The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
Pectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the rel...
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doaj-8e8e3df62caa4b0aade6e982d56577962021-01-15T04:35:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-01-011110.3389/fmicb.2020.621391621391The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant PathosystemsUljana Kravchenko0Natalia Gogoleva1Natalia Gogoleva2Nastassia Kalubaka3Alla Kruk4Yuliya Diubo5Yuri Gogolev6Yuri Gogolev7Yevgeny Nikolaichik8Department of Molecular Biology, Belarusian State University, Minsk, BelarusFederal Research Center “Kazan Scientific Center of RAS”, Kazan Institute of Biochemistry and Biophysics, Kazan, RussiaLaboratory of Extreme Biology, Kazan Federal University Institute of Fundamental Medicine and Biology, Kazan, RussiaDepartment of Molecular Biology, Belarusian State University, Minsk, BelarusDepartment of Molecular Biology, Belarusian State University, Minsk, BelarusDepartment of Molecular Biology, Belarusian State University, Minsk, BelarusFederal Research Center “Kazan Scientific Center of RAS”, Kazan Institute of Biochemistry and Biophysics, Kazan, RussiaDepartment of Biochemistry, Biotechnology and Pharmacology, Kazan Federal University Institute of Fundamental Medicine and Biology, Kazan, RussiaDepartment of Molecular Biology, Belarusian State University, Minsk, BelarusPectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the relevant information is available only for related species and is rather limited. The PhoPQ two-component system, originally described in pectobacteria as PehRS, was previously shown to regulate a single gene, pehA. Using an insertional phoP mutant of Pectobacterium versatile (earlier—P. carotovorum), we demonstrate that PhoP regulates at least 115 genes with a majority of them specific for pectobacteria. The functions performed by PhoP-controlled genes include degradation, transport and metabolism of plant-derived carbon sources (polygalacturonate, arabinose-containing polysaccharides and citrate), modification of bacterial cell envelope and stress resistance. We also demonstrated PhoP involvement in establishing the order of plant cell wall decomposition and utilisation of the corresponding breakdown products. Based on experimental data and in silico analysis, we defined a PhoP binding site motif and provided proof for its universality in enteric bacteria. Scanning P. versatile genome for the locations of this motif suggested a much larger PhoP regulon enriched with the genes important for a plant pathogen, which makes PhoP a global virulence regulator. Potential PhoP targets include many regulatory genes and PhoP control over one of them, expI, was confirmed experimentally, highlighting the link between the PhoPQ two-component and quorum sensing systems. High concentrations of calcium and magnesium ions were found to abolish the PhoPQ-dependent transcription activation but did not relieve repression. Reduced PhoP expression and minimisation of PhoP dependence of regulon members’ expression in P. versatile cells isolated from potato tuber tissues suggest that PhoPQ system is a key switch of expression levels of multiple virulence-related genes fine-tuned to control the development of P. versatile-host plant pathosystem.https://www.frontiersin.org/articles/10.3389/fmicb.2020.621391/fullPectobacterium versatilePhoPQtwo-component systempectinarabinosecitrate |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Uljana Kravchenko Natalia Gogoleva Natalia Gogoleva Nastassia Kalubaka Alla Kruk Yuliya Diubo Yuri Gogolev Yuri Gogolev Yevgeny Nikolaichik |
spellingShingle |
Uljana Kravchenko Natalia Gogoleva Natalia Gogoleva Nastassia Kalubaka Alla Kruk Yuliya Diubo Yuri Gogolev Yuri Gogolev Yevgeny Nikolaichik The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems Frontiers in Microbiology Pectobacterium versatile PhoPQ two-component system pectin arabinose citrate |
author_facet |
Uljana Kravchenko Natalia Gogoleva Natalia Gogoleva Nastassia Kalubaka Alla Kruk Yuliya Diubo Yuri Gogolev Yuri Gogolev Yevgeny Nikolaichik |
author_sort |
Uljana Kravchenko |
title |
The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems |
title_short |
The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems |
title_full |
The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems |
title_fullStr |
The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems |
title_full_unstemmed |
The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems |
title_sort |
phopq two-component system is the major regulator of cell surface properties, stress responses and plant-derived substrate utilisation during development of pectobacterium versatile-host plant pathosystems |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2021-01-01 |
description |
Pectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the relevant information is available only for related species and is rather limited. The PhoPQ two-component system, originally described in pectobacteria as PehRS, was previously shown to regulate a single gene, pehA. Using an insertional phoP mutant of Pectobacterium versatile (earlier—P. carotovorum), we demonstrate that PhoP regulates at least 115 genes with a majority of them specific for pectobacteria. The functions performed by PhoP-controlled genes include degradation, transport and metabolism of plant-derived carbon sources (polygalacturonate, arabinose-containing polysaccharides and citrate), modification of bacterial cell envelope and stress resistance. We also demonstrated PhoP involvement in establishing the order of plant cell wall decomposition and utilisation of the corresponding breakdown products. Based on experimental data and in silico analysis, we defined a PhoP binding site motif and provided proof for its universality in enteric bacteria. Scanning P. versatile genome for the locations of this motif suggested a much larger PhoP regulon enriched with the genes important for a plant pathogen, which makes PhoP a global virulence regulator. Potential PhoP targets include many regulatory genes and PhoP control over one of them, expI, was confirmed experimentally, highlighting the link between the PhoPQ two-component and quorum sensing systems. High concentrations of calcium and magnesium ions were found to abolish the PhoPQ-dependent transcription activation but did not relieve repression. Reduced PhoP expression and minimisation of PhoP dependence of regulon members’ expression in P. versatile cells isolated from potato tuber tissues suggest that PhoPQ system is a key switch of expression levels of multiple virulence-related genes fine-tuned to control the development of P. versatile-host plant pathosystem. |
topic |
Pectobacterium versatile PhoPQ two-component system pectin arabinose citrate |
url |
https://www.frontiersin.org/articles/10.3389/fmicb.2020.621391/full |
work_keys_str_mv |
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