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Genome-Wide Annotation and Comparative Analysis of Cytochrome P450 Monooxygenases in Basidiomycete Biotrophic Plant Pathogens

Identifieur interne : 000639 ( Ncbi/Merge ); précédent : 000638; suivant : 000640

Genome-Wide Annotation and Comparative Analysis of Cytochrome P450 Monooxygenases in Basidiomycete Biotrophic Plant Pathogens

Auteurs : Lehlohonolo Benedict Qhanya [Afrique du Sud] ; Godfrey Matowane [Afrique du Sud] ; Wanping Chen [République populaire de Chine] ; Yuxin Sun [République populaire de Chine] ; Elizabeth Mpholoseng Letsimo [Afrique du Sud] ; Mohammad Parvez [Afrique du Sud] ; Jae-Hyuk Yu [États-Unis] ; Samson Sitheni Mashele [Afrique du Sud] ; Khajamohiddin Syed [Afrique du Sud]

Source :

RBID : PMC:4633277

Descripteurs français

English descriptors

Abstract

Fungi are an exceptional source of diverse and novel cytochrome P450 monooxygenases (P450s), heme-thiolate proteins, with catalytic versatility. Agaricomycotina saprophytes have yielded most of the available information on basidiomycete P450s. This resulted in observing similar P450 family types in basidiomycetes with few differences in P450 families among Agaricomycotina saprophytes. The present study demonstrated the presence of unique P450 family patterns in basidiomycete biotrophic plant pathogens that could possibly have originated from the adaptation of these species to different ecological niches (host influence). Systematic analysis of P450s in basidiomycete biotrophic plant pathogens belonging to three different orders, Agaricomycotina (Armillaria mellea), Pucciniomycotina (Melampsora laricis-populina, M. lini, Mixia osmundae and Puccinia graminis) and Ustilaginomycotina (Ustilago maydis, Sporisorium reilianum and Tilletiaria anomala), revealed the presence of numerous putative P450s ranging from 267 (A. mellea) to 14 (M. osmundae). Analysis of P450 families revealed the presence of 41 new P450 families and 27 new P450 subfamilies in these biotrophic plant pathogens. Order-level comparison of P450 families between biotrophic plant pathogens revealed the presence of unique P450 family patterns in these organisms, possibly reflecting the characteristics of their order. Further comparison of P450 families with basidiomycete non-pathogens confirmed that biotrophic plant pathogens harbour the unique P450 families in their genomes. The CYP63, CYP5037, CYP5136, CYP5137 and CYP5341 P450 families were expanded in A. mellea when compared to other Agaricomycotina saprophytes and the CYP5221 and CYP5233 P450 families in P. graminis and M. laricis-populina. The present study revealed that expansion of these P450 families is due to paralogous evolution of member P450s. The presence of unique P450 families in these organisms serves as evidence of how a host/ecological niche can influence shaping the P450 content of an organism. The present study initiates our understanding of P450 family patterns in basidiomycete biotrophic plant pathogens.


Url:
DOI: 10.1371/journal.pone.0142100
PubMed: 26536121
PubMed Central: 4633277

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PMC:4633277

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<term>Basidiomycota (classification)</term>
<term>Basidiomycota (enzymology)</term>
<term>Basidiomycota (genetics)</term>
<term>Cytochrome P-450 Enzyme System (genetics)</term>
<term>Cytochrome P-450 Enzyme System (metabolism)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Fungal Proteins (genetics)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Genome, Fungal (MeSH)</term>
<term>Genomics (methods)</term>
<term>Molecular Sequence Annotation (MeSH)</term>
<term>Multigene Family (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Annotation de séquence moléculaire (MeSH)</term>
<term>Basidiomycota (classification)</term>
<term>Basidiomycota (enzymologie)</term>
<term>Basidiomycota (génétique)</term>
<term>Cytochrome P-450 enzyme system (génétique)</term>
<term>Cytochrome P-450 enzyme system (métabolisme)</term>
<term>Famille multigénique (MeSH)</term>
<term>Génome fongique (MeSH)</term>
<term>Génomique (méthodes)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Phylogenèse (MeSH)</term>
<term>Protéines fongiques (génétique)</term>
<term>Protéines fongiques (métabolisme)</term>
<term>Évolution moléculaire (MeSH)</term>
</keywords>
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<term>Cytochrome P-450 Enzyme System</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="en">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Basidiomycota</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Basidiomycota</term>
<term>Cytochrome P-450 enzyme system</term>
<term>Maladies des plantes</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Cytochrome P-450 Enzyme System</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="methods" xml:lang="en">
<term>Genomics</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Cytochrome P-450 enzyme system</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" qualifier="méthodes" xml:lang="fr">
<term>Génomique</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Evolution, Molecular</term>
<term>Genome, Fungal</term>
<term>Molecular Sequence Annotation</term>
<term>Multigene Family</term>
<term>Phylogeny</term>
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<term>Annotation de séquence moléculaire</term>
<term>Famille multigénique</term>
<term>Génome fongique</term>
<term>Phylogenèse</term>
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<div type="abstract" xml:lang="en">
<p>Fungi are an exceptional source of diverse and novel cytochrome P450 monooxygenases (P450s), heme-thiolate proteins, with catalytic versatility. Agaricomycotina saprophytes have yielded most of the available information on basidiomycete P450s. This resulted in observing similar P450 family types in basidiomycetes with few differences in P450 families among Agaricomycotina saprophytes. The present study demonstrated the presence of unique P450 family patterns in basidiomycete biotrophic plant pathogens that could possibly have originated from the adaptation of these species to different ecological niches (host influence). Systematic analysis of P450s in basidiomycete biotrophic plant pathogens belonging to three different orders, Agaricomycotina (
<italic>Armillaria mellea</italic>
), Pucciniomycotina (
<italic>Melampsora laricis-populina</italic>
,
<italic>M</italic>
.
<italic>lini</italic>
,
<italic>Mixia osmundae</italic>
and
<italic>Puccinia graminis</italic>
) and Ustilaginomycotina (
<italic>Ustilago maydis</italic>
,
<italic>Sporisorium reilianum</italic>
and
<italic>Tilletiaria anomala</italic>
), revealed the presence of numerous putative P450s ranging from 267 (
<italic>A</italic>
.
<italic>mellea)</italic>
to 14 (
<italic>M</italic>
.
<italic>osmundae</italic>
). Analysis of P450 families revealed the presence of 41 new P450 families and 27 new P450 subfamilies in these biotrophic plant pathogens. Order-level comparison of P450 families between biotrophic plant pathogens revealed the presence of unique P450 family patterns in these organisms, possibly reflecting the characteristics of their order. Further comparison of P450 families with basidiomycete non-pathogens confirmed that biotrophic plant pathogens harbour the unique P450 families in their genomes. The CYP63, CYP5037, CYP5136, CYP5137 and CYP5341 P450 families were expanded in
<italic>A</italic>
.
<italic>mellea</italic>
when compared to other Agaricomycotina saprophytes and the CYP5221 and CYP5233 P450 families in
<italic>P</italic>
.
<italic>graminis</italic>
and
<italic>M</italic>
.
<italic>laricis-populina</italic>
. The present study revealed that expansion of these P450 families is due to paralogous evolution of member P450s. The presence of unique P450 families in these organisms serves as evidence of how a host/ecological niche can influence shaping the P450 content of an organism. The present study initiates our understanding of P450 family patterns in basidiomycete biotrophic plant pathogens.</p>
</div>
</front>
<back>
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<name sortKey="Yamazaki, H" uniqKey="Yamazaki H">H Yamazaki</name>
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<title level="j">PLoS ONE</title>
<idno type="eISSN">1932-6203</idno>
<imprint>
<date when="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
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<profileDesc>
<textClass></textClass>
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</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>Fungi are an exceptional source of diverse and novel cytochrome P450 monooxygenases (P450s), heme-thiolate proteins, with catalytic versatility. Agaricomycotina saprophytes have yielded most of the available information on basidiomycete P450s. This resulted in observing similar P450 family types in basidiomycetes with few differences in P450 families among Agaricomycotina saprophytes. The present study demonstrated the presence of unique P450 family patterns in basidiomycete biotrophic plant pathogens that could possibly have originated from the adaptation of these species to different ecological niches (host influence). Systematic analysis of P450s in basidiomycete biotrophic plant pathogens belonging to three different orders, Agaricomycotina (
<italic>Armillaria mellea</italic>
), Pucciniomycotina (
<italic>Melampsora laricis-populina</italic>
,
<italic>M</italic>
.
<italic>lini</italic>
,
<italic>Mixia osmundae</italic>
and
<italic>Puccinia graminis</italic>
) and Ustilaginomycotina (
<italic>Ustilago maydis</italic>
,
<italic>Sporisorium reilianum</italic>
and
<italic>Tilletiaria anomala</italic>
), revealed the presence of numerous putative P450s ranging from 267 (
<italic>A</italic>
.
<italic>mellea)</italic>
to 14 (
<italic>M</italic>
.
<italic>osmundae</italic>
). Analysis of P450 families revealed the presence of 41 new P450 families and 27 new P450 subfamilies in these biotrophic plant pathogens. Order-level comparison of P450 families between biotrophic plant pathogens revealed the presence of unique P450 family patterns in these organisms, possibly reflecting the characteristics of their order. Further comparison of P450 families with basidiomycete non-pathogens confirmed that biotrophic plant pathogens harbour the unique P450 families in their genomes. The CYP63, CYP5037, CYP5136, CYP5137 and CYP5341 P450 families were expanded in
<italic>A</italic>
.
<italic>mellea</italic>
when compared to other Agaricomycotina saprophytes and the CYP5221 and CYP5233 P450 families in
<italic>P</italic>
.
<italic>graminis</italic>
and
<italic>M</italic>
.
<italic>laricis-populina</italic>
. The present study revealed that expansion of these P450 families is due to paralogous evolution of member P450s. The presence of unique P450 families in these organisms serves as evidence of how a host/ecological niche can influence shaping the P450 content of an organism. The present study initiates our understanding of P450 family patterns in basidiomycete biotrophic plant pathogens.</p>
</div>
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</author>
<author>
<name sortKey="Yu, Jae Hyuk" sort="Yu, Jae Hyuk" uniqKey="Yu J" first="Jae-Hyuk" last="Yu">Jae-Hyuk Yu</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Bacteriology, University of Wisconsin-Madison, 3155 MSB, 1550 Linden Drive, Madison, WI, 53706, United States of America.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Bacteriology, University of Wisconsin-Madison, 3155 MSB, 1550 Linden Drive, Madison, WI, 53706</wicri:regionArea>
<wicri:noRegion>53706</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Mashele, Samson Sitheni" sort="Mashele, Samson Sitheni" uniqKey="Mashele S" first="Samson Sitheni" last="Mashele">Samson Sitheni Mashele</name>
<affiliation wicri:level="1">
<nlm:affiliation>Unit for Drug Discovery Research, Department of Health Sciences, Faculty of Health and Environmental Sciences, Central University of Technology, Bloemfontein 9300, Free State, South Africa.</nlm:affiliation>
<country xml:lang="fr">Afrique du Sud</country>
<wicri:regionArea>Unit for Drug Discovery Research, Department of Health Sciences, Faculty of Health and Environmental Sciences, Central University of Technology, Bloemfontein 9300, Free State</wicri:regionArea>
<wicri:noRegion>Free State</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Syed, Khajamohiddin" sort="Syed, Khajamohiddin" uniqKey="Syed K" first="Khajamohiddin" last="Syed">Khajamohiddin Syed</name>
<affiliation wicri:level="1">
<nlm:affiliation>Unit for Drug Discovery Research, Department of Health Sciences, Faculty of Health and Environmental Sciences, Central University of Technology, Bloemfontein 9300, Free State, South Africa.</nlm:affiliation>
<country xml:lang="fr">Afrique du Sud</country>
<wicri:regionArea>Unit for Drug Discovery Research, Department of Health Sciences, Faculty of Health and Environmental Sciences, Central University of Technology, Bloemfontein 9300, Free State</wicri:regionArea>
<wicri:noRegion>Free State</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j">PloS one</title>
<idno type="eISSN">1932-6203</idno>
<imprint>
<date when="2015" type="published">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="KwdEn" xml:lang="en">
<term>Basidiomycota (classification)</term>
<term>Basidiomycota (enzymology)</term>
<term>Basidiomycota (genetics)</term>
<term>Cytochrome P-450 Enzyme System (genetics)</term>
<term>Cytochrome P-450 Enzyme System (metabolism)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Fungal Proteins (genetics)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Genome, Fungal (MeSH)</term>
<term>Genomics (methods)</term>
<term>Molecular Sequence Annotation (MeSH)</term>
<term>Multigene Family (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Annotation de séquence moléculaire (MeSH)</term>
<term>Basidiomycota (classification)</term>
<term>Basidiomycota (enzymologie)</term>
<term>Basidiomycota (génétique)</term>
<term>Cytochrome P-450 enzyme system (génétique)</term>
<term>Cytochrome P-450 enzyme system (métabolisme)</term>
<term>Famille multigénique (MeSH)</term>
<term>Génome fongique (MeSH)</term>
<term>Génomique (méthodes)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Phylogenèse (MeSH)</term>
<term>Protéines fongiques (génétique)</term>
<term>Protéines fongiques (métabolisme)</term>
<term>Évolution moléculaire (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Cytochrome P-450 Enzyme System</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="en">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Basidiomycota</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Basidiomycota</term>
<term>Cytochrome P-450 enzyme system</term>
<term>Maladies des plantes</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Cytochrome P-450 Enzyme System</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="methods" xml:lang="en">
<term>Genomics</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Cytochrome P-450 enzyme system</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" qualifier="méthodes" xml:lang="fr">
<term>Génomique</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Evolution, Molecular</term>
<term>Genome, Fungal</term>
<term>Molecular Sequence Annotation</term>
<term>Multigene Family</term>
<term>Phylogeny</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Annotation de séquence moléculaire</term>
<term>Famille multigénique</term>
<term>Génome fongique</term>
<term>Phylogenèse</term>
<term>Évolution moléculaire</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Fungi are an exceptional source of diverse and novel cytochrome P450 monooxygenases (P450s), heme-thiolate proteins, with catalytic versatility. Agaricomycotina saprophytes have yielded most of the available information on basidiomycete P450s. This resulted in observing similar P450 family types in basidiomycetes with few differences in P450 families among Agaricomycotina saprophytes. The present study demonstrated the presence of unique P450 family patterns in basidiomycete biotrophic plant pathogens that could possibly have originated from the adaptation of these species to different ecological niches (host influence). Systematic analysis of P450s in basidiomycete biotrophic plant pathogens belonging to three different orders, Agaricomycotina (Armillaria mellea), Pucciniomycotina (Melampsora laricis-populina, M. lini, Mixia osmundae and Puccinia graminis) and Ustilaginomycotina (Ustilago maydis, Sporisorium reilianum and Tilletiaria anomala), revealed the presence of numerous putative P450s ranging from 267 (A. mellea) to 14 (M. osmundae). Analysis of P450 families revealed the presence of 41 new P450 families and 27 new P450 subfamilies in these biotrophic plant pathogens. Order-level comparison of P450 families between biotrophic plant pathogens revealed the presence of unique P450 family patterns in these organisms, possibly reflecting the characteristics of their order. Further comparison of P450 families with basidiomycete non-pathogens confirmed that biotrophic plant pathogens harbour the unique P450 families in their genomes. The CYP63, CYP5037, CYP5136, CYP5137 and CYP5341 P450 families were expanded in A. mellea when compared to other Agaricomycotina saprophytes and the CYP5221 and CYP5233 P450 families in P. graminis and M. laricis-populina. The present study revealed that expansion of these P450 families is due to paralogous evolution of member P450s. The presence of unique P450 families in these organisms serves as evidence of how a host/ecological niche can influence shaping the P450 content of an organism. The present study initiates our understanding of P450 family patterns in basidiomycete biotrophic plant pathogens.</div>
</front>
</TEI>
</pubmed>
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