41–48CrossRefGoogle Scholar
Matringe, M, Camadro, J-M, Labbe, P, Scalla, R (1989) Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem J 260:231–235CrossRefGoogle ScholarPubMed
Meschede, DK, Oliveira, RS Jr, Constantin, J, Scapim, CA (2002) Período crítico de interferência de Euphorbia heterophylla na cultura da soja sob baixa densidade de semeadura. Planta Daninha 20:381–387CrossRefGoogle Scholar
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
Prigol, A, Galon, L, Forte, CT, Kujawiski, R, Concenço, G, Trezzi, MM, Trevisol, R, Radünz, AL, Perin, GF (2014) Avaliação de biótipos de leiteiro com suspeita de resistência a herbicidas inibidores da ALS e Protox. Rev Bras Herbic 13:216–224Google 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 10:568CrossRefGoogle ScholarPubMed
Ritz, C, Baty, F, Streibig, JC, Gerhard, D (2015) Dose-response analysis using R. PLoS ONE 10:e0146021CrossRefGoogle ScholarPubMed
Rojano-Delgado, AM, Pauma-Bautista, C, Varquez-Garcia, J, Mora, DA, Rosario, JM, Portugal, J, De Prado, R (2019) Influence of Cyp450 in the resistance to PPO-inhibiting herbicides: case of a Euphorbia heterophylla biotype. Proc Weed Sci Soc Am 59:126. New Orleans LA, USAGoogle 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
Sarangi, D, Stephens, T, Barker, AL, Patterson, EL, Gaines, TA, Jhala, AJ (2019) Protoporphyrinogen oxidase (PPO) inhibitor–resistant waterhemp (Amaranthus tuberculatus) from Nebraska is multiple herbicide resistant: confirmation, mechanism of resistance, and management. Weed Sci 67:510–520CrossRefGoogle Scholar
Strang, RH, Rogers, RL (1974) Behavior and fate of two phenylpyridazinone herbicides in cotton, corn, and soybean. J Agric Food Chem 22:1119–1125CrossRefGoogle ScholarPubMed
Streibig, JC (1988) Herbicide bioassay. Weed Res 28:479–484CrossRefGoogle Scholar
Takano, HK, Beffa, R, Preston, C, Westra, P, Dayan, FE (2019) Reactive oxygen species trigger the fast action of glufosinate. Planta 249:1837–1849CrossRefGoogle ScholarPubMed
Takano, HK, Fernandes, VNA, Adegas, FS, Oliveira, RS Jr, Westra, P, Gaines, TA, Dayan, FE (2020) A novel TIPT double mutation in EPSPS conferring glyphosate resistance in tetraploid Bidens subalternans. Pest Management Science 76:95–102CrossRefGoogle ScholarPubMed
Trezzi, MM, Felippi, CL, Mattei, D, Silva, HL, Nunes, AL, Debastiani, C, Vidal, RA, Marques, A (2005) Multiple resistance of acetolactate synthase and protoporphyrinogen oxidase inhibitors in Euphorbia heterophylla biotypes. J Environ Sci Health Part B 40:101–109CrossRefGoogle ScholarPubMed
Trezzi, MM, Nunes, AL, da Silva Portes, E (2009) Interação entre inseticida organofosforado e herbicidas inibidores da PROTOX e sua implicação na resistência de Euphorbia heterophylla. Scientia Agraria 10:423–428CrossRefGoogle Scholar
Trezzi, MM, Vidal, RA, Kruse, ND, Nunes, AL (2006) Greenhouse and laboratory bioassays for identification of Euphorbia heterophylla biotypes with multiple resistance to Protox and ALS-inhibiting herbicides. Planta Daninha 24:563–571CrossRefGoogle Scholar
Varanasi, VK, Brabham, C, Norsworthy, JK (2018) 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 (2017) 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
Warabi, E, Usui, K, Tanaka, Y, Matsumoto, H (2001) Resistance of a soybean cell line to oxyfluorfen by overproduction of mitochondrial protoporphyrinogen oxidase. Pest Manag Sci 57:743–748CrossRefGoogle ScholarPubMed
Watanabe, H, Ohori, Y, Sandmann, G, Wakabayashi, K, Böger, P (1992) Quantitative correlation between short-term accumulation of protoporphyrin IX and peroxidative activity of cyclic imides. Pestic Biochem Physiol 42:99–109CrossRefGoogle Scholar
Watanabe, N, Che, F-S, Iwano, M, Takayama, S, Yoshida, S (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
Wiersma, A, Gaines, T, Preston, C, Hamilton, J, Giacomini, D, Robin Buell, C, Leach, J, Westra, P (2015) Gene amplification of 5-enol-pyruvylshikimate-3-phosphate synthase in glyphosate-resistant Kochia scoparia. Planta 241:463–474CrossRefGoogle ScholarPubMed
Xavier, E, Trezzi, MM, Oliveira, MC, Vidal, RA, Brusamarello, AP (2018) Activity of antioxidant enzymes in Euphorbia heterophylla biotypes and their relation to cross resistance to ALS and Protox inhibitors. Planta Daninha 36:e018176629CrossRefGoogle Scholar