Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins
The water status of plant leaves depends on the efficiency of the water supply, from the vasculature to inner tissues. This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (K ros ) is higher in...
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| Veröffentlicht in: | The Plant cell 2013-03, Vol.25 (3), p.1029-1039 |
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| creator | Prado, Karine Boursiac, Yann Tournaire-Roux, Colette Monneuse, Jean-Marc Postaire, Olivier Da Ines, Olivier Schäffner, Anton R. Hem, Sonia Santoni, Véronique Maurel, Christophe |
| description | The water status of plant leaves depends on the efficiency of the water supply, from the vasculature to inner tissues. This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (K ros ) is higher in darkness than it is during the day. Knockout plants showed that three plasma membrane intrinsic proteins (PIPs) sharing expression in veins (PIP1;2, PIP2;1, and PIP2;6) contribute to rosette water transport, and PIP2;1 can fully account for K ros responsiveness to darkness. Directed expression of PIP2;1 in veins of a pip2;1 mutant was sufficient to restore K ros . In addition, a positive correlation, in both wild-type and PIP2;1-overexpressing plants, was found between K ros and the osmotic water permeability of protoplasts from the veins but not from the mesophyll. Thus, living cells in veins form a major hydraulic resistance in leaves. Quantitative proteomic analyses showed that light-dependent regulation of K ros is linked to diphosphorylation of PIP2;1 at Ser-280 and Ser-283. Expression in pip2;1 of phosphomimetic and phosphorylation-deficient forms of PIP2;1 demonstrated that phosphorylation at these two sites is necessary for K ros enhancement under darkness. These findings establish how regulation of a single aquaporin isoform in leaf veins critically determines leaf hydraulics. |
| doi_str_mv | 10.1105/tpc.112.108456 |
| format | Article |
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This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (K ros ) is higher in darkness than it is during the day. Knockout plants showed that three plasma membrane intrinsic proteins (PIPs) sharing expression in veins (PIP1;2, PIP2;1, and PIP2;6) contribute to rosette water transport, and PIP2;1 can fully account for K ros responsiveness to darkness. Directed expression of PIP2;1 in veins of a pip2;1 mutant was sufficient to restore K ros . In addition, a positive correlation, in both wild-type and PIP2;1-overexpressing plants, was found between K ros and the osmotic water permeability of protoplasts from the veins but not from the mesophyll. Thus, living cells in veins form a major hydraulic resistance in leaves. Quantitative proteomic analyses showed that light-dependent regulation of K ros is linked to diphosphorylation of PIP2;1 at Ser-280 and Ser-283. Expression in pip2;1 of phosphomimetic and phosphorylation-deficient forms of PIP2;1 demonstrated that phosphorylation at these two sites is necessary for K ros enhancement under darkness. These findings establish how regulation of a single aquaporin isoform in leaf veins critically determines leaf hydraulics.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.112.108456</identifier><identifier>PMID: 23532070</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Aquaporins ; Aquaporins - genetics ; Aquaporins - metabolism ; Arabidopsis ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis - radiation effects ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Biological Transport ; Cell Membrane - genetics ; Cell Membrane - metabolism ; Cell membranes ; Darkness ; fluid mechanics ; Gene Expression Regulation, Plant ; Hydraulics ; leaves ; Life Sciences ; Light ; Mesophyll ; Mesophyll Cells - metabolism ; Osmosis ; permeability ; Phosphorylation ; Physiological regulation ; Plant cells ; Plant Leaves - genetics ; Plant Leaves - metabolism ; Plant Leaves - radiation effects ; Plant Transpiration ; Plants ; Plants, Genetically Modified - genetics ; Plants, Genetically Modified - metabolism ; Plants, Genetically Modified - radiation effects ; Protein isoforms ; Protein Isoforms - genetics ; Protein Isoforms - metabolism ; proteomics ; Protoplasts ; Vegetal Biology ; Water - metabolism</subject><ispartof>The Plant cell, 2013-03, Vol.25 (3), p.1029-1039</ispartof><rights>2013 American Society of Plant Biologists</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</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-c545t-f95cee36f69e2d6758d1974453c696c33b1aa79a41e85e63c09a5f07870a15b53</citedby><cites>FETCH-LOGICAL-c545t-f95cee36f69e2d6758d1974453c696c33b1aa79a41e85e63c09a5f07870a15b53</cites><orcidid>0000-0002-4255-6440 ; 0000-0003-1903-0464 ; 0000-0002-1437-0921 ; 0000-0002-2966-5597 ; 0000-0002-1868-3781 ; 0000-0002-9545-9003</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23483164$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23483164$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,27903,27904,57996,58229</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23532070$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00921030$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Prado, Karine</creatorcontrib><creatorcontrib>Boursiac, Yann</creatorcontrib><creatorcontrib>Tournaire-Roux, Colette</creatorcontrib><creatorcontrib>Monneuse, Jean-Marc</creatorcontrib><creatorcontrib>Postaire, Olivier</creatorcontrib><creatorcontrib>Da Ines, Olivier</creatorcontrib><creatorcontrib>Schäffner, Anton R.</creatorcontrib><creatorcontrib>Hem, Sonia</creatorcontrib><creatorcontrib>Santoni, Véronique</creatorcontrib><creatorcontrib>Maurel, Christophe</creatorcontrib><title>Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>The water status of plant leaves depends on the efficiency of the water supply, from the vasculature to inner tissues. This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (K ros ) is higher in darkness than it is during the day. Knockout plants showed that three plasma membrane intrinsic proteins (PIPs) sharing expression in veins (PIP1;2, PIP2;1, and PIP2;6) contribute to rosette water transport, and PIP2;1 can fully account for K ros responsiveness to darkness. Directed expression of PIP2;1 in veins of a pip2;1 mutant was sufficient to restore K ros . In addition, a positive correlation, in both wild-type and PIP2;1-overexpressing plants, was found between K ros and the osmotic water permeability of protoplasts from the veins but not from the mesophyll. Thus, living cells in veins form a major hydraulic resistance in leaves. Quantitative proteomic analyses showed that light-dependent regulation of K ros is linked to diphosphorylation of PIP2;1 at Ser-280 and Ser-283. Expression in pip2;1 of phosphomimetic and phosphorylation-deficient forms of PIP2;1 demonstrated that phosphorylation at these two sites is necessary for K ros enhancement under darkness. These findings establish how regulation of a single aquaporin isoform in leaf veins critically determines leaf hydraulics.</description><subject>Aquaporins</subject><subject>Aquaporins - genetics</subject><subject>Aquaporins - metabolism</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis - radiation effects</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Biological Transport</subject><subject>Cell Membrane - genetics</subject><subject>Cell Membrane - metabolism</subject><subject>Cell membranes</subject><subject>Darkness</subject><subject>fluid mechanics</subject><subject>Gene Expression Regulation, Plant</subject><subject>Hydraulics</subject><subject>leaves</subject><subject>Life Sciences</subject><subject>Light</subject><subject>Mesophyll</subject><subject>Mesophyll Cells - metabolism</subject><subject>Osmosis</subject><subject>permeability</subject><subject>Phosphorylation</subject><subject>Physiological regulation</subject><subject>Plant cells</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Leaves - radiation effects</subject><subject>Plant Transpiration</subject><subject>Plants</subject><subject>Plants, Genetically Modified - genetics</subject><subject>Plants, Genetically Modified - metabolism</subject><subject>Plants, Genetically Modified - radiation effects</subject><subject>Protein isoforms</subject><subject>Protein Isoforms - genetics</subject><subject>Protein Isoforms - metabolism</subject><subject>proteomics</subject><subject>Protoplasts</subject><subject>Vegetal Biology</subject><subject>Water - metabolism</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1v1DAQxSMEoqVw5QbKkR6yHX8mviCtSmErrVSEAHGzvM5k4yobp3ay0v73eJVSLVw4-cnzmzdjvyx7S2BBCIircbBJ0AWBigv5LDsngtGCqurX86SBQ8GlIGfZqxjvAYCURL3MzihLFJRwnrlvuJ06Mzrf577Jl8FsXO2H6GK-RtPkq0MdzNQ5G_Pbfu-7PaaC27Zj8QkH7Gvsx_xr6-PQ-nA48XmYzOCD62Pu-vwnJvE6e9GYLuKbx_Mi-_H55vv1qljffbm9Xq4LK7gYi0YJi8hkIxXSWpaiqokqORfMSiUtYxtiTKkMJ1gJlMyCMqKBsirBELER7CL7OPsO02aHtU0bBtPpIbidCQftjdN_V3rX6q3fayYZT_OSweVs0P7Ttlqu9fEOQFECDPYksR8ehwX_MGEc9c5Fi11nevRT1PT455QxKv6LkjRdVAyESuhiRm3wMQZsntYgoI-x6xR7ElTPsaeG96dvfsL_5JyAdzNwH0cfTuq8YkRy9hvWjbLq</recordid><startdate>20130301</startdate><enddate>20130301</enddate><creator>Prado, Karine</creator><creator>Boursiac, Yann</creator><creator>Tournaire-Roux, Colette</creator><creator>Monneuse, Jean-Marc</creator><creator>Postaire, Olivier</creator><creator>Da Ines, Olivier</creator><creator>Schäffner, Anton R.</creator><creator>Hem, Sonia</creator><creator>Santoni, Véronique</creator><creator>Maurel, Christophe</creator><general>American Society of Plant Biologists</general><general>American Society of Plant Biologists (ASPB)</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>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4255-6440</orcidid><orcidid>https://orcid.org/0000-0003-1903-0464</orcidid><orcidid>https://orcid.org/0000-0002-1437-0921</orcidid><orcidid>https://orcid.org/0000-0002-2966-5597</orcidid><orcidid>https://orcid.org/0000-0002-1868-3781</orcidid><orcidid>https://orcid.org/0000-0002-9545-9003</orcidid></search><sort><creationdate>20130301</creationdate><title>Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins</title><author>Prado, Karine ; Boursiac, Yann ; Tournaire-Roux, Colette ; Monneuse, Jean-Marc ; Postaire, Olivier ; Da Ines, Olivier ; Schäffner, Anton R. ; Hem, Sonia ; Santoni, Véronique ; Maurel, Christophe</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c545t-f95cee36f69e2d6758d1974453c696c33b1aa79a41e85e63c09a5f07870a15b53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Aquaporins</topic><topic>Aquaporins - genetics</topic><topic>Aquaporins - metabolism</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis - radiation effects</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Biological Transport</topic><topic>Cell Membrane - genetics</topic><topic>Cell Membrane - metabolism</topic><topic>Cell membranes</topic><topic>Darkness</topic><topic>fluid mechanics</topic><topic>Gene Expression Regulation, Plant</topic><topic>Hydraulics</topic><topic>leaves</topic><topic>Life Sciences</topic><topic>Light</topic><topic>Mesophyll</topic><topic>Mesophyll Cells - metabolism</topic><topic>Osmosis</topic><topic>permeability</topic><topic>Phosphorylation</topic><topic>Physiological regulation</topic><topic>Plant cells</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Leaves - radiation effects</topic><topic>Plant Transpiration</topic><topic>Plants</topic><topic>Plants, Genetically Modified - genetics</topic><topic>Plants, Genetically Modified - metabolism</topic><topic>Plants, Genetically Modified - radiation effects</topic><topic>Protein isoforms</topic><topic>Protein Isoforms - genetics</topic><topic>Protein Isoforms - metabolism</topic><topic>proteomics</topic><topic>Protoplasts</topic><topic>Vegetal Biology</topic><topic>Water - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Prado, Karine</creatorcontrib><creatorcontrib>Boursiac, Yann</creatorcontrib><creatorcontrib>Tournaire-Roux, Colette</creatorcontrib><creatorcontrib>Monneuse, Jean-Marc</creatorcontrib><creatorcontrib>Postaire, Olivier</creatorcontrib><creatorcontrib>Da Ines, Olivier</creatorcontrib><creatorcontrib>Schäffner, Anton R.</creatorcontrib><creatorcontrib>Hem, Sonia</creatorcontrib><creatorcontrib>Santoni, Véronique</creatorcontrib><creatorcontrib>Maurel, Christophe</creatorcontrib><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>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Prado, Karine</au><au>Boursiac, Yann</au><au>Tournaire-Roux, Colette</au><au>Monneuse, Jean-Marc</au><au>Postaire, Olivier</au><au>Da Ines, Olivier</au><au>Schäffner, Anton R.</au><au>Hem, Sonia</au><au>Santoni, Véronique</au><au>Maurel, Christophe</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2013-03-01</date><risdate>2013</risdate><volume>25</volume><issue>3</issue><spage>1029</spage><epage>1039</epage><pages>1029-1039</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><abstract>The water status of plant leaves depends on the efficiency of the water supply, from the vasculature to inner tissues. This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (K ros ) is higher in darkness than it is during the day. Knockout plants showed that three plasma membrane intrinsic proteins (PIPs) sharing expression in veins (PIP1;2, PIP2;1, and PIP2;6) contribute to rosette water transport, and PIP2;1 can fully account for K ros responsiveness to darkness. Directed expression of PIP2;1 in veins of a pip2;1 mutant was sufficient to restore K ros . In addition, a positive correlation, in both wild-type and PIP2;1-overexpressing plants, was found between K ros and the osmotic water permeability of protoplasts from the veins but not from the mesophyll. Thus, living cells in veins form a major hydraulic resistance in leaves. Quantitative proteomic analyses showed that light-dependent regulation of K ros is linked to diphosphorylation of PIP2;1 at Ser-280 and Ser-283. Expression in pip2;1 of phosphomimetic and phosphorylation-deficient forms of PIP2;1 demonstrated that phosphorylation at these two sites is necessary for K ros enhancement under darkness. These findings establish how regulation of a single aquaporin isoform in leaf veins critically determines leaf hydraulics.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>23532070</pmid><doi>10.1105/tpc.112.108456</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-4255-6440</orcidid><orcidid>https://orcid.org/0000-0003-1903-0464</orcidid><orcidid>https://orcid.org/0000-0002-1437-0921</orcidid><orcidid>https://orcid.org/0000-0002-2966-5597</orcidid><orcidid>https://orcid.org/0000-0002-1868-3781</orcidid><orcidid>https://orcid.org/0000-0002-9545-9003</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Aquaporins Aquaporins - genetics Aquaporins - metabolism Arabidopsis Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis - radiation effects Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Biological Transport Cell Membrane - genetics Cell Membrane - metabolism Cell membranes Darkness fluid mechanics Gene Expression Regulation, Plant Hydraulics leaves Life Sciences Light Mesophyll Mesophyll Cells - metabolism Osmosis permeability Phosphorylation Physiological regulation Plant cells Plant Leaves - genetics Plant Leaves - metabolism Plant Leaves - radiation effects Plant Transpiration Plants Plants, Genetically Modified - genetics Plants, Genetically Modified - metabolism Plants, Genetically Modified - radiation effects Protein isoforms Protein Isoforms - genetics Protein Isoforms - metabolism proteomics Protoplasts Vegetal Biology Water - metabolism |
| title | Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins |
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