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Drought resistance is mediated by divergent strategies in closely related Brassicaceae
Droughts cause severe crop losses worldwide and climate change is projected to increase their prevalence in the future. Similar to the situation for many crops, the reference plant Arabidopsis thaliana (Ath) is considered drought-sensitive, whereas, as we demonstrate, its close relatives Arabidopsis...
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Published in: | The New phytologist 2019-07, Vol.223 (2), p.783-797 |
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description | Droughts cause severe crop losses worldwide and climate change is projected to increase their prevalence in the future. Similar to the situation for many crops, the reference plant Arabidopsis thaliana (Ath) is considered drought-sensitive, whereas, as we demonstrate, its close relatives Arabidopsis lyrata (Aly) and Eutrema salsugineum (Esa) are drought-resistant.
To understand the molecular basis for this plasticity we conducted a deep phenotypic, biochemical and transcriptomic comparison using developmentally matched plants.
We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations and signaling network rewiring. By contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, ABA signaling transcripts and late growth responses. The stress-sensitive Ath responds later than Aly and earlier than Esa, although its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath.
Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance. |
doi_str_mv | 10.1111/nph.15841 |
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To understand the molecular basis for this plasticity we conducted a deep phenotypic, biochemical and transcriptomic comparison using developmentally matched plants.
We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations and signaling network rewiring. By contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, ABA signaling transcripts and late growth responses. The stress-sensitive Ath responds later than Aly and earlier than Esa, although its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath.
Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.15841</identifier><identifier>PMID: 30955214</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Abscisic Acid - metabolism ; Adaptation, Physiological ; Arabidopsis ; Brassicaceae ; Brassicaceae - genetics ; Brassicaceae - growth & development ; Brassicaceae - physiology ; Cluster Analysis ; comparative phenotyping ; drought ; Droughts ; Gene Expression Regulation, Plant ; high‐throughput phenotyping ; Life Sciences ; Plant Leaves - growth & development ; Signal Transduction ; Species Specificity ; stress resistance ; Stress, Physiological ; systems biology ; transcriptome ; Transcriptome - genetics ; Vegetal Biology ; Water</subject><ispartof>The New phytologist, 2019-07, Vol.223 (2), p.783-797</ispartof><rights>2019 The Authors © 2019 New Phytologist Trust</rights><rights>2019 The Authors. New Phytologist © 2019 New Phytologist Trust</rights><rights>2019 The Authors. New Phytologist © 2019 New Phytologist Trust.</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5371-9357f885cec88c654ed65fe50b5769aafb5310ec902e11d36816659c0c3c3d763</citedby><cites>FETCH-LOGICAL-c5371-9357f885cec88c654ed65fe50b5769aafb5310ec902e11d36816659c0c3c3d763</cites><orcidid>0000-0003-4402-2191 ; 0000-0002-2509-0562 ; 0000-0003-2012-6746 ; 0000-0002-3946-1758 ; 0000-0002-3217-8407 ; 0000-0002-9066-2264</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26742307$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26742307$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30955214$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02627707$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>la Rosa, Nora Marín-de</creatorcontrib><creatorcontrib>Lin, Chung-Wen</creatorcontrib><creatorcontrib>Kang, Yang Jae</creatorcontrib><creatorcontrib>Dhondt, Stijn</creatorcontrib><creatorcontrib>Gonzalez, Nathalie</creatorcontrib><creatorcontrib>Inzé, Dirk</creatorcontrib><creatorcontrib>Falter-Braun, Pascal</creatorcontrib><title>Drought resistance is mediated by divergent strategies in closely related Brassicaceae</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Droughts cause severe crop losses worldwide and climate change is projected to increase their prevalence in the future. Similar to the situation for many crops, the reference plant Arabidopsis thaliana (Ath) is considered drought-sensitive, whereas, as we demonstrate, its close relatives Arabidopsis lyrata (Aly) and Eutrema salsugineum (Esa) are drought-resistant.
To understand the molecular basis for this plasticity we conducted a deep phenotypic, biochemical and transcriptomic comparison using developmentally matched plants.
We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations and signaling network rewiring. By contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, ABA signaling transcripts and late growth responses. The stress-sensitive Ath responds later than Aly and earlier than Esa, although its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath.
Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance.</description><subject>Abscisic Acid - metabolism</subject><subject>Adaptation, Physiological</subject><subject>Arabidopsis</subject><subject>Brassicaceae</subject><subject>Brassicaceae - genetics</subject><subject>Brassicaceae - growth & development</subject><subject>Brassicaceae - physiology</subject><subject>Cluster Analysis</subject><subject>comparative phenotyping</subject><subject>drought</subject><subject>Droughts</subject><subject>Gene Expression Regulation, Plant</subject><subject>high‐throughput phenotyping</subject><subject>Life Sciences</subject><subject>Plant Leaves - growth & development</subject><subject>Signal Transduction</subject><subject>Species Specificity</subject><subject>stress resistance</subject><subject>Stress, Physiological</subject><subject>systems biology</subject><subject>transcriptome</subject><subject>Transcriptome - genetics</subject><subject>Vegetal Biology</subject><subject>Water</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kV1PwjAYhRujEUQv_AGa3XoxaNe13W5MFD8wIeqFGu-a0r2DkrGRdmD27y0g-JHYmzZvn3Ny8h6ETgnuEn965XzSJSyJyR5qk5inYUKo2EdtjKMk5DF_b6Ej56YY45Tx6BC1qH-wiMRt9HZjq8V4UgcWnHG1KjUExgUzyIyqIQtGTZCZJdgxlHXgauuHYwMuMGWgi8pB0XhlsUavrXLOaKVBwTE6yFXh4OTr7qDXu9uX_iAcPt0_9K-GoWZUkDClTORJwjToJNGcxZBxlgPDIyZ4qlQ-YpRg0CmOgJCM8oRwzlKNNdU0E5x20OXGd74Y-czap7SqkHNrZso2slJG_v4pzUSOq6XkQhAWY29wsTGY_JENroZyNcMRj4TAYkm-WW0r5yzkOwHBclWE9EXIdRGePf8ZbEduN--B3gb4MAU0_zvJx-fB1vJso5i6urI7RcRFHFEs6CfLt51D</recordid><startdate>201907</startdate><enddate>201907</enddate><creator>la Rosa, Nora Marín-de</creator><creator>Lin, Chung-Wen</creator><creator>Kang, Yang Jae</creator><creator>Dhondt, Stijn</creator><creator>Gonzalez, Nathalie</creator><creator>Inzé, Dirk</creator><creator>Falter-Braun, Pascal</creator><general>Wiley</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4402-2191</orcidid><orcidid>https://orcid.org/0000-0002-2509-0562</orcidid><orcidid>https://orcid.org/0000-0003-2012-6746</orcidid><orcidid>https://orcid.org/0000-0002-3946-1758</orcidid><orcidid>https://orcid.org/0000-0002-3217-8407</orcidid><orcidid>https://orcid.org/0000-0002-9066-2264</orcidid></search><sort><creationdate>201907</creationdate><title>Drought resistance is mediated by divergent strategies in closely related Brassicaceae</title><author>la Rosa, Nora Marín-de ; Lin, Chung-Wen ; Kang, Yang Jae ; Dhondt, Stijn ; Gonzalez, Nathalie ; Inzé, Dirk ; Falter-Braun, Pascal</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5371-9357f885cec88c654ed65fe50b5769aafb5310ec902e11d36816659c0c3c3d763</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Abscisic Acid - metabolism</topic><topic>Adaptation, Physiological</topic><topic>Arabidopsis</topic><topic>Brassicaceae</topic><topic>Brassicaceae - genetics</topic><topic>Brassicaceae - growth & development</topic><topic>Brassicaceae - physiology</topic><topic>Cluster Analysis</topic><topic>comparative phenotyping</topic><topic>drought</topic><topic>Droughts</topic><topic>Gene Expression Regulation, Plant</topic><topic>high‐throughput phenotyping</topic><topic>Life Sciences</topic><topic>Plant Leaves - growth & development</topic><topic>Signal Transduction</topic><topic>Species Specificity</topic><topic>stress resistance</topic><topic>Stress, Physiological</topic><topic>systems biology</topic><topic>transcriptome</topic><topic>Transcriptome - genetics</topic><topic>Vegetal Biology</topic><topic>Water</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>la Rosa, Nora Marín-de</creatorcontrib><creatorcontrib>Lin, Chung-Wen</creatorcontrib><creatorcontrib>Kang, Yang Jae</creatorcontrib><creatorcontrib>Dhondt, Stijn</creatorcontrib><creatorcontrib>Gonzalez, Nathalie</creatorcontrib><creatorcontrib>Inzé, Dirk</creatorcontrib><creatorcontrib>Falter-Braun, Pascal</creatorcontrib><collection>Wiley Open Access Journals</collection><collection>Wiley Free Archive</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>la Rosa, Nora Marín-de</au><au>Lin, Chung-Wen</au><au>Kang, Yang Jae</au><au>Dhondt, Stijn</au><au>Gonzalez, Nathalie</au><au>Inzé, Dirk</au><au>Falter-Braun, Pascal</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Drought resistance is mediated by divergent strategies in closely related Brassicaceae</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2019-07</date><risdate>2019</risdate><volume>223</volume><issue>2</issue><spage>783</spage><epage>797</epage><pages>783-797</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Droughts cause severe crop losses worldwide and climate change is projected to increase their prevalence in the future. Similar to the situation for many crops, the reference plant Arabidopsis thaliana (Ath) is considered drought-sensitive, whereas, as we demonstrate, its close relatives Arabidopsis lyrata (Aly) and Eutrema salsugineum (Esa) are drought-resistant.
To understand the molecular basis for this plasticity we conducted a deep phenotypic, biochemical and transcriptomic comparison using developmentally matched plants.
We demonstrate that Aly responds most sensitively to decreasing water availability with early growth reduction, metabolic adaptations and signaling network rewiring. By contrast, Esa is in a constantly prepared mode as evidenced by high basal proline levels, ABA signaling transcripts and late growth responses. The stress-sensitive Ath responds later than Aly and earlier than Esa, although its responses tend to be more extreme. All species detect water scarcity with similar sensitivity; response differences are encoded in downstream signaling and response networks. Moreover, several signaling genes expressed at higher basal levels in both Aly and Esa have been shown to increase water-use efficiency and drought resistance when overexpressed in Ath.
Our data demonstrate contrasting strategies of closely related Brassicaceae to achieve drought resistance.</abstract><cop>England</cop><pub>Wiley</pub><pmid>30955214</pmid><doi>10.1111/nph.15841</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-4402-2191</orcidid><orcidid>https://orcid.org/0000-0002-2509-0562</orcidid><orcidid>https://orcid.org/0000-0003-2012-6746</orcidid><orcidid>https://orcid.org/0000-0002-3946-1758</orcidid><orcidid>https://orcid.org/0000-0002-3217-8407</orcidid><orcidid>https://orcid.org/0000-0002-9066-2264</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Abscisic Acid - metabolism Adaptation, Physiological Arabidopsis Brassicaceae Brassicaceae - genetics Brassicaceae - growth & development Brassicaceae - physiology Cluster Analysis comparative phenotyping drought Droughts Gene Expression Regulation, Plant high‐throughput phenotyping Life Sciences Plant Leaves - growth & development Signal Transduction Species Specificity stress resistance Stress, Physiological systems biology transcriptome Transcriptome - genetics Vegetal Biology Water |
title | Drought resistance is mediated by divergent strategies in closely related Brassicaceae |
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