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Evolution of stomatal closure to optimize water‐use efficiency in response to dehydration in ferns and seed plants
Summary Plants control water‐use efficiency (WUE) by regulating water loss and CO2 diffusion through stomata. Variation in stomatal control has been reported among lineages of vascular plants, thus giving rise to the possibility that different lineages may show distinct WUE dynamics in response to w...
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Published in: | The New phytologist 2021-06, Vol.230 (5), p.2001-2010 |
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container_end_page | 2010 |
container_issue | 5 |
container_start_page | 2001 |
container_title | The New phytologist |
container_volume | 230 |
creator | Yang, Yu‐Jie Bi, Min‐Hui Nie, Zheng‐Fei Jiang, Hui Liu, Xu‐Dong Fang, Xiang‐Wen Brodribb, Timothy J. |
description | Summary
Plants control water‐use efficiency (WUE) by regulating water loss and CO2 diffusion through stomata. Variation in stomatal control has been reported among lineages of vascular plants, thus giving rise to the possibility that different lineages may show distinct WUE dynamics in response to water stress.
Here, we compared the response of gas exchange to decreasing leaf water potential among four ferns and nine seed plant species exposed to a gradually intensifying water deficit. The data collected were combined with those from 339 phylogenetically diverse species obtained from previous studies.
In well‐watered angiosperms, the maximum stomatal conductance was high and greater than that required for maximum WUE, but drought stress caused a rapid reduction in stomatal conductance and an increase in WUE in response to elevated concentrations of abscisic acid. However, in ferns, stomata did not open beyond the optimum point corresponding to maximum WUE and actually exhibited a steady WUE in response to dehydration. Thus, seed plants showed improved photosynthetic WUE under water stress.
The ability of seed plants to increase WUE could provide them with an advantage over ferns under drought conditions, thereby presumably increasing their fitness under selection pressure by drought. |
doi_str_mv | 10.1111/nph.17278 |
format | article |
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Plants control water‐use efficiency (WUE) by regulating water loss and CO2 diffusion through stomata. Variation in stomatal control has been reported among lineages of vascular plants, thus giving rise to the possibility that different lineages may show distinct WUE dynamics in response to water stress.
Here, we compared the response of gas exchange to decreasing leaf water potential among four ferns and nine seed plant species exposed to a gradually intensifying water deficit. The data collected were combined with those from 339 phylogenetically diverse species obtained from previous studies.
In well‐watered angiosperms, the maximum stomatal conductance was high and greater than that required for maximum WUE, but drought stress caused a rapid reduction in stomatal conductance and an increase in WUE in response to elevated concentrations of abscisic acid. However, in ferns, stomata did not open beyond the optimum point corresponding to maximum WUE and actually exhibited a steady WUE in response to dehydration. Thus, seed plants showed improved photosynthetic WUE under water stress.
The ability of seed plants to increase WUE could provide them with an advantage over ferns under drought conditions, thereby presumably increasing their fitness under selection pressure by drought.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17278</identifier><identifier>PMID: 33586157</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Abscisic Acid ; abscisic acid (ABA) ; Angiosperms ; Carbon dioxide ; Conductance ; Dehydration ; Drought ; drought stress ; Droughts ; fern ; Ferns ; Flowers & plants ; Gas exchange ; Leaves ; Optimization ; Photosynthesis ; Phylogeny ; Plant Leaves ; Plant species ; Plant Stomata ; Plants ; Resistance ; seed plant ; Seeds ; Species diversity ; Stomata ; Stomatal conductance ; Water ; Water deficit ; Water loss ; Water potential ; Water stress ; water‐use efficiency</subject><ispartof>The New phytologist, 2021-06, Vol.230 (5), p.2001-2010</ispartof><rights>2021 The Authors © 2021 New Phytologist Foundation</rights><rights>2021 The Authors New Phytologist © 2021 New Phytologist Foundation.</rights><rights>Copyright © 2021 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4548-d2b4df73661357109c00b662e098775dcc997d70dc1dd6cb361856fc44d284a13</citedby><cites>FETCH-LOGICAL-c4548-d2b4df73661357109c00b662e098775dcc997d70dc1dd6cb361856fc44d284a13</cites><orcidid>0000-0002-4067-1154 ; 0000-0001-6700-2703 ; 0000-0003-2227-2800 ; 0000-0002-4964-6107</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33586157$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Yu‐Jie</creatorcontrib><creatorcontrib>Bi, Min‐Hui</creatorcontrib><creatorcontrib>Nie, Zheng‐Fei</creatorcontrib><creatorcontrib>Jiang, Hui</creatorcontrib><creatorcontrib>Liu, Xu‐Dong</creatorcontrib><creatorcontrib>Fang, Xiang‐Wen</creatorcontrib><creatorcontrib>Brodribb, Timothy J.</creatorcontrib><title>Evolution of stomatal closure to optimize water‐use efficiency in response to dehydration in ferns and seed plants</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Plants control water‐use efficiency (WUE) by regulating water loss and CO2 diffusion through stomata. Variation in stomatal control has been reported among lineages of vascular plants, thus giving rise to the possibility that different lineages may show distinct WUE dynamics in response to water stress.
Here, we compared the response of gas exchange to decreasing leaf water potential among four ferns and nine seed plant species exposed to a gradually intensifying water deficit. The data collected were combined with those from 339 phylogenetically diverse species obtained from previous studies.
In well‐watered angiosperms, the maximum stomatal conductance was high and greater than that required for maximum WUE, but drought stress caused a rapid reduction in stomatal conductance and an increase in WUE in response to elevated concentrations of abscisic acid. However, in ferns, stomata did not open beyond the optimum point corresponding to maximum WUE and actually exhibited a steady WUE in response to dehydration. Thus, seed plants showed improved photosynthetic WUE under water stress.
The ability of seed plants to increase WUE could provide them with an advantage over ferns under drought conditions, thereby presumably increasing their fitness under selection pressure by drought.</description><subject>Abscisic Acid</subject><subject>abscisic acid (ABA)</subject><subject>Angiosperms</subject><subject>Carbon dioxide</subject><subject>Conductance</subject><subject>Dehydration</subject><subject>Drought</subject><subject>drought stress</subject><subject>Droughts</subject><subject>fern</subject><subject>Ferns</subject><subject>Flowers & plants</subject><subject>Gas exchange</subject><subject>Leaves</subject><subject>Optimization</subject><subject>Photosynthesis</subject><subject>Phylogeny</subject><subject>Plant Leaves</subject><subject>Plant species</subject><subject>Plant Stomata</subject><subject>Plants</subject><subject>Resistance</subject><subject>seed plant</subject><subject>Seeds</subject><subject>Species diversity</subject><subject>Stomata</subject><subject>Stomatal conductance</subject><subject>Water</subject><subject>Water deficit</subject><subject>Water loss</subject><subject>Water potential</subject><subject>Water stress</subject><subject>water‐use efficiency</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp1kb9uFDEQhy0EIkeg4AWQJRpSbGJ7_W9LFIUEKQIKkOgsnz2rONq1F9tLdFQ8As_Ik2DuAgUS00wx33wazQ-h55Sc0lZncbk5pYop_QBtKJdDp2mvHqINIUx3ksvPR-hJKbeEkEFI9hgd9b3Qkgq1QfXia5rWGlLEacSlptlWO2E3pbJmwDXhtNQwh2-A72yF_PP7j7UAhnEMLkB0OxwizlCWFMse93Cz89nujW00Qo4F2-hxAfB4mWys5Sl6NNqpwLP7fow-vbn4eH7VXb-_fHv--rpzXHDdebblflS9lLQXipLBEbKVkgEZtFLCOzcMyiviHfVeum0vqRZydJx7prml_TF6dfAuOX1ZoVQzh-JgakdAWothXA9i0G2voS__QW_TmmO7zjBBB0YUYaJRJwfK5VRKhtEsOcw27wwl5ncUpkVh9lE09sW9cd3O4P-Sf37fgLMDcBcm2P3fZN59uDoofwFJbZSJ</recordid><startdate>202106</startdate><enddate>202106</enddate><creator>Yang, Yu‐Jie</creator><creator>Bi, Min‐Hui</creator><creator>Nie, Zheng‐Fei</creator><creator>Jiang, Hui</creator><creator>Liu, Xu‐Dong</creator><creator>Fang, Xiang‐Wen</creator><creator>Brodribb, Timothy J.</creator><general>Wiley Subscription Services, Inc</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>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><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-4067-1154</orcidid><orcidid>https://orcid.org/0000-0001-6700-2703</orcidid><orcidid>https://orcid.org/0000-0003-2227-2800</orcidid><orcidid>https://orcid.org/0000-0002-4964-6107</orcidid></search><sort><creationdate>202106</creationdate><title>Evolution of stomatal closure to optimize water‐use efficiency in response to dehydration in ferns and seed plants</title><author>Yang, Yu‐Jie ; Bi, Min‐Hui ; Nie, Zheng‐Fei ; Jiang, Hui ; Liu, Xu‐Dong ; Fang, Xiang‐Wen ; Brodribb, Timothy J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4548-d2b4df73661357109c00b662e098775dcc997d70dc1dd6cb361856fc44d284a13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abscisic Acid</topic><topic>abscisic acid (ABA)</topic><topic>Angiosperms</topic><topic>Carbon dioxide</topic><topic>Conductance</topic><topic>Dehydration</topic><topic>Drought</topic><topic>drought stress</topic><topic>Droughts</topic><topic>fern</topic><topic>Ferns</topic><topic>Flowers & plants</topic><topic>Gas exchange</topic><topic>Leaves</topic><topic>Optimization</topic><topic>Photosynthesis</topic><topic>Phylogeny</topic><topic>Plant Leaves</topic><topic>Plant species</topic><topic>Plant Stomata</topic><topic>Plants</topic><topic>Resistance</topic><topic>seed plant</topic><topic>Seeds</topic><topic>Species diversity</topic><topic>Stomata</topic><topic>Stomatal conductance</topic><topic>Water</topic><topic>Water deficit</topic><topic>Water loss</topic><topic>Water potential</topic><topic>Water stress</topic><topic>water‐use efficiency</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Yu‐Jie</creatorcontrib><creatorcontrib>Bi, Min‐Hui</creatorcontrib><creatorcontrib>Nie, Zheng‐Fei</creatorcontrib><creatorcontrib>Jiang, Hui</creatorcontrib><creatorcontrib>Liu, Xu‐Dong</creatorcontrib><creatorcontrib>Fang, Xiang‐Wen</creatorcontrib><creatorcontrib>Brodribb, Timothy J.</creatorcontrib><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><collection>MEDLINE - Academic</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Yu‐Jie</au><au>Bi, Min‐Hui</au><au>Nie, Zheng‐Fei</au><au>Jiang, Hui</au><au>Liu, Xu‐Dong</au><au>Fang, Xiang‐Wen</au><au>Brodribb, Timothy J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of stomatal closure to optimize water‐use efficiency in response to dehydration in ferns and seed plants</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2021-06</date><risdate>2021</risdate><volume>230</volume><issue>5</issue><spage>2001</spage><epage>2010</epage><pages>2001-2010</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
Plants control water‐use efficiency (WUE) by regulating water loss and CO2 diffusion through stomata. Variation in stomatal control has been reported among lineages of vascular plants, thus giving rise to the possibility that different lineages may show distinct WUE dynamics in response to water stress.
Here, we compared the response of gas exchange to decreasing leaf water potential among four ferns and nine seed plant species exposed to a gradually intensifying water deficit. The data collected were combined with those from 339 phylogenetically diverse species obtained from previous studies.
In well‐watered angiosperms, the maximum stomatal conductance was high and greater than that required for maximum WUE, but drought stress caused a rapid reduction in stomatal conductance and an increase in WUE in response to elevated concentrations of abscisic acid. However, in ferns, stomata did not open beyond the optimum point corresponding to maximum WUE and actually exhibited a steady WUE in response to dehydration. Thus, seed plants showed improved photosynthetic WUE under water stress.
The ability of seed plants to increase WUE could provide them with an advantage over ferns under drought conditions, thereby presumably increasing their fitness under selection pressure by drought.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33586157</pmid><doi>10.1111/nph.17278</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-4067-1154</orcidid><orcidid>https://orcid.org/0000-0001-6700-2703</orcidid><orcidid>https://orcid.org/0000-0003-2227-2800</orcidid><orcidid>https://orcid.org/0000-0002-4964-6107</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Abscisic Acid abscisic acid (ABA) Angiosperms Carbon dioxide Conductance Dehydration Drought drought stress Droughts fern Ferns Flowers & plants Gas exchange Leaves Optimization Photosynthesis Phylogeny Plant Leaves Plant species Plant Stomata Plants Resistance seed plant Seeds Species diversity Stomata Stomatal conductance Water Water deficit Water loss Water potential Water stress water‐use efficiency |
title | Evolution of stomatal closure to optimize water‐use efficiency in response to dehydration in ferns and seed plants |
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