Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens

Broad-spectrum biocontrol by Pseudomonas protegens CHA0 and other fluorescent pseudomonads is achieved through the generation of various secondary metabolites with antibiotic activities against not only other microbes but, also, nematodes and insects present in the rhizosphere. A previous metabolomi...

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Main Authors: Kasumi Takeuchi, Masayo Ogiso, Tomohiro Morohoshi, Shigemi Seo
Format: Article
Language:English
Published: The American Phytopathological Society 2023-06-01
Series:Molecular Plant-Microbe Interactions
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-22-0178-R
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author Kasumi Takeuchi
Masayo Ogiso
Tomohiro Morohoshi
Shigemi Seo
author_facet Kasumi Takeuchi
Masayo Ogiso
Tomohiro Morohoshi
Shigemi Seo
author_sort Kasumi Takeuchi
collection DOAJ
description Broad-spectrum biocontrol by Pseudomonas protegens CHA0 and other fluorescent pseudomonads is achieved through the generation of various secondary metabolites with antibiotic activities against not only other microbes but, also, nematodes and insects present in the rhizosphere. A previous metabolomic study demonstrated that intracellular low–molecular weight effectors, such as guanosine tetraphosphate and γ-aminobutyrate, function as important signals in niche adaptation by strain CHA0 to plant roots. We investigated the role of amino acids in the biocontrol trait of P. protegens Cab57 towards Pythium damping off and root rot in cucumber. Among the 11 amino acids tested, only glutamate markedly enhanced the efficacy of biocontrol. An RNA-Seq analysis revealed that glutamate upregulated the expression of a chitinase gene cluster (c21370-c21380, in which the c21370 gene was annotated as a gene encoding the chitin-binding protein cbp and the c21380 gene encoded chitinase chiC) in strain CHA0. Glutamate upregulated the expression of the regulatory small RNA rsmZ but reduced the production levels of other Gac/Rsm-regulated biocontrol factors, such as 2,4-diacetylphloroglucinol and pyoluteorin. The promoter activity of cbp and chitinase activity were characterized in detail; their activities were up-regulated in response to glutamate and their expression was under the control of GacA. Therefore, glutamate appears to be essential for biocontrol activity in which chitinase production is regulated in response to glutamate. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
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spelling doaj.art-b4cf09a47158473589dc41012683676b2023-07-29T23:10:10ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062023-06-0136632333310.1094/MPMI-09-22-0178-RGlutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegensKasumi Takeuchi0Masayo Ogiso1Tomohiro Morohoshi2Shigemi Seo3Division of Plant Molecular Regulation, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8518, JapanDivision of Plant Molecular Regulation, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8518, JapanGraduate School of Regional Development and Creativity, Utsunomiya University, 7-1-2 Yoto, Utsunomiya, Tochigi 321-8585, JapanDivision of Plant Molecular Regulation, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8518, JapanBroad-spectrum biocontrol by Pseudomonas protegens CHA0 and other fluorescent pseudomonads is achieved through the generation of various secondary metabolites with antibiotic activities against not only other microbes but, also, nematodes and insects present in the rhizosphere. A previous metabolomic study demonstrated that intracellular low–molecular weight effectors, such as guanosine tetraphosphate and γ-aminobutyrate, function as important signals in niche adaptation by strain CHA0 to plant roots. We investigated the role of amino acids in the biocontrol trait of P. protegens Cab57 towards Pythium damping off and root rot in cucumber. Among the 11 amino acids tested, only glutamate markedly enhanced the efficacy of biocontrol. An RNA-Seq analysis revealed that glutamate upregulated the expression of a chitinase gene cluster (c21370-c21380, in which the c21370 gene was annotated as a gene encoding the chitin-binding protein cbp and the c21380 gene encoded chitinase chiC) in strain CHA0. Glutamate upregulated the expression of the regulatory small RNA rsmZ but reduced the production levels of other Gac/Rsm-regulated biocontrol factors, such as 2,4-diacetylphloroglucinol and pyoluteorin. The promoter activity of cbp and chitinase activity were characterized in detail; their activities were up-regulated in response to glutamate and their expression was under the control of GacA. Therefore, glutamate appears to be essential for biocontrol activity in which chitinase production is regulated in response to glutamate. [Graphic: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-22-0178-RbiocontrolchitinaseGac/Rsm systempseudomonads
spellingShingle Kasumi Takeuchi
Masayo Ogiso
Tomohiro Morohoshi
Shigemi Seo
Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens
Molecular Plant-Microbe Interactions
biocontrol
chitinase
Gac/Rsm system
pseudomonads
title Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens
title_full Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens
title_fullStr Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens
title_full_unstemmed Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens
title_short Glutamate Positively Regulates Chitinase Activity and the Biocontrol Efficacy of Pseudomonas protegens
title_sort glutamate positively regulates chitinase activity and the biocontrol efficacy of pseudomonas protegens
topic biocontrol
chitinase
Gac/Rsm system
pseudomonads
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-22-0178-R
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