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Limited induction of ethylene and cyanide synthesis are observed in quinclorac-resistant barnyardgrass (Echinochloa crus-galli) in Uruguay

Published online by Cambridge University Press:  28 April 2020

Manuel Diez Vignola ,
Martha Sainz ,
Néstor E. Saldain ,
Claudia Marchesi ,
Victoria Bonnecarrère  and
Pedro Díaz Gadea Open the ORCID record for Pedro Díaz Gadea [Opens in a new window]
Manuel Diez Vignola
Affiliation:
Graduate Student, Laboratorio de Bioquímica, Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay
Martha Sainz
Affiliation:
Research Assistant, Laboratorio de Bioquímica, Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay
Néstor E. Saldain
Affiliation:
Principal Researcher, Programa Producción Arroz, Estación Experimental INIA Treinta y Tres, Instituto Nacional de Investigación Agropecuaria (INIA, National Institute of Agricultural Research), Uruguay
Claudia Marchesi
Affiliation:
Associate Researcher, Programa Producción de Arroz, Estación Experimental INIA Tacuarembó, Instituto Nacional de Investigación Agropecuaria (INIA, National Institute of Agricultural Research), Uruguay
Victoria Bonnecarrère
Affiliation:
Principal Researcher, Biotechnology Unit, Wilson Ferreira Aldunate Experimental Station, Instituto Nacional de Investigación Agropecuaria (INIA, National Institute of Agricultural Research), Uruguay
Pedro Díaz Gadea*
Affiliation:
Associate Professor, Laboratorio de Bioquímica, Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay
*
Author for correspondence: Pedro Díaz Gadea, Associate Professor, Facultad de Agronomía, Universidad de la República, Avenida Garzón 809, Montevideo, Uruguay12900. E-mail: [email protected]
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Abstract

Barnyardgrass [Echinochloa crus-galli (L.) P. Beauv] is the foremost weed in rice (Oryza sativa L.) systems, and its control is crucial to successful rice production. Quinclorac, a synthetic auxin herbicide, has been used effectively to manage E. crus-galli. However, occurrences of quinclorac-resistant genotypes are frequently reported, and its resistance evolution has led to questions about the continued utility of quinclorac for grass control. Identification of the resistance mechanism(s) of resistant genotypes will facilitate development of integrated weed management strategies that sustain quinclorac use for management of E. crus-galli. We evaluated the responses to quinclorac of two contrasting genotypes: E7 (resistant, R) and LM04 (susceptible, S). Quinclorac induced ethylene and cyanide biosynthesis in the S-genotype. Both genotypes responded similarly to an increasing application of exogenous 1-carboxylic acid aminocyclopropane (ACC) and potassium cyanide, and their growth was inhibited at higher doses. The key mechanism for cyanide (HCN) detoxification in plants, β-cyanoalanine synthase (β-CAS) activity, was evaluated in both genotypes, and no significant difference was observed in the basal activity. However, quinclorac significantly induced β-CAS–like activity in the S-genotype, which is consistent with the increased synthesis of ethylene and cyanide. This work suggests that the resistance to quinclorac of the E7 R-genotype is likely related to an alteration in the auxin signal transduction pathway, causing a lower stimulation of ACC synthase and, therefore, limited synthesis of ethylene and HCN after quinclorac treatment.

Keywords

β-cyanoalanine synthaseauxin herbicideresistancerice
Type
Research Article
Information
Weed Science , Volume 68 , Issue 4 , July 2020 , pp. 348 - 357
Copyright
© Weed Science Society of America, 2020

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Footnotes

Associate Editor: Ian Burke, Washington State University

References

Abdallah, I, Fischer, AJ, Elmore, CL, Saltveit, ME, Zaki, M (2006) Mechanism of resistance to quinclorac in smooth crabgrass (Digitaria ischaemum). Pestic Biochem Phys 84:38–48CrossRefGoogle Scholar
Beers, RF, Sizer, IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140Google ScholarPubMed
Blumenthal, SG, Hendrickson, HR, Conn, EE (1968) Cyanide metabolism in higher plants: III. The biosynthesis of β cyanoalanine. J Biol Chem 25:5302–5307Google Scholar
Bradford, KJ, Yang, SF (1980a) Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiol 65:322–326CrossRefGoogle ScholarPubMed
Bradford, KJ, Yang, SF (1980b) Stress-induced ethylene production in the ethylene-requiring tomato mutant Diageotopica. Plant Physiol 65:327–330CrossRefGoogle Scholar
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle ScholarPubMed
Chayapakdee, P, Sunohara, Y, Endo, M, Yamaguchi, T, Fan, L, Uchino, A, Matsumoto, H, Iwakami, S (2019) Quinclorac resistance in Echinochloa phyllopogon is associated with reduced ethylene synthesis rather than enhanced cyanide detoxification by β-cyanoalanine synthase. Pest Manag Sci 76:1195–1204CrossRefGoogle ScholarPubMed
Chen, GX, Asada, K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30:897–998Google Scholar
Concenço, G, Silva, A, Ferreira, E (2009) Effect of dose and application site on quinclorac absorption by barnyard grass genotypes. Planta Daninha 27:541–548CrossRefGoogle Scholar
Dhindsa, RS, Matowe, W (1981) Drought tolerance in two mosses: correlated with defence against lipid peroxidation. J Exp Bot 32:79–91CrossRefGoogle Scholar
Di Rienzo, JA, Casanoves, F, Balzarini, MG, Gonzalez, L, Tablada, M, Robledo, CW (2011) Grupo InfoStat, FCA. Córdoba, Argentina: Universidad Nacional de Córdoba. http://www.infostat.com.ar. Accessed: July 15, 2019Google Scholar
English, PJ, Lycett, GW, Roberts, JA, Jackson, MB (1995) Increased 1-aminocyclopropane-1-carboxylic acid oxidase activity in shoots of flooded tomato plants raises ethylene production to physiologically active levels. Plant Physiol 109:1435–1440CrossRefGoogle ScholarPubMed
Gleason, C, Foley, RC, Singh, KB (2011) Mutant analysis in Arabidopsis provides insight into the molecular mode of action of the auxinic herbicide dicamba. PLoS ONE 6:e17245CrossRefGoogle ScholarPubMed
Goudey, JS, Tittle, FL, Spencer, MS (1989) A role for ethylene in the metabolism of cyanide by higher plants. Plant Physiol 89:1306–1310CrossRefGoogle Scholar
Grossmann, K (1996) A role for cyanide, derived from ethylene biosynthesis, in the development of stress symptoms. Physiol Plant 97:772–775CrossRefGoogle Scholar
Grossmann, K (1998) Quinclorac belongs to a new class of highly selective auxin herbicides. Weed Sci 46:707–716CrossRefGoogle Scholar
Grossmann, K (2000) Mode of action of auxin herbicides: a new ending to a long, drawn out story. Trends Plant Sci 5:506–508CrossRefGoogle ScholarPubMed
Grossmann, K (2010) Auxin herbicides: current status of mechanism and mode of action. Pest Manag Sci 66:113–120CrossRefGoogle ScholarPubMed
Grossmann, K, Kwiatkowski, J (1993) Selective induction of ethylene and cyanide biosynthesis appears to be involved in the selectivity of the herbicide quinclorac between rice and barnyardgrass. J Plant Physiol 142:457–466CrossRefGoogle Scholar
Grossmann, K, Kwiatkowski, J (1995) Evidence for a causative role of cyanide, derived from ethylene biosynthesis, in the herbicidal mode of action of quinclorac in barnyard grass. Pestic Biochem Phys 51:150–160CrossRefGoogle Scholar
Grossmann, K, Kwiatkowski, J (2000) The mechanism of quinclorac selectivity in grasses. Pestic Biochem Phys 66:83–91CrossRefGoogle Scholar
Grossmann, K, Kwiatkowski, J, Tresch, S (2001) Auxin herbicides induce H2O2 over production and tissue damage in cleavers (Galium aparine L.). J Exp Bot 52:1811–1816CrossRefGoogle Scholar
Grossmann, K, Scheltrup, F (1997) Selective induction of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase activity is involved in the selectivity of the auxin herbicide quinclorac between barnyard grass and rice. Pestic Biochem Phys 58:145–153CrossRefGoogle Scholar
Gupta, N, Balomajumder, C, Agarwal, VK (2010) Enzymatic mechanism and biochemistry for cyanide degradation: a review. J Hazard Mater 176:1–13CrossRefGoogle ScholarPubMed
Hansen, H, Grossmann, K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448CrossRefGoogle ScholarPubMed
Heap, I (2019) The International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed: October 25, 2019Google Scholar
Hoagland, DR, Arnon, DI (1950) The Water-Culture Method for Growing Plants without Soil. Berkeley: California Agricultural Experiment Station Circular-347. 39 pGoogle Scholar
Knezevic, SZ, Streibig, JC, Ritz, C (2007) Utilizing R software package for dose-response studies: the concept and data analysis. Weed Technol 21:840–848CrossRefGoogle Scholar
Lambert, JL, Ramasamy, J, Paukstelis, JV (1975) Stable reagents for the colorimetric determination of cyanide by modified König reactions. Anal Chem 47:916–918CrossRefGoogle Scholar
Lee, S, Sundaram, S, Armitage, L, Evans, JP, Hawkes, T, Kepinski, S, Ferro, N, Napier, RM (2014) Defining binding efficiency and specificity of auxins for SCFTIR1/AFBAux/IAA co-receptor complex formation. ACS Chem Biol 9:673–682CrossRefGoogle Scholar
Leeson, JY, Thomas, AG, Hall, LM, Brenzil, CA, Andrews, T, Brown, KR, Van Acker, RC (2005) Prairie Weed Surveys of Cereal, Oilseed and Pulse Crops from the 1970s to the 2000s. Weed Survey Series Publication 05-1. Saskatoon Research Centre, SK, Saskatchewan, Canada: Agriculture and Agri-Food Canada. 395 pGoogle Scholar
Liang, WS, Li, DB (2001) The two β-cyanoalanine synthase isozymes of tobacco showed different antioxidative abilities. Plant Sci 161:1171–1177CrossRefGoogle Scholar
López-Martínez, N, Marshall, G, De Prado, R (1997) Resistance of barnyardgrass (Echinochloa crus-galli) to atrazine and quinclorac. Pestic Sci 51:171–1753.0.CO;2-7>CrossRefGoogle Scholar
Lovelace, ML, Talbert, RE, Hoagland, RE, Scherder, EF (2007) Quinclorac absorption and translocation characteristics in quinclorac and propanil-resistant and susceptible barnyardgrass (Echinochloa crus-galli) genotypes. Weed Technol 21:683–687CrossRefGoogle Scholar
Machingura, M, Ebbs, SD (2014) Functional redundancies in cyanide tolerance provided by β-cyanoalanine pathway genes in Arabidopsis thaliana. Int J Plant Sci 175:346–358CrossRefGoogle Scholar
Machingura, M, Sidibe, A, Wood, AJ, Ebbs, SD (2013) The β-cyanoalanine pathway is involved in the response to water deficit in Arabidopsis thaliana. Plant Physiol Biochem 63:159–169CrossRefGoogle ScholarPubMed
Marchesi, C, Saldain, NE (2019) First report of herbicide-resistant Echinochloa crus-galli in Uruguayan rice fields. Agronomy 9: 790CrossRefGoogle Scholar
Maruyama, A, Ishizawa, K, Takagi, T (2000) Purification and characterization of beta-cyanoalanine synthase and cysteine synthases from potato tubers: are beta-cyanoalanine synthase and mitochondrial cysteine synthase same enzyme? Plant Cell Physiol 41:200–208CrossRefGoogle ScholarPubMed
Maruyama, A, Ishizawa, K, Takagi, T, Esashi, Y (1998) Cytosolic β-cyanoalanine synthase activity attributed to cysteine synthases in cocklebur seeds: purification and characterization of cytosolic cysteine synthases. Plant Cell Physiol 39:671–680CrossRefGoogle ScholarPubMed
McManus, MT (2012) The Plant Hormone Ethylene. Annual Plant Reviews 44. Hoboken, NJ: Wiley-Blackwell. 416 pCrossRefGoogle Scholar
Miller, JM, Conn, EE (1980) Metabolism of hydrogen cyanide by higher plants. Plant Physiol 65:1199–1202CrossRefGoogle ScholarPubMed
Nandula, VK, Riechers, DE, Ferhatoglu, Y, Barrett, M, Duke, SO, Dayan, FE, Goldberg-Cavalleri, A, Tétard-Jones, C, Wortley, DJ, Onkokesung, N, Brazier-Hicks, M, Edwards, R, Gaines, T, Iwakami, S, Jugulam, M, Ma, R (2019) Herbicide metabolism: crop selectivity, bioactivation, weed resistance, and regulation. Weed Sci 67:149–175CrossRefGoogle Scholar
Oerke, EC (2006) Crop losses to pests. J Agric Sci 144:31–43CrossRefGoogle Scholar
Peng, Q, Han, H, Yang, X, Bai, L, Yu, Q, Powles, SB (2019). Quinclorac resistance in Echinochloa crus-galli from China. Rice Sci 26:300–308Google Scholar
R Development Core Team (2010) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical ComputingGoogle Scholar
Ritz, C (2010) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29:220–229CrossRefGoogle Scholar
Ritz, C, Baty, F, Streibig, JC, Gerhard, D (2015). Dose-response analysis using R. PLoS ONE 10: e0146021CrossRefGoogle ScholarPubMed
Romero-Puertas, MC, McCarthy, I, Gomez, M, Sandalio, LM, Corpas, FJ, Del Rio, LA, Palma, JM (2004) Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ 27:1135–1148CrossRefGoogle Scholar
Saldain, NE, Sosa, B (2016) ¿Qué papel juega la resistencia metabólica en la expresión de la resistencia a Quinclorac y a Kifix® en algunos biotipos de capín de la zona este del Uruguay? Pages 15–17in Jornada anual arroz, 2016, INIA Treinta y Tres, UY. Arroz: resultados experimentales 2015–2016. INIA Serie Actividades de Difusión 765. Treinta y Tres, Uruguay: INIAGoogle Scholar
Sambrook, J, Fritschi, E, Maniatis, T (1989) Molecular Cloning: A Laboratory Manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 1546 pGoogle Scholar
Scheltrup, F, Grossmann, K (1995) Abscisic acid is a causative factor in the mode of action of the auxinic herbicide quinmerac in cleaver (Galium aparine L.). J Plant Physiol 147:118–126CrossRefGoogle Scholar
Solomanson, LP (1981) Cyanide as a metabolic inhibitor. Pages 11–28in Vennesland, EE, Conn, EE, Knowles, CJ, Westley, J, Wissing, F, eds. Cyanide in Biology. London: AcademicGoogle Scholar
Sunohara, Y, Shirai, S, Yamazaki, H, Matsumoto, H (2011) Involvement of antioxidant capacity in quinclorac tolerance in Eleusine indica. Environ Exp Bot 74:74–81CrossRefGoogle Scholar
Van de Poel, B, Van Der Staeten, D (2014) 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 5:640CrossRefGoogle ScholarPubMed
Walsh, TA, Neal, R, Owens Merlo, A, Honma, M, Hicks, GR, Wolff, K, Matsumura, W, Davies, JP (2006) Mutations in an auxin receptor homolog AFB5 and in SGT1b confer resistance to synthetic picolinate auxins and not to 2,4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis. Plant Physiol 142:542–552CrossRefGoogle ScholarPubMed
Wellburn, AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313CrossRefGoogle Scholar
Yasuor, H, Milan, M, Eckert, JW, Fischer, AJ (2011) Quinclorac resistance: a concerted hormonal and enzymatic effort in Echinochloa phyllopogon. Pest Manag Sci 68:108–115CrossRefGoogle ScholarPubMed
Yip, WK, Yang, S (1988) Cyanide metabolism in relation to ethylene production in plant tissues. Plant Physiol 88:473–476CrossRefGoogle ScholarPubMed
Yu, Q, Powles, S (2014) 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
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