Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani

The fungicide SYP-14288 has a high efficiency, low toxicity, and broad spectrum in inhibiting both fungi and oomycetes, but its mode of action (MoA) remains unclear on inhibiting fungi. In this study, the MoA was determined by analyzing the metabolism and respiratory activities of Rhizoctonia solani...

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Main Authors: Li Liang, Xingkai Cheng, Tan Dai, Zhiwen Wang, Jin Li, Xueming Li, Bin Lei, Pengfei Liu, Jianjun Hao, Xili Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.574039/full
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author Li Liang
Xingkai Cheng
Tan Dai
Zhiwen Wang
Jin Li
Xueming Li
Bin Lei
Pengfei Liu
Jianjun Hao
Xili Liu
author_facet Li Liang
Xingkai Cheng
Tan Dai
Zhiwen Wang
Jin Li
Xueming Li
Bin Lei
Pengfei Liu
Jianjun Hao
Xili Liu
author_sort Li Liang
collection DOAJ
description The fungicide SYP-14288 has a high efficiency, low toxicity, and broad spectrum in inhibiting both fungi and oomycetes, but its mode of action (MoA) remains unclear on inhibiting fungi. In this study, the MoA was determined by analyzing the metabolism and respiratory activities of Rhizoctonia solani treated by SYP-14288. Wild-type strains and SYP-14288-resistant mutants of R. solani were incubated on potato dextrose agar amended with either SYP-14288 or one of select fungicides acting on fungal respiration, including complex I, II, and III inhibitors; uncouplers; and ATP synthase inhibitors. Mycelial growth was measured under fungicides treatments. ATP content was determined using an ATP assay kit, membrane potential of mitochondria was detected with the JC-1 kit, and respiratory rate was calculated based on the measurement of oxygen consumption of R. solani. A model of metabolic fingerprinting cluster was established to separate oxidation inhibitors and phosphorylation inhibitors. All the results together displayed a clear discrimination between oxidation inhibitors and phosphorylation inhibitors, and the latter inhibited ATP synthase production having or uncoupling activities. Based on the model, SYP-14288 was placed in phosphorylation inhibitor group, because it significantly reduced ATP content and membrane potential of mitochondria while increasing respiratory rate in R. solani. Therefore, the MoA of SYP-14288 on R. solani was confirmed to involve phosphorylation inhibition and possibly uncoupling activity.
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spelling doaj.art-a28b4603f57445cda018f2ec2ca410622022-12-21T23:34:40ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-12-011110.3389/fmicb.2020.574039574039Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solaniLi Liang0Xingkai Cheng1Tan Dai2Zhiwen Wang3Jin Li4Xueming Li5Bin Lei6Pengfei Liu7Jianjun Hao8Xili Liu9Department of Plant Pathology, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology, China Agricultural University, Beijing, ChinaDepartment of Plant Pathology, China Agricultural University, Beijing, ChinaInstitute of Nuclear and Biological Technologies, Xinjiang Academy of Agricultural Sciences, Urumqi, ChinaDepartment of Plant Pathology, China Agricultural University, Beijing, ChinaInstitute of Nuclear and Biological Technologies, Xinjiang Academy of Agricultural Sciences, Urumqi, ChinaDepartment of Plant Pathology, China Agricultural University, Beijing, ChinaSchool of Food and Agriculture, University of Maine, Orono, ME, United StatesDepartment of Plant Pathology, China Agricultural University, Beijing, ChinaThe fungicide SYP-14288 has a high efficiency, low toxicity, and broad spectrum in inhibiting both fungi and oomycetes, but its mode of action (MoA) remains unclear on inhibiting fungi. In this study, the MoA was determined by analyzing the metabolism and respiratory activities of Rhizoctonia solani treated by SYP-14288. Wild-type strains and SYP-14288-resistant mutants of R. solani were incubated on potato dextrose agar amended with either SYP-14288 or one of select fungicides acting on fungal respiration, including complex I, II, and III inhibitors; uncouplers; and ATP synthase inhibitors. Mycelial growth was measured under fungicides treatments. ATP content was determined using an ATP assay kit, membrane potential of mitochondria was detected with the JC-1 kit, and respiratory rate was calculated based on the measurement of oxygen consumption of R. solani. A model of metabolic fingerprinting cluster was established to separate oxidation inhibitors and phosphorylation inhibitors. All the results together displayed a clear discrimination between oxidation inhibitors and phosphorylation inhibitors, and the latter inhibited ATP synthase production having or uncoupling activities. Based on the model, SYP-14288 was placed in phosphorylation inhibitor group, because it significantly reduced ATP content and membrane potential of mitochondria while increasing respiratory rate in R. solani. Therefore, the MoA of SYP-14288 on R. solani was confirmed to involve phosphorylation inhibition and possibly uncoupling activity.https://www.frontiersin.org/articles/10.3389/fmicb.2020.574039/fulluncouplerATP synthase inhibitormembrane potential of mitochondriarespiration inhibitorphosphorylation inhibitor
spellingShingle Li Liang
Xingkai Cheng
Tan Dai
Zhiwen Wang
Jin Li
Xueming Li
Bin Lei
Pengfei Liu
Jianjun Hao
Xili Liu
Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani
Frontiers in Microbiology
uncoupler
ATP synthase inhibitor
membrane potential of mitochondria
respiration inhibitor
phosphorylation inhibitor
title Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani
title_full Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani
title_fullStr Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani
title_full_unstemmed Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani
title_short Metabolic Fingerprinting for Identifying the Mode of Action of the Fungicide SYP-14288 on Rhizoctonia solani
title_sort metabolic fingerprinting for identifying the mode of action of the fungicide syp 14288 on rhizoctonia solani
topic uncoupler
ATP synthase inhibitor
membrane potential of mitochondria
respiration inhibitor
phosphorylation inhibitor
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.574039/full
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