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Nematicidal Activity of Benzyloxyalkanols Against Pine Wood Nematode

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Nematicidal Activity of Benzyloxyalkanols Against Pine Wood Nematode biomolecules Article Nematicidal Activity of Benzyloxyalkanols against Pine Wood Nematode Junheon Kim 1,*,† , Su Jin Lee 1,†,‡ , Joon Oh Park 1,§ and Kyungjae Andrew Yoon 2 1 Forest Insect Pests and Disease Division, National Institute of Forest Science, Seoul 02455, Korea; [email protected] (S.J.L.); [email protected] (J.O.P.) 2 Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul 08826, Korea; [email protected] * Correspondence: [email protected]; Tel.: +82-2-961-2672 † These authors contributed equally to this study. ‡ Present address: Division of Life Sciences & Convergence Research Center for Insect Vectors, College of Life Science and Bioengineering, Incheon National University, Incheon 22012, Korea. § Present address: Urban Forest Clinic, Boryeong 33455, Korea. Abstract: Pine wilt disease (PWD) is caused by the pine wood nematode (PWN; Bursaphelenchus xylophilus) and causes severe environmental damage to global pine forest ecosystems. The current strategies used to control PWN are mainly chemical treatments. However, the continuous use of these reagents could result in the development of pesticide-resistant nematodes. Therefore, the present study was undertaken to find potential alternatives to the currently used PWN control agents abamectin and emamectin. Benzyloxyalkanols (BzOROH; R = C2–C9) were synthesized and the nematicidal activity of the synthetic compounds was investigated. Enzymatic inhibitory assays (acetylcholinesterase (AChE) and glutathione S-transferase (GST)) were performed with BzOC8OH and BzOC9OH to understand their mode of action. The benzyloxyalkanols showed higher Citation: Kim, J.; Lee, S.J.; Park, J.O.; nematicidal activity than did benzyl alcohol. Among the tested BzOROHs, BzC8OH and BzC9OH Yoon, K.A. Nematicidal Activity of showed the strongest nematicidal activity. The LD50 values of BzC8OH and BzC9OH were 246.1 and Benzyloxyalkanols against Pine 158.0 ppm, respectively. No enzyme inhibitory activity was observed for BzC8OH and BzC9OH. The Biomolecules 2021 Wood Nematode. , results suggested that benzyloxyalcohols could be an alternative nematicidal agent. 11, 384. https://doi.org/10.3390/ biom11030384 Keywords: pine wood nematode; pine wilt disease; benzyloxyalkanol; mode of action Academic Editor: Manuel Galvão de Melo e Mota Received: 15 January 2021 1. Introduction Accepted: 2 March 2021 Pine wilt disease (PWD), caused by the pine wood nematode (PWN; Bursaphelenchus Published: 5 March 2021 xylophilus), causes severe environmental damage to global pine forest ecosystems [1]. PWD has become and is becoming a serious concern over multiple continents including Asia and Publisher’s Note: MDPI stays neutral Europe [2–7]. Since its first reported sighting in 1988 in Korea [8], it has spread nationwide with regard to jurisdictional claims in and ca. 490,000 trees are affected by PWD [9]. The majority of pine species affected by published maps and institutional affil- PWD are red pine (Pinus densiflora), black pine (P. thunbergii) and P. koraiensis in Asia, while iations. P. pinaster, P. nigra and P. radiata are affected in Europe [1,3,10]. As Pinus species are the predominant tree species in Korean forests and highly affected by PWD, the ecological and economic damage is substantial. The current strategies used to control PWN are mainly chemical treatments, which in- Copyright: © 2021 by the authors. clude nematicide injection in trunks for PWD prevention and fumigation of wood material. Licensee MDPI, Basel, Switzerland. The most frequently used nematicides in Korea are abamectin and emamectin benzoate, This article is an open access article which belong to the avermectin family [11,12]. These agents are known to be highly effec- distributed under the terms and tive against PWN and are also considered environmentally safe [13,14]. However, it could conditions of the Creative Commons be inferred that the continuous use of these nematicides will induce selection pressure and Attribution (CC BY) license (https:// almost certainly produce resistant PWNs, as has been reported previously for nematodes creativecommons.org/licenses/by/ that developed resistance to avermectins [15–17]. 4.0/). Biomolecules 2021, 11, 384. https://doi.org/10.3390/biom11030384 https://www.mdpi.com/journal/biomolecules Biomolecules 2021, 11, x FOR PEER REVIEW 2 of 9 Biomolecules 2021, 11, 384 could be inferred that the continuous use of these nematicides will induce selection pres- 2 of 9 sure and almost certainly produce resistant PWNs, as has been reported previously for nematodes that developed resistance to avermectins [15–17]. As nematicidesAs nematicides against against PWN PWNare applied are applied in closed in closed systems, systems, such as such trunk as trunkinjection, injection, the possibilitythe possibility of developing of developing resistance resistance against against avermectins avermectins is low is and low opportunities and opportunities for for selectedselected nematode nematode strains strains to spread to spread in natural in natural populations populations is limited. is limited. However, However, because because the nematicidalthe nematicidal effect effect of avermectins of avermectins is no ist always not always successful, successful, the possibility the possibility of develop- of developing ing resistanceresistance and and spreading spreading by by insect insect vector vectorss in in natural natural populations remains. AlthoughAlthough PWN PWN hashas notnot yetyet been been reported reported to to show show resistance resistance to to abamectin, abamectin, the the alternative alternative use use of of diverse diverseagents agents is recommendedis recommended to avoidto avoid the the development development of resistanceof resistance and and to achieveto achieve efficient efficientcontrol control of PWN.of PWN. In In recent recent decades, decades, as as PWN PWN control control agents, agents, the the use use of of microorganism microor- ganismextracts, extracts, plant plant extracts, extracts, essential essential oils oils and and volatiles volatiles has has been been suggested suggested [18 [18–23].–23]. It has Itbeen has reported been reported that metabolic that metabolic resistance resistance in insects in insects involves involves some somedetoxifying detoxifying enzymesenzymes which which are areresponsible responsible for for breaking breaking down down toxins toxins enteringentering theirtheir bodies bodies [24 [24].]. Among Amongthose those enzymes, enzymes, acetylcholinesterase acetylcholinesterase (AChE) (AChE) and and glutathione glutathioneS-transferase S-transferase (GST) (GST) have been have beenassessed assessed to obtain to obtain an understanding an understanding of the modeof the ofmode action of and action the and extent the of extent its detoxification of its detoxificationin the target in the species target [species24–26]. [24–26]. Inhibition Inhibition of AChE of causes AChE overstimulationcauses overstimulation of the neurons, of the neurons,twitching twitching of muscles of muscles and insect and death insect [27 de]ath and [27] GST and is involved GST is involved in resistance in resistance development developmentin insects in through insects through detoxifying detoxifying of toxins of [28 toxins]. [28]. Recently,Recently, the nematicidal the nematicidal effect effect of alkyloxyethanols of alkyloxyethanols (ROR’OH, (ROR’OH, R’ R’ = =ethyl), ethyl), which which mod- modifiedified hydroxy hydroxy groups groups (-OH) (-OH) to to ɷ-hydroxyalkyl -hydroxyalkyl groups groups (-OROH) (-OROH) in in aliphatic aliphatic compounds, com- pounds,against against PWN PWN was was investigated investigated [29 ].[29]. The The effect effect of modificationof modification of theof the modified modified hydroxy hydroxygroup group to theto the-hydroxyalkyl ɷ-hydroxyalkyl group group in in aromatic aromatic compounds compounds has has not not been been investigated inves- tigatedin in PWN. PWN. In In the the present present study, study, we we synthesized synthesized benzyloxyalcohol benzyloxyalcohol (BzOROH; (BzOROH; R =R C=2 –C9), C2–C9evaluated), evaluated the the nematicidal nematicidal effects effects of 8of benzyloxyalcohols 8 benzyloxyalcohols and and investigated investigated their their mode of modeaction of action using using AChE AChE and and GST GST inhibition inhibition assays. assays. 2. Materials2. Materials and Methods and Methods 2.1. Nematodes 2.1. Nematodes Bursaphelenchus xylophilus was provided by the National Institute of Forest Science, Bursaphelenchus xylophilus was provided by the National Institute of Forest Science, South Korea. The identification of B. xylophilus was confirmed using morphological char- South Korea. The identification of B. xylophilus was confirmed using morphological char- acteristics and genetic differences, which were confirmed by the RFLP method [30]. The acteristics and genetic differences, which were confirmed by the RFLP method [30]. The B. xylophilus were reared on a fungal mat of Botrytis cinerea on potato dextrose agar (PDA) B. xylophilus were reared on a fungal mat of Botrytis cinerea on potato dextrose agar (PDA) medium at 25 ± 1 ◦C and 40% humidity for several generations. medium at 25 ± 1 °C and 40% humidity for several generations. 2.2. Preparation of Benzyloxyalcohols 2.2. Preparation of Benzyloxyalcohols Benzyloxyalkanols (1–8) were synthesized by modifying the method of Tanabe and BenzyloxyalkanolsPeters [31] (Scheme (11-).8) The were general synthesized procedure by modifying was as follows:
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