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Comprehensive Mitochondrial Metabolic Shift during the Critical Node of Seed Ageing in Rice
The critical node (CN) in seed aging in rice (Oryza sativa) is the transformation from Phase I (P-I) to Phase II (P-II) of the reverse S-shaped curve (RS-SC). Although mitochondrial dysfunction plays a key role in seed ageing, the metabolic shift in the CN remains poorly understood. Here, we investi...
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Published in: | PloS one 2016-04, Vol.11 (4), p.e0148013-e0148013 |
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description | The critical node (CN) in seed aging in rice (Oryza sativa) is the transformation from Phase I (P-I) to Phase II (P-II) of the reverse S-shaped curve (RS-SC). Although mitochondrial dysfunction plays a key role in seed ageing, the metabolic shift in the CN remains poorly understood. Here, we investigated the mitochondrial regulatory mechanisms during the CN of rice seed ageing. We showed that during the CN of seed ageing, the mitochondrial ultrastructure was impaired, causing oxygen consumption to decrease, along with cytochrome c (cyt c) oxidase and malate dehydrogenase (MDH) activity. In addition, the transcript levels for the alternative pathway of the electron transport chain (ETC) were significantly induced, whereas the transcripts of the cytochrome oxidase (COX) pathway were inhibited. These changes were concomitant with the down-regulation of mitochondrial protein levels related to carbon and nitrogen metabolism, ATP synthase (ATPase) complex, tricarboxylic acid cycle (TCA) cycle, mitochondrial oxidative enzymes, and a variety of other proteins. Therefore, while these responses inhibit the production of ATP and its intermediates, signals from mitochondria (such as the decrease of cyt c and accumulation of reactive oxygen species (ROS)) may also induce oxidative damage. These events provide considerable information about the mitochondrial metabolic shifts involved in the progression of seed ageing in the CN. |
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Although mitochondrial dysfunction plays a key role in seed ageing, the metabolic shift in the CN remains poorly understood. Here, we investigated the mitochondrial regulatory mechanisms during the CN of rice seed ageing. We showed that during the CN of seed ageing, the mitochondrial ultrastructure was impaired, causing oxygen consumption to decrease, along with cytochrome c (cyt c) oxidase and malate dehydrogenase (MDH) activity. In addition, the transcript levels for the alternative pathway of the electron transport chain (ETC) were significantly induced, whereas the transcripts of the cytochrome oxidase (COX) pathway were inhibited. These changes were concomitant with the down-regulation of mitochondrial protein levels related to carbon and nitrogen metabolism, ATP synthase (ATPase) complex, tricarboxylic acid cycle (TCA) cycle, mitochondrial oxidative enzymes, and a variety of other proteins. Therefore, while these responses inhibit the production of ATP and its intermediates, signals from mitochondria (such as the decrease of cyt c and accumulation of reactive oxygen species (ROS)) may also induce oxidative damage. These events provide considerable information about the mitochondrial metabolic shifts involved in the progression of seed ageing in the CN.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0148013</identifier><identifier>PMID: 27124767</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adenosine triphosphatase ; Adenosine Triphosphatases - metabolism ; Adenosine triphosphate ; Aging ; Aging (Biology) ; Aging - metabolism ; Apoptosis ; Arabidopsis ; ATP ; ATP synthase ; Biology and Life Sciences ; Biosynthesis ; Carbon - metabolism ; Citric Acid Cycle - physiology ; Crop science ; Cytochrome ; Cytochrome c ; Cytochromes c - metabolism ; Damage accumulation ; Down-Regulation - physiology ; Electron transport ; Electron transport chain ; Electron Transport Complex IV - metabolism ; Enzymes ; Gene expression ; Intermediates ; Malate ; Malate dehydrogenase ; Malate Dehydrogenase - metabolism ; Metabolism ; Mitochondria ; Mitochondria - metabolism ; Mitochondrial Proteins - metabolism ; Nitrogen - metabolism ; Oryza - metabolism ; Oryza sativa ; Oxidase ; Oxidation-Reduction ; Oxidative stress ; Oxidative Stress - physiology ; Oxygen ; Oxygen consumption ; Oxygen Consumption - physiology ; Pennisetum glaucum ; Phase transitions ; Physiological aspects ; Plant metabolism ; Plant mitochondria ; Proteins ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Regulatory mechanisms (biology) ; Research and Analysis Methods ; Rice ; Seeds ; Seeds - metabolism ; Studies ; Transcription ; Transformation ; Tricarboxylic acid cycle ; Ultrastructure</subject><ispartof>PloS one, 2016-04, Vol.11 (4), p.e0148013-e0148013</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Yin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Yin et al 2016 Yin et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-3a2666a196bcd1d5aae16172e2d7ec37e8e9601851af38a6fbac1dc71fe5119b3</citedby><cites>FETCH-LOGICAL-c692t-3a2666a196bcd1d5aae16172e2d7ec37e8e9601851af38a6fbac1dc71fe5119b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1785219987/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1785219987?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27124767$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Araujo, Wagner L.</contributor><creatorcontrib>Yin, Guangkun</creatorcontrib><creatorcontrib>Whelan, James</creatorcontrib><creatorcontrib>Wu, Shuhua</creatorcontrib><creatorcontrib>Zhou, Jing</creatorcontrib><creatorcontrib>Chen, Baoyin</creatorcontrib><creatorcontrib>Chen, Xiaoling</creatorcontrib><creatorcontrib>Zhang, Jinmei</creatorcontrib><creatorcontrib>He, Juanjuan</creatorcontrib><creatorcontrib>Xin, Xia</creatorcontrib><creatorcontrib>Lu, Xinxiong</creatorcontrib><title>Comprehensive Mitochondrial Metabolic Shift during the Critical Node of Seed Ageing in Rice</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The critical node (CN) in seed aging in rice (Oryza sativa) is the transformation from Phase I (P-I) to Phase II (P-II) of the reverse S-shaped curve (RS-SC). Although mitochondrial dysfunction plays a key role in seed ageing, the metabolic shift in the CN remains poorly understood. Here, we investigated the mitochondrial regulatory mechanisms during the CN of rice seed ageing. We showed that during the CN of seed ageing, the mitochondrial ultrastructure was impaired, causing oxygen consumption to decrease, along with cytochrome c (cyt c) oxidase and malate dehydrogenase (MDH) activity. In addition, the transcript levels for the alternative pathway of the electron transport chain (ETC) were significantly induced, whereas the transcripts of the cytochrome oxidase (COX) pathway were inhibited. These changes were concomitant with the down-regulation of mitochondrial protein levels related to carbon and nitrogen metabolism, ATP synthase (ATPase) complex, tricarboxylic acid cycle (TCA) cycle, mitochondrial oxidative enzymes, and a variety of other proteins. Therefore, while these responses inhibit the production of ATP and its intermediates, signals from mitochondria (such as the decrease of cyt c and accumulation of reactive oxygen species (ROS)) may also induce oxidative damage. These events provide considerable information about the mitochondrial metabolic shifts involved in the progression of seed ageing in the CN.</description><subject>Adenosine triphosphatase</subject><subject>Adenosine Triphosphatases - metabolism</subject><subject>Adenosine triphosphate</subject><subject>Aging</subject><subject>Aging (Biology)</subject><subject>Aging - metabolism</subject><subject>Apoptosis</subject><subject>Arabidopsis</subject><subject>ATP</subject><subject>ATP synthase</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Carbon - metabolism</subject><subject>Citric Acid Cycle - physiology</subject><subject>Crop science</subject><subject>Cytochrome</subject><subject>Cytochrome c</subject><subject>Cytochromes c - metabolism</subject><subject>Damage accumulation</subject><subject>Down-Regulation - physiology</subject><subject>Electron transport</subject><subject>Electron transport chain</subject><subject>Electron Transport Complex IV - metabolism</subject><subject>Enzymes</subject><subject>Gene expression</subject><subject>Intermediates</subject><subject>Malate</subject><subject>Malate dehydrogenase</subject><subject>Malate Dehydrogenase - metabolism</subject><subject>Metabolism</subject><subject>Mitochondria</subject><subject>Mitochondria - metabolism</subject><subject>Mitochondrial Proteins - metabolism</subject><subject>Nitrogen - metabolism</subject><subject>Oryza - metabolism</subject><subject>Oryza sativa</subject><subject>Oxidase</subject><subject>Oxidation-Reduction</subject><subject>Oxidative stress</subject><subject>Oxidative Stress - physiology</subject><subject>Oxygen</subject><subject>Oxygen consumption</subject><subject>Oxygen Consumption - physiology</subject><subject>Pennisetum glaucum</subject><subject>Phase transitions</subject><subject>Physiological aspects</subject><subject>Plant metabolism</subject><subject>Plant mitochondria</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Regulatory mechanisms (biology)</subject><subject>Research and Analysis Methods</subject><subject>Rice</subject><subject>Seeds</subject><subject>Seeds - metabolism</subject><subject>Studies</subject><subject>Transcription</subject><subject>Transformation</subject><subject>Tricarboxylic acid cycle</subject><subject>Ultrastructure</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99v0zAQxyMEYmPwHyCIhITgoSWOE9t5QaoqflTamLQCLzxYjn1OXKVxZzsT_Pe4azY1aA_ID7bOn_ue73yXJC9RNkeYog8bO7hedPOd7WGeoYJlCD9KTlGF8xnJM_z46HySPPN-k2UlZoQ8TU5yivKCEnqa_Fra7c5BC703N5BemGBla3vljOjSCwiitp2R6bo1OqRqcKZv0tBCunQmGBmZb1ZBanW6BlDpooE9YPr0ykh4njzRovPwYtzPkh-fP31ffp2dX35ZLRfnM0mqPMywyAkhAlWklgqpUghABNEcckVBYgoMKpIhViKhMRNE10IiJSnSUCJU1fgseX3Q3XXW87EuniPKyhxVFaORWB0IZcWG75zZCveHW2H4rcG6hgsX8-mAU62LUguMaiULwXQNKs9KVQuFy1g1FLU-jtGGegtKQh-c6Cai05vetLyxN7xgRUVvBd6NAs5eD-AD3xovoetED3Y4vJuWGSNVRN_8gz6c3Ug1IiZgem1jXLkX5YuixAViOGeRmj9AxaVga2RsIm2ifeLwfuIQmQC_QyMG7_lqffX_7OXPKfv2iG1BdKH1thuCsb2fgsUBlM5670DfFxllfD8Dd9Xg-xng4wxEt1fHH3TvdNf0-C-I6AGJ</recordid><startdate>20160428</startdate><enddate>20160428</enddate><creator>Yin, Guangkun</creator><creator>Whelan, James</creator><creator>Wu, Shuhua</creator><creator>Zhou, Jing</creator><creator>Chen, Baoyin</creator><creator>Chen, Xiaoling</creator><creator>Zhang, Jinmei</creator><creator>He, Juanjuan</creator><creator>Xin, Xia</creator><creator>Lu, Xinxiong</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20160428</creationdate><title>Comprehensive Mitochondrial Metabolic Shift during the Critical Node of Seed Ageing in Rice</title><author>Yin, Guangkun ; Whelan, James ; Wu, Shuhua ; Zhou, Jing ; Chen, Baoyin ; Chen, Xiaoling ; Zhang, Jinmei ; He, Juanjuan ; Xin, Xia ; Lu, Xinxiong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-3a2666a196bcd1d5aae16172e2d7ec37e8e9601851af38a6fbac1dc71fe5119b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adenosine triphosphatase</topic><topic>Adenosine Triphosphatases - metabolism</topic><topic>Adenosine triphosphate</topic><topic>Aging</topic><topic>Aging (Biology)</topic><topic>Aging - metabolism</topic><topic>Apoptosis</topic><topic>Arabidopsis</topic><topic>ATP</topic><topic>ATP synthase</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Carbon - metabolism</topic><topic>Citric Acid Cycle - physiology</topic><topic>Crop science</topic><topic>Cytochrome</topic><topic>Cytochrome c</topic><topic>Cytochromes c - metabolism</topic><topic>Damage accumulation</topic><topic>Down-Regulation - physiology</topic><topic>Electron transport</topic><topic>Electron transport chain</topic><topic>Electron Transport Complex IV - metabolism</topic><topic>Enzymes</topic><topic>Gene expression</topic><topic>Intermediates</topic><topic>Malate</topic><topic>Malate dehydrogenase</topic><topic>Malate Dehydrogenase - metabolism</topic><topic>Metabolism</topic><topic>Mitochondria</topic><topic>Mitochondria - metabolism</topic><topic>Mitochondrial Proteins - 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Although mitochondrial dysfunction plays a key role in seed ageing, the metabolic shift in the CN remains poorly understood. Here, we investigated the mitochondrial regulatory mechanisms during the CN of rice seed ageing. We showed that during the CN of seed ageing, the mitochondrial ultrastructure was impaired, causing oxygen consumption to decrease, along with cytochrome c (cyt c) oxidase and malate dehydrogenase (MDH) activity. In addition, the transcript levels for the alternative pathway of the electron transport chain (ETC) were significantly induced, whereas the transcripts of the cytochrome oxidase (COX) pathway were inhibited. These changes were concomitant with the down-regulation of mitochondrial protein levels related to carbon and nitrogen metabolism, ATP synthase (ATPase) complex, tricarboxylic acid cycle (TCA) cycle, mitochondrial oxidative enzymes, and a variety of other proteins. Therefore, while these responses inhibit the production of ATP and its intermediates, signals from mitochondria (such as the decrease of cyt c and accumulation of reactive oxygen species (ROS)) may also induce oxidative damage. These events provide considerable information about the mitochondrial metabolic shifts involved in the progression of seed ageing in the CN.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27124767</pmid><doi>10.1371/journal.pone.0148013</doi><oa>free_for_read</oa></addata></record> |
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subjects | Adenosine triphosphatase Adenosine Triphosphatases - metabolism Adenosine triphosphate Aging Aging (Biology) Aging - metabolism Apoptosis Arabidopsis ATP ATP synthase Biology and Life Sciences Biosynthesis Carbon - metabolism Citric Acid Cycle - physiology Crop science Cytochrome Cytochrome c Cytochromes c - metabolism Damage accumulation Down-Regulation - physiology Electron transport Electron transport chain Electron Transport Complex IV - metabolism Enzymes Gene expression Intermediates Malate Malate dehydrogenase Malate Dehydrogenase - metabolism Metabolism Mitochondria Mitochondria - metabolism Mitochondrial Proteins - metabolism Nitrogen - metabolism Oryza - metabolism Oryza sativa Oxidase Oxidation-Reduction Oxidative stress Oxidative Stress - physiology Oxygen Oxygen consumption Oxygen Consumption - physiology Pennisetum glaucum Phase transitions Physiological aspects Plant metabolism Plant mitochondria Proteins Reactive oxygen species Reactive Oxygen Species - metabolism Regulatory mechanisms (biology) Research and Analysis Methods Rice Seeds Seeds - metabolism Studies Transcription Transformation Tricarboxylic acid cycle Ultrastructure |
title | Comprehensive Mitochondrial Metabolic Shift during the Critical Node of Seed Ageing in Rice |
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