The Mitochondrial Sulfur Dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 Is Required for Amino Acid Catabolism during Carbohydrate Starvation and Embryo Development in Arabidopsis
The sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 (ETHE1) catalyzes the oxidation of persulfides in the mitochondrial matrix and is essential for early embryo development in Arabidopsis (Arabidopsis thaliana). We investigated the biochemical and physiological functions of ETHE1 in plant me...
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| Veröffentlicht in: | Plant physiology (Bethesda) 2014-05, Vol.165 (1), p.92-104 |
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| creator | Krüßel, Lena Junemann, Johannes Wirtz, Markus Birke, Hannah Thornton, Jeremy D. Browning, Luke W. Poschet, Gernot Hell, Rüdiger Balk, Janneke Braun, Hans-Peter Hildebrandt, Tatjana M. |
| description | The sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 (ETHE1) catalyzes the oxidation of persulfides in the mitochondrial matrix and is essential for early embryo development in Arabidopsis (Arabidopsis thaliana). We investigated the biochemical and physiological functions of ETHE1 in plant metabolism using recombinant Arabidopsis ETHE1 and three transfer DNA insertion lines with 50% to 99% decreased sulfur dioxygenase activity. Our results identified a new mitochondrial pathway catalyzing the detoxification of reduced sulfur species derived from cysteine catabolism by oxidation to thiosulfate. Knockdown of the sulfur dioxygenase impaired embryo development and produced phenotypes of starvation-induced chlorosis during short-day growth conditions and extended darkness, indicating that ETHE1 has a key function in situations of high protein turnover, such as seed production and the use of amino acids as alternative respiratory substrates during carbohydrate starvation. The amino acid profile of mutant plants was similar to that caused by defects in the electron-transfer flavoprotein/electron-transfer flavoprotein: ubiquinone oxidoreductase complex and associated dehydrogenases. Thus, in addition to sulfur amino acid catabolism, ETHE1 also affects the oxidation of branched-chain amino acids and lysine. |
| doi_str_mv | 10.1104/pp.114.239764 |
| format | Article |
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We investigated the biochemical and physiological functions of ETHE1 in plant metabolism using recombinant Arabidopsis ETHE1 and three transfer DNA insertion lines with 50% to 99% decreased sulfur dioxygenase activity. Our results identified a new mitochondrial pathway catalyzing the detoxification of reduced sulfur species derived from cysteine catabolism by oxidation to thiosulfate. Knockdown of the sulfur dioxygenase impaired embryo development and produced phenotypes of starvation-induced chlorosis during short-day growth conditions and extended darkness, indicating that ETHE1 has a key function in situations of high protein turnover, such as seed production and the use of amino acids as alternative respiratory substrates during carbohydrate starvation. The amino acid profile of mutant plants was similar to that caused by defects in the electron-transfer flavoprotein/electron-transfer flavoprotein: ubiquinone oxidoreductase complex and associated dehydrogenases. Thus, in addition to sulfur amino acid catabolism, ETHE1 also affects the oxidation of branched-chain amino acids and lysine.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.114.239764</identifier><identifier>PMID: 24692429</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Amino acid metabolism ; Amino acids ; Amino Acids - metabolism ; Arabidopsis ; Arabidopsis - embryology ; Arabidopsis - enzymology ; Arabidopsis - growth & development ; Arabidopsis Proteins - metabolism ; BIOCHEMISTRY AND METABOLISM ; Carbohydrate Metabolism ; Catabolism ; Dehydrogenases ; Dioxygenases - metabolism ; DNA, Bacterial - genetics ; embryogenesis ; encephalopathy ; Gene Knockdown Techniques ; Glutathione - metabolism ; hydrogen sulfide ; Metabolic Networks and Pathways ; Mitochondria ; Mitochondria - enzymology ; Models, Biological ; Mutagenesis, Insertional - genetics ; Oxidation ; Oxidation-Reduction ; Phenotype ; Plants ; Seeds - embryology ; Seeds - enzymology ; starvation ; Substrate Specificity ; Sulfides ; Sulfides - metabolism ; Sulfites ; Sulfites - metabolism ; Sulfur ; Sulfur - metabolism ; thiosulfates</subject><ispartof>Plant physiology (Bethesda), 2014-05, Vol.165 (1), p.92-104</ispartof><rights>2014 American Society of Plant Biologists</rights><rights>2014 American Society of Plant Biologists. All Rights Reserved. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c508t-64a9cbcd7ee9de98683335e5d8c5bd48ea5e6cde25082ef9c75f6795c21f3993</citedby><cites>FETCH-LOGICAL-c508t-64a9cbcd7ee9de98683335e5d8c5bd48ea5e6cde25082ef9c75f6795c21f3993</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43190938$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43190938$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24692429$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Krüßel, Lena</creatorcontrib><creatorcontrib>Junemann, Johannes</creatorcontrib><creatorcontrib>Wirtz, Markus</creatorcontrib><creatorcontrib>Birke, Hannah</creatorcontrib><creatorcontrib>Thornton, Jeremy D.</creatorcontrib><creatorcontrib>Browning, Luke W.</creatorcontrib><creatorcontrib>Poschet, Gernot</creatorcontrib><creatorcontrib>Hell, Rüdiger</creatorcontrib><creatorcontrib>Balk, Janneke</creatorcontrib><creatorcontrib>Braun, Hans-Peter</creatorcontrib><creatorcontrib>Hildebrandt, Tatjana M.</creatorcontrib><title>The Mitochondrial Sulfur Dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 Is Required for Amino Acid Catabolism during Carbohydrate Starvation and Embryo Development in Arabidopsis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>The sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 (ETHE1) catalyzes the oxidation of persulfides in the mitochondrial matrix and is essential for early embryo development in Arabidopsis (Arabidopsis thaliana). We investigated the biochemical and physiological functions of ETHE1 in plant metabolism using recombinant Arabidopsis ETHE1 and three transfer DNA insertion lines with 50% to 99% decreased sulfur dioxygenase activity. Our results identified a new mitochondrial pathway catalyzing the detoxification of reduced sulfur species derived from cysteine catabolism by oxidation to thiosulfate. Knockdown of the sulfur dioxygenase impaired embryo development and produced phenotypes of starvation-induced chlorosis during short-day growth conditions and extended darkness, indicating that ETHE1 has a key function in situations of high protein turnover, such as seed production and the use of amino acids as alternative respiratory substrates during carbohydrate starvation. The amino acid profile of mutant plants was similar to that caused by defects in the electron-transfer flavoprotein/electron-transfer flavoprotein: ubiquinone oxidoreductase complex and associated dehydrogenases. Thus, in addition to sulfur amino acid catabolism, ETHE1 also affects the oxidation of branched-chain amino acids and lysine.</description><subject>Amino acid metabolism</subject><subject>Amino acids</subject><subject>Amino Acids - metabolism</subject><subject>Arabidopsis</subject><subject>Arabidopsis - embryology</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>BIOCHEMISTRY AND METABOLISM</subject><subject>Carbohydrate Metabolism</subject><subject>Catabolism</subject><subject>Dehydrogenases</subject><subject>Dioxygenases - metabolism</subject><subject>DNA, Bacterial - genetics</subject><subject>embryogenesis</subject><subject>encephalopathy</subject><subject>Gene Knockdown Techniques</subject><subject>Glutathione - metabolism</subject><subject>hydrogen sulfide</subject><subject>Metabolic Networks and Pathways</subject><subject>Mitochondria</subject><subject>Mitochondria - enzymology</subject><subject>Models, Biological</subject><subject>Mutagenesis, Insertional - genetics</subject><subject>Oxidation</subject><subject>Oxidation-Reduction</subject><subject>Phenotype</subject><subject>Plants</subject><subject>Seeds - embryology</subject><subject>Seeds - enzymology</subject><subject>starvation</subject><subject>Substrate Specificity</subject><subject>Sulfides</subject><subject>Sulfides - metabolism</subject><subject>Sulfites</subject><subject>Sulfites - metabolism</subject><subject>Sulfur</subject><subject>Sulfur - metabolism</subject><subject>thiosulfates</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUtv00AUhS0EoqGwZAmaJZuUednxbJAs15BIaRK12bCyxjPXyVS2x52xI_K_-IFMlBK1q3Mfn8690omizwTfEIL5974Pym8oE7OEv4kmJGZ0SmOevo0mGIcap6m4ij54_4gxJozw99EV5YmgnIpJ9He7B3RnBqv2ttPOyAY9jE09OnRr7J_jDjrpARXb-e_lXbZcrxY5KlZ5sZmHZpOFMdrcr7fFYkXQwqN7eBqNA41q61DWms6iTBmNcjnIyjbGt0iPznS7MHGV3R-1kwOgh0G6gxyM7ZDsNCrayh0tuoUDNLZvoRuQ6VDmZGW07b3xH6N3tWw8fHrW62j7s9jm8-ly_WuRZ8upinE6TBMuhaqUngEIDSJNUsZYDLFOVVxpnoKMIVEaaKAp1ELN4jqZiVhRUjMh2HX042zbj1ULWoVHnGzK3plWumNppSlfbzqzL3f2UHJMaIJnweDbs4GzTyP4oWyNV9A0sgM7-pKeEqGnTAI6PaPKWe8d1JczBJenoMu-D8rLc9CB__rytwv9P9kAfDkDj36w7rLnjAgsWMr-Abser-M</recordid><startdate>20140501</startdate><enddate>20140501</enddate><creator>Krüßel, Lena</creator><creator>Junemann, Johannes</creator><creator>Wirtz, Markus</creator><creator>Birke, Hannah</creator><creator>Thornton, Jeremy D.</creator><creator>Browning, Luke W.</creator><creator>Poschet, Gernot</creator><creator>Hell, Rüdiger</creator><creator>Balk, Janneke</creator><creator>Braun, Hans-Peter</creator><creator>Hildebrandt, Tatjana M.</creator><general>American Society of Plant Biologists</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>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20140501</creationdate><title>The Mitochondrial Sulfur Dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 Is Required for Amino Acid Catabolism during Carbohydrate Starvation and Embryo Development in Arabidopsis</title><author>Krüßel, Lena ; Junemann, Johannes ; Wirtz, Markus ; Birke, Hannah ; Thornton, Jeremy D. ; Browning, Luke W. ; Poschet, Gernot ; Hell, Rüdiger ; Balk, Janneke ; Braun, Hans-Peter ; Hildebrandt, Tatjana M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c508t-64a9cbcd7ee9de98683335e5d8c5bd48ea5e6cde25082ef9c75f6795c21f3993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amino acid metabolism</topic><topic>Amino acids</topic><topic>Amino Acids - metabolism</topic><topic>Arabidopsis</topic><topic>Arabidopsis - embryology</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BIOCHEMISTRY AND METABOLISM</topic><topic>Carbohydrate Metabolism</topic><topic>Catabolism</topic><topic>Dehydrogenases</topic><topic>Dioxygenases - metabolism</topic><topic>DNA, Bacterial - genetics</topic><topic>embryogenesis</topic><topic>encephalopathy</topic><topic>Gene Knockdown Techniques</topic><topic>Glutathione - metabolism</topic><topic>hydrogen sulfide</topic><topic>Metabolic Networks and Pathways</topic><topic>Mitochondria</topic><topic>Mitochondria - enzymology</topic><topic>Models, Biological</topic><topic>Mutagenesis, Insertional - genetics</topic><topic>Oxidation</topic><topic>Oxidation-Reduction</topic><topic>Phenotype</topic><topic>Plants</topic><topic>Seeds - embryology</topic><topic>Seeds - enzymology</topic><topic>starvation</topic><topic>Substrate Specificity</topic><topic>Sulfides</topic><topic>Sulfides - metabolism</topic><topic>Sulfites</topic><topic>Sulfites - metabolism</topic><topic>Sulfur</topic><topic>Sulfur - metabolism</topic><topic>thiosulfates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Krüßel, Lena</creatorcontrib><creatorcontrib>Junemann, Johannes</creatorcontrib><creatorcontrib>Wirtz, Markus</creatorcontrib><creatorcontrib>Birke, Hannah</creatorcontrib><creatorcontrib>Thornton, Jeremy D.</creatorcontrib><creatorcontrib>Browning, Luke W.</creatorcontrib><creatorcontrib>Poschet, Gernot</creatorcontrib><creatorcontrib>Hell, Rüdiger</creatorcontrib><creatorcontrib>Balk, Janneke</creatorcontrib><creatorcontrib>Braun, Hans-Peter</creatorcontrib><creatorcontrib>Hildebrandt, Tatjana M.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><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>Krüßel, Lena</au><au>Junemann, Johannes</au><au>Wirtz, Markus</au><au>Birke, Hannah</au><au>Thornton, Jeremy D.</au><au>Browning, Luke W.</au><au>Poschet, Gernot</au><au>Hell, Rüdiger</au><au>Balk, Janneke</au><au>Braun, Hans-Peter</au><au>Hildebrandt, Tatjana M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Mitochondrial Sulfur Dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 Is Required for Amino Acid Catabolism during Carbohydrate Starvation and Embryo Development in Arabidopsis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2014-05-01</date><risdate>2014</risdate><volume>165</volume><issue>1</issue><spage>92</spage><epage>104</epage><pages>92-104</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><abstract>The sulfur dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 (ETHE1) catalyzes the oxidation of persulfides in the mitochondrial matrix and is essential for early embryo development in Arabidopsis (Arabidopsis thaliana). We investigated the biochemical and physiological functions of ETHE1 in plant metabolism using recombinant Arabidopsis ETHE1 and three transfer DNA insertion lines with 50% to 99% decreased sulfur dioxygenase activity. Our results identified a new mitochondrial pathway catalyzing the detoxification of reduced sulfur species derived from cysteine catabolism by oxidation to thiosulfate. Knockdown of the sulfur dioxygenase impaired embryo development and produced phenotypes of starvation-induced chlorosis during short-day growth conditions and extended darkness, indicating that ETHE1 has a key function in situations of high protein turnover, such as seed production and the use of amino acids as alternative respiratory substrates during carbohydrate starvation. The amino acid profile of mutant plants was similar to that caused by defects in the electron-transfer flavoprotein/electron-transfer flavoprotein: ubiquinone oxidoreductase complex and associated dehydrogenases. Thus, in addition to sulfur amino acid catabolism, ETHE1 also affects the oxidation of branched-chain amino acids and lysine.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>24692429</pmid><doi>10.1104/pp.114.239764</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino acid metabolism Amino acids Amino Acids - metabolism Arabidopsis Arabidopsis - embryology Arabidopsis - enzymology Arabidopsis - growth & development Arabidopsis Proteins - metabolism BIOCHEMISTRY AND METABOLISM Carbohydrate Metabolism Catabolism Dehydrogenases Dioxygenases - metabolism DNA, Bacterial - genetics embryogenesis encephalopathy Gene Knockdown Techniques Glutathione - metabolism hydrogen sulfide Metabolic Networks and Pathways Mitochondria Mitochondria - enzymology Models, Biological Mutagenesis, Insertional - genetics Oxidation Oxidation-Reduction Phenotype Plants Seeds - embryology Seeds - enzymology starvation Substrate Specificity Sulfides Sulfides - metabolism Sulfites Sulfites - metabolism Sulfur Sulfur - metabolism thiosulfates |
| title | The Mitochondrial Sulfur Dioxygenase ETHYLMALONIC ENCEPHALOPATHY PROTEIN1 Is Required for Amino Acid Catabolism during Carbohydrate Starvation and Embryo Development in Arabidopsis |
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