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Genomes and Transcriptomes of Partners in Plant-Fungal- Interactions between Canola (Brassica napus) and Two Leptosphaeria Species

Identifieur interne : 001C67 ( Ncbi/Merge ); précédent : 001C66; suivant : 001C68

Genomes and Transcriptomes of Partners in Plant-Fungal- Interactions between Canola (Brassica napus) and Two Leptosphaeria Species

Auteurs : Rohan G. T. Lowe [Australie] ; Andrew Cassin [Australie] ; Jonathan Grandaubert [France] ; Bethany L. Clark [Australie] ; Angela P. Van De Wouw [Australie] ; Thierry Rouxel [France] ; Barbara J. Howlett [Australie]

Source :

RBID : PMC:4113356

Descripteurs français

English descriptors

Abstract

Leptosphaeria maculans ‘brassicae’ is a damaging fungal pathogen of canola (Brassica napus), causing lesions on cotyledons and leaves, and cankers on the lower stem. A related species, L. biglobosa ‘canadensis’, colonises cotyledons but causes few stem cankers. We describe the complement of genes encoding carbohydrate-active enzymes (CAZys) and peptidases of these fungi, as well as of four related plant pathogens. We also report dual-organism RNA-seq transcriptomes of these two Leptosphaeria species and B. napus during disease. During the first seven days of infection L. biglobosa ‘canadensis’, a necrotroph, expressed more cell wall degrading genes than L. maculans ‘brassicae’, a hemi-biotroph. L. maculans ‘brassicae’ expressed many genes in the Carbohydrate Binding Module class of CAZy, particularly CBM50 genes, with potential roles in the evasion of basal innate immunity in the host plant. At this time, three avirulence genes were amongst the top 20 most highly upregulated L. maculans ‘brassicae’ genes in planta. The two fungi had a similar number of peptidase genes, and trypsin was transcribed at high levels by both fungi early in infection. L. biglobosa ‘canadensis’ infection activated the jasmonic acid and salicylic acid defence pathways in B. napus, consistent with defence against necrotrophs. L. maculans ‘brassicae’ triggered a high level of expression of isochorismate synthase 1, a reporter for salicylic acid signalling. L. biglobosa ‘canadensis’ infection triggered coordinated shutdown of photosynthesis genes, and a concomitant increase in transcription of cell wall remodelling genes of the host plant. Expression of particular classes of CAZy genes and the triggering of host defence and particular metabolic pathways are consistent with the necrotrophic lifestyle of L. biglobosa ‘canadensis’, and the hemibiotrophic life style of L. maculans ‘brassicae’.


Url:
DOI: 10.1371/journal.pone.0103098
PubMed: 25068644
PubMed Central: 4113356

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PMC:4113356

Le document en format XML

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<term>Ascomycota (genetics)</term>
<term>Brassica napus (genetics)</term>
<term>Brassica napus (microbiology)</term>
<term>Cluster Analysis</term>
<term>Cotyledon (genetics)</term>
<term>Cotyledon (microbiology)</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Gene Expression Regulation, Plant</term>
<term>Genome, Fungal</term>
<term>Genome, Plant</term>
<term>Genomics</term>
<term>Host-Pathogen Interactions (genetics)</term>
<term>Peptide Hydrolases (chemistry)</term>
<term>Peptide Hydrolases (genetics)</term>
<term>Phenotype</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de regroupements</term>
<term>Ascomycota (génétique)</term>
<term>Brassica napus (génétique)</term>
<term>Brassica napus (microbiologie)</term>
<term>Cotylédon (génétique)</term>
<term>Cotylédon (microbiologie)</term>
<term>Génome fongique</term>
<term>Génome végétal</term>
<term>Génomique</term>
<term>Interactions hôte-pathogène (génétique)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Peptide hydrolases ()</term>
<term>Peptide hydrolases (génétique)</term>
<term>Phénotype</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Peptide Hydrolases</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Ascomycota</term>
<term>Brassica napus</term>
<term>Cotyledon</term>
<term>Host-Pathogen Interactions</term>
<term>Peptide Hydrolases</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Ascomycota</term>
<term>Brassica napus</term>
<term>Cotylédon</term>
<term>Interactions hôte-pathogène</term>
<term>Maladies des plantes</term>
<term>Peptide hydrolases</term>
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<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Brassica napus</term>
<term>Cotylédon</term>
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Brassica napus</term>
<term>Cotyledon</term>
<term>Plant Diseases</term>
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<term>Cluster Analysis</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Gene Expression Regulation, Plant</term>
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<term>Genome, Plant</term>
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<term>Phenotype</term>
<term>Transcriptome</term>
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<div type="abstract" xml:lang="en">
<p>
<italic>Leptosphaeria maculans</italic>
‘brassicae’ is a damaging fungal pathogen of canola (
<italic>Brassica napus</italic>
), causing lesions on cotyledons and leaves, and cankers on the lower stem. A related species,
<italic>L. biglobosa</italic>
‘canadensis’, colonises cotyledons but causes few stem cankers. We describe the complement of genes encoding carbohydrate-active enzymes (CAZys) and peptidases of these fungi, as well as of four related plant pathogens. We also report dual-organism RNA-seq transcriptomes of these two
<italic>Leptosphaeria</italic>
species and
<italic>B. napus</italic>
during disease. During the first seven days of infection
<italic>L. biglobosa</italic>
‘canadensis’, a necrotroph, expressed more cell wall degrading genes than
<italic>L. maculans</italic>
‘brassicae’, a hemi-biotroph.
<italic>L. maculans</italic>
‘brassicae’ expressed many genes in the Carbohydrate Binding Module class of CAZy, particularly CBM50 genes, with potential roles in the evasion of basal innate immunity in the host plant. At this time, three avirulence genes were amongst the top 20 most highly upregulated
<italic>L. maculans</italic>
‘brassicae’ genes
<italic>in planta</italic>
. The two fungi had a similar number of peptidase genes, and trypsin was transcribed at high levels by both fungi early in infection.
<italic>L. biglobosa</italic>
‘canadensis’ infection activated the jasmonic acid and salicylic acid defence pathways in
<italic>B. napus</italic>
, consistent with defence against necrotrophs.
<italic>L. maculans</italic>
‘brassicae’ triggered a high level of expression of isochorismate synthase 1, a reporter for salicylic acid signalling.
<italic>L. biglobosa</italic>
‘canadensis’ infection triggered coordinated shutdown of photosynthesis genes, and a concomitant increase in transcription of cell wall remodelling genes of the host plant. Expression of particular classes of CAZy genes and the triggering of host defence and particular metabolic pathways are consistent with the necrotrophic lifestyle of
<italic>L. biglobosa</italic>
‘canadensis’, and the hemibiotrophic life style of
<italic>L. maculans</italic>
‘brassicae’.</p>
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<author>
<name sortKey="Grandaubert, Jonathan" sort="Grandaubert, Jonathan" uniqKey="Grandaubert J" first="Jonathan" last="Grandaubert">Jonathan Grandaubert</name>
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<addr-line>INRA-Bioger, UR1290, Thiverval-Grignon, France</addr-line>
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<name sortKey="Clark, Bethany L" sort="Clark, Bethany L" uniqKey="Clark B" first="Bethany L." last="Clark">Bethany L. Clark</name>
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<author>
<name sortKey="Van De Wouw, Angela P" sort="Van De Wouw, Angela P" uniqKey="Van De Wouw A" first="Angela P." last="Van De Wouw">Angela P. Van De Wouw</name>
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<name sortKey="Rouxel, Thierry" sort="Rouxel, Thierry" uniqKey="Rouxel T" first="Thierry" last="Rouxel">Thierry Rouxel</name>
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<title xml:lang="en" level="a" type="main">Genomes and Transcriptomes of Partners in Plant-Fungal- Interactions between Canola (
<italic>Brassica napus)</italic>
and Two
<italic>Leptosphaeria</italic>
Species</title>
<author>
<name sortKey="Lowe, Rohan G T" sort="Lowe, Rohan G T" uniqKey="Lowe R" first="Rohan G. T." last="Lowe">Rohan G. T. Lowe</name>
<affiliation wicri:level="4">
<nlm:aff id="aff1">
<addr-line>School of Botany, The University of Melbourne, Parkville, Victoria, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Cassin, Andrew" sort="Cassin, Andrew" uniqKey="Cassin A" first="Andrew" last="Cassin">Andrew Cassin</name>
<affiliation wicri:level="4">
<nlm:aff id="aff2">
<addr-line>ARC Centre of Excellence in Plant Cell Walls, School of Botany, The University of Melbourne, Parkville, Victoria, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>ARC Centre of Excellence in Plant Cell Walls, School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Grandaubert, Jonathan" sort="Grandaubert, Jonathan" uniqKey="Grandaubert J" first="Jonathan" last="Grandaubert">Jonathan Grandaubert</name>
<affiliation wicri:level="1">
<nlm:aff id="aff3">
<addr-line>INRA-Bioger, UR1290, Thiverval-Grignon, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA-Bioger, UR1290, Thiverval-Grignon</wicri:regionArea>
<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Clark, Bethany L" sort="Clark, Bethany L" uniqKey="Clark B" first="Bethany L." last="Clark">Bethany L. Clark</name>
<affiliation wicri:level="4">
<nlm:aff id="aff1">
<addr-line>School of Botany, The University of Melbourne, Parkville, Victoria, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Van De Wouw, Angela P" sort="Van De Wouw, Angela P" uniqKey="Van De Wouw A" first="Angela P." last="Van De Wouw">Angela P. Van De Wouw</name>
<affiliation wicri:level="4">
<nlm:aff id="aff1">
<addr-line>School of Botany, The University of Melbourne, Parkville, Victoria, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Rouxel, Thierry" sort="Rouxel, Thierry" uniqKey="Rouxel T" first="Thierry" last="Rouxel">Thierry Rouxel</name>
<affiliation wicri:level="1">
<nlm:aff id="aff3">
<addr-line>INRA-Bioger, UR1290, Thiverval-Grignon, France</addr-line>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA-Bioger, UR1290, Thiverval-Grignon</wicri:regionArea>
<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Howlett, Barbara J" sort="Howlett, Barbara J" uniqKey="Howlett B" first="Barbara J." last="Howlett">Barbara J. Howlett</name>
<affiliation wicri:level="4">
<nlm:aff id="aff1">
<addr-line>School of Botany, The University of Melbourne, Parkville, Victoria, Australia</addr-line>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint>
<date when="2014">2014</date>
</imprint>
</series>
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<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>
<italic>Leptosphaeria maculans</italic>
‘brassicae’ is a damaging fungal pathogen of canola (
<italic>Brassica napus</italic>
), causing lesions on cotyledons and leaves, and cankers on the lower stem. A related species,
<italic>L. biglobosa</italic>
‘canadensis’, colonises cotyledons but causes few stem cankers. We describe the complement of genes encoding carbohydrate-active enzymes (CAZys) and peptidases of these fungi, as well as of four related plant pathogens. We also report dual-organism RNA-seq transcriptomes of these two
<italic>Leptosphaeria</italic>
species and
<italic>B. napus</italic>
during disease. During the first seven days of infection
<italic>L. biglobosa</italic>
‘canadensis’, a necrotroph, expressed more cell wall degrading genes than
<italic>L. maculans</italic>
‘brassicae’, a hemi-biotroph.
<italic>L. maculans</italic>
‘brassicae’ expressed many genes in the Carbohydrate Binding Module class of CAZy, particularly CBM50 genes, with potential roles in the evasion of basal innate immunity in the host plant. At this time, three avirulence genes were amongst the top 20 most highly upregulated
<italic>L. maculans</italic>
‘brassicae’ genes
<italic>in planta</italic>
. The two fungi had a similar number of peptidase genes, and trypsin was transcribed at high levels by both fungi early in infection.
<italic>L. biglobosa</italic>
‘canadensis’ infection activated the jasmonic acid and salicylic acid defence pathways in
<italic>B. napus</italic>
, consistent with defence against necrotrophs.
<italic>L. maculans</italic>
‘brassicae’ triggered a high level of expression of isochorismate synthase 1, a reporter for salicylic acid signalling.
<italic>L. biglobosa</italic>
‘canadensis’ infection triggered coordinated shutdown of photosynthesis genes, and a concomitant increase in transcription of cell wall remodelling genes of the host plant. Expression of particular classes of CAZy genes and the triggering of host defence and particular metabolic pathways are consistent with the necrotrophic lifestyle of
<italic>L. biglobosa</italic>
‘canadensis’, and the hemibiotrophic life style of
<italic>L. maculans</italic>
‘brassicae’.</p>
</div>
</front>
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</affiliation>
</author>
<author>
<name sortKey="Van De Wouw, Angela P" sort="Van De Wouw, Angela P" uniqKey="Van De Wouw A" first="Angela P" last="Van De Wouw">Angela P. Van De Wouw</name>
<affiliation wicri:level="4">
<nlm:affiliation>School of Botany, The University of Melbourne, Parkville, Victoria, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Rouxel, Thierry" sort="Rouxel, Thierry" uniqKey="Rouxel T" first="Thierry" last="Rouxel">Thierry Rouxel</name>
<affiliation wicri:level="1">
<nlm:affiliation>INRA-Bioger, UR1290, Thiverval-Grignon, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA-Bioger, UR1290, Thiverval-Grignon</wicri:regionArea>
<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Howlett, Barbara J" sort="Howlett, Barbara J" uniqKey="Howlett B" first="Barbara J" last="Howlett">Barbara J. Howlett</name>
<affiliation wicri:level="4">
<nlm:affiliation>School of Botany, The University of Melbourne, Parkville, Victoria, Australia.</nlm:affiliation>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>School of Botany, The University of Melbourne, Parkville, Victoria</wicri:regionArea>
<orgName type="university">Université de Melbourne</orgName>
<placeName>
<settlement type="city">Melbourne</settlement>
<region type="état">Victoria (État)</region>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">PloS one</title>
<idno type="eISSN">1932-6203</idno>
<imprint>
<date when="2014" type="published">2014</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Ascomycota (genetics)</term>
<term>Brassica napus (genetics)</term>
<term>Brassica napus (microbiology)</term>
<term>Cluster Analysis</term>
<term>Cotyledon (genetics)</term>
<term>Cotyledon (microbiology)</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Gene Expression Regulation, Plant</term>
<term>Genome, Fungal</term>
<term>Genome, Plant</term>
<term>Genomics</term>
<term>Host-Pathogen Interactions (genetics)</term>
<term>Peptide Hydrolases (chemistry)</term>
<term>Peptide Hydrolases (genetics)</term>
<term>Phenotype</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de regroupements</term>
<term>Ascomycota (génétique)</term>
<term>Brassica napus (génétique)</term>
<term>Brassica napus (microbiologie)</term>
<term>Cotylédon (génétique)</term>
<term>Cotylédon (microbiologie)</term>
<term>Génome fongique</term>
<term>Génome végétal</term>
<term>Génomique</term>
<term>Interactions hôte-pathogène (génétique)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Peptide hydrolases ()</term>
<term>Peptide hydrolases (génétique)</term>
<term>Phénotype</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Peptide Hydrolases</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Ascomycota</term>
<term>Brassica napus</term>
<term>Cotyledon</term>
<term>Host-Pathogen Interactions</term>
<term>Peptide Hydrolases</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Ascomycota</term>
<term>Brassica napus</term>
<term>Cotylédon</term>
<term>Interactions hôte-pathogène</term>
<term>Maladies des plantes</term>
<term>Peptide hydrolases</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Brassica napus</term>
<term>Cotylédon</term>
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Brassica napus</term>
<term>Cotyledon</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Cluster Analysis</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Gene Expression Regulation, Plant</term>
<term>Genome, Fungal</term>
<term>Genome, Plant</term>
<term>Genomics</term>
<term>Phenotype</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de regroupements</term>
<term>Génome fongique</term>
<term>Génome végétal</term>
<term>Génomique</term>
<term>Peptide hydrolases</term>
<term>Phénotype</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Transcriptome</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Leptosphaeria maculans 'brassicae' is a damaging fungal pathogen of canola (Brassica napus), causing lesions on cotyledons and leaves, and cankers on the lower stem. A related species, L. biglobosa 'canadensis', colonises cotyledons but causes few stem cankers. We describe the complement of genes encoding carbohydrate-active enzymes (CAZys) and peptidases of these fungi, as well as of four related plant pathogens. We also report dual-organism RNA-seq transcriptomes of these two Leptosphaeria species and B. napus during disease. During the first seven days of infection L. biglobosa 'canadensis', a necrotroph, expressed more cell wall degrading genes than L. maculans 'brassicae', a hemi-biotroph. L. maculans 'brassicae' expressed many genes in the Carbohydrate Binding Module class of CAZy, particularly CBM50 genes, with potential roles in the evasion of basal innate immunity in the host plant. At this time, three avirulence genes were amongst the top 20 most highly upregulated L. maculans 'brassicae' genes in planta. The two fungi had a similar number of peptidase genes, and trypsin was transcribed at high levels by both fungi early in infection. L. biglobosa 'canadensis' infection activated the jasmonic acid and salicylic acid defence pathways in B. napus, consistent with defence against necrotrophs. L. maculans 'brassicae' triggered a high level of expression of isochorismate synthase 1, a reporter for salicylic acid signalling. L. biglobosa 'canadensis' infection triggered coordinated shutdown of photosynthesis genes, and a concomitant increase in transcription of cell wall remodelling genes of the host plant. Expression of particular classes of CAZy genes and the triggering of host defence and particular metabolic pathways are consistent with the necrotrophic lifestyle of L. biglobosa 'canadensis', and the hemibiotrophic life style of L. maculans 'brassicae'.</div>
</front>
</TEI>
</pubmed>
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