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Article: A Phosphate Uptake System Is Required for

Sattrapai, Nutthakan / Chaiprom, Usawadee / Lindow, Steven E / Chatnaparat, Tiyakhon

Molecular plant-microbe interactions : MPMI

2023 Volume 36, Issue 5, Page(s) 261–272

Abstract: The genes encoding the phosphate uptake system ... ...

Abstract	The genes encoding the phosphate uptake system in
MeSH term(s)	Glycine max/microbiology ; Phosphates ; Glycine ; Virulence/genetics ; Xanthomonas/genetics ; Xanthomonas/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Plant Diseases/microbiology
Chemical Substances	Phosphates ; Glycine (TE7660XO1C) ; Bacterial Proteins
Language	English
Publishing date	2023-03-20
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-11-22-0241-R
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Article ; Online: A Phosphate Uptake System Is Required for Xanthomonas citri pv. glycines Virulence in Soybean

Sattrapai, Nutthakan / Chaiprom, Usawadee / Lindow, Steven E. / Chatnaparat, Tiyakhon

Molecular Plant-Microbe Interactions. 2023 May, v. 36, no. 5 p.261-272

2023

Abstract: The genes encoding the phosphate uptake system in Xanthomonas citri pv. glycines 12-2 were previously found to be upregulated when in soybean leaves. This study thus explored the role of the phosphate uptake system on its virulence to soybean. While phoB ...

Abstract	The genes encoding the phosphate uptake system in Xanthomonas citri pv. glycines 12-2 were previously found to be upregulated when in soybean leaves. This study thus explored the role of the phosphate uptake system on its virulence to soybean. While phoB and pstSCAB mutants were greatly impaired in both inciting disease symptoms and growth in soybean, the virulence and growth in soybean of a phoU mutant was not reduced when compared with the wild-type strain. The expression of phoB and pstSCAB was highly induced in phosphate-deficient media. In addition, the expression of phoB, assessed with a fusion to a promoterless ice nucleation reporter gene, was greatly increased in soybean leaves, confirming that the soybean apoplast is a phosphorus-limited habitat for X. citri pv. glycines. Global gene expression profiles of phoB and phoU mutants of X. citri pv. glycines conducted under phosphate-limitation conditions in vitro, using RNA-seq, revealed that PhoB positively regulated genes involved in signal transduction, the xcs cluster type II secretion system, cell motility, and chemotaxis, while negatively regulating cell wall and membrane biogenesis, DNA replication and recombination and repair, and several genes with unknown function. PhoU also positively regulated the same genes involved in cell motility and chemotaxis. The severity of bacterial pustule disease was decreased in soybean plants grown under high phosphate fertilization conditions, demonstrating that high phosphate availability in soybean plants can affect infection by X. citri pv. glycines by modulation of the expression of phosphate uptake systems. Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
Keywords	DNA replication ; Xanthomonas citri ; apoplast ; biogenesis ; cell movement ; cell walls ; chemotaxis ; gene expression ; habitats ; ice nucleation ; mutants ; phosphates ; reporter genes ; secretion ; sequence analysis ; signal transduction ; soybeans ; virulence ; bacterial pustule ; phosphate regulon ; phosphorus ; soybean apoplast ; Xanthomonas citri pv. glycines
Language	English
Dates of publication	2023-05
Size	p. 261-272.
Publishing place	The American Phytopathological Society
Document type	Article ; Online
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-11-22-0241-R
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Article ; Online: The stringent response regulator (p) ppGpp mediates virulence gene expression and survival in Erwinia amylovora.

Yang, Ho-Wen / Yu, Menghao / Lee, Jae Hoon / Chatnaparat, Tiyakhon / Zhao, Youfu

BMC genomics

2020 Volume 21, Issue 1, Page(s) 261

Abstract: Background: The nucleotide second messengers, i.e., guanosine tetraphosphate and pentaphosphate [collectively referred to as (p) ppGpp], trigger the stringent response under nutrient starvation conditions and play an essential role in virulence in the ... ...

Abstract	Background: The nucleotide second messengers, i.e., guanosine tetraphosphate and pentaphosphate [collectively referred to as (p) ppGpp], trigger the stringent response under nutrient starvation conditions and play an essential role in virulence in the fire blight pathogen Erwinia amylovora. Here, we present transcriptomic analyses to uncover the overall effect of (p) ppGpp-mediated stringent response in E. amylovora in the hrp-inducing minimal medium (HMM). Results: In this study, we investigated the transcriptomic changes of the (p) ppGpp Conclusion: These findings suggested that in HMM environment, E. amylovora might use (p) ppGpp as a signal to activate virulence gene expression, and simultaneously mediate the balance between virulence and survival by negatively regulating DNA replication, translation, cell division, as well as biosynthesis of nucleotide, amino acid, fatty acid, and lipid. Therefore, (p) ppGpp could be a promising target for developing novel control measures to fight against this devastating disease of apples and pears.
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Biofilms/growth & development ; Chromosomes, Bacterial/genetics ; Erwinia amylovora/genetics ; Erwinia amylovora/pathogenicity ; Gene Expression Regulation, Bacterial/genetics ; Gene Expression Regulation, Bacterial/physiology ; Guanosine Pentaphosphate/genetics ; Guanosine Pentaphosphate/metabolism ; RNA-Seq ; Type III Secretion Systems/genetics ; Type III Secretion Systems/metabolism ; Virulence/genetics ; Virulence/physiology ; Virulence Factors/genetics ; Virulence Factors/metabolism
Chemical Substances	Bacterial Proteins ; Type III Secretion Systems ; Virulence Factors ; Guanosine Pentaphosphate (38918-96-6)
Language	English
Publishing date	2020-03-30
Publishing country	England
Document type	Journal Article
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/s12864-020-6699-5
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Article: The RNA-Binding Protein CsrA Controls Virulence in

Lee, Jae Hoon / Ancona, Veronica / Chatnaparat, Tiyakhon / Yang, Ho-Wen / Zhao, Youfu

Molecular plant-microbe interactions : MPMI

2019 Volume 32, Issue 10, Page(s) 1448–1459

Abstract: CsrA, an RNA-binding protein, binds to target transcripts and alters their translation or stability. ... ...

Abstract	CsrA, an RNA-binding protein, binds to target transcripts and alters their translation or stability. In
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Erwinia amylovora/genetics ; Erwinia amylovora/pathogenicity ; Gene Expression Regulation, Bacterial/genetics ; Mutation ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism ; Transcriptome ; Virulence/genetics
Chemical Substances	Bacterial Proteins ; RNA-Binding Proteins
Language	English
Publishing date	2019-08-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-03-19-0077-R
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Article: Global Pattern of Gene Expression of Xanthomonas axonopodis pv. glycines Within Soybean Leaves.

Chatnaparat, Tiyakhon / Prathuangwong, Sutruedee / Lindow, Steven E

Molecular plant-microbe interactions : MPMI

2016 Volume 29, Issue 6, Page(s) 508–522

Abstract: To better understand the behavior of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean within its host, its global transcriptome within soybean leaves was compared with that in a minimal medium in vitro, using deep ... ...

Abstract	To better understand the behavior of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean within its host, its global transcriptome within soybean leaves was compared with that in a minimal medium in vitro, using deep sequencing of mRNA. Of 5,062 genes predicted from a draft genome of X. axonopodis pv. glycines, 534 were up-regulated in the plant, while 289 were down-regulated. Genes encoding YapH, a cell-surface adhesin, as well as several others encoding cell-surface proteins, were down-regulated in soybean. Many genes encoding the type III secretion system and effector proteins, cell wall-degrading enzymes and phosphate transporter proteins were strongly expressed at early stages of infection. Several genes encoding RND multidrug efflux pumps were induced in planta and by isoflavonoids in vitro and were required for full virulence of X. axonopodis pv. glycines, as well as resistance to soybean phytoalexins. Genes encoding consumption of malonate, a compound abundant in soybean, were induced in planta and by malonate in vitro. Disruption of the malonate decarboxylase operon blocked growth in minimal media with malonate as the sole carbon source but did not significantly alter growth in soybean, apparently because genes for sucrose and fructose uptake were also induced in planta. Many genes involved in phosphate metabolism and uptake were induced in planta. While disruption of genes encoding high-affinity phosphate transport did not alter growth in media varying in phosphate concentration, the mutants were severely attenuated for growth in soybean. This global transcriptional profiling has provided insight into both the intercellular environment of this soybean pathogen and traits used by X. axonopodis pv. glycines to promote disease.
MeSH term(s)	Gene Expression Regulation, Bacterial ; Host-Pathogen Interactions/genetics ; Malonates/metabolism ; Phosphorus/metabolism ; Plant Leaves/microbiology ; Glycine max/microbiology ; Xanthomonas axonopodis/genetics ; Xanthomonas axonopodis/pathogenicity
Chemical Substances	Malonates ; Phosphorus (27YLU75U4W) ; malonic acid (9KX7ZMG0MK)
Language	English
Publishing date	2016-05-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-01-16-0007-R
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Comparative transcriptomic analysis of global gene expression mediated by (p) ppGpp reveals common regulatory networks in Pseudomonas syringae.

Liu, Jun / Yu, Menghao / Chatnaparat, Tiyakhon / Lee, Jae Hoon / Tian, Yanli / Hu, Baishi / Zhao, Youfu

BMC genomics

2020 Volume 21, Issue 1, Page(s) 296

Abstract: Background: Pseudomonas syringae is an important plant pathogen, which could adapt many different environmental conditions. Under the nutrient-limited and other stress conditions, P. syringae produces nucleotide signal molecules, i.e., guanosine tetra/ ... ...

Abstract	Background: Pseudomonas syringae is an important plant pathogen, which could adapt many different environmental conditions. Under the nutrient-limited and other stress conditions, P. syringae produces nucleotide signal molecules, i.e., guanosine tetra/pentaphosphate ((p)ppGpp), to globally regulate gene expression. Previous studies showed that (p) ppGpp played an important role in regulating virulence factors in P. syringae pv. tomato DC3000 (PstDC3000) and P. syringae pv. syringae B728a (PssB728a). Here we present a comparative transcriptomic analysis to uncover the overall effects of (p)ppGpp-mediated stringent response in P. syringae. Results: In this study, we investigated global gene expression profiles of PstDC3000 and PssB728a and their corresponding (p)ppGpp Conclusion: In this study, comparative transcriptomic analysis reveals common regulatory networks in both PstDC3000 and PssB728a mediated by (p) ppGpp in HMM. In both P. syringae systems, (p) ppGpp re-allocate cellular resources by suppressing multiple basic physiological activities and enhancing virulence gene expression, suggesting a balance between growth, survival and virulence. Our research is important in that due to similar global gene expression mediated by (p) ppGpp in both PstDC3000 and PssB728a, it is reasonable to propose that (p) ppGpp could be used as a target to develop novel control measures to fight against important plant bacterial diseases.
MeSH term(s)	Bacterial Proteins/genetics ; Cluster Analysis ; Gene Expression Profiling/methods ; Gene Expression Regulation, Bacterial ; Gene Regulatory Networks ; Guanosine Pentaphosphate/metabolism ; Lycopersicon esculentum/microbiology ; Plant Diseases/microbiology ; Pseudomonas syringae/classification ; Pseudomonas syringae/growth & development ; Pseudomonas syringae/pathogenicity ; Sequence Analysis, RNA ; Virulence Factors/genetics ; Whole Exome Sequencing
Chemical Substances	Bacterial Proteins ; Virulence Factors ; Guanosine Pentaphosphate (38918-96-6)
Language	English
Publishing date	2020-04-10
Publishing country	England
Document type	Journal Article
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/s12864-020-6701-2
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Global Pattern of Gene Expression of Xanthomonas axonopodis pv. glycines Within Soybean Leaves

Chatnaparat, Tiyakhon / Lindow Steven E / Prathuangwong Sutruedee

Molecular plant-microbe interactions. 2016 June, v. 29, no. 6

2016

Abstract	To better understand the behavior of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean within its host, its global transcriptome within soybean leaves was compared with that in a minimal medium in vitro, using deep sequencing of mRNA. Of 5,062 genes predicted from a draft genome of X. axonopodis pv. glycines, 534 were up-regulated in the plant, while 289 were down-regulated. Genes encoding YapH, a cell-surface adhesin, as well as several others encoding cell-surface proteins, were down-regulated in soybean. Many genes encoding the type III secretion system and effector proteins, cell wallâdegrading enzymes and phosphate transporter proteins were strongly expressed at early stages of infection. Several genes encoding RND multidrug efflux pumps were induced in planta and by isoflavonoids in vitro and were required for full virulence of X. axonopodis pv. glycines, as well as resistance to soybean phytoalexins. Genes encoding consumption of malonate, a compound abundant in soybean, were induced in planta and by malonate in vitro. Disruption of the malonate decarboxylase operon blocked growth in minimal media with malonate as the sole carbon source but did not significantly alter growth in soybean, apparently because genes for sucrose and fructose uptake were also induced in planta. Many genes involved in phosphate metabolism and uptake were induced in planta. While disruption of genes encoding high-affinity phosphate transport did not alter growth in media varying in phosphate concentration, the mutants were severely attenuated for growth in soybean. This global transcriptional profiling has provided insight into both the intercellular environment of this soybean pathogen and traits used by X. axonopodis pv. glycines to promote disease.
Keywords	adhesins ; carbon ; culture media ; enzymes ; fructose ; gene expression regulation ; high-throughput nucleotide sequencing ; isoflavonoids ; leaves ; messenger RNA ; metabolism ; mutants ; operon ; pathogens ; phosphates ; phytoalexins ; soybeans ; sucrose ; transcription (genetics) ; transcriptome ; transporters ; type III secretion system ; virulence ; Xanthomonas axonopodis pv. glycines
Language	English
Dates of publication	2016-06
Size	p. 508-522.
Publishing place	Molecular Plant-Microbe Interactions
Document type	Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094%2FMPMI-01-16-0007-R
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Conserved aspartate and lysine residues of RcsB are required for amylovoran biosynthesis, virulence, and DNA binding in Erwinia amylovora.

Ancona, Veronica / Chatnaparat, Tiyakhon / Zhao, Youfu

Molecular genetics and genomics : MGG

2015 Volume 290, Issue 4, Page(s) 1265–1276

Abstract: In Erwinia amylovora, the Rcs phosphorelay system is essential for amylovoran production and virulence. To further understand the role of conserved aspartate residue (D56) in the phosphor receiver (PR) domain and lysine (K180) residue in the function ... ...

Abstract	In Erwinia amylovora, the Rcs phosphorelay system is essential for amylovoran production and virulence. To further understand the role of conserved aspartate residue (D56) in the phosphor receiver (PR) domain and lysine (K180) residue in the function domain of RcsB, amino acid substitutions of RcsB mutant alleles were generated by site-directed mutagenesis and complementation of various rcs mutants were performed. A D56E substitution of RcsB, which mimics the phosphorylation state of RcsB, complemented the rcsB mutant, resulting in increased amylovoran production and gene expression, reduced swarming motility, and restored pathogenicity. In contrast, D56N and K180A or K180Q substitutions of RcsB did not complement the rcsB mutant. Electrophoresis mobility shift assays showed that D56E, but not D56N, K180Q and K180A substitutions of RcsB bound to promoters of amsG and flhD, indicating that both D56 and K180 are required for DNA binding. Interestingly, the RcsBD56E allele could also complement rcsAB, rcsBC and rcsABCD mutants with restored virulence and increased amylovoran production, indicating that RcsB phosphorylation is essential for virulence of E. amylovora. In addition, mutations of T904 and A905, but not phosphorylation mimic mutation of D876 in the PR domain of RcsC, constitutively activate the Rcs system, suggesting that phosphor transfer is required for activating the Rcs system and indicating both A905 and T904 are required for the phosphatase activity of RcsC. Our results demonstrated that RcsB phosphorylation and dephosphorylation, phosphor transfer from RcsC are essential for the function of the Rcs system, and also suggested that constitutive activation of the Rcs system could reduce the fitness of E. amylovora.
MeSH term(s)	Amino Acid Sequence ; Aspartic Acid/genetics ; Aspartic Acid/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Conserved Sequence/genetics ; DNA, Bacterial/metabolism ; Erwinia amylovora/genetics ; Erwinia amylovora/metabolism ; Erwinia amylovora/pathogenicity ; Gene Expression Regulation, Bacterial ; Genetic Complementation Test ; Lysine/genetics ; Lysine/metabolism ; Malus/microbiology ; Models, Genetic ; Mutagenesis, Site-Directed ; Mutation, Missense ; Operon ; Phosphorylation ; Plant Diseases/microbiology ; Polysaccharides, Bacterial/biosynthesis ; Promoter Regions, Genetic/genetics ; Protein Binding ; Pyrus/microbiology ; Reverse Transcriptase Polymerase Chain Reaction ; Signal Transduction/genetics ; Virulence/genetics
Chemical Substances	Bacterial Proteins ; DNA, Bacterial ; Polysaccharides, Bacterial ; amylovoran ; RcsB protein, Bacteria (127737-30-8) ; Aspartic Acid (30KYC7MIAI) ; Lysine (K3Z4F929H6)
Language	English
Publishing date	2015-08
Publishing country	Germany
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2044817-X
ISSN	1617-4623 ; 1617-4615
ISSN (online)	1617-4623
ISSN	1617-4615
DOI	10.1007/s00438-015-0988-8
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Article: The RNA-Binding Protein CsrA Controls Virulence in Erwinia amylovora by Regulating RelA, RcsB, and FlhD at the Posttranscriptional Level

Lee, Jae Hoon / Ancona, Veronica / Chatnaparat, Tiyakhon / Yang, Ho-wen / Zhao, Youfu

Molecular plant-microbe interactions. 2019 Oct., v. 32, no. 10

2019

Abstract: CsrA, an RNA-binding protein, binds to target transcripts and alters their translation or stability. In Erwinia amylovora, CsrA positively regulates the expression of type III secretion system (T3SS), exopolysaccharide amylovoran, and motility. In this ... ...

Abstract	CsrA, an RNA-binding protein, binds to target transcripts and alters their translation or stability. In Erwinia amylovora, CsrA positively regulates the expression of type III secretion system (T3SS), exopolysaccharide amylovoran, and motility. In this study, the global effect of CsrA and its noncoding small RNA (ncsRNA) csrB in E. amylovora was determined by RNA-seq, and potential molecular mechanisms of CsrA-dependent virulence regulation were examined. Transcriptomic analyses under the T3SS-inducing condition revealed that mutation in the csrA gene led to differential expression of more than 20% of genes in the genome. Among them, T3SS genes and those required for cell growth and viability were significantly downregulated. On the other hand, the csrB mutant exhibited significant upregulation of most major virulence genes, suggesting an antagonistic effect of csrB on CsrA targets. Direct interaction between CsrA protein and csrB was further confirmed through the RNA electrophoretic mobility shift assay (REMSA). However, no direct interaction between CsrA and hrpL and hrpS transcripts was detected, suggesting that HrpL and HrpS are not targets of CsrA, whereas three CsrA targets (relA, rcsB, and flhD) were identified and confirmed by REMSA, site-directed mutagenesis, and LacZ reporter gene assays. These findings might partially explain how CsrA positively controls E. amylovora virulence by targeting major regulators at the posttranscriptional level.
Keywords	cell growth ; Erwinia amylovora ; exopolysaccharides ; gel electrophoresis ; gene expression regulation ; messenger RNA ; mutants ; reporter genes ; RNA-binding proteins ; sequence analysis ; site-directed mutagenesis ; transcriptomics ; type III secretion system ; viability ; virulence
Language	English
Dates of publication	2019-10
Size	p. 1448-1459.
Publishing place	Molecular Plant-Microbe Interactions
Document type	Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-03-19-0077-R
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Many plant pathogenic Pseudomonas savastanoi pv glycinea isolates possess an inactive quorum sensing ahlR gene via a point mutation.

Degrassi, Giuliano / Mortato, Valentina / Devescovi, Giulia / Hoshino, Rodrigo / Chatnaparat, Tiyakhon / Kojic, Milan / Carpentieri-Pipolo, Valeria / Zhao, Youfu / Venturi, Vittorio

FEMS microbiology letters

2019 Volume 366, Issue 12

Abstract: Many plant bacterial pathogens monitor their group behaviour and their population density via production of N-acyl homoserine lactone signals which regulate the expression of several genes via the LuxI/R homologs. This regulatory network, termed quorum ... ...

Abstract	Many plant bacterial pathogens monitor their group behaviour and their population density via production of N-acyl homoserine lactone signals which regulate the expression of several genes via the LuxI/R homologs. This regulatory network, termed quorum sensing (QS), is present in the soybean bacterial pathogen Pseudomonas savastanoi pv glycinea (Psg). The sequenced genomes of two strains of Psg, race 4 and B076, contain an N-acyl homoserine lactone (AHL) based LuxI/R QS system named AhlI/R. While studying the QS system of Psg strains race 4 and B076 isolated in USA, LMG5066 in New Zealand and IBSBF355 in Brazil, we found that B076, LMG5066 and IBSBF355 possess a point mutation in the ahlR gene that causes a frameshift resulting in a truncated AhlR protein. Psg race 4 does not possess the mutation in ahlR and the QS system is functional. The same mutation in the ahlR gene was found to be also present in 9 of 19 Psg strains isolated from diseased soybean in Illinois. Phenotypic analysis of strains showed that swarming motility is repressed whereas phosphate solubilisation was activated by QS in Psg. Analysing the secretome, we also found that four proteins were under QS regulation.
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Gene Expression Regulation, Bacterial/genetics ; Point Mutation/genetics ; Pseudomonas/genetics ; Pseudomonas/pathogenicity ; Quorum Sensing/genetics ; Quorum Sensing/physiology ; Glycine max/microbiology
Chemical Substances	Bacterial Proteins
Language	English
Publishing date	2019-07-22
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	752343-9
ISSN	1574-6968 ; 0378-1097
ISSN (online)	1574-6968
ISSN	0378-1097
DOI	10.1093/femsle/fnz149
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