SUMOylation of PHYTOCHROME INTERACTING FACTOR 3 promotes photomorphogenesis in Arabidopsis thaliana
Summary In Arabidopsis thaliana, phytochrome B (phyB) is the dominant receptor of photomorphogenic development under red light. Phytochrome B interacts with a set of downstream regulatory proteins, including PHYTOCHROME INTERACTING FACTOR 3 (PIF3). The interaction between PIF3 and photoactivated phy...
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creator | Bernula, Péter Pettkó‐Szandtner, Aladár Hajdu, Anita Kozma‐Bognár, László Josse, Eve‐Marie Ádám, Éva Nagy, Ferenc Viczián, András |
description | Summary
In Arabidopsis thaliana, phytochrome B (phyB) is the dominant receptor of photomorphogenic development under red light. Phytochrome B interacts with a set of downstream regulatory proteins, including PHYTOCHROME INTERACTING FACTOR 3 (PIF3). The interaction between PIF3 and photoactivated phyB leads to the rapid phosphorylation and degradation of PIF3 and also to the degradation of phyB, events which are required for proper photomorphogenesis.
Here we report that PIF3 is SUMOylated at the Lys13 (K13) residue and that we could detect this posttranslational modification in a heterologous experimental system and also in planta.
We also found that the SUMO acceptor site mutant PIF3(K13R) binds more strongly to the target promoters than its SUMOylated, wild‐type counterpart. Seedlings expressing PIF3(K13R) show an elongated hypocotyl response, elevated photoprotection and higher transcriptional induction of red‐light responsive genes compared with plantlets expressing wild‐type PIF3.
These observations are supported by the lower level of phyB in plants which possess only PIF3(K13R), indicating that SUMOylation of PIF3 also alters photomorphogenesis via the regulation of phyB levels. In conclusion, whereas SUMOylation is generally connected to different stress responses, it also fine‐tunes light signalling by reducing the biological activity of PIF3, thus promoting photomorphogenesis. |
doi_str_mv | 10.1111/nph.17013 |
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In Arabidopsis thaliana, phytochrome B (phyB) is the dominant receptor of photomorphogenic development under red light. Phytochrome B interacts with a set of downstream regulatory proteins, including PHYTOCHROME INTERACTING FACTOR 3 (PIF3). The interaction between PIF3 and photoactivated phyB leads to the rapid phosphorylation and degradation of PIF3 and also to the degradation of phyB, events which are required for proper photomorphogenesis.
Here we report that PIF3 is SUMOylated at the Lys13 (K13) residue and that we could detect this posttranslational modification in a heterologous experimental system and also in planta.
We also found that the SUMO acceptor site mutant PIF3(K13R) binds more strongly to the target promoters than its SUMOylated, wild‐type counterpart. Seedlings expressing PIF3(K13R) show an elongated hypocotyl response, elevated photoprotection and higher transcriptional induction of red‐light responsive genes compared with plantlets expressing wild‐type PIF3.
These observations are supported by the lower level of phyB in plants which possess only PIF3(K13R), indicating that SUMOylation of PIF3 also alters photomorphogenesis via the regulation of phyB levels. In conclusion, whereas SUMOylation is generally connected to different stress responses, it also fine‐tunes light signalling by reducing the biological activity of PIF3, thus promoting photomorphogenesis.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17013</identifier><identifier>PMID: 33078389</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - radiation effects ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Biological activity ; Cellular stress response ; Degradation ; Genes ; Light ; light signalling ; Phosphorylation ; Photomorphogenesis ; phytochrome ; Phytochrome B ; Phytochrome B - genetics ; Phytochrome B - metabolism ; PIF3 ; Plantlets ; Receptors ; Regulatory proteins ; Seedlings ; SUMO ; SUMO protein ; SUMOylation ; Transcription</subject><ispartof>The New phytologist, 2021-02, Vol.229 (4), p.2050-2061</ispartof><rights>2020 The Authors New Phytologist © 2020 New Phytologist Foundation</rights><rights>2020 The Authors New Phytologist © 2020 New Phytologist Foundation.</rights><rights>Copyright © 2021 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3883-b915c702e5ce5230cc8cb6cffed35dc93f1c3410ce18b7be450cb9a1dd0c47f13</citedby><cites>FETCH-LOGICAL-c3883-b915c702e5ce5230cc8cb6cffed35dc93f1c3410ce18b7be450cb9a1dd0c47f13</cites><orcidid>0000-0002-3286-8264 ; 0000-0002-6157-9269 ; 0000-0002-5295-5568 ; 0000-0003-3946-5158 ; 0000-0002-9145-4686 ; 0000-0003-2055-3430 ; 0000-0002-8289-193X</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%2Fnph.17013$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.17013$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33078389$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bernula, Péter</creatorcontrib><creatorcontrib>Pettkó‐Szandtner, Aladár</creatorcontrib><creatorcontrib>Hajdu, Anita</creatorcontrib><creatorcontrib>Kozma‐Bognár, László</creatorcontrib><creatorcontrib>Josse, Eve‐Marie</creatorcontrib><creatorcontrib>Ádám, Éva</creatorcontrib><creatorcontrib>Nagy, Ferenc</creatorcontrib><creatorcontrib>Viczián, András</creatorcontrib><title>SUMOylation of PHYTOCHROME INTERACTING FACTOR 3 promotes photomorphogenesis in Arabidopsis thaliana</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
In Arabidopsis thaliana, phytochrome B (phyB) is the dominant receptor of photomorphogenic development under red light. Phytochrome B interacts with a set of downstream regulatory proteins, including PHYTOCHROME INTERACTING FACTOR 3 (PIF3). The interaction between PIF3 and photoactivated phyB leads to the rapid phosphorylation and degradation of PIF3 and also to the degradation of phyB, events which are required for proper photomorphogenesis.
Here we report that PIF3 is SUMOylated at the Lys13 (K13) residue and that we could detect this posttranslational modification in a heterologous experimental system and also in planta.
We also found that the SUMO acceptor site mutant PIF3(K13R) binds more strongly to the target promoters than its SUMOylated, wild‐type counterpart. Seedlings expressing PIF3(K13R) show an elongated hypocotyl response, elevated photoprotection and higher transcriptional induction of red‐light responsive genes compared with plantlets expressing wild‐type PIF3.
These observations are supported by the lower level of phyB in plants which possess only PIF3(K13R), indicating that SUMOylation of PIF3 also alters photomorphogenesis via the regulation of phyB levels. In conclusion, whereas SUMOylation is generally connected to different stress responses, it also fine‐tunes light signalling by reducing the biological activity of PIF3, thus promoting photomorphogenesis.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - radiation effects</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Biological activity</subject><subject>Cellular stress response</subject><subject>Degradation</subject><subject>Genes</subject><subject>Light</subject><subject>light signalling</subject><subject>Phosphorylation</subject><subject>Photomorphogenesis</subject><subject>phytochrome</subject><subject>Phytochrome B</subject><subject>Phytochrome B - genetics</subject><subject>Phytochrome B - metabolism</subject><subject>PIF3</subject><subject>Plantlets</subject><subject>Receptors</subject><subject>Regulatory proteins</subject><subject>Seedlings</subject><subject>SUMO</subject><subject>SUMO protein</subject><subject>SUMOylation</subject><subject>Transcription</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp1kM1qwkAURofSUq3toi9QBrppF9H5STKTpYgaQY1YhXYVJpNJjcRMmokU375jtV0UejffvXA4XD4A7jHqYju9stp0MUOYXoA2dv3A4ZiyS9BGiHDHd_3XFrgxZosQCjyfXIMWpYhxyoM2kC_rWXQoRJPrEuoMLsK3VTQIl9FsCCfz1XDZH6wm8zEc2YyWkMKq1jvdKAOrjW7sWtt8V6UyuYF5Cfu1SPJUV8ez2YgiF6W4BVeZKIy6O2cHrEfD1SB0ptF4MuhPHUk5p04SYE8yRJQnlUcokpLLxJdZplLqpTKgGZbUxUgqzBOWKNdDMgkETlMkXZZh2gFPJ6_98WOvTBPvciNVUYhS6b2JiesRDzHKiUUf_6Bbva9L-52lGGckIMy11POJkrU2plZZXNX5TtSHGKP42Hxsm4-_m7fsw9m4T3Yq_SV_qrZA7wR85oU6_G-K54vwpPwCH6aLfQ</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Bernula, Péter</creator><creator>Pettkó‐Szandtner, Aladár</creator><creator>Hajdu, Anita</creator><creator>Kozma‐Bognár, László</creator><creator>Josse, Eve‐Marie</creator><creator>Ádám, Éva</creator><creator>Nagy, Ferenc</creator><creator>Viczián, András</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><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>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3286-8264</orcidid><orcidid>https://orcid.org/0000-0002-6157-9269</orcidid><orcidid>https://orcid.org/0000-0002-5295-5568</orcidid><orcidid>https://orcid.org/0000-0003-3946-5158</orcidid><orcidid>https://orcid.org/0000-0002-9145-4686</orcidid><orcidid>https://orcid.org/0000-0003-2055-3430</orcidid><orcidid>https://orcid.org/0000-0002-8289-193X</orcidid></search><sort><creationdate>202102</creationdate><title>SUMOylation of PHYTOCHROME INTERACTING FACTOR 3 promotes photomorphogenesis in Arabidopsis thaliana</title><author>Bernula, Péter ; Pettkó‐Szandtner, Aladár ; Hajdu, Anita ; Kozma‐Bognár, László ; Josse, Eve‐Marie ; Ádám, Éva ; Nagy, Ferenc ; Viczián, András</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3883-b915c702e5ce5230cc8cb6cffed35dc93f1c3410ce18b7be450cb9a1dd0c47f13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - radiation effects</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Biological activity</topic><topic>Cellular stress response</topic><topic>Degradation</topic><topic>Genes</topic><topic>Light</topic><topic>light signalling</topic><topic>Phosphorylation</topic><topic>Photomorphogenesis</topic><topic>phytochrome</topic><topic>Phytochrome B</topic><topic>Phytochrome B - genetics</topic><topic>Phytochrome B - metabolism</topic><topic>PIF3</topic><topic>Plantlets</topic><topic>Receptors</topic><topic>Regulatory proteins</topic><topic>Seedlings</topic><topic>SUMO</topic><topic>SUMO protein</topic><topic>SUMOylation</topic><topic>Transcription</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bernula, Péter</creatorcontrib><creatorcontrib>Pettkó‐Szandtner, Aladár</creatorcontrib><creatorcontrib>Hajdu, Anita</creatorcontrib><creatorcontrib>Kozma‐Bognár, László</creatorcontrib><creatorcontrib>Josse, Eve‐Marie</creatorcontrib><creatorcontrib>Ádám, Éva</creatorcontrib><creatorcontrib>Nagy, Ferenc</creatorcontrib><creatorcontrib>Viczián, András</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Online Library Free Content</collection><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>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</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 New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bernula, Péter</au><au>Pettkó‐Szandtner, Aladár</au><au>Hajdu, Anita</au><au>Kozma‐Bognár, László</au><au>Josse, Eve‐Marie</au><au>Ádám, Éva</au><au>Nagy, Ferenc</au><au>Viczián, András</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>SUMOylation of PHYTOCHROME INTERACTING FACTOR 3 promotes photomorphogenesis in Arabidopsis thaliana</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2021-02</date><risdate>2021</risdate><volume>229</volume><issue>4</issue><spage>2050</spage><epage>2061</epage><pages>2050-2061</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
In Arabidopsis thaliana, phytochrome B (phyB) is the dominant receptor of photomorphogenic development under red light. Phytochrome B interacts with a set of downstream regulatory proteins, including PHYTOCHROME INTERACTING FACTOR 3 (PIF3). The interaction between PIF3 and photoactivated phyB leads to the rapid phosphorylation and degradation of PIF3 and also to the degradation of phyB, events which are required for proper photomorphogenesis.
Here we report that PIF3 is SUMOylated at the Lys13 (K13) residue and that we could detect this posttranslational modification in a heterologous experimental system and also in planta.
We also found that the SUMO acceptor site mutant PIF3(K13R) binds more strongly to the target promoters than its SUMOylated, wild‐type counterpart. Seedlings expressing PIF3(K13R) show an elongated hypocotyl response, elevated photoprotection and higher transcriptional induction of red‐light responsive genes compared with plantlets expressing wild‐type PIF3.
These observations are supported by the lower level of phyB in plants which possess only PIF3(K13R), indicating that SUMOylation of PIF3 also alters photomorphogenesis via the regulation of phyB levels. In conclusion, whereas SUMOylation is generally connected to different stress responses, it also fine‐tunes light signalling by reducing the biological activity of PIF3, thus promoting photomorphogenesis.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33078389</pmid><doi>10.1111/nph.17013</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-3286-8264</orcidid><orcidid>https://orcid.org/0000-0002-6157-9269</orcidid><orcidid>https://orcid.org/0000-0002-5295-5568</orcidid><orcidid>https://orcid.org/0000-0003-3946-5158</orcidid><orcidid>https://orcid.org/0000-0002-9145-4686</orcidid><orcidid>https://orcid.org/0000-0003-2055-3430</orcidid><orcidid>https://orcid.org/0000-0002-8289-193X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - radiation effects Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Biological activity Cellular stress response Degradation Genes Light light signalling Phosphorylation Photomorphogenesis phytochrome Phytochrome B Phytochrome B - genetics Phytochrome B - metabolism PIF3 Plantlets Receptors Regulatory proteins Seedlings SUMO SUMO protein SUMOylation Transcription |
title | SUMOylation of PHYTOCHROME INTERACTING FACTOR 3 promotes photomorphogenesis in Arabidopsis thaliana |
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