Cellular Redox-Related Transcription Factor Nrf2 Mediation of HaTrf Response to Host Plant Allelochemical 2-Tridecanone in Helicoverpa armigera

Zhang, Lei; Lv, Shenglan; Liu, Ying; Yang, Liwen; Liang, Pei; Gao, Xiwu

doi:10.1021/acs.jafc.0c02080

Cited by 2 publications

(4 citation statements)

References 39 publications

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“…This type of preadaptation has been observed in other organisms, including insects and bacteria ( 23 , 28 – 32 ). For instance, flavonoids induce the overexpression of the P450 gene in whitefly ( Bemisia tabaci ), leading to metabolic detoxification and resistance to insecticides thiamethoxam and flufenoxuron ( 23 ).…”

Section: Discussionsupporting

confidence: 53%

Multidrug resistance of Botrytis cinerea associated with its adaptation to plant secondary metabolites

Wu,

Bi,

Zhang

et al. 2024

mBio

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Fungicides are an effective way to control gray mold of grapes, but the pathogen Botrytis cinerea can develop resistance, overcoming the effectiveness of a fungicide that is repeatedly applied. More importantly, the emergence of multidrug resistance (MDR) in the field, where multiple fungicides with different modes of action simultaneously lose their efficacies, is a significant concern. MDR is associated with ATP-binding cassette (ABC) transporters of the pathogen, and certain plant secondary metabolites (PSMs) stimulate the upregulation of ABC transporters, we hypothesized that the pathogen’s preadaptation to PSMs might contribute to MDR development. To test this in B. cinerea, ten PSMs, namely, resveratrol, reserpine, chalcone, flavanone, eugenol, farnesol, anethene, camptothecin, salicylic acid, and psoralen, were selected based on their association with ABC transporters involved in fungicide resistance. B. cinerea strain B05.10 was continuously transferred for 15 generations on potato dextrose agar amended with a PSM (PDAP), and sensitivities to PSMs and fungicides were examined on the 5th, 10th, and 15th generations. RNA was extracted from B. cinerea from the selected generations. After 15 generations of culture transfers, an up-regulation was observed in the expression of ABC transporter-encoding genes BcatrB, BcatrD, and BcatrK using quantitative polymerase chain reaction (qPCR). This upregulation was found to contribute to MDR of B. cinerea against two or more fungicides, among azoxystrobin, boscalid, fludioxonil, difenoconazole, prochloraz, and pyrimethanil. This finding was confirmed through genetic transformation. The decreased sensitivity of B. cinerea to fungicides was confirmed as a subsequent MDR phenotype after exposure to camptothecin, flavanone, and resveratrol. Besides, transcriptome analysis also revealed the upregulation of transcription factors related to ABC expression following resveratrol exposure. This suggests that PSMs contributed to inducing preadaptation of B. cinerea, leading to subsequent MDR. IMPORTANCE The emergence of MDR in plant pathogens is a threat to plant disease management and leads to the use of excessive fungicides. Botrytis cinerea is of particular concern because its MDR has widely emerged in the field. Understanding its genesis is the first step for controlling MDR. In this study, the contribution of PSMs to MDR has been examined. Effective management of this pathogen in agroecosystems relies on a better understanding of how it copes with phytochemicals or fungicides.

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Section: Discussionsupporting

confidence: 53%

Multidrug resistance of Botrytis cinerea associated with its adaptation to plant secondary metabolites

Wu,

Bi,

Zhang

et al. 2024

mBio

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“…Xenobiotic transcription factors play important roles in the regulation of detoxification genes involved in xenobiotic metabolism [8]. It was also reported that Nrf2 and AhR transcription factors are involved in the regulation of some three-phase enzyme gene members responsible for insecticide resistance [13,26,27].…”

Section: Discussionmentioning

confidence: 99%

“…The homologous H. armigera fat body cell line was generously provided by Dr. Huan Zhang (Zoology, CAS, China). The cell line was routinely maintained with sf900-III insect serum-free medium (Thermo Fisher Scientific, USA) supplemented with 10% heatinactivated fetal bovine serum (Gibco, USA) at 37 • C. The full-length coding regions of HaNrf2 and HaAhR were constructed into pAcV5His vector [13]. The H. armigera fat body cells were seeded into 96-well plates (1 × 10 4 cells/ well) then transiently co-transfected with different gene promoters fused to pGL4 luciferase reporter constructs (1 mg/well) combined with pAcV5His-Red-HaNrf2 (0.5 mg/well), pAcV5His-GFP-HaAhR (0.5 mg/well), dsNrf2 (4 µg/well) or dsAhR (4 µg/well).…”

Section: Transient Transfection and Dual Luciferase Assaymentioning

confidence: 99%

“…In Bemisia tabaci, a recent study reported that a P450 gene mediated resistance to imidacloprid by a mitogen-activated protein kinases (MAPKs) pathway [10]. Notably, recent studies in multiple insect species reported that insects have co-opted a xenobiotic stress response pathway that involves reactive oxygen species and the transcription factors Nrf2 (nuclear factor erythroid-2 related factor-2) or AhR (aryl hydrocarbon receptor) to up-regulate the expression of some detoxification gene members involved in insecticides resistance [11][12][13].…”

Section: Introductionmentioning

confidence: 99%

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A General Signal Pathway to Regulate Multiple Detoxification Genes Drives the Evolution of Helicoverpa armigera Adaptation to Xenobiotics

Zhang

et al. 2022

IJMS

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The study of insect adaptation to the defensive metabolites of host plants and various kinds of insecticides in order to acquire resistance is a hot topic in the pest-control field, but the mechanism is still unclear. In our study, we found that a general signal pathway exists in H. armigera which can regulate multiple P450s, GSTs and UGTs genes to help insects decrease their susceptibility to xenobiotics. Knockdown of HaNrf2 and HaAhR expression could significantly increase the toxicity of xenobiotics to H. armigera, and simultaneously decrease the gene expression of P450s, GSTs and UGTs which are related to the xenobiotic metabolism and synthesis of insect hormone pathways. Then, we used EMSA and dual luciferase assay to verify that a crosstalk exists between AhR and Nrf2 to regulate multiple P450s, GSTs and UGTs genes to mediate H. armigera susceptibility to plant allelochemicals and insecticides. The detoxification genes’ expression network which can be regulated by Nrf2 and AhR is still unknown, and there were also no reports about the crosstalk between AhR and Nrf2 that exist in insects and can regulate multiple detoxification genes’ expression. Our results provide a new general signaling pathway to reveal the adaptive mechanism of insects to xenobiotics and provides further insight into designing effective pest-management strategies to avoid the overuse of insecticides.

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Cellular Redox-Related Transcription Factor Nrf2 Mediation of HaTrf Response to Host Plant Allelochemical 2-Tridecanone in Helicoverpa armigera

Cited by 2 publications

References 39 publications

Multidrug resistance of Botrytis cinerea associated with its adaptation to plant secondary metabolites

Multidrug resistance of Botrytis cinerea associated with its adaptation to plant secondary metabolites

A General Signal Pathway to Regulate Multiple Detoxification Genes Drives the Evolution of Helicoverpa armigera Adaptation to Xenobiotics

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