Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots

The main role of RALF small signaling peptides was reported to be the alkalization control of the apoplast for improvement of nutrient absorption; however, the exact function of individual RALF peptides such as RALF34 remains unknown. The Arabidopsis RALF34 (<i>At</i>RALF34) peptide was...

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Main Authors: Julia Shumilina, Alexey S. Kiryushkin, Nadezhda Frolova, Valeria Mashkina, Elena L. Ilina, Vera A. Puchkova, Katerina Danko, Svetlana Silinskaya, Evgeny B. Serebryakov, Alena Soboleva, Tatiana Bilova, Anastasia Orlova, Elizaveta D. Guseva, Egor Repkin, Katharina Pawlowski, Andrej Frolov, Kirill N. Demchenko
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:International Journal of Molecular Sciences
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Online Access:https://www.mdpi.com/1422-0067/24/8/7654
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author Julia Shumilina
Alexey S. Kiryushkin
Nadezhda Frolova
Valeria Mashkina
Elena L. Ilina
Vera A. Puchkova
Katerina Danko
Svetlana Silinskaya
Evgeny B. Serebryakov
Alena Soboleva
Tatiana Bilova
Anastasia Orlova
Elizaveta D. Guseva
Egor Repkin
Katharina Pawlowski
Andrej Frolov
Kirill N. Demchenko
author_facet Julia Shumilina
Alexey S. Kiryushkin
Nadezhda Frolova
Valeria Mashkina
Elena L. Ilina
Vera A. Puchkova
Katerina Danko
Svetlana Silinskaya
Evgeny B. Serebryakov
Alena Soboleva
Tatiana Bilova
Anastasia Orlova
Elizaveta D. Guseva
Egor Repkin
Katharina Pawlowski
Andrej Frolov
Kirill N. Demchenko
author_sort Julia Shumilina
collection DOAJ
description The main role of RALF small signaling peptides was reported to be the alkalization control of the apoplast for improvement of nutrient absorption; however, the exact function of individual RALF peptides such as RALF34 remains unknown. The Arabidopsis RALF34 (<i>At</i>RALF34) peptide was proposed to be part of the gene regulatory network of lateral root initiation. Cucumber is an excellent model for studying a special form of lateral root initiation taking place in the meristem of the parental root. We attempted to elucidate the role of the regulatory pathway in which RALF34 is a participant using cucumber transgenic hairy roots overexpressing <i>CsRALF34</i> for comprehensive, integrated metabolomics and proteomics studies, focusing on the analysis of stress response markers. <i>Cs</i>RALF34 overexpression resulted in the inhibition of root growth and regulation of cell proliferation, specifically in blocking the G2/M transition in cucumber roots. Based on these results, we propose that <i>CsRALF34</i> is not part of the gene regulatory networks involved in the early steps of lateral root initiation. Instead, we suggest that <i>Cs</i>RALF34 modulates ROS homeostasis and triggers the controlled production of hydroxyl radicals in root cells, possibly associated with intracellular signal transduction. Altogether, our results support the role of RALF peptides as ROS regulators.
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spelling doaj.art-600960858b8848b0b73fd67390cd087f2023-11-17T19:43:47ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-04-01248765410.3390/ijms24087654Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber RootsJulia Shumilina0Alexey S. Kiryushkin1Nadezhda Frolova2Valeria Mashkina3Elena L. Ilina4Vera A. Puchkova5Katerina Danko6Svetlana Silinskaya7Evgeny B. Serebryakov8Alena Soboleva9Tatiana Bilova10Anastasia Orlova11Elizaveta D. Guseva12Egor Repkin13Katharina Pawlowski14Andrej Frolov15Kirill N. Demchenko16Saint Petersburg State University, 199034 Saint Petersburg, RussiaLaboratory of Cellular and Molecular Mechanisms of Plant Development, Komarov Botanical Institute, Russian Academy of Sciences, 197022 Saint Petersburg, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaLaboratory of Cellular and Molecular Mechanisms of Plant Development, Komarov Botanical Institute, Russian Academy of Sciences, 197022 Saint Petersburg, RussiaLaboratory of Cellular and Molecular Mechanisms of Plant Development, Komarov Botanical Institute, Russian Academy of Sciences, 197022 Saint Petersburg, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaLaboratory of Analytical Biochemistry and Biotechnology, Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, 127276 Moscow, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaLaboratory of Analytical Biochemistry and Biotechnology, Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, 127276 Moscow, RussiaLaboratory of Cellular and Molecular Mechanisms of Plant Development, Komarov Botanical Institute, Russian Academy of Sciences, 197022 Saint Petersburg, RussiaSaint Petersburg State University, 199034 Saint Petersburg, RussiaDepartment of Ecology, Environment and Plant Sciences, Stockholm University, 10691 Stockholm, SwedenLaboratory of Analytical Biochemistry and Biotechnology, Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, 127276 Moscow, RussiaLaboratory of Cellular and Molecular Mechanisms of Plant Development, Komarov Botanical Institute, Russian Academy of Sciences, 197022 Saint Petersburg, RussiaThe main role of RALF small signaling peptides was reported to be the alkalization control of the apoplast for improvement of nutrient absorption; however, the exact function of individual RALF peptides such as RALF34 remains unknown. The Arabidopsis RALF34 (<i>At</i>RALF34) peptide was proposed to be part of the gene regulatory network of lateral root initiation. Cucumber is an excellent model for studying a special form of lateral root initiation taking place in the meristem of the parental root. We attempted to elucidate the role of the regulatory pathway in which RALF34 is a participant using cucumber transgenic hairy roots overexpressing <i>CsRALF34</i> for comprehensive, integrated metabolomics and proteomics studies, focusing on the analysis of stress response markers. <i>Cs</i>RALF34 overexpression resulted in the inhibition of root growth and regulation of cell proliferation, specifically in blocking the G2/M transition in cucumber roots. Based on these results, we propose that <i>CsRALF34</i> is not part of the gene regulatory networks involved in the early steps of lateral root initiation. Instead, we suggest that <i>Cs</i>RALF34 modulates ROS homeostasis and triggers the controlled production of hydroxyl radicals in root cells, possibly associated with intracellular signal transduction. Altogether, our results support the role of RALF peptides as ROS regulators.https://www.mdpi.com/1422-0067/24/8/7654<i>Cucumis sativus</i> (cucumber)small signaling peptidesRALF34root developmentoverexpressionhairy root transformation
spellingShingle Julia Shumilina
Alexey S. Kiryushkin
Nadezhda Frolova
Valeria Mashkina
Elena L. Ilina
Vera A. Puchkova
Katerina Danko
Svetlana Silinskaya
Evgeny B. Serebryakov
Alena Soboleva
Tatiana Bilova
Anastasia Orlova
Elizaveta D. Guseva
Egor Repkin
Katharina Pawlowski
Andrej Frolov
Kirill N. Demchenko
Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots
International Journal of Molecular Sciences
<i>Cucumis sativus</i> (cucumber)
small signaling peptides
RALF34
root development
overexpression
hairy root transformation
title Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots
title_full Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots
title_fullStr Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots
title_full_unstemmed Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots
title_short Integrative Proteomics and Metabolomics Analysis Reveals the Role of Small Signaling Peptide Rapid Alkalinization Factor 34 (RALF34) in Cucumber Roots
title_sort integrative proteomics and metabolomics analysis reveals the role of small signaling peptide rapid alkalinization factor 34 ralf34 in cucumber roots
topic <i>Cucumis sativus</i> (cucumber)
small signaling peptides
RALF34
root development
overexpression
hairy root transformation
url https://www.mdpi.com/1422-0067/24/8/7654
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