The C-terminal domain of the type III secretion chaperone HpaB contributes to dissociation of chaperone-effector complex in Xanthomonas campestris pv. campestris

Gan, Yong-Liang; Yang, Liyan; Lü, Yuan; Li, Wan-Lian; Liang, Xuelian; Jiang, Wei; Jiang, Guo‐Feng; Hang, Xiao-Hong; Yang, Mei; Tang, Ji‐Liang; Jiang, Bo-Le

doi:10.1371/journal.pone.0246033

Cited by 2 publications

(3 citation statements)

References 63 publications

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“…It was, therefore, proposed that HpaB releases XopB from the membrane in order to facilitate its export by the T3S system. HpaB was previously shown to interact with and to promote the translocation of different T3Es ( Büttner et al, 2004 ; Schulze et al, 2012 ; Lonjon et al, 2017 ; Scheibner et al, 2018 ; Gan et al, 2021 ). Notably, however, HpaB also interacts with several cytoplasmic components of the T3S system, suggesting an association with the sorting platform ( Büttner et al, 2004 ; Lorenz and Büttner, 2009 ).…”

Section: Introductionmentioning

confidence: 99%

“…Notably, however, HpaB also interacts with several cytoplasmic components of the T3S system, suggesting an association with the sorting platform ( Büttner et al, 2004 ; Lorenz and Büttner, 2009 ). HpaB-effector complexes are presumably dissociated by the ATPase HrcN, which might thus facilitate the entry of effectors into the inner transport channel ( Lorenz and Büttner, 2009 ; Gan et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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Recognition of a translocation motif in the regulator HpaA from Xanthomonas euvesicatoria is controlled by the type III secretion chaperone HpaB

Drehkopf

Otten²,

Büttner³

2022

Front. Plant Sci.

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The Gram-negative plant-pathogenic bacterium Xanthomonas euvesicatoria is the causal agent of bacterial spot disease in pepper and tomato plants. Pathogenicity of X. euvesicatoria depends on a type III secretion (T3S) system which translocates effector proteins into plant cells and is associated with an extracellular pilus and a translocon in the plant plasma membrane. Effector protein translocation is activated by the cytoplasmic T3S chaperone HpaB which presumably targets effectors to the T3S system. We previously reported that HpaB is controlled by the translocated regulator HpaA which binds to and inactivates HpaB during the assembly of the T3S system. In the present study, we show that translocation of HpaA depends on the T3S substrate specificity switch protein HpaC and likely occurs after pilus and translocon assembly. Translocation of HpaA requires the presence of a translocation motif (TrM) in the N-terminal region. The TrM consists of an arginine-and proline-rich amino acid sequence and is also essential for the in vivo function of HpaA. Mutation of the TrM allowed the translocation of HpaA in hpaB mutant strains but not in the wild-type strain, suggesting that the recognition of the TrM depends on HpaB. Strikingly, the contribution of HpaB to the TrM-dependent translocation of HpaA was independent of the presence of the C-terminal HpaB-binding site in HpaA. We propose that HpaB generates a recognition site for the TrM at the T3S system and thus restricts the access to the secretion channel to effector proteins. Possible docking sites for HpaA at the T3S system were identified by in vivo and in vitro interaction studies and include the ATPase HrcN and components of the predicted cytoplasmic sorting platform of the T3S system. Notably, the TrM interfered with the efficient interaction of HpaA with several T3S system components, suggesting that it prevents premature binding of HpaA. Taken together, our data highlight a yet unknown contribution of the TrM and HpaB to substrate recognition and suggest that the TrM increases the binding specificity between HpaA and T3S system components.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Recognition of a translocation motif in the regulator HpaA from Xanthomonas euvesicatoria is controlled by the type III secretion chaperone HpaB

Drehkopf

Otten²,

Büttner³

2022

Front. Plant Sci.

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“…In addition to discharging virulence factors, T3SS also plays a key role in host cell sensing and modulation of gene expression post-attachment to the eukaryotic host. This function is primarily regulated by the T3SS-specific chaperone CesT/HpaB ( 73 , 74 ), which was downregulated 2.8-fold in the mutant strain at 16 hours. The mRNA levels of four genes coding for type III effector proteins, HpaF, XopK, AvrXv4, and F-box, were significantly decreased between 2.5-fold and 1.8-fold in the mutant strain at 16 hours.…”

Section: Resultsmentioning

confidence: 99%

Transcriptome profiling of type VI secretion system core gene tssM mutant of Xanthomonas perforans highlights regulators controlling diverse functions ranging from virulence to metabolism

Ramamoorthy,

Pena,

Ghosh

et al. 2024

Microbiol Spectr

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Type VI secretion system (T6SS) is a versatile, contact-dependent contractile nano-weapon in Gram-negative bacteria that fires proteinaceous effector molecules directly into prokaryotic and eukaryotic cells aiding in manipulation of the host and killing of competitors in complex niches. In plant pathogenic xanthomonads, T6SS has been demonstrated to play these diverse roles in individual pathosystems. However, the molecular network underlying the regulation of T6SS is still elusive in Xanthomonas spp. To bridge this knowledge gap, we conducted an in vitro transcriptome screen using plant apoplast mimicking minimal medium, XVM2 medium, to decipher the effect of tssM deletion, a core gene belonging to T6SS-cluster i3*, on the regulation of gene expression in Xanthomonas perforans strain AL65. Transcriptomic data revealed that a total of 277 and 525 genes were upregulated, while 307 and 392 genes were downregulated in the mutant strain after 8 and 16 hours of growth in XVM2 medium. The transcript abundance of several genes associated with flagellum and pilus biogenesis as well as type III secretion system was downregulated in the mutant strain. Deletion of tssM of cluster-i3* resulted in upregulation of several T6SS genes belonging to cluster-i3*** and genes involved in biofilm and cell wall biogenesis. Similarly, transcription regulators like rpoN , Pho regulon, rpoE , and csrA were identified to be upregulated in the mutant strain. Our results suggest that T6SS modulates the expression of global regulators like csrA , rpoN , and pho regulons, triggering a signaling cascade, and co-ordinates the expression of suite of virulence factors, stress response genes, and metabolic genes. IMPORTANCE T6SS has received attention due to its significance in mediating interorganismal competition through contact-dependent release of effector molecules into prokaryotic and eukaryotic cells. Reverse-genetic studies have indicated the role of T6SS in virulence in a variety of plant pathogenic bacteria, including the one studied here, Xanthomonas . However, it is not clear whether such effect on virulence is merely due to a shift in the microbiome-mediated protection or if T6SS is involved in a complex virulence regulatory network. In this study, we conducted in vitro transcriptome profiling in minimal medium to decipher the signaling pathways regulated by tssM-i3* in X. perforans AL65. We show that TssM-i3* regulates the expression of a suite of genes associated with virulence and metabolism either directly or indirectly by altering the transcription of several regulators. These findings further expand our knowledge on the intricate molecular circuits regulated by T6SS in phytopathogenic bacteria.

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The C-terminal domain of the type III secretion chaperone HpaB contributes to dissociation of chaperone-effector complex in Xanthomonas campestris pv. campestris

Cited by 2 publications

References 63 publications

Recognition of a translocation motif in the regulator HpaA from Xanthomonas euvesicatoria is controlled by the type III secretion chaperone HpaB

Recognition of a translocation motif in the regulator HpaA from Xanthomonas euvesicatoria is controlled by the type III secretion chaperone HpaB

Transcriptome profiling of type VI secretion system core gene tssM mutant of Xanthomonas perforans highlights regulators controlling diverse functions ranging from virulence to metabolism

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