Pepper ubiquitin‐specific protease, CaUBP12, positively modulates dehydration resistance by enhancing CaSnRK2.6 stability
SUMMARY Abscisic acid (ABA) is a plant hormone that activates adaptive mechanisms to environmental stress conditions. Plant adaptive mechanisms are complex and highly modulated processes induced by stress‐responsive proteins; however, the precise mechanisms by which these processes function under ad...
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| Veröffentlicht in: | The Plant journal : for cell and molecular biology 2021-08, Vol.107 (4), p.1148-1165 |
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| container_title | The Plant journal : for cell and molecular biology |
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| creator | Lim, Chae Woo Baek, Woonhee Lim, Junsub Hong, Eunji Lee, Sung Chul |
| description | SUMMARY
Abscisic acid (ABA) is a plant hormone that activates adaptive mechanisms to environmental stress conditions. Plant adaptive mechanisms are complex and highly modulated processes induced by stress‐responsive proteins; however, the precise mechanisms by which these processes function under adverse conditions remain unclear. Here, we isolated CaUBP12 (Capsicum annuum ubiquitin‐specific protease 12) from pepper (C. annuum) leaves. We show that CaUBP12 expression is significantly induced after exposure to abiotic stress treatments. We conducted loss‐of‐function and gain‐of‐function genetic studies to elucidate the biological functions of CaUBP12 in response to ABA and dehydration stress. CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively; these phenotypes were characterized by regulation of transpirational water loss and stomatal aperture. Under dehydration stress conditions, CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants exhibited lower and higher expression levels of stress‐related genes, respectively, than the control plants. We isolated a CaUBP12 interaction protein, CaSnRK2.6, which is a homolog of Arabidopsis OST1; degradation of this protein was partially inhibited by CaUBP12. Similar to CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants, CaSnRK2.6‐silenced pepper plants and CaSnRK2.6‐overexpressing Arabidopsis displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively. Our findings suggest that CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation.
Significance Statement
This study reports the functional characterization of CaUBP12 in response to dehydration stress. CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation. This study provides insight into the involvement of UBPs in the dehydration stress response, including modulation of transpirational water loss, stomatal aperture, and stress‐related gene expression. |
| doi_str_mv | 10.1111/tpj.15374 |
| format | Article |
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Abscisic acid (ABA) is a plant hormone that activates adaptive mechanisms to environmental stress conditions. Plant adaptive mechanisms are complex and highly modulated processes induced by stress‐responsive proteins; however, the precise mechanisms by which these processes function under adverse conditions remain unclear. Here, we isolated CaUBP12 (Capsicum annuum ubiquitin‐specific protease 12) from pepper (C. annuum) leaves. We show that CaUBP12 expression is significantly induced after exposure to abiotic stress treatments. We conducted loss‐of‐function and gain‐of‐function genetic studies to elucidate the biological functions of CaUBP12 in response to ABA and dehydration stress. CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively; these phenotypes were characterized by regulation of transpirational water loss and stomatal aperture. Under dehydration stress conditions, CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants exhibited lower and higher expression levels of stress‐related genes, respectively, than the control plants. We isolated a CaUBP12 interaction protein, CaSnRK2.6, which is a homolog of Arabidopsis OST1; degradation of this protein was partially inhibited by CaUBP12. Similar to CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants, CaSnRK2.6‐silenced pepper plants and CaSnRK2.6‐overexpressing Arabidopsis displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively. Our findings suggest that CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation.
Significance Statement
This study reports the functional characterization of CaUBP12 in response to dehydration stress. CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation. This study provides insight into the involvement of UBPs in the dehydration stress response, including modulation of transpirational water loss, stomatal aperture, and stress‐related gene expression.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.15374</identifier><identifier>PMID: 34145668</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Abscisic acid ; Abscisic Acid - pharmacology ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Biodegradation ; Capsicum - physiology ; Capsicum annuum ; CaUBP12 ; Degradation ; Dehydration ; Dehydration - genetics ; dehydration stress ; Environmental conditions ; Environmental stress ; Gene Expression Regulation, Plant ; Germination - drug effects ; Homology ; Mutation ; pepper ; Peppers ; Phenotypes ; Plant hormones ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified ; Protease ; Protein Kinases - genetics ; Protein Stability ; Proteinase ; Proteins ; Seeds - drug effects ; Seeds - physiology ; Stomata ; Transpiration ; Ubiquitin ; Ubiquitin-Specific Proteases - genetics ; Ubiquitin-Specific Proteases - metabolism ; Vegetables ; virus‐induced gene silencing ; Water loss</subject><ispartof>The Plant journal : for cell and molecular biology, 2021-08, Vol.107 (4), p.1148-1165</ispartof><rights>2021 Society for Experimental Biology and John Wiley & Sons Ltd</rights><rights>2021 Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2021 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3884-c457b79a274c915f4839719a348b995a404967e145181c177769300f5347a3733</citedby><cites>FETCH-LOGICAL-c3884-c457b79a274c915f4839719a348b995a404967e145181c177769300f5347a3733</cites><orcidid>0000-0003-2725-0854</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.15374$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.15374$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34145668$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lim, Chae Woo</creatorcontrib><creatorcontrib>Baek, Woonhee</creatorcontrib><creatorcontrib>Lim, Junsub</creatorcontrib><creatorcontrib>Hong, Eunji</creatorcontrib><creatorcontrib>Lee, Sung Chul</creatorcontrib><title>Pepper ubiquitin‐specific protease, CaUBP12, positively modulates dehydration resistance by enhancing CaSnRK2.6 stability</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Abscisic acid (ABA) is a plant hormone that activates adaptive mechanisms to environmental stress conditions. Plant adaptive mechanisms are complex and highly modulated processes induced by stress‐responsive proteins; however, the precise mechanisms by which these processes function under adverse conditions remain unclear. Here, we isolated CaUBP12 (Capsicum annuum ubiquitin‐specific protease 12) from pepper (C. annuum) leaves. We show that CaUBP12 expression is significantly induced after exposure to abiotic stress treatments. We conducted loss‐of‐function and gain‐of‐function genetic studies to elucidate the biological functions of CaUBP12 in response to ABA and dehydration stress. CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively; these phenotypes were characterized by regulation of transpirational water loss and stomatal aperture. Under dehydration stress conditions, CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants exhibited lower and higher expression levels of stress‐related genes, respectively, than the control plants. We isolated a CaUBP12 interaction protein, CaSnRK2.6, which is a homolog of Arabidopsis OST1; degradation of this protein was partially inhibited by CaUBP12. Similar to CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants, CaSnRK2.6‐silenced pepper plants and CaSnRK2.6‐overexpressing Arabidopsis displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively. Our findings suggest that CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation.
Significance Statement
This study reports the functional characterization of CaUBP12 in response to dehydration stress. CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation. This study provides insight into the involvement of UBPs in the dehydration stress response, including modulation of transpirational water loss, stomatal aperture, and stress‐related gene expression.</description><subject>Abscisic acid</subject><subject>Abscisic Acid - pharmacology</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Biodegradation</subject><subject>Capsicum - physiology</subject><subject>Capsicum annuum</subject><subject>CaUBP12</subject><subject>Degradation</subject><subject>Dehydration</subject><subject>Dehydration - genetics</subject><subject>dehydration stress</subject><subject>Environmental conditions</subject><subject>Environmental stress</subject><subject>Gene Expression Regulation, Plant</subject><subject>Germination - drug effects</subject><subject>Homology</subject><subject>Mutation</subject><subject>pepper</subject><subject>Peppers</subject><subject>Phenotypes</subject><subject>Plant hormones</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Protease</subject><subject>Protein Kinases - genetics</subject><subject>Protein Stability</subject><subject>Proteinase</subject><subject>Proteins</subject><subject>Seeds - drug effects</subject><subject>Seeds - physiology</subject><subject>Stomata</subject><subject>Transpiration</subject><subject>Ubiquitin</subject><subject>Ubiquitin-Specific Proteases - genetics</subject><subject>Ubiquitin-Specific Proteases - metabolism</subject><subject>Vegetables</subject><subject>virus‐induced gene silencing</subject><subject>Water loss</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc1O3DAURi1ExUyBRV-gssSGSmTGjh07XrajlraMxIgfiV3kODcdjzJJsBOqqBsegWfkSeoSYFGJu_GVfHTkzx9CHyiZ0TDzrt3MaMIk30FTykQSMcpudtGUKEEiyWk8Qe-93xBCJRN8D00YpzwRIp2iPytoW3C4z-1tbztbP94_-BaMLa3BrWs60B5O8EJff1nR-AS3jQ_UHVQD3jZFX-kOPC5gPRROd7apsQNvfadrAzgfMNTrsNr6VzBc1hdn8UzgcJvbynbDAXpX6srD4fO5j66_fb1afI-W56c_Fp-XkWFpyiPDE5lLpWPJjaJJyVOmJFWa8TRXKtGccCUkhEQ0pYZKKYVihJQJ41Izydg-Oh69Ic9tD77LttYbqCpdQ9P7LE4445zFKQno0X_opuldHV4XKKHCf4on4aeRMq7x3kGZtc5utRsySrJ_jWShkeypkcB-fDb2-RaKV_KlggDMR-C3rWB425RdrX6Oyr8st5R9</recordid><startdate>202108</startdate><enddate>202108</enddate><creator>Lim, Chae Woo</creator><creator>Baek, Woonhee</creator><creator>Lim, Junsub</creator><creator>Hong, Eunji</creator><creator>Lee, Sung Chul</creator><general>Blackwell Publishing Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-2725-0854</orcidid></search><sort><creationdate>202108</creationdate><title>Pepper ubiquitin‐specific protease, CaUBP12, positively modulates dehydration resistance by enhancing CaSnRK2.6 stability</title><author>Lim, Chae Woo ; Baek, Woonhee ; Lim, Junsub ; Hong, Eunji ; Lee, Sung Chul</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3884-c457b79a274c915f4839719a348b995a404967e145181c177769300f5347a3733</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abscisic acid</topic><topic>Abscisic Acid - pharmacology</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Biodegradation</topic><topic>Capsicum - physiology</topic><topic>Capsicum annuum</topic><topic>CaUBP12</topic><topic>Degradation</topic><topic>Dehydration</topic><topic>Dehydration - genetics</topic><topic>dehydration stress</topic><topic>Environmental conditions</topic><topic>Environmental stress</topic><topic>Gene Expression Regulation, Plant</topic><topic>Germination - drug effects</topic><topic>Homology</topic><topic>Mutation</topic><topic>pepper</topic><topic>Peppers</topic><topic>Phenotypes</topic><topic>Plant hormones</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Protease</topic><topic>Protein Kinases - genetics</topic><topic>Protein Stability</topic><topic>Proteinase</topic><topic>Proteins</topic><topic>Seeds - drug effects</topic><topic>Seeds - physiology</topic><topic>Stomata</topic><topic>Transpiration</topic><topic>Ubiquitin</topic><topic>Ubiquitin-Specific Proteases - genetics</topic><topic>Ubiquitin-Specific Proteases - metabolism</topic><topic>Vegetables</topic><topic>virus‐induced gene silencing</topic><topic>Water loss</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lim, Chae Woo</creatorcontrib><creatorcontrib>Baek, Woonhee</creatorcontrib><creatorcontrib>Lim, Junsub</creatorcontrib><creatorcontrib>Hong, Eunji</creatorcontrib><creatorcontrib>Lee, Sung Chul</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lim, Chae Woo</au><au>Baek, Woonhee</au><au>Lim, Junsub</au><au>Hong, Eunji</au><au>Lee, Sung Chul</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pepper ubiquitin‐specific protease, CaUBP12, positively modulates dehydration resistance by enhancing CaSnRK2.6 stability</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2021-08</date><risdate>2021</risdate><volume>107</volume><issue>4</issue><spage>1148</spage><epage>1165</epage><pages>1148-1165</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Abscisic acid (ABA) is a plant hormone that activates adaptive mechanisms to environmental stress conditions. Plant adaptive mechanisms are complex and highly modulated processes induced by stress‐responsive proteins; however, the precise mechanisms by which these processes function under adverse conditions remain unclear. Here, we isolated CaUBP12 (Capsicum annuum ubiquitin‐specific protease 12) from pepper (C. annuum) leaves. We show that CaUBP12 expression is significantly induced after exposure to abiotic stress treatments. We conducted loss‐of‐function and gain‐of‐function genetic studies to elucidate the biological functions of CaUBP12 in response to ABA and dehydration stress. CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively; these phenotypes were characterized by regulation of transpirational water loss and stomatal aperture. Under dehydration stress conditions, CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants exhibited lower and higher expression levels of stress‐related genes, respectively, than the control plants. We isolated a CaUBP12 interaction protein, CaSnRK2.6, which is a homolog of Arabidopsis OST1; degradation of this protein was partially inhibited by CaUBP12. Similar to CaUBP12‐silenced pepper plants and CaUBP12‐overexpressing Arabidopsis plants, CaSnRK2.6‐silenced pepper plants and CaSnRK2.6‐overexpressing Arabidopsis displayed dehydration‐sensitive and dehydration‐tolerant phenotypes, respectively. Our findings suggest that CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation.
Significance Statement
This study reports the functional characterization of CaUBP12 in response to dehydration stress. CaUBP12 positively modulates the dehydration stress response by suppressing CaSnRK2.6 protein degradation. This study provides insight into the involvement of UBPs in the dehydration stress response, including modulation of transpirational water loss, stomatal aperture, and stress‐related gene expression.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>34145668</pmid><doi>10.1111/tpj.15374</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0003-2725-0854</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Abscisic acid Abscisic Acid - pharmacology Arabidopsis Arabidopsis - genetics Arabidopsis - physiology Arabidopsis Proteins - genetics Biodegradation Capsicum - physiology Capsicum annuum CaUBP12 Degradation Dehydration Dehydration - genetics dehydration stress Environmental conditions Environmental stress Gene Expression Regulation, Plant Germination - drug effects Homology Mutation pepper Peppers Phenotypes Plant hormones Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified Protease Protein Kinases - genetics Protein Stability Proteinase Proteins Seeds - drug effects Seeds - physiology Stomata Transpiration Ubiquitin Ubiquitin-Specific Proteases - genetics Ubiquitin-Specific Proteases - metabolism Vegetables virus‐induced gene silencing Water loss |
| title | Pepper ubiquitin‐specific protease, CaUBP12, positively modulates dehydration resistance by enhancing CaSnRK2.6 stability |
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