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Growth Platform-Dependent and -Independent Phenotypic and Metabolic Responses of Arabidopsis and Its Halophytic Relative, Eutrema salsugineum, to Salt Stress
Comparative studies of the stress-tolerant Arabidopsis (Arabidopsis thaliana) halophytic relative, Eutrema salsugineum, have proven a fruitful approach to understanding natural stress tolerance. Here, we performed comparative phenotyping of Arabidopsis and E. salsugineum vegetative development under...
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Published in: | Plant physiology (Bethesda) 2013-07, Vol.162 (3), p.1583-1598 |
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description | Comparative studies of the stress-tolerant Arabidopsis (Arabidopsis thaliana) halophytic relative, Eutrema salsugineum, have proven a fruitful approach to understanding natural stress tolerance. Here, we performed comparative phenotyping of Arabidopsis and E. salsugineum vegetative development under control and salt-stress conditions, and then compared the metabolic responses of the two species on different growth platforms in a defined leaf developmental stage. Our results reveal both growth platform-dependent and -independent phenotypes and metabolic responses. Leaf emergence was affected in a similar way in both species grown in vitro but the effects observed in Arabidopsis occurred at higher salt concentrations in E. salsugineum. No differences in leaf emergence were observed on soil. A new effect of a salt-mediated reduction in E. salsugineum leaf area was unmasked. On soil, leaf area reduction in E. salsugineum was mainly due to a fall in cell number, whereas both cell number and cell size contributed to the decrease in Arabidopsis leaf area. Common growth platform-independent leaf metabolic signatures such as high raffinose and malate, and low fumarate contents that could reflect core stress tolerance mechanisms, as well as growth platform-dependent metabolic responses were identified. In particular, the in vitro growth platform led to repression of accumulation of many metabolites including sugars, sugar phosphates, and amino acids in E. salsugineum compared with the soil system where these same metabolites accumulated to higher levels in E. salsugineum than in Arabidopsis. The observation that E. salsugineum maintains salt tolerance despite growth platform-specific phenotypes and metabolic responses suggests a considerable degree of phenotypic and metabolic adaptive plasticity in this extremophile. |
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Here, we performed comparative phenotyping of Arabidopsis and E. salsugineum vegetative development under control and salt-stress conditions, and then compared the metabolic responses of the two species on different growth platforms in a defined leaf developmental stage. Our results reveal both growth platform-dependent and -independent phenotypes and metabolic responses. Leaf emergence was affected in a similar way in both species grown in vitro but the effects observed in Arabidopsis occurred at higher salt concentrations in E. salsugineum. No differences in leaf emergence were observed on soil. A new effect of a salt-mediated reduction in E. salsugineum leaf area was unmasked. On soil, leaf area reduction in E. salsugineum was mainly due to a fall in cell number, whereas both cell number and cell size contributed to the decrease in Arabidopsis leaf area. Common growth platform-independent leaf metabolic signatures such as high raffinose and malate, and low fumarate contents that could reflect core stress tolerance mechanisms, as well as growth platform-dependent metabolic responses were identified. In particular, the in vitro growth platform led to repression of accumulation of many metabolites including sugars, sugar phosphates, and amino acids in E. salsugineum compared with the soil system where these same metabolites accumulated to higher levels in E. salsugineum than in Arabidopsis. The observation that E. salsugineum maintains salt tolerance despite growth platform-specific phenotypes and metabolic responses suggests a considerable degree of phenotypic and metabolic adaptive plasticity in this extremophile.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.113.217844</identifier><identifier>PMID: 23735509</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Adaptation, Physiological ; Arabidopsis ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis - physiology ; Biological and medical sciences ; Brassicaceae - growth & development ; Brassicaceae - metabolism ; Brassicaceae - physiology ; Cell Size ; Eutrema salsugineum ; Fumarates - metabolism ; Fundamental and applied biological sciences. Psychology ; halophytes ; Leaf area ; Leaves ; Malates - metabolism ; metabolism ; Metabolites ; Phenotype ; Plant cells ; Plant growth ; Plant Leaves - cytology ; Plant Leaves - growth & development ; Plant physiology and development ; Plants ; Raffinose - metabolism ; salt stress ; Salt Tolerance ; Salt-Tolerant Plants - physiology ; Salts ; Seedlings ; SIGNALING AND RESPONSE ; Soil ; Soil salts ; Species Specificity ; Stress, Physiological ; Table salt</subject><ispartof>Plant physiology (Bethesda), 2013-07, Vol.162 (3), p.1583-1598</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>2014 INIST-CNRS</rights><rights>2013 American Society of Plant Biologists. All Rights Reserved. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c472t-ac4e460437765b37e2e0318420a321a944483b4a38cd0ae70073c16b47687ef93</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41943500$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41943500$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,58213,58446</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27519548$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23735509$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kazachkova, Yana</creatorcontrib><creatorcontrib>Batushansky, Albert</creatorcontrib><creatorcontrib>Cisneros, Aroldo</creatorcontrib><creatorcontrib>Tel-Zur, Noemi</creatorcontrib><creatorcontrib>Fait, Aaron</creatorcontrib><creatorcontrib>Barak, Simon</creatorcontrib><title>Growth Platform-Dependent and -Independent Phenotypic and Metabolic Responses of Arabidopsis and Its Halophytic Relative, Eutrema salsugineum, to Salt Stress</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Comparative studies of the stress-tolerant Arabidopsis (Arabidopsis thaliana) halophytic relative, Eutrema salsugineum, have proven a fruitful approach to understanding natural stress tolerance. Here, we performed comparative phenotyping of Arabidopsis and E. salsugineum vegetative development under control and salt-stress conditions, and then compared the metabolic responses of the two species on different growth platforms in a defined leaf developmental stage. Our results reveal both growth platform-dependent and -independent phenotypes and metabolic responses. Leaf emergence was affected in a similar way in both species grown in vitro but the effects observed in Arabidopsis occurred at higher salt concentrations in E. salsugineum. No differences in leaf emergence were observed on soil. A new effect of a salt-mediated reduction in E. salsugineum leaf area was unmasked. On soil, leaf area reduction in E. salsugineum was mainly due to a fall in cell number, whereas both cell number and cell size contributed to the decrease in Arabidopsis leaf area. Common growth platform-independent leaf metabolic signatures such as high raffinose and malate, and low fumarate contents that could reflect core stress tolerance mechanisms, as well as growth platform-dependent metabolic responses were identified. In particular, the in vitro growth platform led to repression of accumulation of many metabolites including sugars, sugar phosphates, and amino acids in E. salsugineum compared with the soil system where these same metabolites accumulated to higher levels in E. salsugineum than in Arabidopsis. The observation that E. salsugineum maintains salt tolerance despite growth platform-specific phenotypes and metabolic responses suggests a considerable degree of phenotypic and metabolic adaptive plasticity in this extremophile.</description><subject>Adaptation, Physiological</subject><subject>Arabidopsis</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - physiology</subject><subject>Biological and medical sciences</subject><subject>Brassicaceae - growth & development</subject><subject>Brassicaceae - metabolism</subject><subject>Brassicaceae - physiology</subject><subject>Cell Size</subject><subject>Eutrema salsugineum</subject><subject>Fumarates - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>halophytes</subject><subject>Leaf area</subject><subject>Leaves</subject><subject>Malates - metabolism</subject><subject>metabolism</subject><subject>Metabolites</subject><subject>Phenotype</subject><subject>Plant cells</subject><subject>Plant growth</subject><subject>Plant Leaves - cytology</subject><subject>Plant Leaves - growth & development</subject><subject>Plant physiology and development</subject><subject>Plants</subject><subject>Raffinose - metabolism</subject><subject>salt stress</subject><subject>Salt Tolerance</subject><subject>Salt-Tolerant Plants - physiology</subject><subject>Salts</subject><subject>Seedlings</subject><subject>SIGNALING AND RESPONSE</subject><subject>Soil</subject><subject>Soil salts</subject><subject>Species Specificity</subject><subject>Stress, Physiological</subject><subject>Table salt</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqFksFu1DAQhi0EokvhyBHkCxKHptixEycXpKqUdqUiKgpna5JMuq6S2NhO0T4M74rZ3W7LidOM_X8az_gfQl5zdsw5kx-cS1Ec51xVUj4hC16IPMsLWT0lC8ZSzqqqPiAvQrhljHHB5XNykAslioLVC_L73NtfcUWvBoi99WP2CR1OHU6RwtTRbJny-4urFU42rp1pN9oXjNDYIZ2-YXB2Chio7emJh8Z01gUTNtgyBnoBg3Wrddyw6SVzh0f0bI4eR6ABhjDfmAnn8YhGS69hiPQ6aSG8JM_6pOKrXTwkPz6ffT-9yC6_ni9PTy6zVqo8ZtBKlCWTQqmyaITCHJnglcwZiJxDLaWsRCNBVG3HABVjSrS8bKQqK4V9LQ7Jx21dNzcjdm2a1sOgnTcj-LW2YPS_ymRW-sbeaaGYKkqRCrzfFfD254wh6tGEFocBJrRz0Pnm70tR8v-iXNSpc1nVRUKzLdp6G4LHft8RZ_qv-9q5FIXeup_4t4_H2NP3difg3Q6A0MLQe5haEx44VfA6rU7i3my52xCt3-uS11IUaav-AK_sw0A</recordid><startdate>20130701</startdate><enddate>20130701</enddate><creator>Kazachkova, Yana</creator><creator>Batushansky, Albert</creator><creator>Cisneros, Aroldo</creator><creator>Tel-Zur, Noemi</creator><creator>Fait, Aaron</creator><creator>Barak, Simon</creator><general>American Society of Plant Biologists</general><scope>IQODW</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20130701</creationdate><title>Growth Platform-Dependent and -Independent Phenotypic and Metabolic Responses of Arabidopsis and Its Halophytic Relative, Eutrema salsugineum, to Salt Stress</title><author>Kazachkova, Yana ; Batushansky, Albert ; Cisneros, Aroldo ; Tel-Zur, Noemi ; Fait, Aaron ; Barak, Simon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c472t-ac4e460437765b37e2e0318420a321a944483b4a38cd0ae70073c16b47687ef93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adaptation, Physiological</topic><topic>Arabidopsis</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - physiology</topic><topic>Biological and medical sciences</topic><topic>Brassicaceae - growth & development</topic><topic>Brassicaceae - metabolism</topic><topic>Brassicaceae - physiology</topic><topic>Cell Size</topic><topic>Eutrema salsugineum</topic><topic>Fumarates - metabolism</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>halophytes</topic><topic>Leaf area</topic><topic>Leaves</topic><topic>Malates - metabolism</topic><topic>metabolism</topic><topic>Metabolites</topic><topic>Phenotype</topic><topic>Plant cells</topic><topic>Plant growth</topic><topic>Plant Leaves - cytology</topic><topic>Plant Leaves - growth & development</topic><topic>Plant physiology and development</topic><topic>Plants</topic><topic>Raffinose - metabolism</topic><topic>salt stress</topic><topic>Salt Tolerance</topic><topic>Salt-Tolerant Plants - physiology</topic><topic>Salts</topic><topic>Seedlings</topic><topic>SIGNALING AND RESPONSE</topic><topic>Soil</topic><topic>Soil salts</topic><topic>Species Specificity</topic><topic>Stress, Physiological</topic><topic>Table salt</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kazachkova, Yana</creatorcontrib><creatorcontrib>Batushansky, Albert</creatorcontrib><creatorcontrib>Cisneros, Aroldo</creatorcontrib><creatorcontrib>Tel-Zur, Noemi</creatorcontrib><creatorcontrib>Fait, Aaron</creatorcontrib><creatorcontrib>Barak, Simon</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</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>Kazachkova, Yana</au><au>Batushansky, Albert</au><au>Cisneros, Aroldo</au><au>Tel-Zur, Noemi</au><au>Fait, Aaron</au><au>Barak, Simon</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Growth Platform-Dependent and -Independent Phenotypic and Metabolic Responses of Arabidopsis and Its Halophytic Relative, Eutrema salsugineum, to Salt Stress</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2013-07-01</date><risdate>2013</risdate><volume>162</volume><issue>3</issue><spage>1583</spage><epage>1598</epage><pages>1583-1598</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>Comparative studies of the stress-tolerant Arabidopsis (Arabidopsis thaliana) halophytic relative, Eutrema salsugineum, have proven a fruitful approach to understanding natural stress tolerance. Here, we performed comparative phenotyping of Arabidopsis and E. salsugineum vegetative development under control and salt-stress conditions, and then compared the metabolic responses of the two species on different growth platforms in a defined leaf developmental stage. Our results reveal both growth platform-dependent and -independent phenotypes and metabolic responses. Leaf emergence was affected in a similar way in both species grown in vitro but the effects observed in Arabidopsis occurred at higher salt concentrations in E. salsugineum. No differences in leaf emergence were observed on soil. A new effect of a salt-mediated reduction in E. salsugineum leaf area was unmasked. On soil, leaf area reduction in E. salsugineum was mainly due to a fall in cell number, whereas both cell number and cell size contributed to the decrease in Arabidopsis leaf area. Common growth platform-independent leaf metabolic signatures such as high raffinose and malate, and low fumarate contents that could reflect core stress tolerance mechanisms, as well as growth platform-dependent metabolic responses were identified. In particular, the in vitro growth platform led to repression of accumulation of many metabolites including sugars, sugar phosphates, and amino acids in E. salsugineum compared with the soil system where these same metabolites accumulated to higher levels in E. salsugineum than in Arabidopsis. The observation that E. salsugineum maintains salt tolerance despite growth platform-specific phenotypes and metabolic responses suggests a considerable degree of phenotypic and metabolic adaptive plasticity in this extremophile.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>23735509</pmid><doi>10.1104/pp.113.217844</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Physiological Arabidopsis Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis - physiology Biological and medical sciences Brassicaceae - growth & development Brassicaceae - metabolism Brassicaceae - physiology Cell Size Eutrema salsugineum Fumarates - metabolism Fundamental and applied biological sciences. Psychology halophytes Leaf area Leaves Malates - metabolism metabolism Metabolites Phenotype Plant cells Plant growth Plant Leaves - cytology Plant Leaves - growth & development Plant physiology and development Plants Raffinose - metabolism salt stress Salt Tolerance Salt-Tolerant Plants - physiology Salts Seedlings SIGNALING AND RESPONSE Soil Soil salts Species Specificity Stress, Physiological Table salt |
title | Growth Platform-Dependent and -Independent Phenotypic and Metabolic Responses of Arabidopsis and Its Halophytic Relative, Eutrema salsugineum, to Salt Stress |
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