Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects

Cyanogenic plants can release toxic hydrogen cyanide (HCN) to defend against herbivory by hydrolyzing the cyanogenic glycosides (CNGs) with its β-glucosidases (β-GLUs). Numerous studies have speculated this CNG-mediated toxicity by a plant-pest interaction manner. However, the specific toxic effect...

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Main Authors: Mufeng Wu, Xiao Liang, Ying Liu, Chunling Wu, Xingkui An, Zihua Zhao, Guifeng Hao, Ijiti Oluwole Gregory, Zhihong Li, Qing Chen
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324015999
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author Mufeng Wu
Xiao Liang
Ying Liu
Chunling Wu
Xingkui An
Zihua Zhao
Guifeng Hao
Ijiti Oluwole Gregory
Zhihong Li
Qing Chen
author_facet Mufeng Wu
Xiao Liang
Ying Liu
Chunling Wu
Xingkui An
Zihua Zhao
Guifeng Hao
Ijiti Oluwole Gregory
Zhihong Li
Qing Chen
author_sort Mufeng Wu
collection DOAJ
description Cyanogenic plants can release toxic hydrogen cyanide (HCN) to defend against herbivory by hydrolyzing the cyanogenic glycosides (CNGs) with its β-glucosidases (β-GLUs). Numerous studies have speculated this CNG-mediated toxicity by a plant-pest interaction manner. However, the specific toxic effect of HCN was not well-demonstrated because of the interference of other ingested metabolites. Additionally, the physiological- and biochemical-based mode of action of HCN were seldom determined. To fill those knowledge gaps, the two-spotted spider mite (TSSM), Tetranychus urticae, was used as a model organism to elucidate the toxic mechanism of HCN. In addition, three CNG-enzyme combinations were screened for effective cyanogenesis and TSSM lethality. Linamarin-β-GLU (lima bean-derived) presented prompt HCN release, and molecular docking indicated higher binding energy and more robust binding sites compared with other two groups, i.e., lotaustralin-β-GLU (lima bean-derived) and amygdalin-β-GLU (almond-derived). Meanwhile, this combination led to higher TSSM mortality. Moreover, we found that the median lethal concentration of this combination will significantly prolong the developmental duration, and decrease the longevity and fecundity of TSSM. Besides, the population growth was also significantly suppressed. Furthermore, the sustainable activation of enzyme activity and the encoding gene expression related to physiological process such as detoxification (cytochrome P450, glutathione S-transferase, UDP-glucuronosyltransferase and β-cyanoalanine synthase), antioxidation (superoxide dismutase, catalase and peroxidase), neural transduction (acetylcholinesterase) and respiration (cytochrome c oxidase) were attributed to the detrimental impact on development and reproduction of TSSM. The present findings can provide insight regarding reasonable utilization of toxic chemicals in pest management and creation of novel pest-resistant germplasm.
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spelling doaj-art-2b751824ef634e06b39471562eb0d8c72025-02-12T05:29:28ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01290117523Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspectsMufeng Wu0Xiao Liang1Ying Liu2Chunling Wu3Xingkui An4Zihua Zhao5Guifeng Hao6Ijiti Oluwole Gregory7Zhihong Li8Qing Chen9MARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China; Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Institute of China Agricultural University, Sanya 572025, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaEnvironment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaEnvironment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaEnvironment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaEnvironment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China; Sanya Institute of China Agricultural University, Sanya 572025, ChinaEnvironment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaEnvironment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, ChinaMARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China; Sanya Institute of China Agricultural University, Sanya 572025, China; Corresponding author at: MARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing 100193, China.Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; Sanya Research Academy, Chinese Academy of Tropical Agriculture Science, Sanya 572000, China; Corresponding author at: Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China.Cyanogenic plants can release toxic hydrogen cyanide (HCN) to defend against herbivory by hydrolyzing the cyanogenic glycosides (CNGs) with its β-glucosidases (β-GLUs). Numerous studies have speculated this CNG-mediated toxicity by a plant-pest interaction manner. However, the specific toxic effect of HCN was not well-demonstrated because of the interference of other ingested metabolites. Additionally, the physiological- and biochemical-based mode of action of HCN were seldom determined. To fill those knowledge gaps, the two-spotted spider mite (TSSM), Tetranychus urticae, was used as a model organism to elucidate the toxic mechanism of HCN. In addition, three CNG-enzyme combinations were screened for effective cyanogenesis and TSSM lethality. Linamarin-β-GLU (lima bean-derived) presented prompt HCN release, and molecular docking indicated higher binding energy and more robust binding sites compared with other two groups, i.e., lotaustralin-β-GLU (lima bean-derived) and amygdalin-β-GLU (almond-derived). Meanwhile, this combination led to higher TSSM mortality. Moreover, we found that the median lethal concentration of this combination will significantly prolong the developmental duration, and decrease the longevity and fecundity of TSSM. Besides, the population growth was also significantly suppressed. Furthermore, the sustainable activation of enzyme activity and the encoding gene expression related to physiological process such as detoxification (cytochrome P450, glutathione S-transferase, UDP-glucuronosyltransferase and β-cyanoalanine synthase), antioxidation (superoxide dismutase, catalase and peroxidase), neural transduction (acetylcholinesterase) and respiration (cytochrome c oxidase) were attributed to the detrimental impact on development and reproduction of TSSM. The present findings can provide insight regarding reasonable utilization of toxic chemicals in pest management and creation of novel pest-resistant germplasm.http://www.sciencedirect.com/science/article/pii/S0147651324015999CyanogenesisTetranychus urticaeDevelopment and reproductionEnzyme activityGene expression
spellingShingle Mufeng Wu
Xiao Liang
Ying Liu
Chunling Wu
Xingkui An
Zihua Zhao
Guifeng Hao
Ijiti Oluwole Gregory
Zhihong Li
Qing Chen
Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects
Ecotoxicology and Environmental Safety
Cyanogenesis
Tetranychus urticae
Development and reproduction
Enzyme activity
Gene expression
title Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects
title_full Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects
title_fullStr Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects
title_full_unstemmed Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects
title_short Mechanisms underlying the effects of cyanogenesis on development and reproduction of Tetranychus urticae: Insights from enzyme activity and gene expression aspects
title_sort mechanisms underlying the effects of cyanogenesis on development and reproduction of tetranychus urticae insights from enzyme activity and gene expression aspects
topic Cyanogenesis
Tetranychus urticae
Development and reproduction
Enzyme activity
Gene expression
url http://www.sciencedirect.com/science/article/pii/S0147651324015999
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