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New insights into plant salt acclimation: the roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system
In this study, we investigated the cellular and molecular mechanisms that regulate salt acclimation. The main objective was to obtain new insights into the molecular mechanisms that control salt acclimation. Therefore, we carried out a multidisciplinary study using proteomic, transcriptomic, subcell...
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Published in: | The New phytologist 2015-01, Vol.205 (1), p.216-239 |
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description | In this study, we investigated the cellular and molecular mechanisms that regulate salt acclimation. The main objective was to obtain new insights into the molecular mechanisms that control salt acclimation. Therefore, we carried out a multidisciplinary study using proteomic, transcriptomic, subcellular and physiological techniques. We obtained a Nicotiana tabacum BY‐2 cell line acclimated to be grown at 258 mM NaCl as a model for this study. The proteomic and transcriptomic data indicate that the molecular response to stress (chaperones, defence proteins, etc.) is highly induced in these salt‐acclimated cells. The subcellular results show that salt induces sodium compartmentalization in the cell vacuoles and seems to be mediated by vesicle trafficking in tobacco salt‐acclimated cells. Our results demonstrate that abscisic acid (ABA) and proline metabolism are crucial in the cellular signalling of salt acclimation, probably regulating reactive oxygen species (ROS) production in the mitochondria. ROS may act as a retrograde signal, regulating the cell response. The network of endoplasmic reticulum and Golgi apparatus is highly altered in salt‐acclimated cells. The molecular and subcellular analysis suggests that the unfolded protein response is induced in salt‐acclimated cells. Finally, we propose that this mechanism may mediate cell death in salt‐acclimated cells. |
doi_str_mv | 10.1111/nph.12997 |
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The main objective was to obtain new insights into the molecular mechanisms that control salt acclimation. Therefore, we carried out a multidisciplinary study using proteomic, transcriptomic, subcellular and physiological techniques. We obtained a Nicotiana tabacum BY‐2 cell line acclimated to be grown at 258 mM NaCl as a model for this study. The proteomic and transcriptomic data indicate that the molecular response to stress (chaperones, defence proteins, etc.) is highly induced in these salt‐acclimated cells. The subcellular results show that salt induces sodium compartmentalization in the cell vacuoles and seems to be mediated by vesicle trafficking in tobacco salt‐acclimated cells. Our results demonstrate that abscisic acid (ABA) and proline metabolism are crucial in the cellular signalling of salt acclimation, probably regulating reactive oxygen species (ROS) production in the mitochondria. ROS may act as a retrograde signal, regulating the cell response. The network of endoplasmic reticulum and Golgi apparatus is highly altered in salt‐acclimated cells. The molecular and subcellular analysis suggests that the unfolded protein response is induced in salt‐acclimated cells. Finally, we propose that this mechanism may mediate cell death in salt‐acclimated cells.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.12997</identifier><identifier>PMID: 25187269</identifier><language>eng</language><publisher>England: Academic Press</publisher><subject>Abscisic acid ; Abscisic Acid - metabolism ; Acclimation ; Acclimatization ; Acclimatization - drug effects ; Apoptosis - drug effects ; Apoptosis - genetics ; Caspases - metabolism ; Cell death ; Cell growth ; Cell Line ; Cell lines ; Cell nucleus ; Cells ; Chaperones ; Cytoplasm ; endomembrane system ; Endoplasmic reticulum ; Fluorescence ; Gene Expression Regulation, Plant - drug effects ; Glutathione - metabolism ; Golgi apparatus ; Hydrogen Peroxide - metabolism ; Image contrast ; Intracellular Membranes - drug effects ; Intracellular Membranes - metabolism ; Intracellular Membranes - ultrastructure ; Malondialdehyde - metabolism ; Metabolism ; Mitochondria ; Mitochondria - drug effects ; Mitochondria - metabolism ; Mitochondria - ultrastructure ; Molecular modelling ; Multidisciplinary research ; Nicotiana - cytology ; Nicotiana - genetics ; Nicotiana - metabolism ; Nicotiana - ultrastructure ; Nicotiana tabacum ; Oxygen ; physiological transport ; Plant cells ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants ; Proline ; Proline - metabolism ; Protein folding ; Proteins ; Proteome - metabolism ; Proteomics ; Reactive oxygen species ; reactive oxygen species (ROS) ; Reactive Oxygen Species - metabolism ; Salt ; salt acclimation ; Salt Tolerance ; Salts ; Signal Transduction - drug effects ; Signaling ; Sodium ; Sodium - metabolism ; Sodium chloride ; Sodium Chloride - pharmacology ; stress response ; Subcellular Fractions - drug effects ; Subcellular Fractions - metabolism ; Tobacco ; Transcriptome - genetics ; transcriptomics ; Transport Vesicles - drug effects ; Transport Vesicles - metabolism ; Transport Vesicles - ultrastructure ; unfolded protein response ; Vacuoles ; vesicle trafficking</subject><ispartof>The New phytologist, 2015-01, Vol.205 (1), p.216-239</ispartof><rights>2015 New Phytologist Trust</rights><rights>2014 The Authors. New Phytologist © 2014 New Phytologist Trust</rights><rights>2014 The Authors. New Phytologist © 2014 New Phytologist Trust.</rights><rights>Copyright © 2014 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5537-ae380ea9ac2e9afdc09f8a6be8f80b6cb4beb3fab31235ea3f131d59c1c553303</citedby><cites>FETCH-LOGICAL-c5537-ae380ea9ac2e9afdc09f8a6be8f80b6cb4beb3fab31235ea3f131d59c1c553303</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/newphytologist.205.1.216$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/newphytologist.205.1.216$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25187269$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Garcia de la Garma, Jesus</creatorcontrib><creatorcontrib>Fernandez‐Garcia, Nieves</creatorcontrib><creatorcontrib>Bardisi, Enas</creatorcontrib><creatorcontrib>Pallol, Beatriz</creatorcontrib><creatorcontrib>Asensio‐Rubio, Jose Salvador</creatorcontrib><creatorcontrib>Bru, Roque</creatorcontrib><creatorcontrib>Olmos, Enrique</creatorcontrib><title>New insights into plant salt acclimation: the roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>In this study, we investigated the cellular and molecular mechanisms that regulate salt acclimation. The main objective was to obtain new insights into the molecular mechanisms that control salt acclimation. Therefore, we carried out a multidisciplinary study using proteomic, transcriptomic, subcellular and physiological techniques. We obtained a Nicotiana tabacum BY‐2 cell line acclimated to be grown at 258 mM NaCl as a model for this study. The proteomic and transcriptomic data indicate that the molecular response to stress (chaperones, defence proteins, etc.) is highly induced in these salt‐acclimated cells. The subcellular results show that salt induces sodium compartmentalization in the cell vacuoles and seems to be mediated by vesicle trafficking in tobacco salt‐acclimated cells. Our results demonstrate that abscisic acid (ABA) and proline metabolism are crucial in the cellular signalling of salt acclimation, probably regulating reactive oxygen species (ROS) production in the mitochondria. ROS may act as a retrograde signal, regulating the cell response. The network of endoplasmic reticulum and Golgi apparatus is highly altered in salt‐acclimated cells. The molecular and subcellular analysis suggests that the unfolded protein response is induced in salt‐acclimated cells. Finally, we propose that this mechanism may mediate cell death in salt‐acclimated cells.</description><subject>Abscisic acid</subject><subject>Abscisic Acid - metabolism</subject><subject>Acclimation</subject><subject>Acclimatization</subject><subject>Acclimatization - drug effects</subject><subject>Apoptosis - drug effects</subject><subject>Apoptosis - genetics</subject><subject>Caspases - metabolism</subject><subject>Cell death</subject><subject>Cell growth</subject><subject>Cell Line</subject><subject>Cell lines</subject><subject>Cell nucleus</subject><subject>Cells</subject><subject>Chaperones</subject><subject>Cytoplasm</subject><subject>endomembrane system</subject><subject>Endoplasmic reticulum</subject><subject>Fluorescence</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Glutathione - metabolism</subject><subject>Golgi apparatus</subject><subject>Hydrogen Peroxide - metabolism</subject><subject>Image contrast</subject><subject>Intracellular Membranes - drug effects</subject><subject>Intracellular Membranes - metabolism</subject><subject>Intracellular Membranes - ultrastructure</subject><subject>Malondialdehyde - metabolism</subject><subject>Metabolism</subject><subject>Mitochondria</subject><subject>Mitochondria - drug effects</subject><subject>Mitochondria - metabolism</subject><subject>Mitochondria - ultrastructure</subject><subject>Molecular modelling</subject><subject>Multidisciplinary research</subject><subject>Nicotiana - cytology</subject><subject>Nicotiana - genetics</subject><subject>Nicotiana - metabolism</subject><subject>Nicotiana - ultrastructure</subject><subject>Nicotiana tabacum</subject><subject>Oxygen</subject><subject>physiological transport</subject><subject>Plant cells</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants</subject><subject>Proline</subject><subject>Proline - metabolism</subject><subject>Protein folding</subject><subject>Proteins</subject><subject>Proteome - metabolism</subject><subject>Proteomics</subject><subject>Reactive oxygen species</subject><subject>reactive oxygen species (ROS)</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Salt</subject><subject>salt acclimation</subject><subject>Salt Tolerance</subject><subject>Salts</subject><subject>Signal Transduction - drug effects</subject><subject>Signaling</subject><subject>Sodium</subject><subject>Sodium - metabolism</subject><subject>Sodium chloride</subject><subject>Sodium Chloride - pharmacology</subject><subject>stress response</subject><subject>Subcellular Fractions - drug effects</subject><subject>Subcellular Fractions - metabolism</subject><subject>Tobacco</subject><subject>Transcriptome - genetics</subject><subject>transcriptomics</subject><subject>Transport Vesicles - drug effects</subject><subject>Transport Vesicles - metabolism</subject><subject>Transport Vesicles - ultrastructure</subject><subject>unfolded protein response</subject><subject>Vacuoles</subject><subject>vesicle trafficking</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNp9kc1u1DAUhS0EosPAghcAS6xYpPXPxInZoQooUlWQoBI7y3GuZzwkdrA9HeZheFecTtsdeHO9-M65R_cg9JKSU1remZ82p5RJ2TxCC7oSsmopbx6jBSGsrcRK_DhBz1LaEkJkLdhTdMJq2jZMyAX6cwV77Hxy601O5ZMDngbtM056yFgbM7hRZxf8O5w3gGMYIOFg8Q0kZwbAOWprnfnp_Bpr3-MI2mR3Azj8PqzB4zSBcUVSFng9DDPmPB5dDmYTfB-dvpXN3uD7MMLYRe0Bp0PKMD5HT6weEry4m0t0_fHD9_OL6vLLp8_n7y8rU9e8qTTwloCW2jCQ2vaGSNtq0UFrW9IJ06066LjVHaeM16C5pZz2tTR01nPCl-jN0XeK4dcOUlbbsIslcFLlVLyVhEv6P4oK1shWzPASvT1SJoaUIlg1xXLDeFCUqLkuVepSt3UV9tWd464boX8g7_spwNkR2LsBDv92UldfL-4tq6Nim3KIDwoP-2lzyGEIa1eCM1IrqhgVhX995K0OSq-jS-r6GyO0JmTOwAT_C7KWvFs</recordid><startdate>201501</startdate><enddate>201501</enddate><creator>Garcia de la Garma, Jesus</creator><creator>Fernandez‐Garcia, Nieves</creator><creator>Bardisi, Enas</creator><creator>Pallol, Beatriz</creator><creator>Asensio‐Rubio, Jose Salvador</creator><creator>Bru, Roque</creator><creator>Olmos, Enrique</creator><general>Academic Press</general><general>New Phytologist Trust</general><general>Wiley Subscription Services, Inc</general><scope>FBQ</scope><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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>201501</creationdate><title>New insights into plant salt acclimation: the roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system</title><author>Garcia de la Garma, Jesus ; Fernandez‐Garcia, Nieves ; Bardisi, Enas ; Pallol, Beatriz ; Asensio‐Rubio, Jose Salvador ; Bru, Roque ; Olmos, Enrique</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5537-ae380ea9ac2e9afdc09f8a6be8f80b6cb4beb3fab31235ea3f131d59c1c553303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Abscisic acid</topic><topic>Abscisic Acid - metabolism</topic><topic>Acclimation</topic><topic>Acclimatization</topic><topic>Acclimatization - drug effects</topic><topic>Apoptosis - drug effects</topic><topic>Apoptosis - genetics</topic><topic>Caspases - metabolism</topic><topic>Cell death</topic><topic>Cell growth</topic><topic>Cell Line</topic><topic>Cell lines</topic><topic>Cell nucleus</topic><topic>Cells</topic><topic>Chaperones</topic><topic>Cytoplasm</topic><topic>endomembrane system</topic><topic>Endoplasmic reticulum</topic><topic>Fluorescence</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Glutathione - metabolism</topic><topic>Golgi apparatus</topic><topic>Hydrogen Peroxide - metabolism</topic><topic>Image contrast</topic><topic>Intracellular Membranes - drug effects</topic><topic>Intracellular Membranes - metabolism</topic><topic>Intracellular Membranes - ultrastructure</topic><topic>Malondialdehyde - metabolism</topic><topic>Metabolism</topic><topic>Mitochondria</topic><topic>Mitochondria - drug effects</topic><topic>Mitochondria - metabolism</topic><topic>Mitochondria - ultrastructure</topic><topic>Molecular modelling</topic><topic>Multidisciplinary research</topic><topic>Nicotiana - cytology</topic><topic>Nicotiana - genetics</topic><topic>Nicotiana - metabolism</topic><topic>Nicotiana - ultrastructure</topic><topic>Nicotiana tabacum</topic><topic>Oxygen</topic><topic>physiological transport</topic><topic>Plant cells</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants</topic><topic>Proline</topic><topic>Proline - metabolism</topic><topic>Protein folding</topic><topic>Proteins</topic><topic>Proteome - metabolism</topic><topic>Proteomics</topic><topic>Reactive oxygen species</topic><topic>reactive oxygen species (ROS)</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Salt</topic><topic>salt acclimation</topic><topic>Salt Tolerance</topic><topic>Salts</topic><topic>Signal Transduction - drug effects</topic><topic>Signaling</topic><topic>Sodium</topic><topic>Sodium - metabolism</topic><topic>Sodium chloride</topic><topic>Sodium Chloride - pharmacology</topic><topic>stress response</topic><topic>Subcellular Fractions - drug effects</topic><topic>Subcellular Fractions - metabolism</topic><topic>Tobacco</topic><topic>Transcriptome - genetics</topic><topic>transcriptomics</topic><topic>Transport Vesicles - drug effects</topic><topic>Transport Vesicles - metabolism</topic><topic>Transport Vesicles - ultrastructure</topic><topic>unfolded protein response</topic><topic>Vacuoles</topic><topic>vesicle trafficking</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Garcia de la Garma, Jesus</creatorcontrib><creatorcontrib>Fernandez‐Garcia, Nieves</creatorcontrib><creatorcontrib>Bardisi, Enas</creatorcontrib><creatorcontrib>Pallol, Beatriz</creatorcontrib><creatorcontrib>Asensio‐Rubio, Jose Salvador</creatorcontrib><creatorcontrib>Bru, Roque</creatorcontrib><creatorcontrib>Olmos, Enrique</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Garcia de la Garma, Jesus</au><au>Fernandez‐Garcia, Nieves</au><au>Bardisi, Enas</au><au>Pallol, Beatriz</au><au>Asensio‐Rubio, Jose Salvador</au><au>Bru, Roque</au><au>Olmos, Enrique</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>New insights into plant salt acclimation: the roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2015-01</date><risdate>2015</risdate><volume>205</volume><issue>1</issue><spage>216</spage><epage>239</epage><pages>216-239</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>In this study, we investigated the cellular and molecular mechanisms that regulate salt acclimation. The main objective was to obtain new insights into the molecular mechanisms that control salt acclimation. Therefore, we carried out a multidisciplinary study using proteomic, transcriptomic, subcellular and physiological techniques. We obtained a Nicotiana tabacum BY‐2 cell line acclimated to be grown at 258 mM NaCl as a model for this study. The proteomic and transcriptomic data indicate that the molecular response to stress (chaperones, defence proteins, etc.) is highly induced in these salt‐acclimated cells. The subcellular results show that salt induces sodium compartmentalization in the cell vacuoles and seems to be mediated by vesicle trafficking in tobacco salt‐acclimated cells. Our results demonstrate that abscisic acid (ABA) and proline metabolism are crucial in the cellular signalling of salt acclimation, probably regulating reactive oxygen species (ROS) production in the mitochondria. ROS may act as a retrograde signal, regulating the cell response. The network of endoplasmic reticulum and Golgi apparatus is highly altered in salt‐acclimated cells. The molecular and subcellular analysis suggests that the unfolded protein response is induced in salt‐acclimated cells. Finally, we propose that this mechanism may mediate cell death in salt‐acclimated cells.</abstract><cop>England</cop><pub>Academic Press</pub><pmid>25187269</pmid><doi>10.1111/nph.12997</doi><tpages>24</tpages></addata></record> |
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subjects | Abscisic acid Abscisic Acid - metabolism Acclimation Acclimatization Acclimatization - drug effects Apoptosis - drug effects Apoptosis - genetics Caspases - metabolism Cell death Cell growth Cell Line Cell lines Cell nucleus Cells Chaperones Cytoplasm endomembrane system Endoplasmic reticulum Fluorescence Gene Expression Regulation, Plant - drug effects Glutathione - metabolism Golgi apparatus Hydrogen Peroxide - metabolism Image contrast Intracellular Membranes - drug effects Intracellular Membranes - metabolism Intracellular Membranes - ultrastructure Malondialdehyde - metabolism Metabolism Mitochondria Mitochondria - drug effects Mitochondria - metabolism Mitochondria - ultrastructure Molecular modelling Multidisciplinary research Nicotiana - cytology Nicotiana - genetics Nicotiana - metabolism Nicotiana - ultrastructure Nicotiana tabacum Oxygen physiological transport Plant cells Plant Proteins - genetics Plant Proteins - metabolism Plants Proline Proline - metabolism Protein folding Proteins Proteome - metabolism Proteomics Reactive oxygen species reactive oxygen species (ROS) Reactive Oxygen Species - metabolism Salt salt acclimation Salt Tolerance Salts Signal Transduction - drug effects Signaling Sodium Sodium - metabolism Sodium chloride Sodium Chloride - pharmacology stress response Subcellular Fractions - drug effects Subcellular Fractions - metabolism Tobacco Transcriptome - genetics transcriptomics Transport Vesicles - drug effects Transport Vesicles - metabolism Transport Vesicles - ultrastructure unfolded protein response Vacuoles vesicle trafficking |
title | New insights into plant salt acclimation: the roles of vesicle trafficking and reactive oxygen species signalling in mitochondria and the endomembrane system |
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