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Loss of NifQ Leads to Accumulation of Porphyrins and Altered Metal-Homeostasis in Nitrogen-Fixing Symbioses.

Identifieur interne : 000069 ( Main/Exploration ); précédent : 000068; suivant : 000070

Loss of NifQ Leads to Accumulation of Porphyrins and Altered Metal-Homeostasis in Nitrogen-Fixing Symbioses.

Auteurs : Maged M. Saad [Suisse] ; Sophie Michalet [Suisse] ; Romain Fossou [Suisse] ; Marina Putnik-Deli ; Michèle Crèvecoeur [Suisse] ; Julien Meyer [Suisse] ; Chloé De Malézieux [Suisse] ; Gérard Hopfgartner [Suisse] ; Ivana Maksimovi ; Xavier Perret [Suisse]

Source :

RBID : pubmed:30070615

Descripteurs français

English descriptors

Abstract

Symbiotic nitrogen fixation between legumes and rhizobia involves a coordinated expression of many plant and bacterial genes as well as finely tuned metabolic activities of micro- and macrosymbionts. In spite of such complex interactions, symbiotic proficiency remains a resilient process, with host plants apparently capable of compensating for some deficiencies in rhizobia. What controls nodule homeostasis is still poorly understood and probably varies between plant species. In this respect, the promiscuous Sinorhizobium (Ensifer) fredii strain NGR234 has become a model to assess the relative contribution of single gene products to many symbioses. Here, we describe how a deletion in nifQ of NGR234 (strain NGRΔnifQ) makes nodules of Vigna unguiculata, V. radiata, and Macroptilium atropurpureum but not of the mimisoid tree Leucaena leucocephala, purple-red. This peculiar dark-nodule phenotype did not necessarily correlate with a decreased proficiency of NGRΔnifQ but coincided with a 20-fold or more accumulation of coproporphyrin III and uroporphyrin III in V. unguiculata nodules. Porphyrin accumulation was not restricted to plant cells infected with bacteroids but also extended to the nodule cortex. Nodule metal-homeostasis was altered but not sufficiently to prevent assembly and functioning of nitrogenase. Although the role of NifQ in donating molybdenum during assembly of nitrogenase cofactor FeMo-co makes it essential in free-living diazotrophs, our results highlight the dispensability of NifQ in many legume species.

DOI: 10.1094/MPMI-07-18-0188-R
PubMed: 30070615


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<term>Nitrogen (metabolism)</term>
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<term>Azote (métabolisme)</term>
<term>Fixation de l'azote (MeSH)</term>
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<term>Protéines bactériennes (génétique)</term>
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<div type="abstract" xml:lang="en">Symbiotic nitrogen fixation between legumes and rhizobia involves a coordinated expression of many plant and bacterial genes as well as finely tuned metabolic activities of micro- and macrosymbionts. In spite of such complex interactions, symbiotic proficiency remains a resilient process, with host plants apparently capable of compensating for some deficiencies in rhizobia. What controls nodule homeostasis is still poorly understood and probably varies between plant species. In this respect, the promiscuous Sinorhizobium (Ensifer) fredii strain NGR234 has become a model to assess the relative contribution of single gene products to many symbioses. Here, we describe how a deletion in nifQ of NGR234 (strain NGRΔnifQ) makes nodules of Vigna unguiculata, V. radiata, and Macroptilium atropurpureum but not of the mimisoid tree Leucaena leucocephala, purple-red. This peculiar dark-nodule phenotype did not necessarily correlate with a decreased proficiency of NGRΔnifQ but coincided with a 20-fold or more accumulation of coproporphyrin III and uroporphyrin III in V. unguiculata nodules. Porphyrin accumulation was not restricted to plant cells infected with bacteroids but also extended to the nodule cortex. Nodule metal-homeostasis was altered but not sufficiently to prevent assembly and functioning of nitrogenase. Although the role of NifQ in donating molybdenum during assembly of nitrogenase cofactor FeMo-co makes it essential in free-living diazotrophs, our results highlight the dispensability of NifQ in many legume species.</div>
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<AbstractText>Symbiotic nitrogen fixation between legumes and rhizobia involves a coordinated expression of many plant and bacterial genes as well as finely tuned metabolic activities of micro- and macrosymbionts. In spite of such complex interactions, symbiotic proficiency remains a resilient process, with host plants apparently capable of compensating for some deficiencies in rhizobia. What controls nodule homeostasis is still poorly understood and probably varies between plant species. In this respect, the promiscuous Sinorhizobium (Ensifer) fredii strain NGR234 has become a model to assess the relative contribution of single gene products to many symbioses. Here, we describe how a deletion in nifQ of NGR234 (strain NGRΔnifQ) makes nodules of Vigna unguiculata, V. radiata, and Macroptilium atropurpureum but not of the mimisoid tree Leucaena leucocephala, purple-red. This peculiar dark-nodule phenotype did not necessarily correlate with a decreased proficiency of NGRΔnifQ but coincided with a 20-fold or more accumulation of coproporphyrin III and uroporphyrin III in V. unguiculata nodules. Porphyrin accumulation was not restricted to plant cells infected with bacteroids but also extended to the nodule cortex. Nodule metal-homeostasis was altered but not sufficiently to prevent assembly and functioning of nitrogenase. Although the role of NifQ in donating molybdenum during assembly of nitrogenase cofactor FeMo-co makes it essential in free-living diazotrophs, our results highlight the dispensability of NifQ in many legume species.</AbstractText>
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<Affiliation>1 University of Geneva, Sciences III, Department of Botany and Plant Biology, Microbiology Unit, 30 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>2 King Abdullah University of Science and Technology (KAUST), Biological and Environmental Sciences and Engineering Division (BESE), Thuwal 6900-2355, Kingdom of Saudi Arabia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Michalet</LastName>
<ForeName>Sophie</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>3 University of Geneva, Mass Spectrometry Core Facility (MZ 2.0), Faculty of Sciences, Bd d'Yvoy 11, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Fossou</LastName>
<ForeName>Romain</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>1 University of Geneva, Sciences III, Department of Botany and Plant Biology, Microbiology Unit, 30 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Putnik-Delić</LastName>
<ForeName>Marina</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>4 University of Novi Sad, Faculty of Agriculture, Novi Sad, Serbia; and.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Crèvecoeur</LastName>
<ForeName>Michèle</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>1 University of Geneva, Sciences III, Department of Botany and Plant Biology, Microbiology Unit, 30 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Meyer</LastName>
<ForeName>Julien</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>3 University of Geneva, Mass Spectrometry Core Facility (MZ 2.0), Faculty of Sciences, Bd d'Yvoy 11, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>de Malézieux</LastName>
<ForeName>Chloé</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>1 University of Geneva, Sciences III, Department of Botany and Plant Biology, Microbiology Unit, 30 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hopfgartner</LastName>
<ForeName>Gérard</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>5 University of Geneva, Department of Inorganic and Analytical Chemistry, Faculty of Sciences, 26 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Maksimović</LastName>
<ForeName>Ivana</ForeName>
<Initials>I</Initials>
<AffiliationInfo>
<Affiliation>4 University of Novi Sad, Faculty of Agriculture, Novi Sad, Serbia; and.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Perret</LastName>
<ForeName>Xavier</ForeName>
<Initials>X</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-8709-5302</Identifier>
<AffiliationInfo>
<Affiliation>1 University of Geneva, Sciences III, Department of Botany and Plant Biology, Microbiology Unit, 30 quai Ernest-Ansermet, CH-1211 Geneva 4, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2018</Year>
<Month>11</Month>
<Day>19</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="D001426">Bacterial Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D008670">Metals</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011166">Porphyrins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>N762921K75</RegistryNumber>
<NameOfSubstance UI="D009584">Nitrogen</NameOfSubstance>
</Chemical>
</ChemicalList>
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<MeshHeading>
<DescriptorName UI="D001426" MajorTopicYN="Y">Bacterial Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006706" MajorTopicYN="N">Homeostasis</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008670" MajorTopicYN="Y">Metals</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009584" MajorTopicYN="Y">Nitrogen</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009586" MajorTopicYN="N">Nitrogen Fixation</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011166" MajorTopicYN="Y">Porphyrins</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="Y">Symbiosis</DescriptorName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
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<Year>2018</Year>
<Month>8</Month>
<Day>3</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2019</Year>
<Month>7</Month>
<Day>26</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2018</Year>
<Month>8</Month>
<Day>3</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">30070615</ArticleId>
<ArticleId IdType="doi">10.1094/MPMI-07-18-0188-R</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Suisse</li>
</country>
<region>
<li>Canton de Genève</li>
</region>
<settlement>
<li>Genève</li>
</settlement>
<orgName>
<li>Université de Genève</li>
</orgName>
</list>
<tree>
<noCountry>
<name sortKey="Maksimovi, Ivana" sort="Maksimovi, Ivana" uniqKey="Maksimovi I" first="Ivana" last="Maksimovi">Ivana Maksimovi</name>
<name sortKey="Putnik Deli, Marina" sort="Putnik Deli, Marina" uniqKey="Putnik Deli M" first="Marina" last="Putnik-Deli">Marina Putnik-Deli</name>
</noCountry>
<country name="Suisse">
<region name="Canton de Genève">
<name sortKey="Saad, Maged M" sort="Saad, Maged M" uniqKey="Saad M" first="Maged M" last="Saad">Maged M. Saad</name>
</region>
<name sortKey="Crevecoeur, Michele" sort="Crevecoeur, Michele" uniqKey="Crevecoeur M" first="Michèle" last="Crèvecoeur">Michèle Crèvecoeur</name>
<name sortKey="De Malezieux, Chloe" sort="De Malezieux, Chloe" uniqKey="De Malezieux C" first="Chloé" last="De Malézieux">Chloé De Malézieux</name>
<name sortKey="Fossou, Romain" sort="Fossou, Romain" uniqKey="Fossou R" first="Romain" last="Fossou">Romain Fossou</name>
<name sortKey="Hopfgartner, Gerard" sort="Hopfgartner, Gerard" uniqKey="Hopfgartner G" first="Gérard" last="Hopfgartner">Gérard Hopfgartner</name>
<name sortKey="Meyer, Julien" sort="Meyer, Julien" uniqKey="Meyer J" first="Julien" last="Meyer">Julien Meyer</name>
<name sortKey="Michalet, Sophie" sort="Michalet, Sophie" uniqKey="Michalet S" first="Sophie" last="Michalet">Sophie Michalet</name>
<name sortKey="Perret, Xavier" sort="Perret, Xavier" uniqKey="Perret X" first="Xavier" last="Perret">Xavier Perret</name>
</country>
</tree>
</affiliations>
</record>

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