Defense Compounds Rather Than Nutrient Availability Shape Aggressiveness Trait Variation Along a Leaf Maturity Gradient in a Biotrophic Plant Pathogen.
Identifieur interne : 000021 ( Main/Exploration ); précédent : 000020; suivant : 000022Defense Compounds Rather Than Nutrient Availability Shape Aggressiveness Trait Variation Along a Leaf Maturity Gradient in a Biotrophic Plant Pathogen.
Auteurs : Agathe Maupetit [France] ; Romain Larbat [France] ; Michaël Pernaci [France] ; Axelle Andrieux [France] ; Cécile Guinet [France] ; Anne-Laure Boutigny [France] ; Bénédicte Fabre [France] ; Pascal Frey [France] ; Fabien Halkett [France]Source :
- Frontiers in plant science [ 1664-462X ] ; 2018.
Abstract
Foliar pathogens face heterogeneous environments depending on the maturity of leaves they interact with. In particular, nutrient availability as well as defense levels may vary significantly, with opposing effects on the success of infection. The present study tested which of these factors have a dominant effect on the pathogen's development. Poplar leaf disks of eight maturity levels were inoculated with the poplar rust fungus Melampsora larici-populina using an innovative single-spore inoculation procedure. A set of quantitative fungal traits (infection efficiency, latent period, uredinia size, mycelium quantity, sporulation rate, sporulation capacity, and spore volume) was measured on each infected leaf disk. Uninfected parts of the leaves were analyzed for their nutrient (sugars, total C and N) and defense compounds (phenolics) content. We found that M. larici-populina is more aggressive on more mature leaves as indicated by wider uredinia and a higher sporulation rate. Other traits varied independently from each other without a consistent pattern. None of the pathogen traits correlated with leaf sugar, total C, or total N content. In contrast, phenolic contents (flavonols, hydroxycinnamic acid esters, and salicinoids) were negatively correlated with uredinia size and sporulation rate. The pathogen's fitness appeared to be more constrained by the constitutive plant defense level than limited by nutrient availability, as evident in the decrease in sporulation.
DOI: 10.3389/fpls.2018.01396
PubMed: 30323821
PubMed Central: PMC6172983
Affiliations:
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type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Larbat, Romain" sort="Larbat, Romain" uniqKey="Larbat R" first="Romain" last="Larbat">Romain Larbat</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, LAE, Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, LAE, Nancy</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Pernaci, Michael" sort="Pernaci, Michael" uniqKey="Pernaci M" first="Michaël" last="Pernaci">Michaël Pernaci</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</nlm:affiliation><country 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sort="Guinet, Cecile" uniqKey="Guinet C" first="Cécile" last="Guinet">Cécile Guinet</name><affiliation wicri:level="1"><nlm:affiliation>ANSES, Laboratoire de la Santé des Végétaux, Unité de Mycologie, Malzéville, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>ANSES, Laboratoire de la Santé des Végétaux, Unité de Mycologie, Malzéville</wicri:regionArea><wicri:noRegion>Malzéville</wicri:noRegion><wicri:noRegion>Malzéville</wicri:noRegion></affiliation></author><author><name sortKey="Boutigny, Anne Laure" sort="Boutigny, Anne Laure" uniqKey="Boutigny A" first="Anne-Laure" last="Boutigny">Anne-Laure Boutigny</name><affiliation wicri:level="1"><nlm:affiliation>ANSES, Laboratoire de la Santé des Végétaux, Unité de Mycologie, Malzéville, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>ANSES, Laboratoire de la Santé des Végétaux, Unité de Mycologie, Malzéville</wicri:regionArea><wicri:noRegion>Malzéville</wicri:noRegion><wicri:noRegion>Malzéville</wicri:noRegion></affiliation></author><author><name sortKey="Fabre, Benedicte" sort="Fabre, Benedicte" uniqKey="Fabre B" first="Bénédicte" last="Fabre">Bénédicte Fabre</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, IAM, Nancy</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Frey, Pascal" sort="Frey, Pascal" uniqKey="Frey P" first="Pascal" last="Frey">Pascal Frey</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, IAM, Nancy</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author><author><name sortKey="Halkett, Fabien" sort="Halkett, Fabien" uniqKey="Halkett F" first="Fabien" last="Halkett">Fabien Halkett</name><affiliation wicri:level="4"><nlm:affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Université de Lorraine, INRA, IAM, Nancy</wicri:regionArea><placeName><region type="region">Grand Est</region><region type="old region">Lorraine (région)</region><settlement type="city">Nancy</settlement></placeName><orgName type="university">Université de Lorraine</orgName></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Foliar pathogens face heterogeneous environments depending on the maturity of leaves they interact with. In particular, nutrient availability as well as defense levels may vary significantly, with opposing effects on the success of infection. The present study tested which of these factors have a dominant effect on the pathogen's development. Poplar leaf disks of eight maturity levels were inoculated with the poplar rust fungus <i>Melampsora larici-populina</i> using an innovative single-spore inoculation procedure. A set of quantitative fungal traits (infection efficiency, latent period, uredinia size, mycelium quantity, sporulation rate, sporulation capacity, and spore volume) was measured on each infected leaf disk. Uninfected parts of the leaves were analyzed for their nutrient (sugars, total C and N) and defense compounds (phenolics) content. We found that <i>M. larici-populina</i> is more aggressive on more mature leaves as indicated by wider uredinia and a higher sporulation rate. Other traits varied independently from each other without a consistent pattern. None of the pathogen traits correlated with leaf sugar, total C, or total N content. In contrast, phenolic contents (flavonols, hydroxycinnamic acid esters, and salicinoids) were negatively correlated with uredinia size and sporulation rate. The pathogen's fitness appeared to be more constrained by the constitutive plant defense level than limited by nutrient availability, as evident in the decrease in sporulation.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30323821</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>9</Volume><PubDate><Year>2018</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>Defense Compounds Rather Than Nutrient Availability Shape Aggressiveness Trait Variation Along a Leaf Maturity Gradient in a Biotrophic Plant Pathogen.</ArticleTitle><Pagination><MedlinePgn>1396</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2018.01396</ELocationID><Abstract><AbstractText>Foliar pathogens face heterogeneous environments depending on the maturity of leaves they interact with. In particular, nutrient availability as well as defense levels may vary significantly, with opposing effects on the success of infection. The present study tested which of these factors have a dominant effect on the pathogen's development. Poplar leaf disks of eight maturity levels were inoculated with the poplar rust fungus <i>Melampsora larici-populina</i> using an innovative single-spore inoculation procedure. A set of quantitative fungal traits (infection efficiency, latent period, uredinia size, mycelium quantity, sporulation rate, sporulation capacity, and spore volume) was measured on each infected leaf disk. Uninfected parts of the leaves were analyzed for their nutrient (sugars, total C and N) and defense compounds (phenolics) content. We found that <i>M. larici-populina</i> is more aggressive on more mature leaves as indicated by wider uredinia and a higher sporulation rate. Other traits varied independently from each other without a consistent pattern. None of the pathogen traits correlated with leaf sugar, total C, or total N content. In contrast, phenolic contents (flavonols, hydroxycinnamic acid esters, and salicinoids) were negatively correlated with uredinia size and sporulation rate. The pathogen's fitness appeared to be more constrained by the constitutive plant defense level than limited by nutrient availability, as evident in the decrease in sporulation.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Maupetit</LastName><ForeName>Agathe</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Larbat</LastName><ForeName>Romain</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, LAE, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pernaci</LastName><ForeName>Michaël</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Andrieux</LastName><ForeName>Axelle</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guinet</LastName><ForeName>Cécile</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>ANSES, Laboratoire de la Santé des Végétaux, Unité de Mycologie, Malzéville, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Boutigny</LastName><ForeName>Anne-Laure</ForeName><Initials>AL</Initials><AffiliationInfo><Affiliation>ANSES, Laboratoire de la Santé des Végétaux, Unité de Mycologie, Malzéville, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fabre</LastName><ForeName>Bénédicte</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Frey</LastName><ForeName>Pascal</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Halkett</LastName><ForeName>Fabien</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Université de Lorraine, INRA, IAM, Nancy, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>09</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">aggressiveness traits</Keyword><Keyword MajorTopicYN="N">constitutive defense</Keyword><Keyword MajorTopicYN="N">nutrient availability</Keyword><Keyword MajorTopicYN="N">plasticity</Keyword><Keyword MajorTopicYN="N">rust fungus</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>04</Month><Day>20</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>09</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>10</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>10</Month><Day>17</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>10</Month><Day>17</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30323821</ArticleId><ArticleId IdType="doi">10.3389/fpls.2018.01396</ArticleId><ArticleId 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sortKey="Andrieux, Axelle" sort="Andrieux, Axelle" uniqKey="Andrieux A" first="Axelle" last="Andrieux">Axelle Andrieux</name><name sortKey="Boutigny, Anne Laure" sort="Boutigny, Anne Laure" uniqKey="Boutigny A" first="Anne-Laure" last="Boutigny">Anne-Laure Boutigny</name><name sortKey="Fabre, Benedicte" sort="Fabre, Benedicte" uniqKey="Fabre B" first="Bénédicte" last="Fabre">Bénédicte Fabre</name><name sortKey="Frey, Pascal" sort="Frey, Pascal" uniqKey="Frey P" first="Pascal" last="Frey">Pascal Frey</name><name sortKey="Guinet, Cecile" sort="Guinet, Cecile" uniqKey="Guinet C" first="Cécile" last="Guinet">Cécile Guinet</name><name sortKey="Halkett, Fabien" sort="Halkett, Fabien" uniqKey="Halkett F" first="Fabien" last="Halkett">Fabien Halkett</name><name sortKey="Larbat, Romain" sort="Larbat, Romain" uniqKey="Larbat R" first="Romain" last="Larbat">Romain Larbat</name><name sortKey="Pernaci, Michael" sort="Pernaci, Michael" uniqKey="Pernaci M" first="Michaël" last="Pernaci">Michaël 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