Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress
The acclimation mechanism of Chlamydomonas reinhardtii to nitric oxide (NO) was studied by exposure to S-nitroso-N-acetylpenicillamine (SNAP), a NO donor. Treatment with 0.1 or 0.3 mM SNAP transiently inhibited photosynthesis within 1 h, followed by a recovery, while 1.0 mM SNAP treatment caused irr...
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| Format: | Article |
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Frontiers Media S.A.
2021-08-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2021.690763/full |
| _version_ | 1818691854133100544 |
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| author | Eva YuHua Kuo Tse-Min Lee Tse-Min Lee |
| author_facet | Eva YuHua Kuo Tse-Min Lee Tse-Min Lee |
| author_sort | Eva YuHua Kuo |
| collection | DOAJ |
| description | The acclimation mechanism of Chlamydomonas reinhardtii to nitric oxide (NO) was studied by exposure to S-nitroso-N-acetylpenicillamine (SNAP), a NO donor. Treatment with 0.1 or 0.3 mM SNAP transiently inhibited photosynthesis within 1 h, followed by a recovery, while 1.0 mM SNAP treatment caused irreversible photosynthesis inhibition and mortality. The SNAP effects are avoided in the presence of the NO scavenger, 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-l-oxyl-3-oxide (cPTIO). RNA-seq, qPCR, and biochemical analyses were conducted to decode the metabolic shifts under NO stress by exposure to 0.3 mM SNAP in the presence or absence of 0.4 mM cPTIO. These findings revealed that the acclimation to NO stress comprises a temporally orchestrated implementation of metabolic processes: (1). modulation of NADPH oxidase (respiratory burst oxidase-like 2, RBOL2) and ROS signaling pathways for downstream mechanism regulation, (2). trigger of NO scavenging elements to reduce NO level; (3). prevention of photo-oxidative risk through photosynthesis inhibition and antioxidant defense system induction; (4). acclimation to nitrogen and sulfur shortage; (5). attenuation of transcriptional and translational activity together with degradation of damaged proteins through protein trafficking machinery (ubiquitin, SNARE, and autophagy) and molecular chaperone system for dynamic regulation of protein homeostasis. In addition, the expression of the gene encoding NADPH oxidase, RBOL2, showed a transient increase while that of RBOL1 was slightly decreased after NO challenge. It reflects that NADPH oxidase, a regulator in ROS-mediated signaling pathway, may be involved in the responses of Chlamydomonas to NO stress. In conclusion, our findings provide insight into the molecular events underlying acclimation mechanisms in Chlamydomonas to NO stress. |
| first_indexed | 2024-12-17T12:48:30Z |
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| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-17T12:48:30Z |
| publishDate | 2021-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-df431eb8080042a185fce569d960c6b62022-12-21T21:47:40ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-08-011210.3389/fpls.2021.690763690763Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide StressEva YuHua Kuo0Tse-Min Lee1Tse-Min Lee2Department of Marine Biotechnology and Resources, National Sun Yat-sen University, Kaohsiung, TaiwanDepartment of Marine Biotechnology and Resources, National Sun Yat-sen University, Kaohsiung, TaiwanDoctoral Degree Program in Marine Biotechnology, National Sun Yat-sen University, Kaohsiung, TaiwanThe acclimation mechanism of Chlamydomonas reinhardtii to nitric oxide (NO) was studied by exposure to S-nitroso-N-acetylpenicillamine (SNAP), a NO donor. Treatment with 0.1 or 0.3 mM SNAP transiently inhibited photosynthesis within 1 h, followed by a recovery, while 1.0 mM SNAP treatment caused irreversible photosynthesis inhibition and mortality. The SNAP effects are avoided in the presence of the NO scavenger, 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-l-oxyl-3-oxide (cPTIO). RNA-seq, qPCR, and biochemical analyses were conducted to decode the metabolic shifts under NO stress by exposure to 0.3 mM SNAP in the presence or absence of 0.4 mM cPTIO. These findings revealed that the acclimation to NO stress comprises a temporally orchestrated implementation of metabolic processes: (1). modulation of NADPH oxidase (respiratory burst oxidase-like 2, RBOL2) and ROS signaling pathways for downstream mechanism regulation, (2). trigger of NO scavenging elements to reduce NO level; (3). prevention of photo-oxidative risk through photosynthesis inhibition and antioxidant defense system induction; (4). acclimation to nitrogen and sulfur shortage; (5). attenuation of transcriptional and translational activity together with degradation of damaged proteins through protein trafficking machinery (ubiquitin, SNARE, and autophagy) and molecular chaperone system for dynamic regulation of protein homeostasis. In addition, the expression of the gene encoding NADPH oxidase, RBOL2, showed a transient increase while that of RBOL1 was slightly decreased after NO challenge. It reflects that NADPH oxidase, a regulator in ROS-mediated signaling pathway, may be involved in the responses of Chlamydomonas to NO stress. In conclusion, our findings provide insight into the molecular events underlying acclimation mechanisms in Chlamydomonas to NO stress.https://www.frontiersin.org/articles/10.3389/fpls.2021.690763/fullacclimationantioxidant defense systemChlamydomonas reinhardtiimembrane trafficking systemnitrogen homeostasisnitrosative stress |
| spellingShingle | Eva YuHua Kuo Tse-Min Lee Tse-Min Lee Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress Frontiers in Plant Science acclimation antioxidant defense system Chlamydomonas reinhardtii membrane trafficking system nitrogen homeostasis nitrosative stress |
| title | Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress |
| title_full | Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress |
| title_fullStr | Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress |
| title_full_unstemmed | Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress |
| title_short | Molecular Mechanisms Underlying the Acclimation of Chlamydomonas reinhardtii Against Nitric Oxide Stress |
| title_sort | molecular mechanisms underlying the acclimation of chlamydomonas reinhardtii against nitric oxide stress |
| topic | acclimation antioxidant defense system Chlamydomonas reinhardtii membrane trafficking system nitrogen homeostasis nitrosative stress |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2021.690763/full |
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