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A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants.

Identifieur interne : 001F12 ( Main/Exploration ); précédent : 001F11; suivant : 001F13

A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants.

Auteurs : Rupesh Kailasrao Deshmukh [Canada] ; Julien Vivancos [Canada] ; Gowsica Ramakrishnan [Canada] ; Valérie Guérin [Canada] ; Gabriel Carpentier [Canada] ; Humira Sonah [Canada] ; Caroline Labbé [Canada] ; Paul Isenring [Canada] ; Francois J. Belzile [Canada] ; Richard R. Bélanger [Canada]

Source :

RBID : pubmed:26095507

Descripteurs français

English descriptors

Abstract

The controversy surrounding silicon (Si) benefits and essentiality in plants is exacerbated by the differential ability of species to absorb this element. This property is seemingly enhanced in species carrying specific nodulin 26-like intrinsic proteins (NIPs), a subclass of aquaporins. In this work, our aim was to characterize plant aquaporins to define the features that confer Si permeability. Through comparative analysis of 985 aquaporins in 25 species with differing abilities to absorb Si, we were able to predict 30 Si transporters and discovered that Si absorption is exclusively confined to species that possess NIP-III aquaporins with a GSGR selectivity filter and a precise distance of 108 amino acids (AA) between the asparagine-proline-alanine (NPA) domains. The latter feature is of particular significance since it had never been reported to be essential for Si selectivity. Functionality assessed in the Xenopus oocyte expression system showed that NIPs with 108 AA spacing exhibited Si permeability, while proteins differing in that distance did not. In subsequent functional studies, a Si transporter from poplar mutated into variants with 109- or 107-AA spacing failed to import, and a tomato NIP gene mutated from 109 to 108 AA exhibited a rare gain of function. These results provide a precise molecular basis to classify higher plants into Si accumulators or excluders.

DOI: 10.1111/tpj.12904
PubMed: 26095507


Affiliations:


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<div type="abstract" xml:lang="en">The controversy surrounding silicon (Si) benefits and essentiality in plants is exacerbated by the differential ability of species to absorb this element. This property is seemingly enhanced in species carrying specific nodulin 26-like intrinsic proteins (NIPs), a subclass of aquaporins. In this work, our aim was to characterize plant aquaporins to define the features that confer Si permeability. Through comparative analysis of 985 aquaporins in 25 species with differing abilities to absorb Si, we were able to predict 30 Si transporters and discovered that Si absorption is exclusively confined to species that possess NIP-III aquaporins with a GSGR selectivity filter and a precise distance of 108 amino acids (AA) between the asparagine-proline-alanine (NPA) domains. The latter feature is of particular significance since it had never been reported to be essential for Si selectivity. Functionality assessed in the Xenopus oocyte expression system showed that NIPs with 108 AA spacing exhibited Si permeability, while proteins differing in that distance did not. In subsequent functional studies, a Si transporter from poplar mutated into variants with 109- or 107-AA spacing failed to import, and a tomato NIP gene mutated from 109 to 108 AA exhibited a rare gain of function. These results provide a precise molecular basis to classify higher plants into Si accumulators or excluders. </div>
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<ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.12904</ELocationID>
<Abstract>
<AbstractText>The controversy surrounding silicon (Si) benefits and essentiality in plants is exacerbated by the differential ability of species to absorb this element. This property is seemingly enhanced in species carrying specific nodulin 26-like intrinsic proteins (NIPs), a subclass of aquaporins. In this work, our aim was to characterize plant aquaporins to define the features that confer Si permeability. Through comparative analysis of 985 aquaporins in 25 species with differing abilities to absorb Si, we were able to predict 30 Si transporters and discovered that Si absorption is exclusively confined to species that possess NIP-III aquaporins with a GSGR selectivity filter and a precise distance of 108 amino acids (AA) between the asparagine-proline-alanine (NPA) domains. The latter feature is of particular significance since it had never been reported to be essential for Si selectivity. Functionality assessed in the Xenopus oocyte expression system showed that NIPs with 108 AA spacing exhibited Si permeability, while proteins differing in that distance did not. In subsequent functional studies, a Si transporter from poplar mutated into variants with 109- or 107-AA spacing failed to import, and a tomato NIP gene mutated from 109 to 108 AA exhibited a rare gain of function. These results provide a precise molecular basis to classify higher plants into Si accumulators or excluders. </AbstractText>
<CopyrightInformation>© 2015 The Authors The Plant Journal © 2015 John Wiley & Sons Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Deshmukh</LastName>
<ForeName>Rupesh Kailasrao</ForeName>
<Initials>RK</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-4167-6552</Identifier>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Vivancos</LastName>
<ForeName>Julien</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ramakrishnan</LastName>
<ForeName>Gowsica</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guérin</LastName>
<ForeName>Valérie</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Carpentier</LastName>
<ForeName>Gabriel</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Nephrology Group, L'Hôtel-Dieu de Québec Institution, Department of Medicine, Faculty of Medicine, Université Laval, Québec, QC, G1R 2J6, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sonah</LastName>
<ForeName>Humira</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Labbé</LastName>
<ForeName>Caroline</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Isenring</LastName>
<ForeName>Paul</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Nephrology Group, L'Hôtel-Dieu de Québec Institution, Department of Medicine, Faculty of Medicine, Université Laval, Québec, QC, G1R 2J6, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Belzile</LastName>
<ForeName>Francois J</ForeName>
<Initials>FJ</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bélanger</LastName>
<ForeName>Richard R</ForeName>
<Initials>RR</Initials>
<AffiliationInfo>
<Affiliation>Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2015</Year>
<Month>07</Month>
<Day>03</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Plant J</MedlineTA>
<NlmUniqueID>9207397</NlmUniqueID>
<ISSNLinking>0960-7412</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D020346">Aquaporins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D009842">Oligopeptides</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C550288">asparagine-proline-alanine</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>Z4152N8IUI</RegistryNumber>
<NameOfSubstance UI="D012825">Silicon</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020346" MajorTopicYN="N">Aquaporins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D023281" MajorTopicYN="N">Genomics</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009842" MajorTopicYN="N">Oligopeptides</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012825" MajorTopicYN="N">Silicon</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014982" MajorTopicYN="N">Xenopus laevis</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">NPA domains</Keyword>
<Keyword MajorTopicYN="N">aquaporins</Keyword>
<Keyword MajorTopicYN="N">comparative genomics</Keyword>
<Keyword MajorTopicYN="N">plant species</Keyword>
<Keyword MajorTopicYN="N">silicon role in plants</Keyword>
<Keyword MajorTopicYN="N">silicon transporter</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2015</Year>
<Month>03</Month>
<Day>13</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2015</Year>
<Month>05</Month>
<Day>15</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2015</Year>
<Month>06</Month>
<Day>01</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2015</Year>
<Month>6</Month>
<Day>23</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2015</Year>
<Month>6</Month>
<Day>23</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2016</Year>
<Month>5</Month>
<Day>10</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">26095507</ArticleId>
<ArticleId IdType="doi">10.1111/tpj.12904</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Canada</li>
</country>
<region>
<li>Québec</li>
</region>
<settlement>
<li>Québec (ville)</li>
</settlement>
<orgName>
<li>Université Laval</li>
</orgName>
</list>
<tree>
<country name="Canada">
<region name="Québec">
<name sortKey="Deshmukh, Rupesh Kailasrao" sort="Deshmukh, Rupesh Kailasrao" uniqKey="Deshmukh R" first="Rupesh Kailasrao" last="Deshmukh">Rupesh Kailasrao Deshmukh</name>
</region>
<name sortKey="Belanger, Richard R" sort="Belanger, Richard R" uniqKey="Belanger R" first="Richard R" last="Bélanger">Richard R. Bélanger</name>
<name sortKey="Belzile, Francois J" sort="Belzile, Francois J" uniqKey="Belzile F" first="Francois J" last="Belzile">Francois J. Belzile</name>
<name sortKey="Carpentier, Gabriel" sort="Carpentier, Gabriel" uniqKey="Carpentier G" first="Gabriel" last="Carpentier">Gabriel Carpentier</name>
<name sortKey="Guerin, Valerie" sort="Guerin, Valerie" uniqKey="Guerin V" first="Valérie" last="Guérin">Valérie Guérin</name>
<name sortKey="Isenring, Paul" sort="Isenring, Paul" uniqKey="Isenring P" first="Paul" last="Isenring">Paul Isenring</name>
<name sortKey="Labbe, Caroline" sort="Labbe, Caroline" uniqKey="Labbe C" first="Caroline" last="Labbé">Caroline Labbé</name>
<name sortKey="Ramakrishnan, Gowsica" sort="Ramakrishnan, Gowsica" uniqKey="Ramakrishnan G" first="Gowsica" last="Ramakrishnan">Gowsica Ramakrishnan</name>
<name sortKey="Sonah, Humira" sort="Sonah, Humira" uniqKey="Sonah H" first="Humira" last="Sonah">Humira Sonah</name>
<name sortKey="Vivancos, Julien" sort="Vivancos, Julien" uniqKey="Vivancos J" first="Julien" last="Vivancos">Julien Vivancos</name>
</country>
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</record>

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