Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae

The phytopathogenic fungus Fusarium mangiferae belongs to the Fusarium fujikuroi species complex (FFSC). Members of this group cause a wide spectrum of devastating diseases on diverse agricultural crops. F. mangiferae is the causal agent of the mango malformation disease (MMD) and as such detrimenta...

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Main Authors: Anna K. Atanasoff-Kardjalieff, Friederike Lünne, Svetlana Kalinina, Joseph Strauss, Hans-Ulrich Humpf, Lena Studt
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-07-01
Series:Frontiers in Fungal Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/ffunb.2021.671796/full
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author Anna K. Atanasoff-Kardjalieff
Friederike Lünne
Svetlana Kalinina
Joseph Strauss
Hans-Ulrich Humpf
Lena Studt
author_facet Anna K. Atanasoff-Kardjalieff
Friederike Lünne
Svetlana Kalinina
Joseph Strauss
Hans-Ulrich Humpf
Lena Studt
author_sort Anna K. Atanasoff-Kardjalieff
collection DOAJ
description The phytopathogenic fungus Fusarium mangiferae belongs to the Fusarium fujikuroi species complex (FFSC). Members of this group cause a wide spectrum of devastating diseases on diverse agricultural crops. F. mangiferae is the causal agent of the mango malformation disease (MMD) and as such detrimental for agriculture in the southern hemisphere. During plant infection, the fungus produces a plethora of bioactive secondary metabolites (SMs), which most often lead to severe adverse defects on plants health. Changes in chromatin structure achieved by posttranslational modifications (PTM) of histones play a key role in regulation of fungal SM biosynthesis. Posttranslational tri-methylation of histone 3 lysine 9 (H3K9me3) is considered a hallmark of heterochromatin and established by the SET-domain protein Kmt1. Here, we show that FmKmt1 is involved in H3K9me3 in F. mangiferae. Loss of FmKmt1 only slightly though significantly affected fungal hyphal growth and stress response and is required for wild type-like conidiation. While FmKmt1 is largely dispensable for the biosynthesis of most known SMs, removal of FmKMT1 resulted in an almost complete loss of fusapyrone and deoxyfusapyrone, γ-pyrones previously only known from Fusarium semitectum. Here, we identified the polyketide synthase (PKS) FmPKS40 to be involved in fusapyrone biosynthesis, delineate putative cluster borders by co-expression studies and provide insights into its regulation.
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spelling doaj.art-0530079806f145c091331f1990251f822022-12-21T18:44:11ZengFrontiers Media S.A.Frontiers in Fungal Biology2673-61282021-07-01210.3389/ffunb.2021.671796671796Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferaeAnna K. Atanasoff-Kardjalieff0Friederike Lünne1Svetlana Kalinina2Joseph Strauss3Hans-Ulrich Humpf4Lena Studt5Department of Applied Genetics and Cell Biology, Institute of Microbial Genetics, University of Natural Resources and Life Sciences, Vienna (BOKU), Tulln an der Donau, AustriaInstitute of Food Chemistry, Westfälische Wilhelms-Universität, Münster, GermanyInstitute of Food Chemistry, Westfälische Wilhelms-Universität, Münster, GermanyDepartment of Applied Genetics and Cell Biology, Institute of Microbial Genetics, University of Natural Resources and Life Sciences, Vienna (BOKU), Tulln an der Donau, AustriaInstitute of Food Chemistry, Westfälische Wilhelms-Universität, Münster, GermanyDepartment of Applied Genetics and Cell Biology, Institute of Microbial Genetics, University of Natural Resources and Life Sciences, Vienna (BOKU), Tulln an der Donau, AustriaThe phytopathogenic fungus Fusarium mangiferae belongs to the Fusarium fujikuroi species complex (FFSC). Members of this group cause a wide spectrum of devastating diseases on diverse agricultural crops. F. mangiferae is the causal agent of the mango malformation disease (MMD) and as such detrimental for agriculture in the southern hemisphere. During plant infection, the fungus produces a plethora of bioactive secondary metabolites (SMs), which most often lead to severe adverse defects on plants health. Changes in chromatin structure achieved by posttranslational modifications (PTM) of histones play a key role in regulation of fungal SM biosynthesis. Posttranslational tri-methylation of histone 3 lysine 9 (H3K9me3) is considered a hallmark of heterochromatin and established by the SET-domain protein Kmt1. Here, we show that FmKmt1 is involved in H3K9me3 in F. mangiferae. Loss of FmKmt1 only slightly though significantly affected fungal hyphal growth and stress response and is required for wild type-like conidiation. While FmKmt1 is largely dispensable for the biosynthesis of most known SMs, removal of FmKMT1 resulted in an almost complete loss of fusapyrone and deoxyfusapyrone, γ-pyrones previously only known from Fusarium semitectum. Here, we identified the polyketide synthase (PKS) FmPKS40 to be involved in fusapyrone biosynthesis, delineate putative cluster borders by co-expression studies and provide insights into its regulation.https://www.frontiersin.org/articles/10.3389/ffunb.2021.671796/fullheterochromatinhistone PTMsFusarium mangiferaeFusarium fujikuroi species complexH3K9me3secondary metabolism
spellingShingle Anna K. Atanasoff-Kardjalieff
Friederike Lünne
Svetlana Kalinina
Joseph Strauss
Hans-Ulrich Humpf
Lena Studt
Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae
Frontiers in Fungal Biology
heterochromatin
histone PTMs
Fusarium mangiferae
Fusarium fujikuroi species complex
H3K9me3
secondary metabolism
title Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae
title_full Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae
title_fullStr Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae
title_full_unstemmed Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae
title_short Biosynthesis of Fusapyrone Depends on the H3K9 Methyltransferase, FmKmt1, in Fusarium mangiferae
title_sort biosynthesis of fusapyrone depends on the h3k9 methyltransferase fmkmt1 in fusarium mangiferae
topic heterochromatin
histone PTMs
Fusarium mangiferae
Fusarium fujikuroi species complex
H3K9me3
secondary metabolism
url https://www.frontiersin.org/articles/10.3389/ffunb.2021.671796/full
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