Protein Carbonylation and Glycation in Legume Nodules1

In legume nodules, selective carbonylation and glycation of proteins occurs during nodule development and may have a role in the regulation of metabolism and senescence. Nitrogen fixation is an agronomically and environmentally important process catalyzed by bacterial nitrogenase within legume root...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Plant physiology (Bethesda) 2018-07, Vol.177 (4), p.1510-1528
Hauptverfasser: Matamoros, Manuel A., Kim, Ahyoung, Peñuelas, María, Ihling, Christian, Griesser, Eva, Hoffmann, Ralf, Fedorova, Maria, Frolov, Andrej, Becana, Manuel
Format: Artikel
Sprache:eng
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1528
container_issue 4
container_start_page 1510
container_title Plant physiology (Bethesda)
container_volume 177
creator Matamoros, Manuel A.
Kim, Ahyoung
Peñuelas, María
Ihling, Christian
Griesser, Eva
Hoffmann, Ralf
Fedorova, Maria
Frolov, Andrej
Becana, Manuel
description In legume nodules, selective carbonylation and glycation of proteins occurs during nodule development and may have a role in the regulation of metabolism and senescence. Nitrogen fixation is an agronomically and environmentally important process catalyzed by bacterial nitrogenase within legume root nodules. These unique symbiotic organs have high metabolic rates and produce large amounts of reactive oxygen species that may modify proteins irreversibly. Here, we examined two types of oxidative posttranslational modifications of nodule proteins: carbonylation, which occurs by direct oxidation of certain amino acids or by interaction with reactive aldehydes arising from cell membrane lipid peroxides; and glycation, which results from the reaction of lysine and arginine residues with reducing sugars or their autooxidation products. We used a strategy based on the enrichment of carbonylated peptides by affinity chromatography followed by liquid chromatography-tandem mass spectrometry to identify 369 oxidized proteins in bean ( Phaseolus vulgaris ) nodules. Of these, 238 corresponded to plant proteins and 131 to bacterial proteins. Lipid peroxidation products induced most carbonylation sites. This study also revealed that carbonylation has major effects on two key nodule proteins. Metal-catalyzed oxidation caused the inactivation of malate dehydrogenase and the aggregation of leghemoglobin. In addition, numerous glycated proteins were identified in vivo, including three key nodule proteins: sucrose synthase, glutamine synthetase, and glutamate synthase. Label-free quantification identified 10 plant proteins and 18 bacterial proteins as age-specifically glycated. Overall, our results suggest that the selective carbonylation or glycation of crucial proteins involved in nitrogen metabolism, transcriptional regulation, and signaling may constitute a mechanism to control cell metabolism and nodule senescence.
doi_str_mv 10.1104/pp.18.00533
format Article
fullrecord <record><control><sourceid>pubmedcentral</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6084676</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>pubmedcentral_primary_oai_pubmedcentral_nih_gov_6084676</sourcerecordid><originalsourceid>FETCH-pubmedcentral_primary_oai_pubmedcentral_nih_gov_60846763</originalsourceid><addsrcrecordid>eNqljLFuwjAURZ8QCNLCxA_kBwjvxU5wFhZUyoBQh-6WIQaMHDtyEqT8PUhl6cx0z9GRLsCcMCFCvqzrhESCmDE2gIgyli7SjIshRIhPRiGKCXw0zQ0RiREfwyQtihVyYhHkP8G32rh4o8LRu96q1ngXK1fG37Y__dkz7_Wlq3R88GVndUNTGJ2VbfTstZ-w3n79bnaLujtWujxp1wZlZR1MpUIvvTLyf3HmKi_-LnMUPF_l7O2DB3cGU4s</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>Protein Carbonylation and Glycation in Legume Nodules1</title><source>JSTOR Archive Collection A-Z Listing</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Matamoros, Manuel A. ; Kim, Ahyoung ; Peñuelas, María ; Ihling, Christian ; Griesser, Eva ; Hoffmann, Ralf ; Fedorova, Maria ; Frolov, Andrej ; Becana, Manuel</creator><creatorcontrib>Matamoros, Manuel A. ; Kim, Ahyoung ; Peñuelas, María ; Ihling, Christian ; Griesser, Eva ; Hoffmann, Ralf ; Fedorova, Maria ; Frolov, Andrej ; Becana, Manuel</creatorcontrib><description>In legume nodules, selective carbonylation and glycation of proteins occurs during nodule development and may have a role in the regulation of metabolism and senescence. Nitrogen fixation is an agronomically and environmentally important process catalyzed by bacterial nitrogenase within legume root nodules. These unique symbiotic organs have high metabolic rates and produce large amounts of reactive oxygen species that may modify proteins irreversibly. Here, we examined two types of oxidative posttranslational modifications of nodule proteins: carbonylation, which occurs by direct oxidation of certain amino acids or by interaction with reactive aldehydes arising from cell membrane lipid peroxides; and glycation, which results from the reaction of lysine and arginine residues with reducing sugars or their autooxidation products. We used a strategy based on the enrichment of carbonylated peptides by affinity chromatography followed by liquid chromatography-tandem mass spectrometry to identify 369 oxidized proteins in bean ( Phaseolus vulgaris ) nodules. Of these, 238 corresponded to plant proteins and 131 to bacterial proteins. Lipid peroxidation products induced most carbonylation sites. This study also revealed that carbonylation has major effects on two key nodule proteins. Metal-catalyzed oxidation caused the inactivation of malate dehydrogenase and the aggregation of leghemoglobin. In addition, numerous glycated proteins were identified in vivo, including three key nodule proteins: sucrose synthase, glutamine synthetase, and glutamate synthase. Label-free quantification identified 10 plant proteins and 18 bacterial proteins as age-specifically glycated. Overall, our results suggest that the selective carbonylation or glycation of crucial proteins involved in nitrogen metabolism, transcriptional regulation, and signaling may constitute a mechanism to control cell metabolism and nodule senescence.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.18.00533</identifier><identifier>PMID: 29970413</identifier><language>eng</language><publisher>American Society of Plant Biologists</publisher><ispartof>Plant physiology (Bethesda), 2018-07, Vol.177 (4), p.1510-1528</ispartof><rights>2018 American Society of Plant Biologists. All rights reserved. 2018</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,27929,27930</link.rule.ids></links><search><creatorcontrib>Matamoros, Manuel A.</creatorcontrib><creatorcontrib>Kim, Ahyoung</creatorcontrib><creatorcontrib>Peñuelas, María</creatorcontrib><creatorcontrib>Ihling, Christian</creatorcontrib><creatorcontrib>Griesser, Eva</creatorcontrib><creatorcontrib>Hoffmann, Ralf</creatorcontrib><creatorcontrib>Fedorova, Maria</creatorcontrib><creatorcontrib>Frolov, Andrej</creatorcontrib><creatorcontrib>Becana, Manuel</creatorcontrib><title>Protein Carbonylation and Glycation in Legume Nodules1</title><title>Plant physiology (Bethesda)</title><description>In legume nodules, selective carbonylation and glycation of proteins occurs during nodule development and may have a role in the regulation of metabolism and senescence. Nitrogen fixation is an agronomically and environmentally important process catalyzed by bacterial nitrogenase within legume root nodules. These unique symbiotic organs have high metabolic rates and produce large amounts of reactive oxygen species that may modify proteins irreversibly. Here, we examined two types of oxidative posttranslational modifications of nodule proteins: carbonylation, which occurs by direct oxidation of certain amino acids or by interaction with reactive aldehydes arising from cell membrane lipid peroxides; and glycation, which results from the reaction of lysine and arginine residues with reducing sugars or their autooxidation products. We used a strategy based on the enrichment of carbonylated peptides by affinity chromatography followed by liquid chromatography-tandem mass spectrometry to identify 369 oxidized proteins in bean ( Phaseolus vulgaris ) nodules. Of these, 238 corresponded to plant proteins and 131 to bacterial proteins. Lipid peroxidation products induced most carbonylation sites. This study also revealed that carbonylation has major effects on two key nodule proteins. Metal-catalyzed oxidation caused the inactivation of malate dehydrogenase and the aggregation of leghemoglobin. In addition, numerous glycated proteins were identified in vivo, including three key nodule proteins: sucrose synthase, glutamine synthetase, and glutamate synthase. Label-free quantification identified 10 plant proteins and 18 bacterial proteins as age-specifically glycated. Overall, our results suggest that the selective carbonylation or glycation of crucial proteins involved in nitrogen metabolism, transcriptional regulation, and signaling may constitute a mechanism to control cell metabolism and nodule senescence.</description><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNqljLFuwjAURZ8QCNLCxA_kBwjvxU5wFhZUyoBQh-6WIQaMHDtyEqT8PUhl6cx0z9GRLsCcMCFCvqzrhESCmDE2gIgyli7SjIshRIhPRiGKCXw0zQ0RiREfwyQtihVyYhHkP8G32rh4o8LRu96q1ngXK1fG37Y__dkz7_Wlq3R88GVndUNTGJ2VbfTstZ-w3n79bnaLujtWujxp1wZlZR1MpUIvvTLyf3HmKi_-LnMUPF_l7O2DB3cGU4s</recordid><startdate>20180703</startdate><enddate>20180703</enddate><creator>Matamoros, Manuel A.</creator><creator>Kim, Ahyoung</creator><creator>Peñuelas, María</creator><creator>Ihling, Christian</creator><creator>Griesser, Eva</creator><creator>Hoffmann, Ralf</creator><creator>Fedorova, Maria</creator><creator>Frolov, Andrej</creator><creator>Becana, Manuel</creator><general>American Society of Plant Biologists</general><scope>5PM</scope></search><sort><creationdate>20180703</creationdate><title>Protein Carbonylation and Glycation in Legume Nodules1</title><author>Matamoros, Manuel A. ; Kim, Ahyoung ; Peñuelas, María ; Ihling, Christian ; Griesser, Eva ; Hoffmann, Ralf ; Fedorova, Maria ; Frolov, Andrej ; Becana, Manuel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-pubmedcentral_primary_oai_pubmedcentral_nih_gov_60846763</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Matamoros, Manuel A.</creatorcontrib><creatorcontrib>Kim, Ahyoung</creatorcontrib><creatorcontrib>Peñuelas, María</creatorcontrib><creatorcontrib>Ihling, Christian</creatorcontrib><creatorcontrib>Griesser, Eva</creatorcontrib><creatorcontrib>Hoffmann, Ralf</creatorcontrib><creatorcontrib>Fedorova, Maria</creatorcontrib><creatorcontrib>Frolov, Andrej</creatorcontrib><creatorcontrib>Becana, Manuel</creatorcontrib><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Matamoros, Manuel A.</au><au>Kim, Ahyoung</au><au>Peñuelas, María</au><au>Ihling, Christian</au><au>Griesser, Eva</au><au>Hoffmann, Ralf</au><au>Fedorova, Maria</au><au>Frolov, Andrej</au><au>Becana, Manuel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Protein Carbonylation and Glycation in Legume Nodules1</atitle><jtitle>Plant physiology (Bethesda)</jtitle><date>2018-07-03</date><risdate>2018</risdate><volume>177</volume><issue>4</issue><spage>1510</spage><epage>1528</epage><pages>1510-1528</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>In legume nodules, selective carbonylation and glycation of proteins occurs during nodule development and may have a role in the regulation of metabolism and senescence. Nitrogen fixation is an agronomically and environmentally important process catalyzed by bacterial nitrogenase within legume root nodules. These unique symbiotic organs have high metabolic rates and produce large amounts of reactive oxygen species that may modify proteins irreversibly. Here, we examined two types of oxidative posttranslational modifications of nodule proteins: carbonylation, which occurs by direct oxidation of certain amino acids or by interaction with reactive aldehydes arising from cell membrane lipid peroxides; and glycation, which results from the reaction of lysine and arginine residues with reducing sugars or their autooxidation products. We used a strategy based on the enrichment of carbonylated peptides by affinity chromatography followed by liquid chromatography-tandem mass spectrometry to identify 369 oxidized proteins in bean ( Phaseolus vulgaris ) nodules. Of these, 238 corresponded to plant proteins and 131 to bacterial proteins. Lipid peroxidation products induced most carbonylation sites. This study also revealed that carbonylation has major effects on two key nodule proteins. Metal-catalyzed oxidation caused the inactivation of malate dehydrogenase and the aggregation of leghemoglobin. In addition, numerous glycated proteins were identified in vivo, including three key nodule proteins: sucrose synthase, glutamine synthetase, and glutamate synthase. Label-free quantification identified 10 plant proteins and 18 bacterial proteins as age-specifically glycated. Overall, our results suggest that the selective carbonylation or glycation of crucial proteins involved in nitrogen metabolism, transcriptional regulation, and signaling may constitute a mechanism to control cell metabolism and nodule senescence.</abstract><pub>American Society of Plant Biologists</pub><pmid>29970413</pmid><doi>10.1104/pp.18.00533</doi></addata></record>
fulltext fulltext
identifier ISSN: 0032-0889
ispartof Plant physiology (Bethesda), 2018-07, Vol.177 (4), p.1510-1528
issn 0032-0889
1532-2548
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6084676
source JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals
title Protein Carbonylation and Glycation in Legume Nodules1
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-14T18%3A34%3A33IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-pubmedcentral&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Protein%20Carbonylation%20and%20Glycation%20in%20Legume%20Nodules1&rft.jtitle=Plant%20physiology%20(Bethesda)&rft.au=Matamoros,%20Manuel%20A.&rft.date=2018-07-03&rft.volume=177&rft.issue=4&rft.spage=1510&rft.epage=1528&rft.pages=1510-1528&rft.issn=0032-0889&rft.eissn=1532-2548&rft_id=info:doi/10.1104/pp.18.00533&rft_dat=%3Cpubmedcentral%3Epubmedcentral_primary_oai_pubmedcentral_nih_gov_6084676%3C/pubmedcentral%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_id=info:pmid/29970413&rfr_iscdi=true