Differential responses of genes and enzymes associated with ROS protective responses in the sugarcane smut fungus.
Identifieur interne : 000185 ( Main/Exploration ); précédent : 000184; suivant : 000186Differential responses of genes and enzymes associated with ROS protective responses in the sugarcane smut fungus.
Auteurs : L P Peters [Brésil] ; N S Teixeira-Silva [Brésil] ; A P Bini [Brésil] ; M M L. Silva [Brésil] ; N. Moraes [Brésil] ; G S Crestana [Brésil] ; S. Creste [Brésil] ; R A Azevedo [Brésil] ; G. Carvalho [Brésil] ; C B Monteiro-Vitorello [Brésil]Source :
- Fungal biology [ 1878-6146 ] ; 2020.
Abstract
The fungal pathogen Sporisorium scitamineum causes sugarcane smut disease. We have previously shown that resistant sugarcane plants induce ROS, coinciding with a delay in fungal colonization. Here, we investigated whether the fungus modifies the enzymatic antioxidant system in vitro and when colonizing sugarcane tissues in response to ROS. In vitro, the exposure to ROS did not affect cell integrity, and a combination of superoxide dismutases (SOD) and catalases (CAT) were active. In vitro, the fungus did not alter the expression of the transcriptional regulator Yap1 and the effector Pep1. The fungus activated distinct enzymes when colonizing plant tissues. Instead of CAT, S. scitamineum induced glutathione peroxidase (Gpx) expression only when colonizing smut-resistant plants. Yap1 had an earlier expression in both smut-susceptible and -resistant plants, with no apparent correlation with the expression of antioxidant genes sod, cat, gpx, or external redox imbalance. The expression of the effector pep1 was induced only in smut-resistant plants, potentially in response to ROS. These results collectively suggest that S. scitamineum copes with oxidative stress by inducing different mechanisms depending on the conditions (in vitro/in planta) and intensity of ROS. Moreover, the effector Pep1 is responsive to the stress imposed only by the sugarcane resistant genotype.
DOI: 10.1016/j.funbio.2020.09.009
PubMed: 33213784
Affiliations:
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Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Universidade Federal Do Acre, Centro de Ciências Biológicas e da Natureza, CEP, 69920-900, Rio Branco, AC, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Universidade Federal Do Acre, Centro de Ciências Biológicas e da Natureza, CEP, 69920-900, Rio Branco, AC</wicri:regionArea><placeName><region type="state">Acre (Brésil)</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Teixeira Silva, N S" sort="Teixeira Silva, N S" uniqKey="Teixeira Silva N" first="N S" last="Teixeira-Silva">N S Teixeira-Silva</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Bini, A P" sort="Bini, A P" uniqKey="Bini A" first="A P" last="Bini">A P Bini</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Instituto Agronômico (IAC), Centro de Cana, CP 206, CEP, 14001-970, Ribeirão Preto, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Instituto Agronômico (IAC), Centro de Cana, CP 206, CEP, 14001-970, Ribeirão Preto, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Silva, M M L" sort="Silva, M M L" uniqKey="Silva M" first="M M L" last="Silva">M M L. Silva</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Moraes, N" sort="Moraes, N" uniqKey="Moraes N" first="N" last="Moraes">N. Moraes</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Crestana, G S" sort="Crestana, G S" uniqKey="Crestana G" first="G S" last="Crestana">G S Crestana</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Creste, S" sort="Creste, S" uniqKey="Creste S" first="S" last="Creste">S. Creste</name><affiliation wicri:level="2"><nlm:affiliation>Instituto Agronômico (IAC), Centro de Cana, CP 206, CEP, 14001-970, Ribeirão Preto, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Instituto Agronômico (IAC), Centro de Cana, CP 206, CEP, 14001-970, Ribeirão Preto, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region></placeName></affiliation></author><author><name sortKey="Azevedo, R A" sort="Azevedo, R A" uniqKey="Azevedo R" first="R A" last="Azevedo">R A Azevedo</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Carvalho, G" sort="Carvalho, G" uniqKey="Carvalho G" first="G" last="Carvalho">G. Carvalho</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Instituto SENAI de Inovação Em Biomassa, CEP, 79604-250, Três Lagoas, MS, Brazil. Electronic address: gisellecarvalho05@gmail.com.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Instituto SENAI de Inovação Em Biomassa, CEP, 79604-250, Três Lagoas, MS</wicri:regionArea><placeName><region type="state">Mato Grosso do Sul</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author><author><name sortKey="Monteiro Vitorello, C B" sort="Monteiro Vitorello, C B" uniqKey="Monteiro Vitorello C" first="C B" last="Monteiro-Vitorello">C B Monteiro-Vitorello</name><affiliation wicri:level="4"><nlm:affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil. Electronic address: cbmontei@usp.br.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP</wicri:regionArea><placeName><region type="state">État de São Paulo</region><settlement type="city">São Paulo</settlement></placeName><orgName type="university">Université de São Paulo</orgName></affiliation></author></analytic><series><title level="j">Fungal biology</title><idno type="ISSN">1878-6146</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The fungal pathogen Sporisorium scitamineum causes sugarcane smut disease. We have previously shown that resistant sugarcane plants induce ROS, coinciding with a delay in fungal colonization. Here, we investigated whether the fungus modifies the enzymatic antioxidant system in vitro and when colonizing sugarcane tissues in response to ROS. In vitro, the exposure to ROS did not affect cell integrity, and a combination of superoxide dismutases (SOD) and catalases (CAT) were active. In vitro, the fungus did not alter the expression of the transcriptional regulator Yap1 and the effector Pep1. The fungus activated distinct enzymes when colonizing plant tissues. Instead of CAT, S. scitamineum induced glutathione peroxidase (Gpx) expression only when colonizing smut-resistant plants. Yap1 had an earlier expression in both smut-susceptible and -resistant plants, with no apparent correlation with the expression of antioxidant genes sod, cat, gpx, or external redox imbalance. The expression of the effector pep1 was induced only in smut-resistant plants, potentially in response to ROS. These results collectively suggest that S. scitamineum copes with oxidative stress by inducing different mechanisms depending on the conditions (in vitro/in planta) and intensity of ROS. Moreover, the effector Pep1 is responsive to the stress imposed only by the sugarcane resistant genotype.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">33213784</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Print">1878-6146</ISSN><JournalIssue CitedMedium="Internet"><Volume>124</Volume><Issue>12</Issue><PubDate><Year>2020</Year><Month>Dec</Month></PubDate></JournalIssue><Title>Fungal biology</Title><ISOAbbreviation>Fungal Biol</ISOAbbreviation></Journal><ArticleTitle>Differential responses of genes and enzymes associated with ROS protective responses in the sugarcane smut fungus.</ArticleTitle><Pagination><MedlinePgn>1039-1051</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S1878-6146(20)30149-5</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.funbio.2020.09.009</ELocationID><Abstract><AbstractText>The fungal pathogen Sporisorium scitamineum causes sugarcane smut disease. We have previously shown that resistant sugarcane plants induce ROS, coinciding with a delay in fungal colonization. Here, we investigated whether the fungus modifies the enzymatic antioxidant system in vitro and when colonizing sugarcane tissues in response to ROS. In vitro, the exposure to ROS did not affect cell integrity, and a combination of superoxide dismutases (SOD) and catalases (CAT) were active. In vitro, the fungus did not alter the expression of the transcriptional regulator Yap1 and the effector Pep1. The fungus activated distinct enzymes when colonizing plant tissues. Instead of CAT, S. scitamineum induced glutathione peroxidase (Gpx) expression only when colonizing smut-resistant plants. Yap1 had an earlier expression in both smut-susceptible and -resistant plants, with no apparent correlation with the expression of antioxidant genes sod, cat, gpx, or external redox imbalance. The expression of the effector pep1 was induced only in smut-resistant plants, potentially in response to ROS. These results collectively suggest that S. scitamineum copes with oxidative stress by inducing different mechanisms depending on the conditions (in vitro/in planta) and intensity of ROS. Moreover, the effector Pep1 is responsive to the stress imposed only by the sugarcane resistant genotype.</AbstractText><CopyrightInformation>Copyright © 2020 The Author(s). Published by Elsevier Ltd.. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Peters</LastName><ForeName>L P</ForeName><Initials>LP</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Universidade Federal Do Acre, Centro de Ciências Biológicas e da Natureza, CEP, 69920-900, Rio Branco, AC, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Teixeira-Silva</LastName><ForeName>N S</ForeName><Initials>NS</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bini</LastName><ForeName>A P</ForeName><Initials>AP</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Instituto Agronômico (IAC), Centro de Cana, CP 206, CEP, 14001-970, Ribeirão Preto, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Silva</LastName><ForeName>M M L</ForeName><Initials>MML</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Moraes</LastName><ForeName>N</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Crestana</LastName><ForeName>G S</ForeName><Initials>GS</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Creste</LastName><ForeName>S</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Instituto Agronômico (IAC), Centro de Cana, CP 206, CEP, 14001-970, Ribeirão Preto, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Azevedo</LastName><ForeName>R A</ForeName><Initials>RA</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Carvalho</LastName><ForeName>G</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil; Instituto SENAI de Inovação Em Biomassa, CEP, 79604-250, Três Lagoas, MS, Brazil. Electronic address: gisellecarvalho05@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Monteiro-Vitorello</LastName><ForeName>C B</ForeName><Initials>CB</Initials><AffiliationInfo><Affiliation>Universidade de São Paulo, Escola Superior de Agricultura "Luiz de Queiroz", Departamento de Genética, Av. Pádua Dias, 11, CP 9, CEP, 13418-900, Piracicaba, SP, Brazil. Electronic address: cbmontei@usp.br.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>04</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Fungal Biol</MedlineTA><NlmUniqueID>101524465</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Antioxidant enzymes</Keyword><Keyword MajorTopicYN="N">Biotrophic fungi</Keyword><Keyword MajorTopicYN="N">Exogenous H(2)O(2)</Keyword><Keyword MajorTopicYN="N">Molecular responses</Keyword><Keyword MajorTopicYN="N">Oxidative burst</Keyword></KeywordList><CoiStatement>Declaration of competing interest The authors declare no competing interests.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>03</Month><Day>30</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>09</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>11</Month><Day>20</Day><Hour>5</Hour><Minute>32</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>11</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>11</Month><Day>21</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33213784</ArticleId><ArticleId IdType="pii">S1878-6146(20)30149-5</ArticleId><ArticleId IdType="doi">10.1016/j.funbio.2020.09.009</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Brésil</li></country><region><li>Acre (Brésil)</li><li>Mato Grosso do Sul</li><li>État de São Paulo</li></region><settlement><li>São Paulo</li></settlement><orgName><li>Université de São Paulo</li></orgName></list><tree><country name="Brésil"><region name="Acre (Brésil)"><name sortKey="Peters, L P" sort="Peters, L P" uniqKey="Peters L" first="L P" last="Peters">L P Peters</name></region><name sortKey="Azevedo, R A" sort="Azevedo, R A" uniqKey="Azevedo R" first="R A" last="Azevedo">R A Azevedo</name><name sortKey="Bini, A P" sort="Bini, A P" uniqKey="Bini A" first="A P" last="Bini">A P Bini</name><name sortKey="Carvalho, G" sort="Carvalho, G" uniqKey="Carvalho G" first="G" last="Carvalho">G. Carvalho</name><name sortKey="Crestana, G S" sort="Crestana, G S" uniqKey="Crestana G" first="G S" last="Crestana">G S Crestana</name><name sortKey="Creste, S" sort="Creste, S" uniqKey="Creste S" first="S" last="Creste">S. Creste</name><name sortKey="Monteiro Vitorello, C B" sort="Monteiro Vitorello, C B" uniqKey="Monteiro Vitorello C" first="C B" last="Monteiro-Vitorello">C B Monteiro-Vitorello</name><name sortKey="Moraes, N" sort="Moraes, N" uniqKey="Moraes N" first="N" last="Moraes">N. Moraes</name><name sortKey="Silva, M M L" sort="Silva, M M L" uniqKey="Silva M" first="M M L" last="Silva">M M L. Silva</name><name sortKey="Teixeira Silva, N S" sort="Teixeira Silva, N S" uniqKey="Teixeira Silva N" first="N S" last="Teixeira-Silva">N S Teixeira-Silva</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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