Loss of trifluralin metabolic resistance in Lolium rigidum plants exposed to prosulfocarb recurrent selection.
annual ryegrass
cytochrome P450 monooxygenase
herbicide resistance
phorate
prosulfocarb
trifluralin
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Dec 2020
Dec 2020
Historique:
received:
11
05
2020
revised:
29
06
2020
accepted:
08
07
2020
pubmed:
9
7
2020
medline:
22
12
2020
entrez:
9
7
2020
Statut:
ppublish
Résumé
Resistance to the dinitroaniline herbicide trifluralin in Lolium rigidum (annual ryegrass) often is mediated by the enhanced capacity to metabolize the herbicide to less toxic polar conjugates and/or by functionally recessive target-site mutations in α-tubulin. In two L. rigidum populations possessing enhanced trifluralin metabolism, resistance was largely reversed by recurrent selection with the thiocarbamate herbicide prosulfocarb (i.e. plant survival was two- to >20-fold lower). Their ability to metabolize trifluralin was significantly decreased (by ≈2.3-fold) following recurrent prosulfocarb selection, to levels comparable to those observed in susceptible plants or when trifluralin metabolism was inhibited by treatment with the insecticide phorate. This study provides evidence that trait(s) enabling efficient trifluralin metabolism in L. rigidum are purged from the population under prosulfocarb recurrent selection. The level of trifluralin metabolism in vitro and its inhibition caused by phorate action on trifluralin-metabolizing enzyme(s) is equivalent to the effect produced by prosulfocarb selection. The hypothetical link between the two phenomena is that the putative monooxygenase(s) conferring trifluralin metabolic resistance also mediate the activation of prosulfocarb to its toxic sulfoxide. Thus, we speculate that survival to prosulfocarb via a lack of metabolic herbicide activation, and survival to trifluralin conferred by enhanced herbicide metabolism, are mutually exclusive. These findings not only open up a new research direction in terms of the interaction between different herbicide resistance mechanisms in L. rigidum, but also offer strategies for immediate management of the population dynamics of metabolism-based resistance in the field. © 2020 Society of Chemical Industry.
Sections du résumé
BACKGROUND
BACKGROUND
Resistance to the dinitroaniline herbicide trifluralin in Lolium rigidum (annual ryegrass) often is mediated by the enhanced capacity to metabolize the herbicide to less toxic polar conjugates and/or by functionally recessive target-site mutations in α-tubulin.
RESULTS
RESULTS
In two L. rigidum populations possessing enhanced trifluralin metabolism, resistance was largely reversed by recurrent selection with the thiocarbamate herbicide prosulfocarb (i.e. plant survival was two- to >20-fold lower). Their ability to metabolize trifluralin was significantly decreased (by ≈2.3-fold) following recurrent prosulfocarb selection, to levels comparable to those observed in susceptible plants or when trifluralin metabolism was inhibited by treatment with the insecticide phorate.
CONCLUSIONS
CONCLUSIONS
This study provides evidence that trait(s) enabling efficient trifluralin metabolism in L. rigidum are purged from the population under prosulfocarb recurrent selection. The level of trifluralin metabolism in vitro and its inhibition caused by phorate action on trifluralin-metabolizing enzyme(s) is equivalent to the effect produced by prosulfocarb selection. The hypothetical link between the two phenomena is that the putative monooxygenase(s) conferring trifluralin metabolic resistance also mediate the activation of prosulfocarb to its toxic sulfoxide. Thus, we speculate that survival to prosulfocarb via a lack of metabolic herbicide activation, and survival to trifluralin conferred by enhanced herbicide metabolism, are mutually exclusive. These findings not only open up a new research direction in terms of the interaction between different herbicide resistance mechanisms in L. rigidum, but also offer strategies for immediate management of the population dynamics of metabolism-based resistance in the field. © 2020 Society of Chemical Industry.
Substances chimiques
Carbamates
0
Herbicides
0
prosulfocarb
52888-80-9
Trifluralin
C8BX46QL7K
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3926-3934Subventions
Organisme : Grains Research and Development Corporation
Informations de copyright
© 2020 Society of Chemical Industry.
Références
Heap I, The international survey of herbicide resistant weeds. Available: www.weedscience.org. [Accessed 20 April, 2020].
D'Emden FH, Llewellyn RS and Burton MP, Factors influencing adoption of conservation tillage in Australian cropping regions. Aust J Agric Resour Econ 52:169-182 (2008).
Christopher JT, Powles SB, Liljegren DR and Holtum JAM, Cross-resistance to herbicides in annual ryegrass (Lolium rigidum) II: chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiol 95:1036-1043 (1991).
Menendez J and De Prado R, Diclofop-methyl cross-resistance in a chlorotoluron-resistant biotype of Alopecurus myosuroides. Pestic Biochem Physiol 56:123-133 (1996).
Beckie HJ, Thomsa AG, Légère A and Kelner DJ, Nature, occurrence, and cost of herbicide-resistant wild oat (Avena fatua) in small grain production areas. Weed Technol 13:612-625 (1999).
Owen MJ, Martinez NJ and Powles SB, Multiple herbicide-resistant Lolium rigidum (annual ryegrass) now dominates across the Western Australian grain belt. Weed Res 54:314-324 (2014).
Han H, Yu Q, Owen MJ, Cawthray GR and Powles SB, Widespread occurrence of both metabolic and target-site herbicide resistance mechanisms in Lolium rigidum populations. Pest Manag Sci 72:255-263 (2016).
Boutsalis P, Gill GS and Preston C, Incidence of herbicide resistance in rigid ryegrass (Lolium rigidum) across southeastern Australia. Weed Technol 26:391-398 (2012).
Broster JC, Pratley JE, Ip RHL, Ang L and Seng KP, A quarter of a century of monitoring herbicide resistance in Lolium rigidum in Australia. Crop Pasture Sci 70:283-293 (2019).
Keshtkar E, Mathiassen SK, Moss SR and Kudsk P, Resistance profile of herbicide-resistant Alopecurus myosuroides (black-grass) populations in Denmark. Crop Prot 69:83-89 (2015).
Brunton DJ, Boutsalis P, Gill G and Preston C, Resistance to multiple PRE herbicides in a field-evolved rigid ryegrass (Lolium rigidum) population. Weed Sci 66:581-585 (2018).
Busi R, Gaines TA, Walsh MJ and Powles SB, Understanding the potential for resistance evolution to the new herbicide pyroxasulfone: field selection at high doses versus recurrent selection at low doses. Weed Res 52:489-499 (2012).
Busi R and Powles SB, Cross-resistance to prosulfocarb and triallate in pyroxasulfone-resistant Lolium rigidum. Pest Manag Sci 69:1379-1384 (2013).
Busi R, Gaines TA and Powles S, Phorate can reverse P450 metabolism-based herbicide resistance in Lolium rigidum. Pest Manag Sci 73:410-417 (2017).
Christopher JT, Preston C and Powles SB, Malathion antagonizes metabolism-based chlorsulfuron resistance in Lolium rigidum. Pestic Biochem Physiol 49:172-182 (1994).
Siminszky B, Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:445-458 (2006).
Ferhatoglu Y, Avdiushko S and Barrett M, The basis for the safening of clomazone by phorate insecticide in cotton and inhibitors of cytochrome P450s. Pestic Biochem Physiol 81:59-70 (2005).
Rasool S and Mohamed R, Plant cytochrome P450s: nomenclature and involvement in natural product biosynthesis. Protoplasma 253:1197-1209 (2016).
Schlaich NL, Flavin-containing monooxygenases in plants: looking beyond detox. Trends Plant Sci 12:412-418 (2007).
Kreuz K, Tommasini R and Martinoia E, Old enzymes for a new job: herbicide detoxification in plants. Plant Physiol 111:349-353 (1996).
Tanaka S, Hoffer BL, Shimabukuro RH, Wien RG and Walsh WC, Identification of the isomeric hydroxylated metabolites of methyl 2-[(4-2,4-dichlorophenoxy)phenoxy]propanoate (diclofop methyl) in wheat. J Agric Food Chem 38:559-565 (1990).
Casida JE, Gray RA and Tilles H, Thiocarbamate sulfoxides: potent, selective, and biodegradable herbicides. Science 184:573-574 (1974).
Casida JE, Kimmel EC, Ohkawa H and Ohkawa R, Sulfoxidation of thiocarbamate herbicides and metabolism of thiocarbamate sulfoxides in living mice and liver enzyme systems. Pestic Biochem Physiol 5:1-11 (1975).
Burnet MWM, Barr AR and Powles SB, Chloroacetamide resistance in rigid ryegrass (Lolium rigidum). Weed Sci 42:153-157 (1994).
McAlister FM, Holtum JAM and Powles SB, Dinitroaniline herbicide resistance in rigid ryegrass (Lolium rigidum). Weed Sci 43:55-62 (1995).
Chen J, Goggin D, Han H, Busi R, Yu Q and Powles S, Enhanced trifluralin metabolism can confer resistance in Lolium rigidum. J Agric Food Chem 66:7589-7596 (2018).
Chen J, Chu Z, Han H, Goggin DE, Yu Q, Sayer C et al., A Val-202-Phe α-tubulin mutation and enhanced metabolism confer dinitroaniline resistance in a single Lolium rigidum population. Pest Manag Sci 76:645-652 (2020).
Chen J, Yu Q, Owen M, Han H and Powles S, Dinitroaniline herbicide resistance in a multiple-resistant Lolium rigidum population. Pest Manag Sci 74:925-932 (2018).
Payne WR Jr, Pope JD Jr and Benner JE, An integrated method for trifluralin, diphenamid, and paraquat in soil and runoff from agricultural land. J Agric Food Chem 22:79-82 (1974).
R Core Team, R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2019) www.R-project.org/.
Venables WN and Ripley BD, Applied Statistics with S-PLUS. Springer Science & Business Media, Berlin, Germany (2013).
Pinheiro JC and Bates DM, Mixed-Effects Models in S and S-Plus. Springer-Verlag Inc, New York, NY (2000).
Bretz F, Hotorn T and Westfall P, Multiple Comparisons Using R. CRC Press, Boca Raton, FL (2011).
Epp JB, Schmitzer PR and Crouse GD, Fifty years of herbicide research: comparing the discovery of trifluralin and halauxifen-methyl. Pest Manag Sci 74:9-16 (2018).
Chen J, Lu H, Han H, Yu Q, Sayer C and Powles S, Genetic inheritance of dinitroaniline resistance in an annual ryegrass population. Plant Sci 283:189-194 (2019).
Saquib Q, Al-Khedhairy AA, Siddiqui MA, Roy AS, Dasgupta S and Musarrat J, Preferential binding of insecticide phorate with sub-domain IIA of human serum albumin induces protein damage and its toxicological significance. Food Chem Toxicol 49:1787-1795 (2011).
Jain M, Gallo M, Chengalrayan K, Shaikh NP, MacDonald GE and Davis JM, Phorate-induced host defence responses condition acquired resistance to tomato spotted wilt in cultivated peanut (Arachis hypogaea L.). J Phytopathol 163:853-866 (2015).
Rani R, Padole P, Juwarkar A and Chakrabarti T, Phytotransformation of phorate by Brassica juncea (Indian mustard). Water Air Soil Pollut 223:1383-1392 (2012).
Baerg RJ, Barrett M and Polge ND, Insecticide and insecticide metabolite interactions with cytochrome P450 mediated activities in maize. Pestic Biochem Physiol 55:10-20 (1996).
Erkog FÜ and Menzer RE, Metabolism of trifluralin in rats. J Agric Food Chem 33:1061-1070 (1985).
Chan D, Fussell RJ, Hetmanski MT, Sinclair CJ, Kay JF, Grant A et al., Investigation of the fate of trifluralin in shrimp. J Agric Food Chem 61:2371-2377 (2013).
Camper ND, Stralka K and Skipper HD, Aerobic and anaerobic degradation of profluralin and trifluralin. J Environ Sci Health, Part B 15:457-473 (1980).
Biswas PK and Hamilton W, Metabolism of trifluralin in peanuts and sweet potatoes. Weed Sci 17:206-211 (1969).
Tiryaki O, Maden S and Tunbilek AS, 14C-residues of trifluralin in soil and melon. Bull Environ Contam Toxicol 59:750-756 (1997).
Kreuger SK and Williams DE, Mammalian flavin-containing monooxygenases: structure/function, genetic polymorphisms and role in drug metabolism. Pharmacol Ther 106:357-387 (2005).
Kern AJ, Peterson DM, Miller EK, Colliver CC and Dyer WE, Triallate resistance in Avena fatua L. is due to reduced herbicide activation. Pest Biochem Physiol 56:163-173 (1996).
Brunton DJ, Boutsalis P, Gill G and Preston C, Resistance to very-long-chain fatty-acid (VLCFA)-inhibiting herbicides in multiple field-selected rigid ryegrass (Lolium rigidum) populations. Weed Sci 67:267-272 (2019).
Brunton DJ, Boutsalis P, Gill G and Preston C, Varying Responses of Field-Selected Herbicide Resistant Rigid Ryegrass (Lolium rigidum) Populations to Combinations of Phorate with Pre-Plant Incorporated Herbicides. Weed Sci in press 68:367-372 (2020).
Neve P and Powles SB, Recurrent selection with reduced herbicide rates results in the rapid evolution of herbicide resistance in Lolium rigidum. 110:1154-1166 (2005).
Neve P, Vila-Aiub MM and Roux F, Evolutionary-thinking in agricultural weed management. New Phytol 184:783-793 (2009).
Manalil S, Busi R, Renton M and Powles SB, Rapid evolution of herbicide resistance by low herbicide doses. Weed Sci 59:210-217 (2011).
Bostamam Y, Malone JM, Dolman FC, Boutsalis P and Preston C, Rigid ryegrass (Lolium rigidum) populations containing a target site mutation in EPSPS and reduced glyphosate translocation are more resistant to glyphosate. Weed Sci 60:474-479 (2012).
Busi R, Powles SB, Beckie SB and Renton M, Rotations and mixtures of soil-applied herbicides delay resistance. Pest Manag Sci 76:487-496 (2020).