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Download PDF (Inglês) DOI: http://dx.doi.org/10.1590/1678-992X-2019-0102 ISSN 1678-992X Plant Physiology and Biochemistry Review ACCase-inhibiting herbicides: mechanism of action, resistance evolution and stewardship Hudson Kagueyama Takano1* , Ramiro Fernando Lopez Ovejero2 , Gustavo Gross Belchior3 , Gizella Potrich Leal Maymone1 , Franck E. Dayan1 1Colorado State University – Bioagricultural Sciences and ABSTRACT: Herbicides play an important role in preventing crop yield losses due to both Pest Management, 300 W Pitkin St. – 80521 – Fort Collins, their weed interference ability and their capacity for increasing soil conservation in no-till CO – USA. systems. Group A herbicides or acetyl-CoA carboxylase (ACCase) are essential tools the 2Bayer Crop Science, Av. das Nações Unidas, 12901 – selective management of glyphosate resistance in grass weed species. In this review, we 04578-000 – São Paulo, SP – Brasil. describe important aspects of ACCase biology and herbicides targeting this enzyme, along 3Core Us Comunicação Científica, R. Tuim, 762 – 04514-103 with a discussion on stewardship programs to delay the evolution of herbicide resistance – São Paulo, SP – Brasil. which can evolve either through target site and/or non-target site mechanisms. Sixteen-point *Corresponding author <[email protected]> mutations have been reported to confer resistance to ACCase inhibitors. Each mutation confers cross resistance to a different group of herbicides. Metabolic resistance can result Edited by: Paulo Cesar Sentelhas in resistance to multiple herbicides with different mechanisms of action (MoA), and herbicide detoxification is often conferred by cytochrome P450 monooxigenases and glutathione-S- Received April 17, 2019 transferases. Regardless of whether resistance mechanisms are target or non-target site, Accepted June 09, 2019 using herbicides with the same MoA will result in resistance evolution. Therefore, while field surveys and resistance mechanism studies are crucial for designing reactive management strategies, integrated weed management plays a central role in both reactive and proactive mitigation of herbicide resistance evolution. Keywords: herbicide resistance, integrated weed management, aryloxyphenoxypropionates, cyclohexanediones, phenylpyrazoline Introduction ACCase and its physiological function Fatty acids are carboxylic acids with long aliphatic The world population has grown over the past chains that perform important physiological functions few decades and is estimated to reach 9.7 billion (e.g. energy storage, cell/organelle membrane structure people in 2050 (Gerland et al., 2014). As the population composition, hormonal regulation) in living organisms. continues to grow, agriculture technologies need to The ubiquitous, biotin-dependent ACCase enzyme increase crop yields to meet the ever-increasing demand catalyzes two irreversible reactions that determine for food (Tester and Langridge, 2010). South America is commitment to the fatty acid synthesis pathway (Dayan a major food producer in the global agriculture chain, et al., 2019). The enzyme consists of three functional encompassing approximately 25 % of the world’s domains: biotin-carboxyl carrier protein (BCCP), biotin total cultivated area with cotton, corn, and soybean, carboxylase (BC), and carboxyltransferase (CT, with representing 1.7, 23.0, and 62.1 million ha, respectively subunits α and β) (Figure 1). The BC and CT domains (USDA, 2018). Weeds are one of the greatest challenges shoulder the catalytic activities that are dependent 2+ – to modern agriculture causing, on average, a 35 % upon ATP, Mg , and HCO3 , which result in acetyl- reduction in crop yield (Oerke, 2006). Herbicides are CoA carboxylation and the formation of malonyl-CoA. extremely efficient tools for weed management and The two reactions catalyzed by the BC and CT subunits have been a key component to maintain no-till systems are presented, respectively, below (Nikolau et al., 2003; in agriculture (Naylor, 2008). Sasaki and Nagano, 2004; Shorrosh et al., 1994): Group A herbicides or acetyl-CoA carboxylase – 2+ (ACCase) inhibitors were first introduced into the (BC) BCCP + HCO3 + Mg + ATP → BCCP + CO2 + market in 1978 (Kaundun, 2014) with the appearance Mg2+ + ADP + Pi of diclofop-methyl. These herbicides provide selective grass weed control in dicot crops and a limited number (CT) BCCP + CO2 + Acetyl-CoA → BCCP + CO2 + of active ingredients for use in monocot crops with an Mg2+ + ADP + Pi estimated treated area of 120 million ha per year (Busi et al., 2018). ACCase-inhibiting herbicides play a key role While malonyl-CoA is necessary for de novo in managing glyphosate-resistant (GR) grasses, one of synthesis of fatty acids in plastids, cytosolic malonyl- the greatest weed management challenges facing South CoA is required for the elongation of very long chain America (Lopez Ovejero et al., 2017). This manuscript fatty acids (VLCFAs) and secondary metabolites such as covers a detailed review of important aspects related to flavonoids and suberins (Harwood, 1988). Plants express ACCase inhibitors along with best stewardship practices plastidic and cytoplasmic ACCase isoforms. The plastidic for herbicide resistance management. isoform is responsible for more than 80 % of total ACCase Sci. Agric. v.78, n.1, e20190102, 2021 Takano et al. A critical review of ACCase inhibitors However, once in the soil, these herbicides can be converted to their acid form, and be absorbed by plant roots and cause damage. The potential for carryover varies from one species to another, soil characteristics, and herbicide dosage, but residual activity was not observed for more than 14 days (Lancaster et al., 2018). Mechanism of action (MoA) ACCase-inhibiting herbicides have specific activity on grasses due to their selective inhibition of homomeric plastidic ACCase which is only found in monocots, with exceptions. Neither heteromeric plastic nor homomeric cytosolic forms are inhibited by ACCase inhibitors, making dicots tolerant to them (Kukorelli et al., 2013). Exceptions include susceptible Geraniaceae species and a few Brassica and Arabidopsis species (Kaundun, 2014) expressing the homomeric ACCase in their chloroplasts. Figure 1 – A tertiary structure view of wheat (T. aestivum) eukaryotic These herbicides halt ACCase activity by blocking ACCase and its domains: biotin carboxylase (BC), biotin carboxyl fatty acid biosynthesis, preventing the formation of carrier protein (BCCP), and carboxyltransferase (CT). lipid and secondary metabolites in susceptible plants. This results in a loss of cell membrane integrity, metabolite leakage, and ultimately cell death (Délye, activity in leaves (Egli et al., 1993; Ashton et al., 1994; De 2005; Kaundun, 2014). This process begins when the Prado et al., 2004). Plants belonging to the Poaceae family herbicide is absorbed by the leaves and translocates to (grasses), possess a homomeric (or eukaryotic) plastidic proliferating meristematic tissues through the phloem ACCase in which the BCCP, BC, and CT domains are where it damages the cell membrane structure, inhibits localized within a single polypeptide chain (Incledon meristematic activity, and restricts the growth of new and Hall, 1997). Both plastidic and cytoplasmic ACCase leaves (Kukorelli et al., 2013). Necrotic symptoms can be in Poaceae become active when homodimerized (Egli et observed in growing tissues after one week of application, al., 1993; Zhang et al., 2003). Dicotyledonous plants have with initial chlorosis and subsequent disintegration of homomeric form in the cytoplasm and heteromeric (or the leaves (Dayan et al., 2019). The efficacy of these prokaryotic) form in the plastids, where each domain is herbicides is positively correlated with higher relative encoded by different genes expressed in a coordinated air humidity due to an increase in molecule uptake and fashion (Sasaki and Nagano, 2004). translocation in the plant (Cieslik et al., 2013). Studies of enzyme kinetics have shown that FOPs and DIMs are 2+ – ACCase-inhibiting (Group A) herbicides non-competitive inhibitors of ATP, Mg , and HCO3 , but Classification and general characteristics are competitive inhibitors of acetyl-CoA substrate. This ACCase-inhibiting or Group A herbicides are divided suggests they act by inhibiting the transcarboxylation into three chemical families: aryloxyphenoxypropionates step (CT domain) rather than the biotin carboxylation (FOPs), cyclohexanodiones (DIMs), and phenylpyrazole step (BC domain) despite binding to the same catalytic (DENs). While FOPs and DIMs were introduced over 45 site in the CT domain (Rendina et al., 1990; Burton et years ago, DEN was launched in 2006 and consists of a al., 1991; Burton, 1997; Devine, 2002). single herbicide, pinoxaden (Hofer, 2006; Dayan et al., Molecular and biochemical data have clearly 2019). All molecules belonging to these chemical groups established that the CT domain in the homomeric consist of a carbon skeleton with polar substituents, ACCase bears the target binding site of FOPs, DIMs, but structures presenting distinct characteristics and DEN (Délye, 2005; Xia et al., 2016) even though (Délye, 2005). Most FOPs are in the form of formulated they bind in distinct regions of the homodimer interface. methyl, butyl or ester, providing more lipophilicity and Crystal structure analyses of Staphylococcus aureus CT increased capacity to cross cellular membranes by acid domain in complex with at least one herbicide from each trapping (Takano et al., 2019b). These herbicides have a group
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