HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia

Mycelial ageing is associated with ROS and autophagy in <i>Lentinula edodes</i>. However, the underlying cellular and molecular mechanisms between ROS and autophagy remain obscure. This study induced autophagy in <i>L. edodes</i> mycelia through exogenous H<sub>2</su...

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Main Authors: Dong Yan, Yangyang Fan, Shuang Song, Yuan Guo, Yu Liu, Xiaoling Xu, Fang Liu, Qi Gao, Shouxian Wang
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/9/4/413
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author Dong Yan
Yangyang Fan
Shuang Song
Yuan Guo
Yu Liu
Xiaoling Xu
Fang Liu
Qi Gao
Shouxian Wang
author_facet Dong Yan
Yangyang Fan
Shuang Song
Yuan Guo
Yu Liu
Xiaoling Xu
Fang Liu
Qi Gao
Shouxian Wang
author_sort Dong Yan
collection DOAJ
description Mycelial ageing is associated with ROS and autophagy in <i>Lentinula edodes</i>. However, the underlying cellular and molecular mechanisms between ROS and autophagy remain obscure. This study induced autophagy in <i>L. edodes</i> mycelia through exogenous H<sub>2</sub>O<sub>2</sub> treatment. Results showed that 100 μM H<sub>2</sub>O<sub>2</sub> treatment for 24 h significantly inhibited mycelial growth. H<sub>2</sub>O<sub>2</sub> caused the depolarisation of MMP and accumulation of TUNEL-positive nuclei, which was similar to the ageing phenotype of <i>L. edodes</i> mycelia. Transcriptome analysis showed that differentially expressed genes were enriched in the mitophagic, autophagic, and MAPK pathways. <i>LeAtg8</i> and <i>LeHog1</i> were selected as hub genes. RNA and protein levels of LeATG8 increased in the H<sub>2</sub>O<sub>2</sub>-treated mycelia. Using fluorescent labelling, we observed for the first time the classic ring structure of autophagosomes in a mushroom, while 3D imaging suggested that these autophagosomes surrounded the nuclei to degrade them at specific growth stages. Phospho-LeHOG1 protein can translocate from the cytoplasm to the nucleus to regulate mycelial cells, resisting ROS-induced oxidative stress. Furthermore, LeATG8 expression was suppressed when LeHOG1 phosphorylation was inhibited. These results suggest that the LeATG8-dependent autophagy in <i>L. edodes</i> mycelial is closely associated with the activity or even phosphorylation of LeHOG1.
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spelling doaj.art-d219c95816024741b168e399a0fde7f12023-11-17T19:57:48ZengMDPI AGJournal of Fungi2309-608X2023-03-019441310.3390/jof9040413HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> MyceliaDong Yan0Yangyang Fan1Shuang Song2Yuan Guo3Yu Liu4Xiaoling Xu5Fang Liu6Qi Gao7Shouxian Wang8Institute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaInstitute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaInstitute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaInstitute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaInstitute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaCollege of Agriculture and Food Engineering, Baise University, 21 Zhongshan Second Street, Youjiang District, Baise 533000, ChinaCollege of Agriculture and Food Engineering, Baise University, 21 Zhongshan Second Street, Youjiang District, Baise 533000, ChinaInstitute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaInstitute of Plant Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing Engineering Research Center for Edible Mushroom, 9 Shuguang Garden Zhonglu, Haidian District, Beijing 100097, ChinaMycelial ageing is associated with ROS and autophagy in <i>Lentinula edodes</i>. However, the underlying cellular and molecular mechanisms between ROS and autophagy remain obscure. This study induced autophagy in <i>L. edodes</i> mycelia through exogenous H<sub>2</sub>O<sub>2</sub> treatment. Results showed that 100 μM H<sub>2</sub>O<sub>2</sub> treatment for 24 h significantly inhibited mycelial growth. H<sub>2</sub>O<sub>2</sub> caused the depolarisation of MMP and accumulation of TUNEL-positive nuclei, which was similar to the ageing phenotype of <i>L. edodes</i> mycelia. Transcriptome analysis showed that differentially expressed genes were enriched in the mitophagic, autophagic, and MAPK pathways. <i>LeAtg8</i> and <i>LeHog1</i> were selected as hub genes. RNA and protein levels of LeATG8 increased in the H<sub>2</sub>O<sub>2</sub>-treated mycelia. Using fluorescent labelling, we observed for the first time the classic ring structure of autophagosomes in a mushroom, while 3D imaging suggested that these autophagosomes surrounded the nuclei to degrade them at specific growth stages. Phospho-LeHOG1 protein can translocate from the cytoplasm to the nucleus to regulate mycelial cells, resisting ROS-induced oxidative stress. Furthermore, LeATG8 expression was suppressed when LeHOG1 phosphorylation was inhibited. These results suggest that the LeATG8-dependent autophagy in <i>L. edodes</i> mycelial is closely associated with the activity or even phosphorylation of LeHOG1.https://www.mdpi.com/2309-608X/9/4/413<i>Lentinula edodes</i>H<sub>2</sub>O<sub>2</sub>autophagyLeATG8LeHOG1
spellingShingle Dong Yan
Yangyang Fan
Shuang Song
Yuan Guo
Yu Liu
Xiaoling Xu
Fang Liu
Qi Gao
Shouxian Wang
HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia
Journal of Fungi
<i>Lentinula edodes</i>
H<sub>2</sub>O<sub>2</sub>
autophagy
LeATG8
LeHOG1
title HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia
title_full HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia
title_fullStr HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia
title_full_unstemmed HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia
title_short HOG1 Mitogen-Activated Protein Kinase Pathway–Related Autophagy Induced by H<sub>2</sub>O<sub>2</sub> in <i>Lentinula edodes</i> Mycelia
title_sort hog1 mitogen activated protein kinase pathway related autophagy induced by h sub 2 sub o sub 2 sub in i lentinula edodes i mycelia
topic <i>Lentinula edodes</i>
H<sub>2</sub>O<sub>2</sub>
autophagy
LeATG8
LeHOG1
url https://www.mdpi.com/2309-608X/9/4/413
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