Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i>
Leaf senescence accompanied by yellowing and Rubisco degradation occurs prematurely in response to various stresses. However, signaling pathways between stress perception and senescence responses are not understood fully, although previous studies suggest the involvement of reactive oxygen species (...
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| Format: | Article |
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MDPI AG
2022-08-01
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| Series: | Plants |
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| Online Access: | https://www.mdpi.com/2223-7747/11/17/2280 |
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| author | Md. Shyduzzaman Roni Md. Arif Sakil Most Mohoshena Aktar Chihiro Takatsuka Kyosuke Mukae Yuko Inoue-Aono Yuji Moriyasu |
| author_facet | Md. Shyduzzaman Roni Md. Arif Sakil Most Mohoshena Aktar Chihiro Takatsuka Kyosuke Mukae Yuko Inoue-Aono Yuji Moriyasu |
| author_sort | Md. Shyduzzaman Roni |
| collection | DOAJ |
| description | Leaf senescence accompanied by yellowing and Rubisco degradation occurs prematurely in response to various stresses. However, signaling pathways between stress perception and senescence responses are not understood fully, although previous studies suggest the involvement of reactive oxygen species (ROS). While investigating the physiological functions of autophagy in <i>Physcomitrium patens</i> using wild-type (WT) and autophagy-deficient <i>atg5</i> strains, we found that <i>Physcomitrium</i> colonies senesce prematurely under dark or nitrogen-deficient conditions, with <i>atg5</i> senescing earlier than WT. In the present study, we measured cellular H<sub>2</sub>O<sub>2</sub>, and examined whether H<sub>2</sub>O<sub>2</sub> mediates premature senescence in <i>Physcomitrium</i> colonies. Methyl viologen, an ROS generator, increased cellular H<sub>2</sub>O<sub>2</sub> levels and caused senescence-like symptoms. H<sub>2</sub>O<sub>2</sub> levels were also elevated to the same plateau levels in WT and <i>atg5</i> under dark or nitrogen-deficient conditions. The ROS scavenger N-acetylcysteine and the ROS source inhibitor carbonyl cyanide m-chlorophenylhydrazone inhibited the increase in H<sub>2</sub>O<sub>2</sub> levels as well as senescence. Upon transfer to a nitrogen-deficient medium, H<sub>2</sub>O<sub>2</sub> levels increased earlier in <i>atg5</i> than in WT by ~18 h, whereas <i>atg5</i> yellowed earlier by >2 days. We conclude that the increased H<sub>2</sub>O<sub>2</sub> levels under dark or nitrogen-deficient conditions mediate premature senescence in <i>Physcomitrium</i> but do not explain the different senescence responses of WT and <i>atg5</i> cells. |
| first_indexed | 2024-03-10T01:23:07Z |
| format | Article |
| id | doaj.art-95533f59e741486b949147417955799c |
| institution | Directory Open Access Journal |
| issn | 2223-7747 |
| language | English |
| last_indexed | 2024-03-10T01:23:07Z |
| publishDate | 2022-08-01 |
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| spelling | doaj.art-95533f59e741486b949147417955799c2023-11-23T13:56:01ZengMDPI AGPlants2223-77472022-08-011117228010.3390/plants11172280Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i>Md. Shyduzzaman Roni0Md. Arif Sakil1Most Mohoshena Aktar2Chihiro Takatsuka3Kyosuke Mukae4Yuko Inoue-Aono5Yuji Moriyasu6Graduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanSchool of Humanities, Tokai University, Shizuoka 424-8610, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanGraduate School of Science and Engineering, Saitama University, Saitama 338-8570, JapanLeaf senescence accompanied by yellowing and Rubisco degradation occurs prematurely in response to various stresses. However, signaling pathways between stress perception and senescence responses are not understood fully, although previous studies suggest the involvement of reactive oxygen species (ROS). While investigating the physiological functions of autophagy in <i>Physcomitrium patens</i> using wild-type (WT) and autophagy-deficient <i>atg5</i> strains, we found that <i>Physcomitrium</i> colonies senesce prematurely under dark or nitrogen-deficient conditions, with <i>atg5</i> senescing earlier than WT. In the present study, we measured cellular H<sub>2</sub>O<sub>2</sub>, and examined whether H<sub>2</sub>O<sub>2</sub> mediates premature senescence in <i>Physcomitrium</i> colonies. Methyl viologen, an ROS generator, increased cellular H<sub>2</sub>O<sub>2</sub> levels and caused senescence-like symptoms. H<sub>2</sub>O<sub>2</sub> levels were also elevated to the same plateau levels in WT and <i>atg5</i> under dark or nitrogen-deficient conditions. The ROS scavenger N-acetylcysteine and the ROS source inhibitor carbonyl cyanide m-chlorophenylhydrazone inhibited the increase in H<sub>2</sub>O<sub>2</sub> levels as well as senescence. Upon transfer to a nitrogen-deficient medium, H<sub>2</sub>O<sub>2</sub> levels increased earlier in <i>atg5</i> than in WT by ~18 h, whereas <i>atg5</i> yellowed earlier by >2 days. We conclude that the increased H<sub>2</sub>O<sub>2</sub> levels under dark or nitrogen-deficient conditions mediate premature senescence in <i>Physcomitrium</i> but do not explain the different senescence responses of WT and <i>atg5</i> cells.https://www.mdpi.com/2223-7747/11/17/2280senescencemethyl viologennitrogen starvationdarkH<sub>2</sub>O<sub>2</sub><i>Physcomitrium</i> |
| spellingShingle | Md. Shyduzzaman Roni Md. Arif Sakil Most Mohoshena Aktar Chihiro Takatsuka Kyosuke Mukae Yuko Inoue-Aono Yuji Moriyasu Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i> Plants senescence methyl viologen nitrogen starvation dark H<sub>2</sub>O<sub>2</sub> <i>Physcomitrium</i> |
| title | Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i> |
| title_full | Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i> |
| title_fullStr | Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i> |
| title_full_unstemmed | Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i> |
| title_short | Hydrogen Peroxide Mediates Premature Senescence Caused by Darkness and Inorganic Nitrogen Starvation in <i>Physcomitrium patens</i> |
| title_sort | hydrogen peroxide mediates premature senescence caused by darkness and inorganic nitrogen starvation in i physcomitrium patens i |
| topic | senescence methyl viologen nitrogen starvation dark H<sub>2</sub>O<sub>2</sub> <i>Physcomitrium</i> |
| url | https://www.mdpi.com/2223-7747/11/17/2280 |
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