S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway

Nitrogen assimilation plays a vital role in plant metabolism. Assimilation of nitrate, the primary source of nitrogen in soil, is linked to the generation of the redox signal nitric oxide (NO). An important mechanism by which NO regulates plant development and stress responses is through S -nitrosyl...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Nature communications 2014-11, Vol.5 (1), p.5401-5401, Article 5401
Hauptverfasser: Frungillo, Lucas, Skelly, Michael J., Loake, Gary J., Spoel, Steven H., Salgado, Ione
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext bestellen
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 5401
container_issue 1
container_start_page 5401
container_title Nature communications
container_volume 5
creator Frungillo, Lucas
Skelly, Michael J.
Loake, Gary J.
Spoel, Steven H.
Salgado, Ione
description Nitrogen assimilation plays a vital role in plant metabolism. Assimilation of nitrate, the primary source of nitrogen in soil, is linked to the generation of the redox signal nitric oxide (NO). An important mechanism by which NO regulates plant development and stress responses is through S -nitrosylation, that is, covalent attachment of NO to cysteine residues to form S -nitrosothiols (SNO). Despite the importance of nitrogen assimilation and NO signalling, it remains largely unknown how these pathways are interconnected. Here we show that SNO signalling suppresses both nitrate uptake and reduction by transporters and reductases, respectively, to fine tune nitrate homeostasis. Moreover, NO derived from nitrate assimilation suppresses the redox enzyme S -nitrosoglutathione Reductase 1 (GSNOR1) by S -nitrosylation, preventing scavenging of S -nitrosoglutathione, a major cellular bio-reservoir of NO. Hence, our data demonstrates that (S)NO controls its own generation and scavenging by modulating nitrate assimilation and GSNOR1 activity. Assimilation of nitrate by plant roots leads to the generation of the signalling molecule, nitric oxide. Here Frungillo et al. show that nitric oxide fine-tunes nitrate homeostasis by feedback regulating nitrate transporters and reductases, while also promoting its own storage.
doi_str_mv 10.1038/ncomms6401
format Article
fullrecord <record><control><sourceid>proquest_C6C</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4229994</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3491038721</sourcerecordid><originalsourceid>FETCH-LOGICAL-c442t-a7c62cd4bd3e5188e598eaaf8a57f397d9395eddfaf118578db535a58c81aebc3</originalsourceid><addsrcrecordid>eNplkc1u1TAQhSMEolXbDQ-ALLFBoLTxX2JvkFAFBakSi8La8rUniavEDrYD9O1xdNtyAW_G8nxzZsanql7g5hw3VFx4E-Y5tazBT6pj0jBc447Qpwf3o-ospdumHCqxYOx5dUQ4FYxKcVwtN7V3OYYU8ujClFCEYZ10BrQ9O4PCL2cBLTHY1WQXPNLeopRD1AMg59EyaZ8TymMM6zCWuK8MAxQ0JTe7orbVLTqPP_XdafWs11OCs_t4Un37-OHr5af6-svV58v317VhjORad6YlxrKdpcCxEMClAK17oXnXU9lZSSUHa3vdYyx4J-yOU665MAJr2Bl6Ur3b6y7rbgZrwOeoJ7VEN-t4p4J26u-Md6Mawg_FCJFSsiLw-l4ghu8rpKxmlwxMZV8Ia1K4JUxSKrquoK_-QW_DGn1Zb6MIbbq23QTf7ClTvjtF6B-HwY3avFR_vCzwy8PxH9EH5wrwdg-kkvIDxIOe_8v9BnAFrhE</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1622307664</pqid></control><display><type>article</type><title>S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway</title><source>Springer Nature OA/Free Journals</source><creator>Frungillo, Lucas ; Skelly, Michael J. ; Loake, Gary J. ; Spoel, Steven H. ; Salgado, Ione</creator><creatorcontrib>Frungillo, Lucas ; Skelly, Michael J. ; Loake, Gary J. ; Spoel, Steven H. ; Salgado, Ione</creatorcontrib><description>Nitrogen assimilation plays a vital role in plant metabolism. Assimilation of nitrate, the primary source of nitrogen in soil, is linked to the generation of the redox signal nitric oxide (NO). An important mechanism by which NO regulates plant development and stress responses is through S -nitrosylation, that is, covalent attachment of NO to cysteine residues to form S -nitrosothiols (SNO). Despite the importance of nitrogen assimilation and NO signalling, it remains largely unknown how these pathways are interconnected. Here we show that SNO signalling suppresses both nitrate uptake and reduction by transporters and reductases, respectively, to fine tune nitrate homeostasis. Moreover, NO derived from nitrate assimilation suppresses the redox enzyme S -nitrosoglutathione Reductase 1 (GSNOR1) by S -nitrosylation, preventing scavenging of S -nitrosoglutathione, a major cellular bio-reservoir of NO. Hence, our data demonstrates that (S)NO controls its own generation and scavenging by modulating nitrate assimilation and GSNOR1 activity. Assimilation of nitrate by plant roots leads to the generation of the signalling molecule, nitric oxide. Here Frungillo et al. show that nitric oxide fine-tunes nitrate homeostasis by feedback regulating nitrate transporters and reductases, while also promoting its own storage.</description><identifier>ISSN: 2041-1723</identifier><identifier>EISSN: 2041-1723</identifier><identifier>DOI: 10.1038/ncomms6401</identifier><identifier>PMID: 25384398</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/443/319 ; 631/449/2675 ; Arabidopsis - metabolism ; Arabidopsis Proteins - metabolism ; Glutathione Reductase - metabolism ; Homeostasis - physiology ; Humanities and Social Sciences ; Models, Biological ; multidisciplinary ; Nitrates - metabolism ; Nitric Oxide - metabolism ; Nitrogen - metabolism ; Oxidation-Reduction ; S-Nitrosothiols - metabolism ; Science ; Science (multidisciplinary) ; Signal Transduction - physiology</subject><ispartof>Nature communications, 2014-11, Vol.5 (1), p.5401-5401, Article 5401</ispartof><rights>Springer Nature Limited 2014</rights><rights>Copyright Nature Publishing Group Nov 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-a7c62cd4bd3e5188e598eaaf8a57f397d9395eddfaf118578db535a58c81aebc3</citedby><cites>FETCH-LOGICAL-c442t-a7c62cd4bd3e5188e598eaaf8a57f397d9395eddfaf118578db535a58c81aebc3</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/PMC4229994/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4229994/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,41120,42189,51576,53791,53793</link.rule.ids><linktorsrc>$$Uhttps://doi.org/10.1038/ncomms6401$$EView_record_in_Springer_Nature$$FView_record_in_$$GSpringer_Nature</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25384398$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Frungillo, Lucas</creatorcontrib><creatorcontrib>Skelly, Michael J.</creatorcontrib><creatorcontrib>Loake, Gary J.</creatorcontrib><creatorcontrib>Spoel, Steven H.</creatorcontrib><creatorcontrib>Salgado, Ione</creatorcontrib><title>S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway</title><title>Nature communications</title><addtitle>Nat Commun</addtitle><addtitle>Nat Commun</addtitle><description>Nitrogen assimilation plays a vital role in plant metabolism. Assimilation of nitrate, the primary source of nitrogen in soil, is linked to the generation of the redox signal nitric oxide (NO). An important mechanism by which NO regulates plant development and stress responses is through S -nitrosylation, that is, covalent attachment of NO to cysteine residues to form S -nitrosothiols (SNO). Despite the importance of nitrogen assimilation and NO signalling, it remains largely unknown how these pathways are interconnected. Here we show that SNO signalling suppresses both nitrate uptake and reduction by transporters and reductases, respectively, to fine tune nitrate homeostasis. Moreover, NO derived from nitrate assimilation suppresses the redox enzyme S -nitrosoglutathione Reductase 1 (GSNOR1) by S -nitrosylation, preventing scavenging of S -nitrosoglutathione, a major cellular bio-reservoir of NO. Hence, our data demonstrates that (S)NO controls its own generation and scavenging by modulating nitrate assimilation and GSNOR1 activity. Assimilation of nitrate by plant roots leads to the generation of the signalling molecule, nitric oxide. Here Frungillo et al. show that nitric oxide fine-tunes nitrate homeostasis by feedback regulating nitrate transporters and reductases, while also promoting its own storage.</description><subject>631/443/319</subject><subject>631/449/2675</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Glutathione Reductase - metabolism</subject><subject>Homeostasis - physiology</subject><subject>Humanities and Social Sciences</subject><subject>Models, Biological</subject><subject>multidisciplinary</subject><subject>Nitrates - metabolism</subject><subject>Nitric Oxide - metabolism</subject><subject>Nitrogen - metabolism</subject><subject>Oxidation-Reduction</subject><subject>S-Nitrosothiols - metabolism</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Signal Transduction - physiology</subject><issn>2041-1723</issn><issn>2041-1723</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNplkc1u1TAQhSMEolXbDQ-ALLFBoLTxX2JvkFAFBakSi8La8rUniavEDrYD9O1xdNtyAW_G8nxzZsanql7g5hw3VFx4E-Y5tazBT6pj0jBc447Qpwf3o-ospdumHCqxYOx5dUQ4FYxKcVwtN7V3OYYU8ujClFCEYZ10BrQ9O4PCL2cBLTHY1WQXPNLeopRD1AMg59EyaZ8TymMM6zCWuK8MAxQ0JTe7orbVLTqPP_XdafWs11OCs_t4Un37-OHr5af6-svV58v317VhjORad6YlxrKdpcCxEMClAK17oXnXU9lZSSUHa3vdYyx4J-yOU665MAJr2Bl6Ur3b6y7rbgZrwOeoJ7VEN-t4p4J26u-Md6Mawg_FCJFSsiLw-l4ghu8rpKxmlwxMZV8Ia1K4JUxSKrquoK_-QW_DGn1Zb6MIbbq23QTf7ClTvjtF6B-HwY3avFR_vCzwy8PxH9EH5wrwdg-kkvIDxIOe_8v9BnAFrhE</recordid><startdate>20141111</startdate><enddate>20141111</enddate><creator>Frungillo, Lucas</creator><creator>Skelly, Michael J.</creator><creator>Loake, Gary J.</creator><creator>Spoel, Steven H.</creator><creator>Salgado, Ione</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>3V.</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7T7</scope><scope>7TM</scope><scope>7TO</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</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>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20141111</creationdate><title>S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway</title><author>Frungillo, Lucas ; Skelly, Michael J. ; Loake, Gary J. ; Spoel, Steven H. ; Salgado, Ione</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-a7c62cd4bd3e5188e598eaaf8a57f397d9395eddfaf118578db535a58c81aebc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>631/443/319</topic><topic>631/449/2675</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Glutathione Reductase - metabolism</topic><topic>Homeostasis - physiology</topic><topic>Humanities and Social Sciences</topic><topic>Models, Biological</topic><topic>multidisciplinary</topic><topic>Nitrates - metabolism</topic><topic>Nitric Oxide - metabolism</topic><topic>Nitrogen - metabolism</topic><topic>Oxidation-Reduction</topic><topic>S-Nitrosothiols - metabolism</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Signal Transduction - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Frungillo, Lucas</creatorcontrib><creatorcontrib>Skelly, Michael J.</creatorcontrib><creatorcontrib>Loake, Gary J.</creatorcontrib><creatorcontrib>Spoel, Steven H.</creatorcontrib><creatorcontrib>Salgado, Ione</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature communications</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Frungillo, Lucas</au><au>Skelly, Michael J.</au><au>Loake, Gary J.</au><au>Spoel, Steven H.</au><au>Salgado, Ione</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway</atitle><jtitle>Nature communications</jtitle><stitle>Nat Commun</stitle><addtitle>Nat Commun</addtitle><date>2014-11-11</date><risdate>2014</risdate><volume>5</volume><issue>1</issue><spage>5401</spage><epage>5401</epage><pages>5401-5401</pages><artnum>5401</artnum><issn>2041-1723</issn><eissn>2041-1723</eissn><abstract>Nitrogen assimilation plays a vital role in plant metabolism. Assimilation of nitrate, the primary source of nitrogen in soil, is linked to the generation of the redox signal nitric oxide (NO). An important mechanism by which NO regulates plant development and stress responses is through S -nitrosylation, that is, covalent attachment of NO to cysteine residues to form S -nitrosothiols (SNO). Despite the importance of nitrogen assimilation and NO signalling, it remains largely unknown how these pathways are interconnected. Here we show that SNO signalling suppresses both nitrate uptake and reduction by transporters and reductases, respectively, to fine tune nitrate homeostasis. Moreover, NO derived from nitrate assimilation suppresses the redox enzyme S -nitrosoglutathione Reductase 1 (GSNOR1) by S -nitrosylation, preventing scavenging of S -nitrosoglutathione, a major cellular bio-reservoir of NO. Hence, our data demonstrates that (S)NO controls its own generation and scavenging by modulating nitrate assimilation and GSNOR1 activity. Assimilation of nitrate by plant roots leads to the generation of the signalling molecule, nitric oxide. Here Frungillo et al. show that nitric oxide fine-tunes nitrate homeostasis by feedback regulating nitrate transporters and reductases, while also promoting its own storage.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>25384398</pmid><doi>10.1038/ncomms6401</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext_linktorsrc
identifier ISSN: 2041-1723
ispartof Nature communications, 2014-11, Vol.5 (1), p.5401-5401, Article 5401
issn 2041-1723
2041-1723
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4229994
source Springer Nature OA/Free Journals
subjects 631/443/319
631/449/2675
Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Glutathione Reductase - metabolism
Homeostasis - physiology
Humanities and Social Sciences
Models, Biological
multidisciplinary
Nitrates - metabolism
Nitric Oxide - metabolism
Nitrogen - metabolism
Oxidation-Reduction
S-Nitrosothiols - metabolism
Science
Science (multidisciplinary)
Signal Transduction - physiology
title S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-21T04%3A26%3A23IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_C6C&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=S-nitrosothiols%20regulate%20nitric%20oxide%20production%20and%20storage%20in%20plants%20through%20the%20nitrogen%20assimilation%20pathway&rft.jtitle=Nature%20communications&rft.au=Frungillo,%20Lucas&rft.date=2014-11-11&rft.volume=5&rft.issue=1&rft.spage=5401&rft.epage=5401&rft.pages=5401-5401&rft.artnum=5401&rft.issn=2041-1723&rft.eissn=2041-1723&rft_id=info:doi/10.1038/ncomms6401&rft_dat=%3Cproquest_C6C%3E3491038721%3C/proquest_C6C%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1622307664&rft_id=info:pmid/25384398&rfr_iscdi=true