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A Viable New Strategy for the Discovery of Peptide Proteolytic Cleavage Products in Plant-Microbe Interactions.

Identifieur interne : 000599 ( Main/Exploration ); précédent : 000598; suivant : 000600

A Viable New Strategy for the Discovery of Peptide Proteolytic Cleavage Products in Plant-Microbe Interactions.

Auteurs : Manuel I. Villalobos Solis [États-Unis] ; Suresh Poudel [États-Unis] ; Clemence Bonnot [France] ; Him K. Shrestha [États-Unis] ; Robert L. Hettich [États-Unis] ; Claire Veneault-Fourrey [France] ; Francis Martin [France] ; Paul E. Abraham [États-Unis]

Source :

RBID : pubmed:32597696

Descripteurs français

English descriptors

Abstract

Small peptides that are proteolytic cleavage products (PCPs) of less than 100 amino acids are emerging as key signaling molecules that mediate cell-to-cell communication and biological processes that occur between and within plants, fungi, and bacteria. Yet, the discovery and characterization of these molecules is largely overlooked. Today, selective enrichment and subsequent characterization by mass spectrometry-based sequencing offers the greatest potential for their comprehensive characterization, however qualitative and quantitative performance metrics are rarely captured. Herein, we addressed this need by benchmarking the performance of an enrichment strategy, optimized specifically for small PCPs, using state-of-the-art de novo-assisted peptide sequencing. As a case study, we implemented this approach to identify PCPs from different root and foliar tissues of the hybrid poplar Populus × canescens 717-1B4 in interaction with the ectomycorrhizal basidiomycete Laccaria bicolor. In total, we identified 1,660 and 2,870 Populus and L. bicolor unique PCPs, respectively. Qualitative results supported the identification of well-known PCPs, like the mature form of the photosystem II complex 5-kDa protein (approximately 3 kDa). A total of 157 PCPs were determined to be significantly more abundant in root tips with established ectomycorrhiza when compared with root tips without established ectomycorrhiza and extramatrical mycelium of L. bicolor. These PCPs mapped to 64 Populus proteins and 69 L. bicolor proteins in our database, with several of them previously implicated in biologically relevant associations between plant and fungus.

DOI: 10.1094/MPMI-04-20-0082-TA
PubMed: 32597696


Affiliations:


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Le document en format XML

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<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Host Microbial Interactions (MeSH)</term>
<term>Laccaria (physiology)</term>
<term>Mycorrhizae (physiology)</term>
<term>Peptides (chemistry)</term>
<term>Plant Roots (chemistry)</term>
<term>Plant Roots (microbiology)</term>
<term>Populus (chemistry)</term>
<term>Populus (microbiology)</term>
<term>Proteolysis (MeSH)</term>
<term>Sequence Analysis, Protein (MeSH)</term>
</keywords>
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<term>Analyse de séquence de protéine (MeSH)</term>
<term>Interactions hôte-microbes (MeSH)</term>
<term>Laccaria (physiologie)</term>
<term>Mycorhizes (physiologie)</term>
<term>Peptides (composition chimique)</term>
<term>Populus (composition chimique)</term>
<term>Populus (microbiologie)</term>
<term>Protéolyse (MeSH)</term>
<term>Racines de plante (composition chimique)</term>
<term>Racines de plante (microbiologie)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
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<term>Peptides</term>
</keywords>
<keywords scheme="MESH" qualifier="chemistry" xml:lang="en">
<term>Plant Roots</term>
<term>Populus</term>
</keywords>
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<term>Peptides</term>
<term>Populus</term>
<term>Racines de plante</term>
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<term>Racines de plante</term>
</keywords>
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<term>Plant Roots</term>
<term>Populus</term>
</keywords>
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</keywords>
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<term>Mycorrhizae</term>
</keywords>
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<term>Proteolysis</term>
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<term>Analyse de séquence de protéine</term>
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<term>Protéolyse</term>
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<div type="abstract" xml:lang="en">Small peptides that are proteolytic cleavage products (PCPs) of less than 100 amino acids are emerging as key signaling molecules that mediate cell-to-cell communication and biological processes that occur between and within plants, fungi, and bacteria. Yet, the discovery and characterization of these molecules is largely overlooked. Today, selective enrichment and subsequent characterization by mass spectrometry-based sequencing offers the greatest potential for their comprehensive characterization, however qualitative and quantitative performance metrics are rarely captured. Herein, we addressed this need by benchmarking the performance of an enrichment strategy, optimized specifically for small PCPs, using state-of-the-art de novo-assisted peptide sequencing. As a case study, we implemented this approach to identify PCPs from different root and foliar tissues of the hybrid poplar
<i>Populus</i>
×
<i>canescens</i>
717-1B4 in interaction with the ectomycorrhizal basidiomycete
<i>Laccaria bicolor</i>
. In total, we identified 1,660 and 2,870
<i>Populus</i>
and
<i>L. bicolor</i>
unique PCPs, respectively. Qualitative results supported the identification of well-known PCPs, like the mature form of the photosystem II complex 5-kDa protein (approximately 3 kDa). A total of 157 PCPs were determined to be significantly more abundant in root tips with established ectomycorrhiza when compared with root tips without established ectomycorrhiza and extramatrical mycelium of
<i>L. bicolor</i>
. These PCPs mapped to 64
<i>Populus</i>
proteins and 69
<i>L. bicolor</i>
proteins in our database, with several of them previously implicated in biologically relevant associations between plant and fungus.</div>
</front>
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<AbstractText>Small peptides that are proteolytic cleavage products (PCPs) of less than 100 amino acids are emerging as key signaling molecules that mediate cell-to-cell communication and biological processes that occur between and within plants, fungi, and bacteria. Yet, the discovery and characterization of these molecules is largely overlooked. Today, selective enrichment and subsequent characterization by mass spectrometry-based sequencing offers the greatest potential for their comprehensive characterization, however qualitative and quantitative performance metrics are rarely captured. Herein, we addressed this need by benchmarking the performance of an enrichment strategy, optimized specifically for small PCPs, using state-of-the-art de novo-assisted peptide sequencing. As a case study, we implemented this approach to identify PCPs from different root and foliar tissues of the hybrid poplar
<i>Populus</i>
×
<i>canescens</i>
717-1B4 in interaction with the ectomycorrhizal basidiomycete
<i>Laccaria bicolor</i>
. In total, we identified 1,660 and 2,870
<i>Populus</i>
and
<i>L. bicolor</i>
unique PCPs, respectively. Qualitative results supported the identification of well-known PCPs, like the mature form of the photosystem II complex 5-kDa protein (approximately 3 kDa). A total of 157 PCPs were determined to be significantly more abundant in root tips with established ectomycorrhiza when compared with root tips without established ectomycorrhiza and extramatrical mycelium of
<i>L. bicolor</i>
. These PCPs mapped to 64
<i>Populus</i>
proteins and 69
<i>L. bicolor</i>
proteins in our database, with several of them previously implicated in biologically relevant associations between plant and fungus.</AbstractText>
</Abstract>
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<ForeName>Robert L</ForeName>
<Initials>RL</Initials>
<AffiliationInfo>
<Affiliation>Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, U.S.A.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Veneault-Fourrey</LastName>
<ForeName>Claire</ForeName>
<Initials>C</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-9778-2659</Identifier>
<AffiliationInfo>
<Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280 Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Martin</LastName>
<ForeName>Francis</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>UMR 1136 INRA-Université de Lorraine 'Interactions Arbres/Microorganismes', Laboratoire d'Excellence ARBRE, Centre INRA-Lorraine, 54280 Champenoux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Abraham</LastName>
<ForeName>Paul E</ForeName>
<Initials>PE</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0003-2685-9123</Identifier>
<AffiliationInfo>
<Affiliation>Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, U.S.A.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>08</Month>
<Day>17</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Mol Plant Microbe Interact</MedlineTA>
<NlmUniqueID>9107902</NlmUniqueID>
<ISSNLinking>0894-0282</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010455">Peptides</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000076662" MajorTopicYN="N">Host Microbial Interactions</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D055399" MajorTopicYN="N">Laccaria</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010455" MajorTopicYN="N">Peptides</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018517" MajorTopicYN="N">Plant Roots</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="Y">chemistry</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059748" MajorTopicYN="Y">Proteolysis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020539" MajorTopicYN="N">Sequence Analysis, Protein</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">de novo peptide sequencing</Keyword>
<Keyword MajorTopicYN="N">liquid chromatography</Keyword>
<Keyword MajorTopicYN="N">small peptides</Keyword>
<Keyword MajorTopicYN="N">tandem mass spectrometry</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="pubmed">
<Year>2020</Year>
<Month>7</Month>
<Day>1</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2020</Year>
<Month>11</Month>
<Day>18</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2020</Year>
<Month>6</Month>
<Day>30</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">32597696</ArticleId>
<ArticleId IdType="doi">10.1094/MPMI-04-20-0082-TA</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>France</li>
<li>États-Unis</li>
</country>
<region>
<li>Grand Est</li>
<li>Lorraine (région)</li>
<li>Tennessee</li>
</region>
<settlement>
<li>Champenoux</li>
</settlement>
</list>
<tree>
<country name="États-Unis">
<region name="Tennessee">
<name sortKey="Villalobos Solis, Manuel I" sort="Villalobos Solis, Manuel I" uniqKey="Villalobos Solis M" first="Manuel I" last="Villalobos Solis">Manuel I. Villalobos Solis</name>
</region>
<name sortKey="Abraham, Paul E" sort="Abraham, Paul E" uniqKey="Abraham P" first="Paul E" last="Abraham">Paul E. Abraham</name>
<name sortKey="Hettich, Robert L" sort="Hettich, Robert L" uniqKey="Hettich R" first="Robert L" last="Hettich">Robert L. Hettich</name>
<name sortKey="Poudel, Suresh" sort="Poudel, Suresh" uniqKey="Poudel S" first="Suresh" last="Poudel">Suresh Poudel</name>
<name sortKey="Shrestha, Him K" sort="Shrestha, Him K" uniqKey="Shrestha H" first="Him K" last="Shrestha">Him K. Shrestha</name>
<name sortKey="Shrestha, Him K" sort="Shrestha, Him K" uniqKey="Shrestha H" first="Him K" last="Shrestha">Him K. Shrestha</name>
<name sortKey="Villalobos Solis, Manuel I" sort="Villalobos Solis, Manuel I" uniqKey="Villalobos Solis M" first="Manuel I" last="Villalobos Solis">Manuel I. Villalobos Solis</name>
</country>
<country name="France">
<region name="Grand Est">
<name sortKey="Bonnot, Clemence" sort="Bonnot, Clemence" uniqKey="Bonnot C" first="Clemence" last="Bonnot">Clemence Bonnot</name>
</region>
<name sortKey="Martin, Francis" sort="Martin, Francis" uniqKey="Martin F" first="Francis" last="Martin">Francis Martin</name>
<name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
</country>
</tree>
</affiliations>
</record>

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