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Mycelial development preceding basidioma formation in Moniliophthora perniciosa is associated to chitin, sugar and nutrient metabolism alterations involving autophagy.

Identifieur interne : 000A61 ( Main/Exploration ); précédent : 000A60; suivant : 000A62

Mycelial development preceding basidioma formation in Moniliophthora perniciosa is associated to chitin, sugar and nutrient metabolism alterations involving autophagy.

Auteurs : Dayane Santos Gomes [Brésil] ; Maíza Alves Lopes [Brésil] ; Sara Pereira Menezes [Brésil] ; Lidiane Figueredo Ribeiro [Brésil] ; Cristiano Villela Dias [Brésil] ; Bruno Silva Andrade [Brésil] ; Raildo Mota De Jesus [Brésil] ; Acassia Benjamin Leal Pires [Brésil] ; Arist Teles Goes-Neto [Brésil] ; Fabienne Micheli [France]

Source :

RBID : pubmed:26701307

Descripteurs français

English descriptors

Abstract

We identified and characterized two chitinases, named MpCHIT1 and MpCHIT2, from the fungus Moniliophthora perniciosa - the etiologic agent of witches' broom disease in cacao tree (Theobroma cacao L.) - during its development, mainly in the mycelia phases preceding the basidioma formation. The expression of MpCHIT1 and MpCHIT2, together with MpCHS and MpATG8 (chitin synthase and autophagy genes, respectively), was analyzed during the M. perniciosa growth and development on bran-based solid medium as well as in liquid medium containing H2O2 or rapamycin (oxidative and nutritional related-autophagy stress agents, respectively). In order to link the expression of chitin metabolism-related genes to nutritional composition influencing fungus development, we also quantified total and reduced sugars, as well as macro- and micronutrients in the bran-based solid medium. The expression analysis showed that the MpCHS expression increased through mycelial development and then decreased in the primordium and basidioma phases, while the expression of MpCHIT1 and MpCHIT2 was higher in basidioma and primordium phases, respectively. Moreover, the expression pattern of MpCHIT1 and MpCHIT2 is distinct, the second correlated with the MpATG8 expression pattern and possibly with autophagy process, while the first may be related to the basidioma formation. The quantification of total and reduced sugars, as well as macro- and micronutrients supported the idea that the cell wall restructuration due to MpCHS, MpCHIT1 and MpCHIT2 is related to stress and fungal nutrient reallocation, allowing the formation and development of the basidioma. Experiments involving M. perniciosa growth on liquid medium containing H2O2 or rapamycin showed that MpCHIT1 and MpCHIT2 were over-expressed in response to oxidative but also to nutritional related-autophagy stresses. Interestingly, the expression level of MpCHS, MpCHIT1 and MpCHIT2 in presence of rapamycin is similar to the one observed in the primordium and basidioma from bran-based solid medium. The analysis of the overall data allowed designing a general scheme of chitin metabolism and autophagy during M. perniciosa development, focusing on the mycelium phases as crucial and environmentally influenced steps preceding the primordium and basidioma formation. These data support the idea that the nutritional environment of M. perniciosa influences its development and life cycle.

DOI: 10.1016/j.fgb.2015.12.008
PubMed: 26701307


Affiliations:


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Le document en format XML

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<name sortKey="Gomes, Dayane Santos" sort="Gomes, Dayane Santos" uniqKey="Gomes D" first="Dayane Santos" last="Gomes">Dayane Santos Gomes</name>
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<nlm:affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</nlm:affiliation>
<country xml:lang="fr">Brésil</country>
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<name sortKey="Lopes, Maiza Alves" sort="Lopes, Maiza Alves" uniqKey="Lopes M" first="Maíza Alves" last="Lopes">Maíza Alves Lopes</name>
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<nlm:affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil; Universidade Estadual de Feira de Santana (UEFS), Departamento de Ciências Biológicas (DCBio), Av. Transnordestina, s/n°, 44036-900 Feira de Santana, BA, Brazil.</nlm:affiliation>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil; Universidade Estadual de Feira de Santana (UEFS), Departamento de Ciências Biológicas (DCBio), Av. Transnordestina, s/n°, 44036-900 Feira de Santana, BA</wicri:regionArea>
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<nlm:affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</nlm:affiliation>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA</wicri:regionArea>
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<name sortKey="Ribeiro, Lidiane Figueredo" sort="Ribeiro, Lidiane Figueredo" uniqKey="Ribeiro L" first="Lidiane Figueredo" last="Ribeiro">Lidiane Figueredo Ribeiro</name>
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<nlm:affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</nlm:affiliation>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA</wicri:regionArea>
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<region type="state">Bahia</region>
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<name sortKey="Dias, Cristiano Villela" sort="Dias, Cristiano Villela" uniqKey="Dias C" first="Cristiano Villela" last="Dias">Cristiano Villela Dias</name>
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<nlm:affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</nlm:affiliation>
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<wicri:regionArea>Universidade Estadual do Sudoeste da Bahia (UESB), Av. José Moreira Sobrinho, 45206-190 Jequié, BA</wicri:regionArea>
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<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Exatas e Tecnológicas (DCET), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA</wicri:regionArea>
<placeName>
<region type="state">Bahia</region>
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<name sortKey="Pires, Acassia Benjamin Leal" sort="Pires, Acassia Benjamin Leal" uniqKey="Pires A" first="Acassia Benjamin Leal" last="Pires">Acassia Benjamin Leal Pires</name>
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<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA</wicri:regionArea>
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<name sortKey="Goes Neto, Arist Teles" sort="Goes Neto, Arist Teles" uniqKey="Goes Neto A" first="Arist Teles" last="Goes-Neto">Arist Teles Goes-Neto</name>
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<country xml:lang="fr">Brésil</country>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil; CIRAD, UMR AGAP, F-34398 Montpellier</wicri:regionArea>
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<title level="j">Fungal genetics and biology : FG & B</title>
<idno type="eISSN">1096-0937</idno>
<imprint>
<date when="2016" type="published">2016</date>
</imprint>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Agaricales (classification)</term>
<term>Agaricales (enzymology)</term>
<term>Agaricales (growth & development)</term>
<term>Autophagy (MeSH)</term>
<term>Cacao (microbiology)</term>
<term>Carbohydrate Metabolism (MeSH)</term>
<term>Carbohydrates (MeSH)</term>
<term>Chitin (metabolism)</term>
<term>Chitinases (genetics)</term>
<term>Chitinases (metabolism)</term>
<term>Fungal Proteins (genetics)</term>
<term>Fungal Proteins (metabolism)</term>
<term>Gene Expression (MeSH)</term>
<term>Genes, Fungal (MeSH)</term>
<term>Mycelium (growth & development)</term>
<term>Phylogeny (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Agaricales (classification)</term>
<term>Agaricales (croissance et développement)</term>
<term>Agaricales (enzymologie)</term>
<term>Autophagie (MeSH)</term>
<term>Cacaoyer (microbiologie)</term>
<term>Chitinase (génétique)</term>
<term>Chitinase (métabolisme)</term>
<term>Chitine (métabolisme)</term>
<term>Expression des gènes (MeSH)</term>
<term>Glucides (MeSH)</term>
<term>Gènes fongiques (MeSH)</term>
<term>Mycelium (croissance et développement)</term>
<term>Métabolisme glucidique (MeSH)</term>
<term>Phylogenèse (MeSH)</term>
<term>Protéines fongiques (génétique)</term>
<term>Protéines fongiques (métabolisme)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Chitinases</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Chitin</term>
<term>Chitinases</term>
<term>Fungal Proteins</term>
</keywords>
<keywords scheme="MESH" type="chemical" xml:lang="en">
<term>Carbohydrates</term>
</keywords>
<keywords scheme="MESH" qualifier="classification" xml:lang="en">
<term>Agaricales</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Agaricales</term>
<term>Mycelium</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Agaricales</term>
</keywords>
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<term>Agaricales</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Agaricales</term>
<term>Mycelium</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Agaricales</term>
<term>Chitinase</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Cacaoyer</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Cacao</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Chitinase</term>
<term>Chitine</term>
<term>Protéines fongiques</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Autophagy</term>
<term>Carbohydrate Metabolism</term>
<term>Gene Expression</term>
<term>Genes, Fungal</term>
<term>Phylogeny</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Autophagie</term>
<term>Expression des gènes</term>
<term>Glucides</term>
<term>Gènes fongiques</term>
<term>Métabolisme glucidique</term>
<term>Phylogenèse</term>
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<front>
<div type="abstract" xml:lang="en">We identified and characterized two chitinases, named MpCHIT1 and MpCHIT2, from the fungus Moniliophthora perniciosa - the etiologic agent of witches' broom disease in cacao tree (Theobroma cacao L.) - during its development, mainly in the mycelia phases preceding the basidioma formation. The expression of MpCHIT1 and MpCHIT2, together with MpCHS and MpATG8 (chitin synthase and autophagy genes, respectively), was analyzed during the M. perniciosa growth and development on bran-based solid medium as well as in liquid medium containing H2O2 or rapamycin (oxidative and nutritional related-autophagy stress agents, respectively). In order to link the expression of chitin metabolism-related genes to nutritional composition influencing fungus development, we also quantified total and reduced sugars, as well as macro- and micronutrients in the bran-based solid medium. The expression analysis showed that the MpCHS expression increased through mycelial development and then decreased in the primordium and basidioma phases, while the expression of MpCHIT1 and MpCHIT2 was higher in basidioma and primordium phases, respectively. Moreover, the expression pattern of MpCHIT1 and MpCHIT2 is distinct, the second correlated with the MpATG8 expression pattern and possibly with autophagy process, while the first may be related to the basidioma formation. The quantification of total and reduced sugars, as well as macro- and micronutrients supported the idea that the cell wall restructuration due to MpCHS, MpCHIT1 and MpCHIT2 is related to stress and fungal nutrient reallocation, allowing the formation and development of the basidioma. Experiments involving M. perniciosa growth on liquid medium containing H2O2 or rapamycin showed that MpCHIT1 and MpCHIT2 were over-expressed in response to oxidative but also to nutritional related-autophagy stresses. Interestingly, the expression level of MpCHS, MpCHIT1 and MpCHIT2 in presence of rapamycin is similar to the one observed in the primordium and basidioma from bran-based solid medium. The analysis of the overall data allowed designing a general scheme of chitin metabolism and autophagy during M. perniciosa development, focusing on the mycelium phases as crucial and environmentally influenced steps preceding the primordium and basidioma formation. These data support the idea that the nutritional environment of M. perniciosa influences its development and life cycle. </div>
</front>
</TEI>
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<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">26701307</PMID>
<DateCompleted>
<Year>2016</Year>
<Month>08</Month>
<Day>31</Day>
</DateCompleted>
<DateRevised>
<Year>2018</Year>
<Month>03</Month>
<Day>06</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1096-0937</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>86</Volume>
<PubDate>
<Year>2016</Year>
<Month>Jan</Month>
</PubDate>
</JournalIssue>
<Title>Fungal genetics and biology : FG & B</Title>
<ISOAbbreviation>Fungal Genet Biol</ISOAbbreviation>
</Journal>
<ArticleTitle>Mycelial development preceding basidioma formation in Moniliophthora perniciosa is associated to chitin, sugar and nutrient metabolism alterations involving autophagy.</ArticleTitle>
<Pagination>
<MedlinePgn>33-46</MedlinePgn>
</Pagination>
<ELocationID EIdType="pii" ValidYN="Y">S1087-1845(15)30056-6</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.fgb.2015.12.008</ELocationID>
<Abstract>
<AbstractText>We identified and characterized two chitinases, named MpCHIT1 and MpCHIT2, from the fungus Moniliophthora perniciosa - the etiologic agent of witches' broom disease in cacao tree (Theobroma cacao L.) - during its development, mainly in the mycelia phases preceding the basidioma formation. The expression of MpCHIT1 and MpCHIT2, together with MpCHS and MpATG8 (chitin synthase and autophagy genes, respectively), was analyzed during the M. perniciosa growth and development on bran-based solid medium as well as in liquid medium containing H2O2 or rapamycin (oxidative and nutritional related-autophagy stress agents, respectively). In order to link the expression of chitin metabolism-related genes to nutritional composition influencing fungus development, we also quantified total and reduced sugars, as well as macro- and micronutrients in the bran-based solid medium. The expression analysis showed that the MpCHS expression increased through mycelial development and then decreased in the primordium and basidioma phases, while the expression of MpCHIT1 and MpCHIT2 was higher in basidioma and primordium phases, respectively. Moreover, the expression pattern of MpCHIT1 and MpCHIT2 is distinct, the second correlated with the MpATG8 expression pattern and possibly with autophagy process, while the first may be related to the basidioma formation. The quantification of total and reduced sugars, as well as macro- and micronutrients supported the idea that the cell wall restructuration due to MpCHS, MpCHIT1 and MpCHIT2 is related to stress and fungal nutrient reallocation, allowing the formation and development of the basidioma. Experiments involving M. perniciosa growth on liquid medium containing H2O2 or rapamycin showed that MpCHIT1 and MpCHIT2 were over-expressed in response to oxidative but also to nutritional related-autophagy stresses. Interestingly, the expression level of MpCHS, MpCHIT1 and MpCHIT2 in presence of rapamycin is similar to the one observed in the primordium and basidioma from bran-based solid medium. The analysis of the overall data allowed designing a general scheme of chitin metabolism and autophagy during M. perniciosa development, focusing on the mycelium phases as crucial and environmentally influenced steps preceding the primordium and basidioma formation. These data support the idea that the nutritional environment of M. perniciosa influences its development and life cycle. </AbstractText>
<CopyrightInformation>Copyright © 2015 Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Gomes</LastName>
<ForeName>Dayane Santos</ForeName>
<Initials>DS</Initials>
<AffiliationInfo>
<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lopes</LastName>
<ForeName>Maíza Alves</ForeName>
<Initials>MA</Initials>
<AffiliationInfo>
<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil; Universidade Estadual de Feira de Santana (UEFS), Departamento de Ciências Biológicas (DCBio), Av. Transnordestina, s/n°, 44036-900 Feira de Santana, BA, Brazil.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Menezes</LastName>
<ForeName>Sara Pereira</ForeName>
<Initials>SP</Initials>
<AffiliationInfo>
<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ribeiro</LastName>
<ForeName>Lidiane Figueredo</ForeName>
<Initials>LF</Initials>
<AffiliationInfo>
<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</Affiliation>
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<Author ValidYN="Y">
<LastName>Dias</LastName>
<ForeName>Cristiano Villela</ForeName>
<Initials>CV</Initials>
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<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Andrade</LastName>
<ForeName>Bruno Silva</ForeName>
<Initials>BS</Initials>
<AffiliationInfo>
<Affiliation>Universidade Estadual do Sudoeste da Bahia (UESB), Av. José Moreira Sobrinho, 45206-190 Jequié, BA, Brazil.</Affiliation>
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</Author>
<Author ValidYN="Y">
<LastName>de Jesus</LastName>
<ForeName>Raildo Mota</ForeName>
<Initials>RM</Initials>
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<LastName>Pires</LastName>
<ForeName>Acassia Benjamin Leal</ForeName>
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<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil.</Affiliation>
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<LastName>Goes-Neto</LastName>
<ForeName>Aristóteles</ForeName>
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<Affiliation>Universidade Estadual de Feira de Santana (UEFS), Departamento de Ciências Biológicas (DCBio), Av. Transnordestina, s/n°, 44036-900 Feira de Santana, BA, Brazil.</Affiliation>
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</Author>
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<LastName>Micheli</LastName>
<ForeName>Fabienne</ForeName>
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<Affiliation>Universidade Estadual de Santa Cruz (UESC), Departamento de Ciências Biológicas (DCB), Centro de Biotecnologia e Genética (CBG), Rodovia Ilhéus-Itabuna, km 16, 45662-900 Ilhéus, BA, Brazil; CIRAD, UMR AGAP, F-34398 Montpellier, France. Electronic address: fabienne.micheli@cirad.fr.</Affiliation>
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<Year>2015</Year>
<Month>12</Month>
<Day>14</Day>
</ArticleDate>
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<MedlineTA>Fungal Genet Biol</MedlineTA>
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<ISSNLinking>1087-1845</ISSNLinking>
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<Chemical>
<RegistryNumber>1398-61-4</RegistryNumber>
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<DescriptorName UI="D000363" MajorTopicYN="N">Agaricales</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D001343" MajorTopicYN="N">Autophagy</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D002099" MajorTopicYN="N">Cacao</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
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<MeshHeading>
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<MeshHeading>
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<li>France</li>
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<li>Languedoc-Roussillon</li>
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