Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis.
Ubiquitin-mediated proteolysis plays crucial roles in plant responses to environmental stress. However, the mechanism by which E3 ubiquitin ligases modulate plant stress response still needs to be elucidated. In this study, we found that rice PLANT U-BOX PROTEIN 16 (OsPUB16), a U-box E3 ubiquitin li...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-11-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1010520 |
| _version_ | 1797973917267132416 |
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| author | Qianlong Lv Xingxing Li Xinkai Jin Ying Sun Yuanyuan Wu Wanmin Wang Junli Huang |
| author_facet | Qianlong Lv Xingxing Li Xinkai Jin Ying Sun Yuanyuan Wu Wanmin Wang Junli Huang |
| author_sort | Qianlong Lv |
| collection | DOAJ |
| description | Ubiquitin-mediated proteolysis plays crucial roles in plant responses to environmental stress. However, the mechanism by which E3 ubiquitin ligases modulate plant stress response still needs to be elucidated. In this study, we found that rice PLANT U-BOX PROTEIN 16 (OsPUB16), a U-box E3 ubiquitin ligase, negatively regulates rice drought response. Loss-of-function mutants of OsPUB16 generated through CRISPR/Cas9 system exhibited the markedly enhanced water-deficit tolerance, while OsPUB16 overexpression lines were hypersensitive to water deficit stress. Moreover, OsPUB16 negatively regulated ABA and JA response, and ospub16 mutants produced more endogenous ABA and JA than wild type when exposed to water deficit. Mechanistic investigations revealed that OsPUB16 mediated the ubiquitination and degradation of OsMADS23, which is the substrate of OSMOTIC STRESS/ABA-ACTIVATED PROTEIN KINASE 9 (SAPK9) and increases rice drought tolerance by promoting ABA biosynthesis. Further, the ChIP-qPCR analysis and transient transactivation activity assays demonstrated that OsMADS23 activated the expression of JA-biosynthetic gene OsAOC by binding to its promoter. Interestingly, SAPK9-mediated phosphorylation on OsMADS23 reduced its ubiquitination level by interfering with the OsPUB16-OsMADS23 interaction, which thus enhanced OsMADS23 stability and promoted OsAOC expression. Collectively, our findings establish that OsPUB16 reduces plant water-deficit tolerance by modulating the 'SAPK9-OsMADS23-OsAOC' pathway to repress ABA and JA biosynthesis. |
| first_indexed | 2024-04-11T04:11:47Z |
| format | Article |
| id | doaj.art-57fb331bc2aa42d89fcefecef916f429 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-11T04:11:47Z |
| publishDate | 2022-11-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-57fb331bc2aa42d89fcefecef916f4292023-01-01T05:32:04ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042022-11-011811e101052010.1371/journal.pgen.1010520Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis.Qianlong LvXingxing LiXinkai JinYing SunYuanyuan WuWanmin WangJunli HuangUbiquitin-mediated proteolysis plays crucial roles in plant responses to environmental stress. However, the mechanism by which E3 ubiquitin ligases modulate plant stress response still needs to be elucidated. In this study, we found that rice PLANT U-BOX PROTEIN 16 (OsPUB16), a U-box E3 ubiquitin ligase, negatively regulates rice drought response. Loss-of-function mutants of OsPUB16 generated through CRISPR/Cas9 system exhibited the markedly enhanced water-deficit tolerance, while OsPUB16 overexpression lines were hypersensitive to water deficit stress. Moreover, OsPUB16 negatively regulated ABA and JA response, and ospub16 mutants produced more endogenous ABA and JA than wild type when exposed to water deficit. Mechanistic investigations revealed that OsPUB16 mediated the ubiquitination and degradation of OsMADS23, which is the substrate of OSMOTIC STRESS/ABA-ACTIVATED PROTEIN KINASE 9 (SAPK9) and increases rice drought tolerance by promoting ABA biosynthesis. Further, the ChIP-qPCR analysis and transient transactivation activity assays demonstrated that OsMADS23 activated the expression of JA-biosynthetic gene OsAOC by binding to its promoter. Interestingly, SAPK9-mediated phosphorylation on OsMADS23 reduced its ubiquitination level by interfering with the OsPUB16-OsMADS23 interaction, which thus enhanced OsMADS23 stability and promoted OsAOC expression. Collectively, our findings establish that OsPUB16 reduces plant water-deficit tolerance by modulating the 'SAPK9-OsMADS23-OsAOC' pathway to repress ABA and JA biosynthesis.https://doi.org/10.1371/journal.pgen.1010520 |
| spellingShingle | Qianlong Lv Xingxing Li Xinkai Jin Ying Sun Yuanyuan Wu Wanmin Wang Junli Huang Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. PLoS Genetics |
| title | Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. |
| title_full | Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. |
| title_fullStr | Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. |
| title_full_unstemmed | Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. |
| title_short | Rice OsPUB16 modulates the 'SAPK9-OsMADS23-OsAOC' pathway to reduce plant water-deficit tolerance by repressing ABA and JA biosynthesis. |
| title_sort | rice ospub16 modulates the sapk9 osmads23 osaoc pathway to reduce plant water deficit tolerance by repressing aba and ja biosynthesis |
| url | https://doi.org/10.1371/journal.pgen.1010520 |
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