Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution.
Identifieur interne : 000443 ( Main/Exploration ); précédent : 000442; suivant : 000444Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution.
Auteurs : Audrey M V. Ah-Fong [États-Unis] ; Meenakshi S. Kagda [États-Unis] ; Melania Abrahamian [États-Unis] ; Howard S. Judelson [États-Unis]Source :
- PLoS pathogens [ 1553-7374 ] ; 2019.
Descripteurs français
- KwdFr :
- Adaptation physiologique (MeSH), Analyse de profil d'expression de gènes (MeSH), Glucan 1,4-alpha-glucosidase (métabolisme), Interactions hôte-parasite (génétique), Maladies des plantes (génétique), Maladies des plantes (parasitologie), Nutriments (métabolisme), Phytophthora (classification), Phytophthora (génétique), Phytophthora (physiologie), Protéines fongiques (génétique), Protéines fongiques (métabolisme), Régulation de l'expression des gènes fongiques (MeSH), Solanum tuberosum (croissance et développement), Solanum tuberosum (métabolisme), Solanum tuberosum (parasitologie), Tubercules (croissance et développement), Tubercules (métabolisme), Tubercules (parasitologie), Évolution moléculaire (MeSH).
- MESH :
- croissance et développement : Solanum tuberosum, Tubercules.
- génétique : Interactions hôte-parasite, Maladies des plantes, Phytophthora, Protéines fongiques.
- métabolisme : Glucan 1,4-alpha-glucosidase, Nutriments, Protéines fongiques, Solanum tuberosum, Tubercules.
- parasitologie : Maladies des plantes, Solanum tuberosum, Tubercules.
- physiologie : Phytophthora.
- Adaptation physiologique, Analyse de profil d'expression de gènes, Régulation de l'expression des gènes fongiques, Évolution moléculaire.
English descriptors
- KwdEn :
- Adaptation, Physiological (MeSH), Evolution, Molecular (MeSH), Fungal Proteins (genetics), Fungal Proteins (metabolism), Gene Expression Profiling (MeSH), Gene Expression Regulation, Fungal (MeSH), Glucan 1,4-alpha-Glucosidase (metabolism), Host-Parasite Interactions (genetics), Nutrients (metabolism), Phytophthora (classification), Phytophthora (genetics), Phytophthora (physiology), Plant Diseases (genetics), Plant Diseases (parasitology), Plant Tubers (growth & development), Plant Tubers (metabolism), Plant Tubers (parasitology), Solanum tuberosum (growth & development), Solanum tuberosum (metabolism), Solanum tuberosum (parasitology).
- MESH :
- chemical , genetics : Fungal Proteins.
- chemical , metabolism : Fungal Proteins, Glucan 1,4-alpha-Glucosidase.
- classification : Phytophthora.
- genetics : Host-Parasite Interactions, Phytophthora, Plant Diseases.
- growth & development : Plant Tubers, Solanum tuberosum.
- metabolism : Nutrients, Plant Tubers, Solanum tuberosum.
- parasitology : Plant Diseases, Plant Tubers, Solanum tuberosum.
- physiology : Phytophthora.
- Adaptation, Physiological, Evolution, Molecular, Gene Expression Profiling, Gene Expression Regulation, Fungal.
Abstract
The use of host nutrients to support pathogen growth is central to disease. We addressed the relationship between metabolism and trophic behavior by comparing metabolic gene expression during potato tuber colonization by two oomycetes, the hemibiotroph Phytophthora infestans and the necrotroph Pythium ultimum. Genes for several pathways including amino acid, nucleotide, and cofactor biosynthesis were expressed more by Ph. infestans during its biotrophic stage compared to Py. ultimum. In contrast, Py. ultimum had higher expression of genes for metabolizing compounds that are normally sequestered within plant cells but released to the pathogen upon plant cell lysis, such as starch and triacylglycerides. The transcription pattern of metabolic genes in Ph. infestans during late infection became more like that of Py. ultimum, consistent with the former's transition to necrotrophy. Interspecific variation in metabolic gene content was limited but included the presence of γ-amylase only in Py. ultimum. The pathogens were also found to employ strikingly distinct strategies for using nitrate. Measurements of mRNA, 15N labeling studies, enzyme assays, and immunoblotting indicated that the assimilation pathway in Ph. infestans was nitrate-insensitive but induced during amino acid and ammonium starvation. In contrast, the pathway was nitrate-induced but not amino acid-repressed in Py. ultimum. The lack of amino acid repression in Py. ultimum appears due to the absence of a transcription factor common to fungi and Phytophthora that acts as a nitrogen metabolite repressor. Evidence for functional diversification in nitrate reductase protein was also observed. Its temperature optimum was adapted to each organism's growth range, and its Km was much lower in Py. ultimum. In summary, we observed divergence in patterns of gene expression, gene content, and enzyme function which contribute to the fitness of each species in its niche.
DOI: 10.1371/journal.ppat.1007729
PubMed: 31002734
PubMed Central: PMC6493774
Affiliations:
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type="abstract" xml:lang="en">The use of host nutrients to support pathogen growth is central to disease. We addressed the relationship between metabolism and trophic behavior by comparing metabolic gene expression during potato tuber colonization by two oomycetes, the hemibiotroph Phytophthora infestans and the necrotroph Pythium ultimum. Genes for several pathways including amino acid, nucleotide, and cofactor biosynthesis were expressed more by Ph. infestans during its biotrophic stage compared to Py. ultimum. In contrast, Py. ultimum had higher expression of genes for metabolizing compounds that are normally sequestered within plant cells but released to the pathogen upon plant cell lysis, such as starch and triacylglycerides. The transcription pattern of metabolic genes in Ph. infestans during late infection became more like that of Py. ultimum, consistent with the former's transition to necrotrophy. Interspecific variation in metabolic gene content was limited but included the presence of γ-amylase only in Py. ultimum. The pathogens were also found to employ strikingly distinct strategies for using nitrate. Measurements of mRNA, 15N labeling studies, enzyme assays, and immunoblotting indicated that the assimilation pathway in Ph. infestans was nitrate-insensitive but induced during amino acid and ammonium starvation. In contrast, the pathway was nitrate-induced but not amino acid-repressed in Py. ultimum. The lack of amino acid repression in Py. ultimum appears due to the absence of a transcription factor common to fungi and Phytophthora that acts as a nitrogen metabolite repressor. Evidence for functional diversification in nitrate reductase protein was also observed. Its temperature optimum was adapted to each organism's growth range, and its Km was much lower in Py. ultimum. In summary, we observed divergence in patterns of gene expression, gene content, and enzyme function which contribute to the fitness of each species in its niche.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">31002734</PMID><DateCompleted><Year>2019</Year><Month>10</Month><Day>18</Day></DateCompleted><DateRevised><Year>2020</Year><Month>05</Month><Day>02</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1553-7374</ISSN><JournalIssue CitedMedium="Internet"><Volume>15</Volume><Issue>4</Issue><PubDate><Year>2019</Year><Month>04</Month></PubDate></JournalIssue><Title>PLoS pathogens</Title><ISOAbbreviation>PLoS Pathog</ISOAbbreviation></Journal><ArticleTitle>Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution.</ArticleTitle><Pagination><MedlinePgn>e1007729</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.ppat.1007729</ELocationID><Abstract><AbstractText>The use of host nutrients to support pathogen growth is central to disease. We addressed the relationship between metabolism and trophic behavior by comparing metabolic gene expression during potato tuber colonization by two oomycetes, the hemibiotroph Phytophthora infestans and the necrotroph Pythium ultimum. Genes for several pathways including amino acid, nucleotide, and cofactor biosynthesis were expressed more by Ph. infestans during its biotrophic stage compared to Py. ultimum. In contrast, Py. ultimum had higher expression of genes for metabolizing compounds that are normally sequestered within plant cells but released to the pathogen upon plant cell lysis, such as starch and triacylglycerides. The transcription pattern of metabolic genes in Ph. infestans during late infection became more like that of Py. ultimum, consistent with the former's transition to necrotrophy. Interspecific variation in metabolic gene content was limited but included the presence of γ-amylase only in Py. ultimum. The pathogens were also found to employ strikingly distinct strategies for using nitrate. Measurements of mRNA, 15N labeling studies, enzyme assays, and immunoblotting indicated that the assimilation pathway in Ph. infestans was nitrate-insensitive but induced during amino acid and ammonium starvation. In contrast, the pathway was nitrate-induced but not amino acid-repressed in Py. ultimum. The lack of amino acid repression in Py. ultimum appears due to the absence of a transcription factor common to fungi and Phytophthora that acts as a nitrogen metabolite repressor. Evidence for functional diversification in nitrate reductase protein was also observed. Its temperature optimum was adapted to each organism's growth range, and its Km was much lower in Py. ultimum. In summary, we observed divergence in patterns of gene expression, gene content, and enzyme function which contribute to the fitness of each species in its niche.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ah-Fong</LastName><ForeName>Audrey M V</ForeName><Initials>AMV</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kagda</LastName><ForeName>Meenakshi S</ForeName><Initials>MS</Initials><Identifier Source="ORCID">0000-0003-0545-0185</Identifier><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Abrahamian</LastName><ForeName>Melania</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Judelson</LastName><ForeName>Howard S</ForeName><Initials>HS</Initials><Identifier Source="ORCID">0000-0001-7865-6235</Identifier><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, United States of America.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>S10 OD016290</GrantID><Acronym>OD</Acronym><Agency>NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>04</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS Pathog</MedlineTA><NlmUniqueID>101238921</NlmUniqueID><ISSNLinking>1553-7366</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D005656">Fungal Proteins</NameOfSubstance></Chemical><Chemical><RegistryNumber>EC 3.2.1.3</RegistryNumber><NameOfSubstance UI="D005087">Glucan 1,4-alpha-Glucosidase</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000222" MajorTopicYN="N">Adaptation, Physiological</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D019143" MajorTopicYN="N">Evolution, Molecular</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005656" MajorTopicYN="N">Fungal Proteins</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D020869" MajorTopicYN="N">Gene Expression Profiling</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015966" MajorTopicYN="N">Gene Expression Regulation, Fungal</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005087" MajorTopicYN="N">Glucan 1,4-alpha-Glucosidase</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D006790" MajorTopicYN="N">Host-Parasite Interactions</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D000078622" MajorTopicYN="N">Nutrients</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName><QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName><QualifierName UI="Q000469" MajorTopicYN="Y">parasitology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D035281" MajorTopicYN="N">Plant Tubers</DescriptorName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011198" MajorTopicYN="N">Solanum tuberosum</DescriptorName><QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName><QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName></MeshHeading></MeshHeadingList><CoiStatement>The authors have declared that no competing interests exist.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>12</Month><Day>04</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>03</Month><Day>25</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2019</Year><Month>05</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>4</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>10</Month><Day>19</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>4</Month><Day>20</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId 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