Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling
The phytohormone abscisic acid (ABA) regulates plant growth, development and responses to biotic and abiotic stresses. The core ABA signaling pathway consists of three major components: ABA receptor (PYR1/PYLs), type 2C Protein Phosphatase (PP2C) and SNF1-related protein kinase 2 (SnRK2). Neverthele...
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| creator | Hou, Yueh-Ju Zhu, Yingfang Wang, Pengcheng Zhao, Yang Xie, Shaojun Batelli, Giorgia Wang, Bangshing Duan, Cheng-Guo Wang, Xingang Xing, Lu Lei, Mingguang Yan, Jun Zhu, Xiaohong Zhu, Jian-Kang |
| description | The phytohormone abscisic acid (ABA) regulates plant growth, development and responses to biotic and abiotic stresses. The core ABA signaling pathway consists of three major components: ABA receptor (PYR1/PYLs), type 2C Protein Phosphatase (PP2C) and SNF1-related protein kinase 2 (SnRK2). Nevertheless, the complexity of ABA signaling remains to be explored. To uncover new components of ABA signal transduction pathways, we performed a yeast two-hybrid screen for SnRK2-interacting proteins. We found that Type One Protein Phosphatase 1 (TOPP1) and its regulatory protein, At Inhibitor-2 (AtI-2), physically interact with SnRK2s and also with PYLs. TOPP1 inhibited the kinase activity of SnRK2.6, and this inhibition could be enhanced by AtI-2. Transactivation assays showed that TOPP1 and AtI-2 negatively regulated the SnRK2.2/3/6-mediated activation of the ABA responsive reporter gene RD29B, supporting a negative role of TOPP1 and AtI-2 in ABA signaling. Consistent with these findings, topp1 and ati-2 mutant plants displayed hypersensitivities to ABA and salt treatments, and transcriptome analysis of TOPP1 and AtI-2 knockout plants revealed an increased expression of multiple ABA-responsive genes in the mutants. Taken together, our results uncover TOPP1 and AtI-2 as negative regulators of ABA signaling. |
| doi_str_mv | 10.1371/journal.pgen.1005835 |
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The core ABA signaling pathway consists of three major components: ABA receptor (PYR1/PYLs), type 2C Protein Phosphatase (PP2C) and SNF1-related protein kinase 2 (SnRK2). Nevertheless, the complexity of ABA signaling remains to be explored. To uncover new components of ABA signal transduction pathways, we performed a yeast two-hybrid screen for SnRK2-interacting proteins. We found that Type One Protein Phosphatase 1 (TOPP1) and its regulatory protein, At Inhibitor-2 (AtI-2), physically interact with SnRK2s and also with PYLs. TOPP1 inhibited the kinase activity of SnRK2.6, and this inhibition could be enhanced by AtI-2. Transactivation assays showed that TOPP1 and AtI-2 negatively regulated the SnRK2.2/3/6-mediated activation of the ABA responsive reporter gene RD29B, supporting a negative role of TOPP1 and AtI-2 in ABA signaling. Consistent with these findings, topp1 and ati-2 mutant plants displayed hypersensitivities to ABA and salt treatments, and transcriptome analysis of TOPP1 and AtI-2 knockout plants revealed an increased expression of multiple ABA-responsive genes in the mutants. Taken together, our results uncover TOPP1 and AtI-2 as negative regulators of ABA signaling.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005835</identifier><identifier>PMID: 26943172</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abscisic acid ; Abscisic Acid - genetics ; Abscisic Acid - metabolism ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biology and Life Sciences ; Cellular signal transduction ; Cold Shock Proteins and Peptides - genetics ; Cold Shock Proteins and Peptides - metabolism ; Deoxyribonucleic acid ; DNA ; Experiments ; Gene expression ; Gene Expression Regulation, Plant ; Kinases ; Membrane Transport Proteins - genetics ; Membrane Transport Proteins - metabolism ; Observations ; Phosphatase ; Phosphatases ; Phosphoprotein Phosphatases - genetics ; Phosphoprotein Phosphatases - metabolism ; Physiological aspects ; Physiology ; Plant Roots - genetics ; Plant Roots - growth & development ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - growth & development ; Protein Kinases - genetics ; Protein Kinases - metabolism ; Protein Phosphatase 1 - biosynthesis ; Protein Phosphatase 1 - genetics ; Protein Phosphatase 1 - metabolism ; Protein-Serine-Threonine Kinases - genetics ; Protein-Serine-Threonine Kinases - metabolism ; Proteins ; Research and Analysis Methods ; Seedlings - genetics ; Seedlings - growth & development ; Seeds ; Senescence ; Signal Transduction</subject><ispartof>PLoS genetics, 2016-03, Vol.12 (3), p.e1005835-e1005835</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Hou Y-J, Zhu Y, Wang P, Zhao Y, Xie S, Batelli G, et al. (2016) Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling. PLoS Genet 12(3): e1005835. doi:10.1371/journal.pgen.1005835</rights><rights>2016 Hou et al 2016 Hou et al</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Hou Y-J, Zhu Y, Wang P, Zhao Y, Xie S, Batelli G, et al. (2016) Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling. PLoS Genet 12(3): e1005835. doi:10.1371/journal.pgen.1005835</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c825t-d1c6d3de9319a38c33e250b66b58dbec73f7a2076d2f0af8d719ae6e2a1022ab3</citedby><cites>FETCH-LOGICAL-c825t-d1c6d3de9319a38c33e250b66b58dbec73f7a2076d2f0af8d719ae6e2a1022ab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4778861/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4778861/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26943172$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Yu, Hao</contributor><creatorcontrib>Hou, Yueh-Ju</creatorcontrib><creatorcontrib>Zhu, Yingfang</creatorcontrib><creatorcontrib>Wang, Pengcheng</creatorcontrib><creatorcontrib>Zhao, Yang</creatorcontrib><creatorcontrib>Xie, Shaojun</creatorcontrib><creatorcontrib>Batelli, Giorgia</creatorcontrib><creatorcontrib>Wang, Bangshing</creatorcontrib><creatorcontrib>Duan, Cheng-Guo</creatorcontrib><creatorcontrib>Wang, Xingang</creatorcontrib><creatorcontrib>Xing, Lu</creatorcontrib><creatorcontrib>Lei, Mingguang</creatorcontrib><creatorcontrib>Yan, Jun</creatorcontrib><creatorcontrib>Zhu, Xiaohong</creatorcontrib><creatorcontrib>Zhu, Jian-Kang</creatorcontrib><title>Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>The phytohormone abscisic acid (ABA) regulates plant growth, development and responses to biotic and abiotic stresses. The core ABA signaling pathway consists of three major components: ABA receptor (PYR1/PYLs), type 2C Protein Phosphatase (PP2C) and SNF1-related protein kinase 2 (SnRK2). Nevertheless, the complexity of ABA signaling remains to be explored. To uncover new components of ABA signal transduction pathways, we performed a yeast two-hybrid screen for SnRK2-interacting proteins. We found that Type One Protein Phosphatase 1 (TOPP1) and its regulatory protein, At Inhibitor-2 (AtI-2), physically interact with SnRK2s and also with PYLs. TOPP1 inhibited the kinase activity of SnRK2.6, and this inhibition could be enhanced by AtI-2. Transactivation assays showed that TOPP1 and AtI-2 negatively regulated the SnRK2.2/3/6-mediated activation of the ABA responsive reporter gene RD29B, supporting a negative role of TOPP1 and AtI-2 in ABA signaling. Consistent with these findings, topp1 and ati-2 mutant plants displayed hypersensitivities to ABA and salt treatments, and transcriptome analysis of TOPP1 and AtI-2 knockout plants revealed an increased expression of multiple ABA-responsive genes in the mutants. Taken together, our results uncover TOPP1 and AtI-2 as negative regulators of ABA signaling.</description><subject>Abscisic acid</subject><subject>Abscisic Acid - genetics</subject><subject>Abscisic Acid - metabolism</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biology and Life Sciences</subject><subject>Cellular signal transduction</subject><subject>Cold Shock Proteins and Peptides - genetics</subject><subject>Cold Shock Proteins and Peptides - metabolism</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Experiments</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Kinases</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Membrane Transport Proteins - metabolism</subject><subject>Observations</subject><subject>Phosphatase</subject><subject>Phosphatases</subject><subject>Phosphoprotein Phosphatases - genetics</subject><subject>Phosphoprotein Phosphatases - metabolism</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Plant Roots - genetics</subject><subject>Plant Roots - growth & development</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - growth & development</subject><subject>Protein Kinases - genetics</subject><subject>Protein Kinases - metabolism</subject><subject>Protein Phosphatase 1 - biosynthesis</subject><subject>Protein Phosphatase 1 - genetics</subject><subject>Protein Phosphatase 1 - metabolism</subject><subject>Protein-Serine-Threonine Kinases - genetics</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Seedlings - genetics</subject><subject>Seedlings - growth & development</subject><subject>Seeds</subject><subject>Senescence</subject><subject>Signal Transduction</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVk11v0zAUhiMEYmPwDxBEQkJw0eKPOE5ukMrER6VpnbbBreXEJ4mr1C6xM9F_j7umVYN2MeQLW8fPef36HJ0oeo3RFFOOPy1t3xnZTtc1mClGiGWUPYlOMWN0whOUPD06n0QvnFsiRFmW8-fRCUnzhGJOTqP6drOGeGEgvuqsB23iq8a6dSO9dBDjWBoVz72Lr6HuW-lttzmAc9PoQodQTOJLqKXXd9Bu9iTEsy-z-EbXwaM29cvoWSVbB6-G_Sz6-e3r7fmPycXi-_x8djEpM8L8ROEyVVRBTnEuaVZSCoShIk0LlqkCSk4rLgniqSIVklWmeOAgBSIxIkQW9Cx6u9Ndt9aJoUZOYJ5hmuM8Z4GY7whl5VKsO72S3UZYqcV9wHa1kJ3XZQuiQsDTJMdVTnAS5DNJFFMZYunWF0dB6_PwWl-sQJVgfCfbkej4xuhG1PZOJJxnWYqDwIdBoLO_e3BerLQroW2lAdvf--Z5yhFnj0A5ThKO0Fb13T_ow4UYqFqGv2pT2WCx3IqKWcIDwFmSBGr6ABWWgpUurYFKh_go4eMoITAe_vha9s6J-c31f7CXj2cXv8bs-yO2Adn6xtm299oaNwaTHVh21rkOqkPvMBLbMdtXTmzHTAxjFtLeHPf9kLSfK_oX5_ofpA</recordid><startdate>20160304</startdate><enddate>20160304</enddate><creator>Hou, Yueh-Ju</creator><creator>Zhu, Yingfang</creator><creator>Wang, Pengcheng</creator><creator>Zhao, Yang</creator><creator>Xie, Shaojun</creator><creator>Batelli, Giorgia</creator><creator>Wang, Bangshing</creator><creator>Duan, Cheng-Guo</creator><creator>Wang, Xingang</creator><creator>Xing, Lu</creator><creator>Lei, Mingguang</creator><creator>Yan, Jun</creator><creator>Zhu, Xiaohong</creator><creator>Zhu, Jian-Kang</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160304</creationdate><title>Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling</title><author>Hou, Yueh-Ju ; Zhu, Yingfang ; Wang, Pengcheng ; Zhao, Yang ; Xie, Shaojun ; Batelli, Giorgia ; Wang, Bangshing ; Duan, Cheng-Guo ; Wang, Xingang ; Xing, Lu ; Lei, Mingguang ; Yan, Jun ; Zhu, Xiaohong ; Zhu, Jian-Kang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c825t-d1c6d3de9319a38c33e250b66b58dbec73f7a2076d2f0af8d719ae6e2a1022ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Abscisic acid</topic><topic>Abscisic Acid - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hou, Yueh-Ju</au><au>Zhu, Yingfang</au><au>Wang, Pengcheng</au><au>Zhao, Yang</au><au>Xie, Shaojun</au><au>Batelli, Giorgia</au><au>Wang, Bangshing</au><au>Duan, Cheng-Guo</au><au>Wang, Xingang</au><au>Xing, Lu</au><au>Lei, Mingguang</au><au>Yan, Jun</au><au>Zhu, Xiaohong</au><au>Zhu, Jian-Kang</au><au>Yu, Hao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2016-03-04</date><risdate>2016</risdate><volume>12</volume><issue>3</issue><spage>e1005835</spage><epage>e1005835</epage><pages>e1005835-e1005835</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>The phytohormone abscisic acid (ABA) regulates plant growth, development and responses to biotic and abiotic stresses. The core ABA signaling pathway consists of three major components: ABA receptor (PYR1/PYLs), type 2C Protein Phosphatase (PP2C) and SNF1-related protein kinase 2 (SnRK2). Nevertheless, the complexity of ABA signaling remains to be explored. To uncover new components of ABA signal transduction pathways, we performed a yeast two-hybrid screen for SnRK2-interacting proteins. We found that Type One Protein Phosphatase 1 (TOPP1) and its regulatory protein, At Inhibitor-2 (AtI-2), physically interact with SnRK2s and also with PYLs. TOPP1 inhibited the kinase activity of SnRK2.6, and this inhibition could be enhanced by AtI-2. Transactivation assays showed that TOPP1 and AtI-2 negatively regulated the SnRK2.2/3/6-mediated activation of the ABA responsive reporter gene RD29B, supporting a negative role of TOPP1 and AtI-2 in ABA signaling. Consistent with these findings, topp1 and ati-2 mutant plants displayed hypersensitivities to ABA and salt treatments, and transcriptome analysis of TOPP1 and AtI-2 knockout plants revealed an increased expression of multiple ABA-responsive genes in the mutants. Taken together, our results uncover TOPP1 and AtI-2 as negative regulators of ABA signaling.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26943172</pmid><doi>10.1371/journal.pgen.1005835</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Abscisic acid Abscisic Acid - genetics Abscisic Acid - metabolism Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biology and Life Sciences Cellular signal transduction Cold Shock Proteins and Peptides - genetics Cold Shock Proteins and Peptides - metabolism Deoxyribonucleic acid DNA Experiments Gene expression Gene Expression Regulation, Plant Kinases Membrane Transport Proteins - genetics Membrane Transport Proteins - metabolism Observations Phosphatase Phosphatases Phosphoprotein Phosphatases - genetics Phosphoprotein Phosphatases - metabolism Physiological aspects Physiology Plant Roots - genetics Plant Roots - growth & development Plants, Genetically Modified - genetics Plants, Genetically Modified - growth & development Protein Kinases - genetics Protein Kinases - metabolism Protein Phosphatase 1 - biosynthesis Protein Phosphatase 1 - genetics Protein Phosphatase 1 - metabolism Protein-Serine-Threonine Kinases - genetics Protein-Serine-Threonine Kinases - metabolism Proteins Research and Analysis Methods Seedlings - genetics Seedlings - growth & development Seeds Senescence Signal Transduction |
| title | Type One Protein Phosphatase 1 and Its Regulatory Protein Inhibitor 2 Negatively Regulate ABA Signaling |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-29T03%3A58%3A45IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Type%20One%20Protein%20Phosphatase%201%20and%20Its%20Regulatory%20Protein%20Inhibitor%202%20Negatively%20Regulate%20ABA%20Signaling&rft.jtitle=PLoS%20genetics&rft.au=Hou,%20Yueh-Ju&rft.date=2016-03-04&rft.volume=12&rft.issue=3&rft.spage=e1005835&rft.epage=e1005835&rft.pages=e1005835-e1005835&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1005835&rft_dat=%3Cgale_plos_%3EA479537544%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1781391995&rft_id=info:pmid/26943172&rft_galeid=A479537544&rft_doaj_id=oai_doaj_org_article_f0e76491f921422a8a2d5d805633e270&rfr_iscdi=true |