Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L.
Identifieur interne : 000160 ( Main/Exploration ); précédent : 000159; suivant : 000161Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in Triticum aestivum L.
Auteurs : Anastasia V. Balakireva [Russie] ; Andrei A. Deviatkin [Russie] ; Victor G. Zgoda [Russie] ; Maxim I. Kartashov [Russie] ; Natalia S. Zhemchuzhina [Russie] ; Vitaly G. Dzhavakhiya [Russie] ; Andrey V. Golovin [Russie] ; Andrey A. Zamyatnin [Russie]Source :
- International journal of molecular sciences [ 1422-0067 ] ; 2018.
Descripteurs français
- KwdFr :
- Ascomycota (pathogénicité), Basidiomycota (pathogénicité), Caspases (métabolisme), Feuilles de plante (génétique), Feuilles de plante (microbiologie), Maladies des plantes (génétique), Maladies des plantes (microbiologie), Peptide hydrolases (métabolisme), Protéomique (méthodes), Subtilisines (génétique), Subtilisines (métabolisme).
- MESH :
- génétique : Feuilles de plante, Maladies des plantes, Subtilisines.
- microbiologie : Feuilles de plante, Maladies des plantes.
- métabolisme : Caspases, Peptide hydrolases, Subtilisines.
- méthodes : Protéomique.
- pathogénicité : Ascomycota, Basidiomycota.
English descriptors
- KwdEn :
- MESH :
- chemical , genetics : Subtilisins.
- chemical , metabolism : Caspases, Peptide Hydrolases, Subtilisins.
- genetics : Plant Diseases, Plant Leaves.
- methods : Proteomics.
- microbiology : Plant Diseases, Plant Leaves.
- pathogenicity : Ascomycota, Basidiomycota.
Abstract
Plants, including Triticum aestivum L., are constantly attacked by various pathogens which induce immune responses. Immune processes in plants are tightly regulated by proteases from different families within their degradome. In this study, a wheat degradome was characterized. Using profile hidden Markov model (HMMer) algorithm and Pfam database, comprehensive analysis of the T. aestivum genome revealed a large number of proteases (1544 in total) belonging to the five major protease families: serine, cysteine, threonine, aspartic, and metallo-proteases. Mass-spectrometry analysis revealed a 30% difference between degradomes of distinct wheat cultivars (Khakasskaya and Darya), and infection by biotrophic (Puccinia recondita Rob. ex Desm f. sp. tritici) or necrotrophic (Stagonospora nodorum) pathogens induced drastic changes in the presence of proteolytic enzymes. This study shows that an early immune response to biotic stress is associated with the same core of proteases from the C1, C48, C65, M24, M41, S10, S9, S8, and A1 families. Further liquid chromatography-mass spectrometry (LC-MS) analysis of the detected protease-derived peptides revealed that infection by both pathogens enhances overall proteolytic activity in wheat cells and leads to activation of proteolytic cascades. Moreover, sites of proteolysis were identified within the proteases, which probably represent targets of autocatalytic activation, or hydrolysis by another protease within the proteolytic cascades. Although predicted substrates of metacaspase-like and caspase-like proteases were similar in biotrophic and necrotrophic infections, proteolytic activation of proteases was not found to be associated with metacaspase-like and caspase-like activities. These findings indicate that the response of T. aestivum to biotic stress is regulated by unique mechanisms.
DOI: 10.3390/ijms19123991
PubMed: 30544979
PubMed Central: PMC6320887
Affiliations:
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Golovin</name><affiliation wicri:level="1"><nlm:affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. golovin.andrey@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia. golovin.andrey@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName><orgName type="university">Université d'État de Moscou</orgName><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation></author><author><name sortKey="Zamyatnin, Andrey A" sort="Zamyatnin, Andrey A" uniqKey="Zamyatnin A" first="Andrey A" last="Zamyatnin">Andrey A. 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Balakireva</name><affiliation wicri:level="1"><nlm:affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. balakireva.anastacia@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation></author><author><name sortKey="Deviatkin, Andrei A" sort="Deviatkin, Andrei A" uniqKey="Deviatkin A" first="Andrei A" last="Deviatkin">Andrei A. Deviatkin</name><affiliation wicri:level="1"><nlm:affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. andreideviatkin@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation></author><author><name sortKey="Zgoda, Victor G" sort="Zgoda, Victor G" uniqKey="Zgoda V" first="Victor G" last="Zgoda">Victor G. Zgoda</name><affiliation wicri:level="1"><nlm:affiliation>Institute of Biomedical Chemistry, Pogodinskaya str., 10, bld. 8, Moscow 119121, Russia. victor.zgoda@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Institute of Biomedical Chemistry, Pogodinskaya str., 10, bld. 8, Moscow 119121</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation></author><author><name sortKey="Kartashov, Maxim I" sort="Kartashov, Maxim I" uniqKey="Kartashov M" first="Maxim I" last="Kartashov">Maxim I. Kartashov</name><affiliation wicri:level="1"><nlm:affiliation>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia. maki505@mail.ru.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050</wicri:regionArea><wicri:noRegion>Moscow region 143050</wicri:noRegion></affiliation></author><author><name sortKey="Zhemchuzhina, Natalia S" sort="Zhemchuzhina, Natalia S" uniqKey="Zhemchuzhina N" first="Natalia S" last="Zhemchuzhina">Natalia S. Zhemchuzhina</name><affiliation wicri:level="1"><nlm:affiliation>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia. zhemch@mail.ru.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050</wicri:regionArea><wicri:noRegion>Moscow region 143050</wicri:noRegion></affiliation></author><author><name sortKey="Dzhavakhiya, Vitaly G" sort="Dzhavakhiya, Vitaly G" uniqKey="Dzhavakhiya V" first="Vitaly G" last="Dzhavakhiya">Vitaly G. Dzhavakhiya</name><affiliation wicri:level="1"><nlm:affiliation>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia. dzhavakhiya@yahoo.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050</wicri:regionArea><wicri:noRegion>Moscow region 143050</wicri:noRegion></affiliation></author><author><name sortKey="Golovin, Andrey V" sort="Golovin, Andrey V" uniqKey="Golovin A" first="Andrey V" last="Golovin">Andrey V. Golovin</name><affiliation wicri:level="1"><nlm:affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. golovin.andrey@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation><affiliation wicri:level="4"><nlm:affiliation>Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia. golovin.andrey@gmail.com.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName><orgName type="university">Université d'État de Moscou</orgName><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation></author><author><name sortKey="Zamyatnin, Andrey A" sort="Zamyatnin, Andrey A" uniqKey="Zamyatnin A" first="Andrey A" last="Zamyatnin">Andrey A. Zamyatnin</name><affiliation wicri:level="1"><nlm:affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. zamyat@belozersky.msu.ru.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow 119992, Russia. zamyat@belozersky.msu.ru.</nlm:affiliation><country xml:lang="fr">Russie</country><wicri:regionArea>Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow 119992</wicri:regionArea><placeName><settlement type="city">Moscou</settlement><region>District fédéral central</region></placeName></affiliation></author></analytic><series><title level="j">International journal of molecular sciences</title><idno type="eISSN">1422-0067</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Ascomycota (pathogenicity)</term><term>Basidiomycota (pathogenicity)</term><term>Caspases (metabolism)</term><term>Peptide Hydrolases (metabolism)</term><term>Plant Diseases (genetics)</term><term>Plant Diseases (microbiology)</term><term>Plant Leaves (genetics)</term><term>Plant Leaves (microbiology)</term><term>Proteomics (methods)</term><term>Subtilisins (genetics)</term><term>Subtilisins (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Ascomycota (pathogénicité)</term><term>Basidiomycota (pathogénicité)</term><term>Caspases (métabolisme)</term><term>Feuilles de plante (génétique)</term><term>Feuilles de plante (microbiologie)</term><term>Maladies des plantes (génétique)</term><term>Maladies des plantes (microbiologie)</term><term>Peptide hydrolases (métabolisme)</term><term>Protéomique (méthodes)</term><term>Subtilisines (génétique)</term><term>Subtilisines (métabolisme)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Subtilisins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Caspases</term><term>Peptide Hydrolases</term><term>Subtilisins</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Plant Diseases</term><term>Plant Leaves</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Feuilles de plante</term><term>Maladies des plantes</term><term>Subtilisines</term></keywords><keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Proteomics</term></keywords><keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr"><term>Feuilles de plante</term><term>Maladies des plantes</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term><term>Plant Leaves</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Caspases</term><term>Peptide hydrolases</term><term>Subtilisines</term></keywords><keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Protéomique</term></keywords><keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en"><term>Ascomycota</term><term>Basidiomycota</term></keywords><keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr"><term>Ascomycota</term><term>Basidiomycota</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Plants, including <i>Triticum aestivum</i> L., are constantly attacked by various pathogens which induce immune responses. Immune processes in plants are tightly regulated by proteases from different families within their degradome. In this study, a wheat degradome was characterized. Using profile hidden Markov model (HMMer) algorithm and Pfam database, comprehensive analysis of the <i>T. aestivum</i> genome revealed a large number of proteases (1544 in total) belonging to the five major protease families: serine, cysteine, threonine, aspartic, and metallo-proteases. Mass-spectrometry analysis revealed a 30% difference between degradomes of distinct wheat cultivars (Khakasskaya and Darya), and infection by biotrophic (<i>Puccinia recondita</i> Rob. ex Desm f. sp. tritici) or necrotrophic (<i>Stagonospora nodorum</i>) pathogens induced drastic changes in the presence of proteolytic enzymes. This study shows that an early immune response to biotic stress is associated with the same core of proteases from the C1, C48, C65, M24, M41, S10, S9, S8, and A1 families. Further liquid chromatography-mass spectrometry (LC-MS) analysis of the detected protease-derived peptides revealed that infection by both pathogens enhances overall proteolytic activity in wheat cells and leads to activation of proteolytic cascades. Moreover, sites of proteolysis were identified within the proteases, which probably represent targets of autocatalytic activation, or hydrolysis by another protease within the proteolytic cascades. Although predicted substrates of metacaspase-like and caspase-like proteases were similar in biotrophic and necrotrophic infections, proteolytic activation of proteases was not found to be associated with metacaspase-like and caspase-like activities. These findings indicate that the response of <i>T. aestivum</i> to biotic stress is regulated by unique mechanisms.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">30544979</PMID><DateCompleted><Year>2019</Year><Month>03</Month><Day>11</Day></DateCompleted><DateRevised><Year>2020</Year><Month>02</Month><Day>25</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1422-0067</ISSN><JournalIssue CitedMedium="Internet"><Volume>19</Volume><Issue>12</Issue><PubDate><Year>2018</Year><Month>Dec</Month><Day>11</Day></PubDate></JournalIssue><Title>International journal of molecular sciences</Title><ISOAbbreviation>Int J Mol Sci</ISOAbbreviation></Journal><ArticleTitle>Proteomics Analysis Reveals That Caspase-Like and Metacaspase-Like Activities Are Dispensable for Activation of Proteases Involved in Early Response to Biotic Stress in <i>Triticum aestivum</i> L.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">E3991</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.3390/ijms19123991</ELocationID><Abstract><AbstractText>Plants, including <i>Triticum aestivum</i> L., are constantly attacked by various pathogens which induce immune responses. Immune processes in plants are tightly regulated by proteases from different families within their degradome. In this study, a wheat degradome was characterized. Using profile hidden Markov model (HMMer) algorithm and Pfam database, comprehensive analysis of the <i>T. aestivum</i> genome revealed a large number of proteases (1544 in total) belonging to the five major protease families: serine, cysteine, threonine, aspartic, and metallo-proteases. Mass-spectrometry analysis revealed a 30% difference between degradomes of distinct wheat cultivars (Khakasskaya and Darya), and infection by biotrophic (<i>Puccinia recondita</i> Rob. ex Desm f. sp. tritici) or necrotrophic (<i>Stagonospora nodorum</i>) pathogens induced drastic changes in the presence of proteolytic enzymes. This study shows that an early immune response to biotic stress is associated with the same core of proteases from the C1, C48, C65, M24, M41, S10, S9, S8, and A1 families. Further liquid chromatography-mass spectrometry (LC-MS) analysis of the detected protease-derived peptides revealed that infection by both pathogens enhances overall proteolytic activity in wheat cells and leads to activation of proteolytic cascades. Moreover, sites of proteolysis were identified within the proteases, which probably represent targets of autocatalytic activation, or hydrolysis by another protease within the proteolytic cascades. Although predicted substrates of metacaspase-like and caspase-like proteases were similar in biotrophic and necrotrophic infections, proteolytic activation of proteases was not found to be associated with metacaspase-like and caspase-like activities. These findings indicate that the response of <i>T. aestivum</i> to biotic stress is regulated by unique mechanisms.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Balakireva</LastName><ForeName>Anastasia V</ForeName><Initials>AV</Initials><AffiliationInfo><Affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. balakireva.anastacia@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Deviatkin</LastName><ForeName>Andrei A</ForeName><Initials>AA</Initials><Identifier Source="ORCID">0000-0003-0789-4601</Identifier><AffiliationInfo><Affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. andreideviatkin@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zgoda</LastName><ForeName>Victor G</ForeName><Initials>VG</Initials><AffiliationInfo><Affiliation>Institute of Biomedical Chemistry, Pogodinskaya str., 10, bld. 8, Moscow 119121, Russia. victor.zgoda@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kartashov</LastName><ForeName>Maxim I</ForeName><Initials>MI</Initials><AffiliationInfo><Affiliation>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia. maki505@mail.ru.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhemchuzhina</LastName><ForeName>Natalia S</ForeName><Initials>NS</Initials><AffiliationInfo><Affiliation>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia. zhemch@mail.ru.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dzhavakhiya</LastName><ForeName>Vitaly G</ForeName><Initials>VG</Initials><AffiliationInfo><Affiliation>All Russian Research Institute of Phytopathology, VNIIF, Bolshie Vyazemi, Odintsovsky distr., Moscow region 143050, Russia. dzhavakhiya@yahoo.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Golovin</LastName><ForeName>Andrey V</ForeName><Initials>AV</Initials><Identifier Source="ORCID">0000-0002-8908-4268</Identifier><AffiliationInfo><Affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. golovin.andrey@gmail.com.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Faculty of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia. golovin.andrey@gmail.com.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zamyatnin</LastName><ForeName>Andrey A</ForeName><Initials>AA</Initials><Suffix>Jr</Suffix><Identifier Source="ORCID">0000-0002-3046-4565</Identifier><AffiliationInfo><Affiliation>Sechenov First Moscow State Medical University, Institute of Molecular Medicine, Trubetskaya str., 8, bld. 2, Moscow 119991, Russia. zamyat@belozersky.msu.ru.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow 119992, Russia. zamyat@belozersky.msu.ru.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>16-15-10410</GrantID><Agency>Russian Science Foundation</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>12</Month><Day>11</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Int J Mol Sci</MedlineTA><NlmUniqueID>101092791</NlmUniqueID><ISSNLinking>1422-0067</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>EC 3.4.-</RegistryNumber><NameOfSubstance 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