Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens

Abstract Background Cryptic peptides (cryptides) are small bioactive molecules generated via degradation of functionally active proteins. Only a few examples of plant cryptides playing an important role in plant defense have been reported to date, hence our knowledge about cryptic signals hidden in...

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Main Authors: Igor Fesenko, Regina Azarkina, Ilya Kirov, Andrei Kniazev, Anna Filippova, Ekaterina Grafskaia, Vassili Lazarev, Victor Zgoda, Ivan Butenko, Olga Bukato, Irina Lyapina, Dmitry Nazarenko, Sergey Elansky, Anna Mamaeva, Vadim Ivanov, Vadim Govorun
Format: Article
Language:English
Published: BMC 2019-01-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-018-1611-z
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author Igor Fesenko
Regina Azarkina
Ilya Kirov
Andrei Kniazev
Anna Filippova
Ekaterina Grafskaia
Vassili Lazarev
Victor Zgoda
Ivan Butenko
Olga Bukato
Irina Lyapina
Dmitry Nazarenko
Sergey Elansky
Anna Mamaeva
Vadim Ivanov
Vadim Govorun
author_facet Igor Fesenko
Regina Azarkina
Ilya Kirov
Andrei Kniazev
Anna Filippova
Ekaterina Grafskaia
Vassili Lazarev
Victor Zgoda
Ivan Butenko
Olga Bukato
Irina Lyapina
Dmitry Nazarenko
Sergey Elansky
Anna Mamaeva
Vadim Ivanov
Vadim Govorun
author_sort Igor Fesenko
collection DOAJ
description Abstract Background Cryptic peptides (cryptides) are small bioactive molecules generated via degradation of functionally active proteins. Only a few examples of plant cryptides playing an important role in plant defense have been reported to date, hence our knowledge about cryptic signals hidden in protein structure remains very limited. Moreover, little is known about how stress conditions influence the size of endogenous peptide pools, and which of these peptides themselves have biological functions is currently unclear. Results Here, we used mass spectrometry to comprehensively analyze the endogenous peptide pools generated from functionally active proteins inside the cell and in the secretome from the model plant Physcomitrella patens. Overall, we identified approximately 4,000 intracellular and approximately 500 secreted peptides. We found that the secretome and cellular peptidomes did not show significant overlap and that respective protein precursors have very different protein degradation patterns. We showed that treatment with the plant stress hormone methyl jasmonate induced specific proteolysis of new functional proteins and the release of bioactive peptides having an antimicrobial activity and capable to elicit the expression of plant defense genes. Finally, we showed that the inhibition of protease activity during methyl jasmonate treatment decreased the secretome antimicrobial potential, suggesting an important role of peptides released from proteins in immune response. Conclusions Using mass-spectrometry, in vitro experiments and bioinformatics analysis, we found that methyl jasmonate acid induces significant changes in the peptide pools and that some of the resulting peptides possess antimicrobial and regulatory activities. Moreover, our study provides a list of peptides for further study of potential plant cryptides.
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spelling doaj.art-32b88290499149f58cd585b88a3384a82022-12-22T00:19:58ZengBMCBMC Plant Biology1471-22292019-01-0119111610.1186/s12870-018-1611-zPhytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patensIgor Fesenko0Regina Azarkina1Ilya Kirov2Andrei Kniazev3Anna Filippova4Ekaterina Grafskaia5Vassili Lazarev6Victor Zgoda7Ivan Butenko8Olga Bukato9Irina Lyapina10Dmitry Nazarenko11Sergey Elansky12Anna Mamaeva13Vadim Ivanov14Vadim Govorun15Laboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesFederal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological AgencyFederal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological AgencyInstitute of Biomedical ChemistryFederal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological AgencyFederal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological AgencyLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesDepartment of Analytical Chemistry, Faculty of Chemistry, Lomonosov Moscow State UniversityBiological Faculty, Lomonosov Moscow State UniversityLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesLaboratory of Proteomics, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of SciencesFederal Research and Clinical Center of Physical-Chemical Medicine of Federal Medical Biological AgencyAbstract Background Cryptic peptides (cryptides) are small bioactive molecules generated via degradation of functionally active proteins. Only a few examples of plant cryptides playing an important role in plant defense have been reported to date, hence our knowledge about cryptic signals hidden in protein structure remains very limited. Moreover, little is known about how stress conditions influence the size of endogenous peptide pools, and which of these peptides themselves have biological functions is currently unclear. Results Here, we used mass spectrometry to comprehensively analyze the endogenous peptide pools generated from functionally active proteins inside the cell and in the secretome from the model plant Physcomitrella patens. Overall, we identified approximately 4,000 intracellular and approximately 500 secreted peptides. We found that the secretome and cellular peptidomes did not show significant overlap and that respective protein precursors have very different protein degradation patterns. We showed that treatment with the plant stress hormone methyl jasmonate induced specific proteolysis of new functional proteins and the release of bioactive peptides having an antimicrobial activity and capable to elicit the expression of plant defense genes. Finally, we showed that the inhibition of protease activity during methyl jasmonate treatment decreased the secretome antimicrobial potential, suggesting an important role of peptides released from proteins in immune response. Conclusions Using mass-spectrometry, in vitro experiments and bioinformatics analysis, we found that methyl jasmonate acid induces significant changes in the peptide pools and that some of the resulting peptides possess antimicrobial and regulatory activities. Moreover, our study provides a list of peptides for further study of potential plant cryptides.http://link.springer.com/article/10.1186/s12870-018-1611-zLC-MS/MSPeptidomePlant immunityPhyscomitrella patensSecretomePhytohormones
spellingShingle Igor Fesenko
Regina Azarkina
Ilya Kirov
Andrei Kniazev
Anna Filippova
Ekaterina Grafskaia
Vassili Lazarev
Victor Zgoda
Ivan Butenko
Olga Bukato
Irina Lyapina
Dmitry Nazarenko
Sergey Elansky
Anna Mamaeva
Vadim Ivanov
Vadim Govorun
Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens
BMC Plant Biology
LC-MS/MS
Peptidome
Plant immunity
Physcomitrella patens
Secretome
Phytohormones
title Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens
title_full Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens
title_fullStr Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens
title_full_unstemmed Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens
title_short Phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the Moss Physcomitrella patens
title_sort phytohormone treatment induces generation of cryptic peptides with antimicrobial activity in the moss physcomitrella patens
topic LC-MS/MS
Peptidome
Plant immunity
Physcomitrella patens
Secretome
Phytohormones
url http://link.springer.com/article/10.1186/s12870-018-1611-z
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