PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis
Light and temperature are major environmental factors that coordinately control plant growth and survival. However, how plants integrate light and temperature signals to better adapt to environmental stresses is poorly understood. PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), a key transcription factor r...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-08, Vol.114 (32), p.E6695-E6702 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Jiang, Bochen Shi, Yiting Zhang, Xiaoyan Xin, Xiaoyun Qi, Lijuan Guo, Hongwei Li, Jigang Yang, Shuhua |
| description | Light and temperature are major environmental factors that coordinately control plant growth and survival. However, how plants integrate light and temperature signals to better adapt to environmental stresses is poorly understood. PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), a key transcription factor repressing photomorphogenesis, has been shown to play a pivotal role in mediating plants’ responses to various environmental signals. In this study, we found that PIF3 functions as a negative regulator of Arabidopsis freezing tolerance by directly binding to the promoters of C-REPEAT BINDING FACTOR (CBF) genes to down-regulate their expression. In addition, two F-box proteins, EIN3-BINDING F-BOX 1 (EBF1) and EBF2, directly target PIF3 for 26S proteasome-mediated degradation. Consistently, ebf1 and ebf2 mutants were more sensitive to freezing than were the wild type, and the pif3 mutation suppressed the freezing-sensitive phenotype of ebf1. Furthermore, cold treatment promoted the degradation of EBF1 and EBF2, leading to increased stability of the PIF3 protein and reduced expression of the CBF genes. Together, our study uncovers an important role of PIF3 in Arabidopsis freezing tolerance by negatively regulating the expression of genes in the CBF pathway. |
| doi_str_mv | 10.1073/pnas.1706226114 |
| format | Article |
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However, how plants integrate light and temperature signals to better adapt to environmental stresses is poorly understood. PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), a key transcription factor repressing photomorphogenesis, has been shown to play a pivotal role in mediating plants’ responses to various environmental signals. In this study, we found that PIF3 functions as a negative regulator of Arabidopsis freezing tolerance by directly binding to the promoters of C-REPEAT BINDING FACTOR (CBF) genes to down-regulate their expression. In addition, two F-box proteins, EIN3-BINDING F-BOX 1 (EBF1) and EBF2, directly target PIF3 for 26S proteasome-mediated degradation. Consistently, ebf1 and ebf2 mutants were more sensitive to freezing than were the wild type, and the pif3 mutation suppressed the freezing-sensitive phenotype of ebf1. Furthermore, cold treatment promoted the degradation of EBF1 and EBF2, leading to increased stability of the PIF3 protein and reduced expression of the CBF genes. Together, our study uncovers an important role of PIF3 in Arabidopsis freezing tolerance by negatively regulating the expression of genes in the CBF pathway.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1706226114</identifier><identifier>PMID: 28739888</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Arabidopsis ; Biological Sciences ; CBF protein ; Cold tolerance ; Cold treatment ; Degradation ; Down-regulation ; Environmental factors ; Environmental stress ; Flowers & plants ; Freezing ; Gene expression ; Genes ; Genotype & phenotype ; Mutants ; Photomorphogenesis ; Phytochrome-interacting factor 3 ; Plant growth ; PNAS Plus ; Promoters ; Proteasome 26S ; Proteins ; Stress response ; Temperature tolerance</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-08, Vol.114 (32), p.E6695-E6702</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Aug 8, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c402t-83c966a3f4b22294e04efa463d6690c268ace4e93a9443c2c9caad25056608303</citedby><cites>FETCH-LOGICAL-c402t-83c966a3f4b22294e04efa463d6690c268ace4e93a9443c2c9caad25056608303</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26486965$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26486965$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28739888$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Bochen</creatorcontrib><creatorcontrib>Shi, Yiting</creatorcontrib><creatorcontrib>Zhang, Xiaoyan</creatorcontrib><creatorcontrib>Xin, Xiaoyun</creatorcontrib><creatorcontrib>Qi, Lijuan</creatorcontrib><creatorcontrib>Guo, Hongwei</creatorcontrib><creatorcontrib>Li, Jigang</creatorcontrib><creatorcontrib>Yang, Shuhua</creatorcontrib><title>PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Light and temperature are major environmental factors that coordinately control plant growth and survival. However, how plants integrate light and temperature signals to better adapt to environmental stresses is poorly understood. PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), a key transcription factor repressing photomorphogenesis, has been shown to play a pivotal role in mediating plants’ responses to various environmental signals. In this study, we found that PIF3 functions as a negative regulator of Arabidopsis freezing tolerance by directly binding to the promoters of C-REPEAT BINDING FACTOR (CBF) genes to down-regulate their expression. In addition, two F-box proteins, EIN3-BINDING F-BOX 1 (EBF1) and EBF2, directly target PIF3 for 26S proteasome-mediated degradation. Consistently, ebf1 and ebf2 mutants were more sensitive to freezing than were the wild type, and the pif3 mutation suppressed the freezing-sensitive phenotype of ebf1. Furthermore, cold treatment promoted the degradation of EBF1 and EBF2, leading to increased stability of the PIF3 protein and reduced expression of the CBF genes. Together, our study uncovers an important role of PIF3 in Arabidopsis freezing tolerance by negatively regulating the expression of genes in the CBF pathway.</description><subject>Arabidopsis</subject><subject>Biological Sciences</subject><subject>CBF protein</subject><subject>Cold tolerance</subject><subject>Cold treatment</subject><subject>Degradation</subject><subject>Down-regulation</subject><subject>Environmental factors</subject><subject>Environmental stress</subject><subject>Flowers & plants</subject><subject>Freezing</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genotype & phenotype</subject><subject>Mutants</subject><subject>Photomorphogenesis</subject><subject>Phytochrome-interacting factor 3</subject><subject>Plant growth</subject><subject>PNAS Plus</subject><subject>Promoters</subject><subject>Proteasome 26S</subject><subject>Proteins</subject><subject>Stress response</subject><subject>Temperature tolerance</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNpdkU1vEzEQhi0EoqFw5gSyxIXLtv5ax74glYhApUpwoGdr4p1NHG3sxd4tKr8eVyktcJrDPPNqXj2EvObsjLOlPB8jlDO-ZFoIzbl6QhacWd5oZdlTsmBMLBujhDohL0rZM8Zsa9hzciLMUlpjzIJcf7tcSxoKBRpxC1O4QZpxOw8wpUxTT6cd0tXHNR1h2v2EWwqxo31G_BXilk5pwAzRIw2RXmTYhC6NJZSX5FkPQ8FX9_OUXK8_fV99aa6-fr5cXVw1XjExNUZ6qzXIXm2EEFYhU9iD0rLT2jIvtAGPCq0Eq5T0wlsP0ImWtVozI5k8JR-OueO8OWDnMU4ZBjfmcIB86xIE9-8mhp3bphvXtq1liteA9_cBOf2YsUzuEIrHYYCIaS6OWyE5163QFX33H7pPc461XqWUVrJWkpU6P1I-p1Iy9g_PcObulLk7Ze5RWb14-3eHB_6Powq8OQL7Up087rUy2upW_gbb0ZsF</recordid><startdate>20170808</startdate><enddate>20170808</enddate><creator>Jiang, Bochen</creator><creator>Shi, Yiting</creator><creator>Zhang, Xiaoyan</creator><creator>Xin, Xiaoyun</creator><creator>Qi, Lijuan</creator><creator>Guo, Hongwei</creator><creator>Li, Jigang</creator><creator>Yang, Shuhua</creator><general>National Academy of Sciences</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170808</creationdate><title>PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis</title><author>Jiang, Bochen ; Shi, Yiting ; Zhang, Xiaoyan ; Xin, Xiaoyun ; Qi, Lijuan ; Guo, Hongwei ; Li, Jigang ; Yang, Shuhua</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c402t-83c966a3f4b22294e04efa463d6690c268ace4e93a9443c2c9caad25056608303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Arabidopsis</topic><topic>Biological Sciences</topic><topic>CBF protein</topic><topic>Cold tolerance</topic><topic>Cold treatment</topic><topic>Degradation</topic><topic>Down-regulation</topic><topic>Environmental factors</topic><topic>Environmental stress</topic><topic>Flowers & plants</topic><topic>Freezing</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genotype & phenotype</topic><topic>Mutants</topic><topic>Photomorphogenesis</topic><topic>Phytochrome-interacting factor 3</topic><topic>Plant growth</topic><topic>PNAS Plus</topic><topic>Promoters</topic><topic>Proteasome 26S</topic><topic>Proteins</topic><topic>Stress response</topic><topic>Temperature tolerance</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Bochen</creatorcontrib><creatorcontrib>Shi, Yiting</creatorcontrib><creatorcontrib>Zhang, Xiaoyan</creatorcontrib><creatorcontrib>Xin, Xiaoyun</creatorcontrib><creatorcontrib>Qi, Lijuan</creatorcontrib><creatorcontrib>Guo, Hongwei</creatorcontrib><creatorcontrib>Li, Jigang</creatorcontrib><creatorcontrib>Yang, Shuhua</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Bochen</au><au>Shi, Yiting</au><au>Zhang, Xiaoyan</au><au>Xin, Xiaoyun</au><au>Qi, Lijuan</au><au>Guo, Hongwei</au><au>Li, Jigang</au><au>Yang, Shuhua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2017-08-08</date><risdate>2017</risdate><volume>114</volume><issue>32</issue><spage>E6695</spage><epage>E6702</epage><pages>E6695-E6702</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Light and temperature are major environmental factors that coordinately control plant growth and survival. However, how plants integrate light and temperature signals to better adapt to environmental stresses is poorly understood. PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), a key transcription factor repressing photomorphogenesis, has been shown to play a pivotal role in mediating plants’ responses to various environmental signals. In this study, we found that PIF3 functions as a negative regulator of Arabidopsis freezing tolerance by directly binding to the promoters of C-REPEAT BINDING FACTOR (CBF) genes to down-regulate their expression. In addition, two F-box proteins, EIN3-BINDING F-BOX 1 (EBF1) and EBF2, directly target PIF3 for 26S proteasome-mediated degradation. Consistently, ebf1 and ebf2 mutants were more sensitive to freezing than were the wild type, and the pif3 mutation suppressed the freezing-sensitive phenotype of ebf1. Furthermore, cold treatment promoted the degradation of EBF1 and EBF2, leading to increased stability of the PIF3 protein and reduced expression of the CBF genes. Together, our study uncovers an important role of PIF3 in Arabidopsis freezing tolerance by negatively regulating the expression of genes in the CBF pathway.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28739888</pmid><doi>10.1073/pnas.1706226114</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Biological Sciences CBF protein Cold tolerance Cold treatment Degradation Down-regulation Environmental factors Environmental stress Flowers & plants Freezing Gene expression Genes Genotype & phenotype Mutants Photomorphogenesis Phytochrome-interacting factor 3 Plant growth PNAS Plus Promoters Proteasome 26S Proteins Stress response Temperature tolerance |
| title | PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis |
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