Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide
Melatonin (MLT), an evolutionarily conserved pleiotropic molecule, is implicated in numerous physiological processes in plants and animals. However, the effects of MLT on microbes have seldom been reported. In this study, we examined the influence of exogenous MLT on the growth and hypocrellin biosy...
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| Format: | Article |
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MDPI AG
2022-08-01
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| Series: | Journal of Fungi |
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| Online Access: | https://www.mdpi.com/2309-608X/8/8/836 |
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| author | Wenjuan Wang Qunyan Huang Yue Wang Xinping Li Jianwen Wang Liping Zheng |
| author_facet | Wenjuan Wang Qunyan Huang Yue Wang Xinping Li Jianwen Wang Liping Zheng |
| author_sort | Wenjuan Wang |
| collection | DOAJ |
| description | Melatonin (MLT), an evolutionarily conserved pleiotropic molecule, is implicated in numerous physiological processes in plants and animals. However, the effects of MLT on microbes have seldom been reported. In this study, we examined the influence of exogenous MLT on the growth and hypocrellin biosynthesis of bambusicolous fungus <i>Shiraia</i> sp. S9. Hypocrellin A (HA) is a photoactivated and photoinduced perylenequinone (PQ) toxin in <i>Shiraia</i>. Exogenous MLT at 100.00 μM not only decreased fungal conidiation and spore germination but inhibited HA contents significantly in fungal cultures under a light/dark (24 h:24 h) shift. MLT treatment was associated with higher activity of antioxidant enzymes (superoxide dismutase, catalase and peroxidase) and a marked decline in reactive oxygen species (ROS) production in the mycelia. Moreover, MLT induced endogenous nitric oxide (NO) production during the culture. The NO donor sodium nitroprusside (SNP) potentiated MLT-induced inhibition of O<sub>2</sub><sup>−</sup> production, but NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) enhanced O<sub>2</sub><sup>−</sup> production, whereas MLT-induced NO level was increased by the ROS scavenger vitamin C (Vc). The changes in NO and H<sub>2</sub>O<sub>2</sub> were proved to be involved in the MLT-induced downregulation of the expressions of HA biosynthetic genes, leading to the suppression of HA production. This study provides new insight into the regulatory roles of MLT on fungal secondary metabolism activities and a basis for understanding self-resistance in phototoxin-producing fungi. |
| first_indexed | 2024-03-09T09:54:49Z |
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| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-09T09:54:49Z |
| publishDate | 2022-08-01 |
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| record_format | Article |
| series | Journal of Fungi |
| spelling | doaj.art-e7421710f4504603be89fd31561acf192023-12-01T23:52:18ZengMDPI AGJournal of Fungi2309-608X2022-08-018883610.3390/jof8080836Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric OxideWenjuan Wang0Qunyan Huang1Yue Wang2Xinping Li3Jianwen Wang4Liping Zheng5College of Pharmaceutical Sciences, Soochow University, Suzhou 215123, ChinaCollege of Pharmaceutical Sciences, Soochow University, Suzhou 215123, ChinaCollege of Pharmaceutical Sciences, Soochow University, Suzhou 215123, ChinaCollege of Pharmaceutical Sciences, Soochow University, Suzhou 215123, ChinaCollege of Pharmaceutical Sciences, Soochow University, Suzhou 215123, ChinaDepartment of Horticultural Sciences, Soochow University, Suzhou 215123, ChinaMelatonin (MLT), an evolutionarily conserved pleiotropic molecule, is implicated in numerous physiological processes in plants and animals. However, the effects of MLT on microbes have seldom been reported. In this study, we examined the influence of exogenous MLT on the growth and hypocrellin biosynthesis of bambusicolous fungus <i>Shiraia</i> sp. S9. Hypocrellin A (HA) is a photoactivated and photoinduced perylenequinone (PQ) toxin in <i>Shiraia</i>. Exogenous MLT at 100.00 μM not only decreased fungal conidiation and spore germination but inhibited HA contents significantly in fungal cultures under a light/dark (24 h:24 h) shift. MLT treatment was associated with higher activity of antioxidant enzymes (superoxide dismutase, catalase and peroxidase) and a marked decline in reactive oxygen species (ROS) production in the mycelia. Moreover, MLT induced endogenous nitric oxide (NO) production during the culture. The NO donor sodium nitroprusside (SNP) potentiated MLT-induced inhibition of O<sub>2</sub><sup>−</sup> production, but NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) enhanced O<sub>2</sub><sup>−</sup> production, whereas MLT-induced NO level was increased by the ROS scavenger vitamin C (Vc). The changes in NO and H<sub>2</sub>O<sub>2</sub> were proved to be involved in the MLT-induced downregulation of the expressions of HA biosynthetic genes, leading to the suppression of HA production. This study provides new insight into the regulatory roles of MLT on fungal secondary metabolism activities and a basis for understanding self-resistance in phototoxin-producing fungi.https://www.mdpi.com/2309-608X/8/8/836melatonin<i>Shiraia</i>hypocrellinreactive oxygen speciesnitric oxide |
| spellingShingle | Wenjuan Wang Qunyan Huang Yue Wang Xinping Li Jianwen Wang Liping Zheng Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide Journal of Fungi melatonin <i>Shiraia</i> hypocrellin reactive oxygen species nitric oxide |
| title | Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide |
| title_full | Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide |
| title_fullStr | Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide |
| title_full_unstemmed | Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide |
| title_short | Melatonin-Induced Inhibition of <i>Shiraia</i> Hypocrellin A Biosynthesis Is Mediated by Hydrogen Peroxide and Nitric Oxide |
| title_sort | melatonin induced inhibition of i shiraia i hypocrellin a biosynthesis is mediated by hydrogen peroxide and nitric oxide |
| topic | melatonin <i>Shiraia</i> hypocrellin reactive oxygen species nitric oxide |
| url | https://www.mdpi.com/2309-608X/8/8/836 |
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