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Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus

Gliotoxin (GT) is a fungal secondary metabolite that has attracted great interest due to its high biological activity since it was discovered by the 1930s. It exhibits a unique structure that contains a N-C = O group as the characteristics of the classical PSII inhibitor. However, GT’s phytotoxicity...

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Autores principales: Guo, Yanjing, Cheng, Jing, Lu, Yuping, Wang, He, Gao, Yazhi, Shi, Jiale, Yin, Cancan, Wang, Xiaoxiong, Chen, Shiguo, Strasser, Reto Jörg, Qiang, Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6999049/
https://www.ncbi.nlm.nih.gov/pubmed/32063907
http://dx.doi.org/10.3389/fpls.2019.01688
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author Guo, Yanjing
Cheng, Jing
Lu, Yuping
Wang, He
Gao, Yazhi
Shi, Jiale
Yin, Cancan
Wang, Xiaoxiong
Chen, Shiguo
Strasser, Reto Jörg
Qiang, Sheng
author_facet Guo, Yanjing
Cheng, Jing
Lu, Yuping
Wang, He
Gao, Yazhi
Shi, Jiale
Yin, Cancan
Wang, Xiaoxiong
Chen, Shiguo
Strasser, Reto Jörg
Qiang, Sheng
author_sort Guo, Yanjing
collection PubMed
description Gliotoxin (GT) is a fungal secondary metabolite that has attracted great interest due to its high biological activity since it was discovered by the 1930s. It exhibits a unique structure that contains a N-C = O group as the characteristics of the classical PSII inhibitor. However, GT’s phytotoxicity, herbicidal activity and primary action targets in plants remain hidden. Here, it is found that GT can cause brown or white leaf spot of various monocotyledonous and dicotyledonous plants, being regarded as a potential herbicidal agent. The multiple sites of GT action are located in two photosystems. GT decreases the rate of oxygen evolution of PSII with an I (50) value of 60 µM. Chlorophyll fluorescence data from Chlamydomonas reinhardtii cells and spinach thylakoids implicate that GT affects both PSII electron transport at the acceptor side and the reduction rate of PSI end electron acceptors’ pool. The major direct action target of GT is the plastoquinone Q(B)-site of the D1 protein in PSII, where GT inserts in the Q(B) binding niche by replacing native plastoquinone (PQ) and then interrupts electron flow beyond plastoquinone Q(A). This leads to severe inactivation of PSII RCs and a significant decrease of PSII overall photosynthetic activity. Based on the simulated modeling of GT docking to the D1 protein of spinach, it is proposed that GT binds to the-Q(B)-site through two hydrogen bonds between GT and D1-Ser264 and D1-His252. A hydrogen bond is formed between the aromatic hydroxyl oxygen of GT and the residue Ser264 in the D1 protein. The 4-carbonyl group of GT provides another hydrogen bond to the residue D1-His252. So, it is concluded that GT is a novel natural PSII inhibitor. In the future, GT may have the potential for development into a bioherbicide or being utilized as a lead compound to design more new derivatives.
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spelling pubmed-69990492020-02-14 Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus Guo, Yanjing Cheng, Jing Lu, Yuping Wang, He Gao, Yazhi Shi, Jiale Yin, Cancan Wang, Xiaoxiong Chen, Shiguo Strasser, Reto Jörg Qiang, Sheng Front Plant Sci Plant Science Gliotoxin (GT) is a fungal secondary metabolite that has attracted great interest due to its high biological activity since it was discovered by the 1930s. It exhibits a unique structure that contains a N-C = O group as the characteristics of the classical PSII inhibitor. However, GT’s phytotoxicity, herbicidal activity and primary action targets in plants remain hidden. Here, it is found that GT can cause brown or white leaf spot of various monocotyledonous and dicotyledonous plants, being regarded as a potential herbicidal agent. The multiple sites of GT action are located in two photosystems. GT decreases the rate of oxygen evolution of PSII with an I (50) value of 60 µM. Chlorophyll fluorescence data from Chlamydomonas reinhardtii cells and spinach thylakoids implicate that GT affects both PSII electron transport at the acceptor side and the reduction rate of PSI end electron acceptors’ pool. The major direct action target of GT is the plastoquinone Q(B)-site of the D1 protein in PSII, where GT inserts in the Q(B) binding niche by replacing native plastoquinone (PQ) and then interrupts electron flow beyond plastoquinone Q(A). This leads to severe inactivation of PSII RCs and a significant decrease of PSII overall photosynthetic activity. Based on the simulated modeling of GT docking to the D1 protein of spinach, it is proposed that GT binds to the-Q(B)-site through two hydrogen bonds between GT and D1-Ser264 and D1-His252. A hydrogen bond is formed between the aromatic hydroxyl oxygen of GT and the residue Ser264 in the D1 protein. The 4-carbonyl group of GT provides another hydrogen bond to the residue D1-His252. So, it is concluded that GT is a novel natural PSII inhibitor. In the future, GT may have the potential for development into a bioherbicide or being utilized as a lead compound to design more new derivatives. Frontiers Media S.A. 2020-01-17 /pmc/articles/PMC6999049/ /pubmed/32063907 http://dx.doi.org/10.3389/fpls.2019.01688 Text en Copyright © 2020 Guo, Cheng, Lu, Wang, Gao, Shi, Yin, Wang, Chen, Strasser and Qiang http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Guo, Yanjing
Cheng, Jing
Lu, Yuping
Wang, He
Gao, Yazhi
Shi, Jiale
Yin, Cancan
Wang, Xiaoxiong
Chen, Shiguo
Strasser, Reto Jörg
Qiang, Sheng
Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus
title Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus
title_full Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus
title_fullStr Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus
title_full_unstemmed Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus
title_short Novel Action Targets of Natural Product Gliotoxin in Photosynthetic Apparatus
title_sort novel action targets of natural product gliotoxin in photosynthetic apparatus
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6999049/
https://www.ncbi.nlm.nih.gov/pubmed/32063907
http://dx.doi.org/10.3389/fpls.2019.01688
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