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Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in Magnaporthe oryzae.

Identifieur interne : 000332 ( Main/Exploration ); précédent : 000331; suivant : 000333

Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in Magnaporthe oryzae.

Auteurs : Ziyi Yin [République populaire de Chine] ; Chen Chen [République populaire de Chine] ; Jie Yang [République populaire de Chine] ; Wanzhen Feng [République populaire de Chine] ; Xinyu Liu [République populaire de Chine] ; Rongfang Zuo [République populaire de Chine] ; Jingzhen Wang [République populaire de Chine] ; Lina Yang [République populaire de Chine] ; Kaili Zhong [République populaire de Chine] ; Chuyun Gao [République populaire de Chine] ; Haifeng Zhang [République populaire de Chine] ; Xiaobo Zheng [République populaire de Chine] ; Ping Wang [États-Unis] ; Zhengguang Zhang [République populaire de Chine]

Source :

RBID : pubmed:30776962

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English descriptors

Abstract

Macroautophagy/autophagy is critical for normal appressorium formation and pathogenicity of the rice blast fungus Magnaporthe oryzae, but the molecular base of autophagy linked to pathogenicity remains elusive in this or other pathogenic fungi. We found that MoHat1, a histone acetyltransferase (HAT) homolog, had a role in the regulation of autophagy through the acetylation of autophagy related proteins MoAtg3 and MoAtg9. We also found that MoHat1 was subject to regulation by the protein kinase MoGsk1 that modulated the translocation of MoHat1 from the nucleus to the cytoplasm with the assistance of MoSsb1, a protein chaperone. The alternation of intracellular location affected MoHat1 in the modification of cytosolic autophagy proteins that maintained normal autophagy. Furthermore, we provided evidence linking acetylation of MoAtg3 and MoAtg9 by MoHat1 to functional appressorium development and pathogenicity. Together with the first report of MoAtg9 being subject to acetylation regulation by MoHat1, our studies depicted how MoHat1 regulated autophagy in conjunction with MoGsk1 and how normal autophagy was linked to appressorium formation and function and pathogenicity of M. oryzae. Abbreviations: A/Ala: alanine; AP: autophagosome; Atg genes/proteins: autophagy-related genes/proteins; BiFC: bimolecular fluorescence complementation; co-IP: co-immunoprecipitation; DAPI: 4', 6-diamidino-2-phenylindole; D/Asp: aspartic acid; GFP: green fluorescent protein; GSK3: glycogen synthase kinase 3; HAT: histone acetyltransferase; Hsp70: heat-shock protein 70; IH: invasive hyphae; K/Lys: lysine; MMS: methyl methanesulfonate; Mo: Magnaporthe oryzae; PAS: phagophore assembly site; PE: phosphatidylethanolamine; PtdIns3K: phosphatidylinositol 3-kinase; R/Arg: arginine; S/Ser: serine; T/Thr: threonine; TOR: target of rapamycin; WT: wild type; YFP: yellow fluorescent protein.

DOI: 10.1080/15548627.2019.1580104
PubMed: 30776962
PubMed Central: PMC6613890


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<name sortKey="Zhong, Kaili" sort="Zhong, Kaili" uniqKey="Zhong K" first="Kaili" last="Zhong">Kaili Zhong</name>
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<name sortKey="Gao, Chuyun" sort="Gao, Chuyun" uniqKey="Gao C" first="Chuyun" last="Gao">Chuyun Gao</name>
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<name sortKey="Zhang, Haifeng" sort="Zhang, Haifeng" uniqKey="Zhang H" first="Haifeng" last="Zhang">Haifeng Zhang</name>
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<name sortKey="Zheng, Xiaobo" sort="Zheng, Xiaobo" uniqKey="Zheng X" first="Xiaobo" last="Zheng">Xiaobo Zheng</name>
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<name sortKey="Wang, Ping" sort="Wang, Ping" uniqKey="Wang P" first="Ping" last="Wang">Ping Wang</name>
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<nlm:affiliation>c Departments of Pediatrics, and Microbiology, Immunology, and Parasitology , Louisiana State University Health Sciences Center , New Orleans , LA , USA.</nlm:affiliation>
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<wicri:regionArea>c Departments of Pediatrics, and Microbiology, Immunology, and Parasitology , Louisiana State University Health Sciences Center , New Orleans , LA </wicri:regionArea>
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<name sortKey="Zhang, Zhengguang" sort="Zhang, Zhengguang" uniqKey="Zhang Z" first="Zhengguang" last="Zhang">Zhengguang Zhang</name>
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<nlm:affiliation>a Department of Plant Pathology, College of Plant Protection , Nanjing Agricultural University , Nanjing , China.</nlm:affiliation>
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<title xml:lang="en">Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in
<i>Magnaporthe oryzae</i>
.</title>
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<name sortKey="Yin, Ziyi" sort="Yin, Ziyi" uniqKey="Yin Z" first="Ziyi" last="Yin">Ziyi Yin</name>
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<name sortKey="Chen, Chen" sort="Chen, Chen" uniqKey="Chen C" first="Chen" last="Chen">Chen Chen</name>
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<name sortKey="Yang, Jie" sort="Yang, Jie" uniqKey="Yang J" first="Jie" last="Yang">Jie Yang</name>
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<name sortKey="Feng, Wanzhen" sort="Feng, Wanzhen" uniqKey="Feng W" first="Wanzhen" last="Feng">Wanzhen Feng</name>
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<name sortKey="Liu, Xinyu" sort="Liu, Xinyu" uniqKey="Liu X" first="Xinyu" last="Liu">Xinyu Liu</name>
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<name sortKey="Zuo, Rongfang" sort="Zuo, Rongfang" uniqKey="Zuo R" first="Rongfang" last="Zuo">Rongfang Zuo</name>
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<name sortKey="Wang, Jingzhen" sort="Wang, Jingzhen" uniqKey="Wang J" first="Jingzhen" last="Wang">Jingzhen Wang</name>
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<nlm:affiliation>a Department of Plant Pathology, College of Plant Protection , Nanjing Agricultural University , Nanjing , China.</nlm:affiliation>
<country xml:lang="fr">République populaire de Chine</country>
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<name sortKey="Zheng, Xiaobo" sort="Zheng, Xiaobo" uniqKey="Zheng X" first="Xiaobo" last="Zheng">Xiaobo Zheng</name>
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<name sortKey="Wang, Ping" sort="Wang, Ping" uniqKey="Wang P" first="Ping" last="Wang">Ping Wang</name>
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<wicri:regionArea>c Departments of Pediatrics, and Microbiology, Immunology, and Parasitology , Louisiana State University Health Sciences Center , New Orleans , LA </wicri:regionArea>
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</placeName>
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<name sortKey="Zhang, Zhengguang" sort="Zhang, Zhengguang" uniqKey="Zhang Z" first="Zhengguang" last="Zhang">Zhengguang Zhang</name>
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<title level="j">Autophagy</title>
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<term>Acetylation (MeSH)</term>
<term>Autophagosomes (metabolism)</term>
<term>Autophagy (genetics)</term>
<term>Autophagy-Related Proteins (chemistry)</term>
<term>Autophagy-Related Proteins (genetics)</term>
<term>Autophagy-Related Proteins (metabolism)</term>
<term>Cell Nucleus (metabolism)</term>
<term>Cytoplasm (enzymology)</term>
<term>Cytoplasm (metabolism)</term>
<term>Gene Expression Regulation, Fungal (MeSH)</term>
<term>Glycogen Synthase Kinases (genetics)</term>
<term>Glycogen Synthase Kinases (metabolism)</term>
<term>Golgi Apparatus (metabolism)</term>
<term>HSP70 Heat-Shock Proteins (metabolism)</term>
<term>Histone Acetyltransferases (chemistry)</term>
<term>Histone Acetyltransferases (genetics)</term>
<term>Histone Acetyltransferases (metabolism)</term>
<term>Hyphae (metabolism)</term>
<term>Magnaporthe (genetics)</term>
<term>Magnaporthe (metabolism)</term>
<term>Magnaporthe (pathogenicity)</term>
<term>Oryza (microbiology)</term>
<term>Phosphorylation (MeSH)</term>
<term>Plant Diseases (microbiology)</term>
<term>Protein Binding (MeSH)</term>
<term>Protein Processing, Post-Translational (genetics)</term>
<term>Signal Transduction (genetics)</term>
<term>Spores, Fungal (genetics)</term>
<term>Spores, Fungal (metabolism)</term>
</keywords>
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<term>Acétylation (MeSH)</term>
<term>Appareil de Golgi (métabolisme)</term>
<term>Autophagie (génétique)</term>
<term>Autophagosomes (métabolisme)</term>
<term>Cytoplasme (enzymologie)</term>
<term>Cytoplasme (métabolisme)</term>
<term>Glycogen Synthase Kinases (génétique)</term>
<term>Glycogen Synthase Kinases (métabolisme)</term>
<term>Histone acetyltransferases (composition chimique)</term>
<term>Histone acetyltransferases (génétique)</term>
<term>Histone acetyltransferases (métabolisme)</term>
<term>Hyphae (métabolisme)</term>
<term>Liaison aux protéines (MeSH)</term>
<term>Magnaporthe (génétique)</term>
<term>Magnaporthe (métabolisme)</term>
<term>Magnaporthe (pathogénicité)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Maturation post-traductionnelle des protéines (génétique)</term>
<term>Noyau de la cellule (métabolisme)</term>
<term>Oryza (microbiologie)</term>
<term>Phosphorylation (MeSH)</term>
<term>Protéines associées à l'autophagie (composition chimique)</term>
<term>Protéines associées à l'autophagie (génétique)</term>
<term>Protéines associées à l'autophagie (métabolisme)</term>
<term>Protéines du choc thermique HSP70 (métabolisme)</term>
<term>Régulation de l'expression des gènes fongiques (MeSH)</term>
<term>Spores fongiques (génétique)</term>
<term>Spores fongiques (métabolisme)</term>
<term>Transduction du signal (génétique)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Autophagy-Related Proteins</term>
<term>Histone Acetyltransferases</term>
</keywords>
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<term>Histone acetyltransferases</term>
<term>Protéines associées à l'autophagie</term>
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<term>Cytoplasme</term>
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<term>Cytoplasm</term>
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<term>Autophagy</term>
<term>Autophagy-Related Proteins</term>
<term>Glycogen Synthase Kinases</term>
<term>Histone Acetyltransferases</term>
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<term>Protein Processing, Post-Translational</term>
<term>Signal Transduction</term>
<term>Spores, Fungal</term>
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<term>Autophagie</term>
<term>Glycogen Synthase Kinases</term>
<term>Histone acetyltransferases</term>
<term>Magnaporthe</term>
<term>Maturation post-traductionnelle des protéines</term>
<term>Protéines associées à l'autophagie</term>
<term>Spores fongiques</term>
<term>Transduction du signal</term>
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<term>Autophagosomes</term>
<term>Autophagy-Related Proteins</term>
<term>Cell Nucleus</term>
<term>Cytoplasm</term>
<term>Glycogen Synthase Kinases</term>
<term>Golgi Apparatus</term>
<term>HSP70 Heat-Shock Proteins</term>
<term>Histone Acetyltransferases</term>
<term>Hyphae</term>
<term>Magnaporthe</term>
<term>Spores, Fungal</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
<term>Oryza</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Oryza</term>
<term>Plant Diseases</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Appareil de Golgi</term>
<term>Autophagosomes</term>
<term>Cytoplasme</term>
<term>Glycogen Synthase Kinases</term>
<term>Histone acetyltransferases</term>
<term>Hyphae</term>
<term>Magnaporthe</term>
<term>Noyau de la cellule</term>
<term>Protéines associées à l'autophagie</term>
<term>Protéines du choc thermique HSP70</term>
<term>Spores fongiques</term>
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<term>Magnaporthe</term>
</keywords>
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<term>Acetylation</term>
<term>Gene Expression Regulation, Fungal</term>
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<term>Protein Binding</term>
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<term>Acétylation</term>
<term>Liaison aux protéines</term>
<term>Phosphorylation</term>
<term>Régulation de l'expression des gènes fongiques</term>
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<front>
<div type="abstract" xml:lang="en">Macroautophagy/autophagy is critical for normal appressorium formation and pathogenicity of the rice blast fungus
<i>Magnaporthe oryzae</i>
, but the molecular base of autophagy linked to pathogenicity remains elusive in this or other pathogenic fungi. We found that MoHat1, a histone acetyltransferase (HAT) homolog, had a role in the regulation of autophagy through the acetylation of autophagy related proteins MoAtg3 and MoAtg9. We also found that MoHat1 was subject to regulation by the protein kinase MoGsk1 that modulated the translocation of MoHat1 from the nucleus to the cytoplasm with the assistance of MoSsb1, a protein chaperone. The alternation of intracellular location affected MoHat1 in the modification of cytosolic autophagy proteins that maintained normal autophagy. Furthermore, we provided evidence linking acetylation of MoAtg3 and MoAtg9 by MoHat1 to functional appressorium development and pathogenicity. Together with the first report of MoAtg9 being subject to acetylation regulation by MoHat1, our studies depicted how MoHat1 regulated autophagy in conjunction with MoGsk1 and how normal autophagy was linked to appressorium formation and function and pathogenicity of
<i>M. oryzae</i>
.
<b>Abbreviations</b>
: A/Ala: alanine; AP: autophagosome; Atg genes/proteins: autophagy-related genes/proteins; BiFC: bimolecular fluorescence complementation; co-IP: co-immunoprecipitation; DAPI: 4', 6-diamidino-2-phenylindole; D/Asp: aspartic acid; GFP: green fluorescent protein; GSK3: glycogen synthase kinase 3; HAT: histone acetyltransferase; Hsp70: heat-shock protein 70; IH: invasive hyphae; K/Lys: lysine; MMS: methyl methanesulfonate; Mo:
<i>Magnaporthe oryzae</i>
; PAS: phagophore assembly site; PE: phosphatidylethanolamine; PtdIns3K: phosphatidylinositol 3-kinase; R/Arg: arginine; S/Ser: serine; T/Thr: threonine; TOR: target of rapamycin; WT: wild type; YFP: yellow fluorescent protein.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">30776962</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>06</Month>
<Day>15</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>06</Month>
<Day>15</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1554-8635</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>15</Volume>
<Issue>7</Issue>
<PubDate>
<Year>2019</Year>
<Month>07</Month>
</PubDate>
</JournalIssue>
<Title>Autophagy</Title>
<ISOAbbreviation>Autophagy</ISOAbbreviation>
</Journal>
<ArticleTitle>Histone acetyltransferase MoHat1 acetylates autophagy-related proteins MoAtg3 and MoAtg9 to orchestrate functional appressorium formation and pathogenicity in
<i>Magnaporthe oryzae</i>
.</ArticleTitle>
<Pagination>
<MedlinePgn>1234-1257</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1080/15548627.2019.1580104</ELocationID>
<Abstract>
<AbstractText>Macroautophagy/autophagy is critical for normal appressorium formation and pathogenicity of the rice blast fungus
<i>Magnaporthe oryzae</i>
, but the molecular base of autophagy linked to pathogenicity remains elusive in this or other pathogenic fungi. We found that MoHat1, a histone acetyltransferase (HAT) homolog, had a role in the regulation of autophagy through the acetylation of autophagy related proteins MoAtg3 and MoAtg9. We also found that MoHat1 was subject to regulation by the protein kinase MoGsk1 that modulated the translocation of MoHat1 from the nucleus to the cytoplasm with the assistance of MoSsb1, a protein chaperone. The alternation of intracellular location affected MoHat1 in the modification of cytosolic autophagy proteins that maintained normal autophagy. Furthermore, we provided evidence linking acetylation of MoAtg3 and MoAtg9 by MoHat1 to functional appressorium development and pathogenicity. Together with the first report of MoAtg9 being subject to acetylation regulation by MoHat1, our studies depicted how MoHat1 regulated autophagy in conjunction with MoGsk1 and how normal autophagy was linked to appressorium formation and function and pathogenicity of
<i>M. oryzae</i>
.
<b>Abbreviations</b>
: A/Ala: alanine; AP: autophagosome; Atg genes/proteins: autophagy-related genes/proteins; BiFC: bimolecular fluorescence complementation; co-IP: co-immunoprecipitation; DAPI: 4', 6-diamidino-2-phenylindole; D/Asp: aspartic acid; GFP: green fluorescent protein; GSK3: glycogen synthase kinase 3; HAT: histone acetyltransferase; Hsp70: heat-shock protein 70; IH: invasive hyphae; K/Lys: lysine; MMS: methyl methanesulfonate; Mo:
<i>Magnaporthe oryzae</i>
; PAS: phagophore assembly site; PE: phosphatidylethanolamine; PtdIns3K: phosphatidylinositol 3-kinase; R/Arg: arginine; S/Ser: serine; T/Thr: threonine; TOR: target of rapamycin; WT: wild type; YFP: yellow fluorescent protein.</AbstractText>
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<AffiliationInfo>
<Affiliation>b Key Laboratory of Integrated Management of Crop Diseases and Pests , Ministry of Education , Nanjing , China.</Affiliation>
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<LastName>Chen</LastName>
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