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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Veröffentlicht in:The New phytologist 2021-02, Vol.229 (4), p.2050-2061
Hauptverfasser: Bernula, Péter, Pettkó‐Szandtner, Aladár, Hajdu, Anita, Kozma‐Bognár, László, Josse, Eve‐Marie, Ádám, Éva, Nagy, Ferenc, Viczián, András
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container_end_page 2061
container_issue 4
container_start_page 2050
container_title The New phytologist
container_volume 229
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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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. 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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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