Substrate recognition of type III secretion machines -testing the RNA signal hypothesis

Sorg, Joseph A.; Miller, Nathan C.; Schneewind, Olaf

doi:10.1111/j.1462-5822.2005.00563.x

Cited by 40 publications

(46 citation statements)

References 87 publications

(124 reference statements)

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“…Despite 15 years of intense research, and even with the three-dimensional structures of the N termini of TTS substrates at hand, the nature of the TTS signal is still enigmatic (24). The fact that the N termini of these substrates do not share any obvious consensus sequence at the primary sequence level makes it difficult to understand how TTS substrates are recognized and secreted even by heterologous TTS machineries (24). Comparisons of Yersinia TTS substrates indicated that a more general property serves as secretion signal.…”

Section: Discussionmentioning

confidence: 99%

Positive Selection of the Hrp Pilin HrpE of the Plant Pathogen Xanthomonas

Weber

Koebnik

2006

J Bacteriol

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The plant-pathogenic bacterium Xanthomonas campestris pv. vesicatoria possesses a type III secretion (TTS) system which is encoded by the 23-kb hrp (hypersensitive response and pathogenicity) gene cluster. The TTS system is necessary for pathogenicity in susceptible hosts and induction of the hypersensitive response in resistant plants. At the cell surface, the TTS system is associated with an extracellular filamentous structure, the Hrp pilus, which serves as a conduit for the transfer of bacterial proteins into the plant cell cytosol. The major pilus component, the HrpE pilin, is unique to xanthomonads. Previous work showed that HrpE contains two regions: a hypervariable surface-exposed domain, including the N-terminal secretion signal, and a Cterminal polymerization domain. In this study, the evolutionary rate of the hrpE gene was analyzed. Twenty-one alleles were cloned, sequenced, and compared with five known hrpE alleles. The ratio of synonymous (K s ) and nonsynonymous (K a ) substitution rates shows that parts of the HrpE N terminus are subjected to positive selection and the C terminus is subjected to purifying selection. The trade-off between positive and purifying selection at the very-N terminus allowed us to ascertain the amphipathic ␣-helical nature of the TTS signal. This is the first report of a surface structure from a plant-pathogenic bacterium that evolved under the constraint of positive selection and hints to the evolutionary adaptation of this extracellular appendage to avoid recognition by the plant defense surveillance system.The type III secretion (TTS) system is a hallmark of many gram-negative bacterial pathogens. This specialized secretion system is responsible for the transport of proteins across the two bacterial membranes, across the host cell plasma membrane, and in some cases across the plant cell wall into the host cell interior. A defect in this system leads to a complete loss of bacterial pathogenicity, as demonstrated for the animal pathogens Yersinia spp., Shigella spp., Salmonella spp., and enteropathogenic and enterohemorrhagic Escherichia coli and for the plant pathogens Ralstonia solanacearum, Pseudomonas syringae, Erwinia spp., and Xanthomonas spp. (10). TTS systems are encoded by approximately 20 genes, 11 of which are conserved between different bacterial species, thus suggesting that they constitute the core of the secretion machinery. While the TTS apparatus is conserved, the secreted substrates differ considerably. The recognition of these proteins by the TTS system is still not well understood. The TTS signal is located in the first 15 to 20 amino acids of the protein and is not conserved on the amino acid level (17, 23). Additionally, the 5Ј region of the corresponding mRNA may contribute to recognition by the secretion machinery (1).Our laboratory studies the plant pathogen Xanthomonas campestris pathovar vesicatoria, which is the causal agent of bacterial spot disease in pepper and tomato plants. The TTS system of X. campestris pv. vesicatoria is encoded by the...

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Section: Discussionmentioning

confidence: 99%

Positive Selection of the Hrp Pilin HrpE of the Plant Pathogen Xanthomonas

Weber

Koebnik

2006

J Bacteriol

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“…Studies from various organisms show numerous silent mutations within the signal sequence have no or little effect on export, implying that the export signal is predominantly encoded in the amino acid sequence [177][178][179]. However, it has also been shown that frameshifted mRNA export sequences can still support the export of substrates and that the mRNA sequence around the start codon plays a role in export ( [180,181], reviewed in [182]), indicating that the effects of mRNA and protein sequence on targeting may be additive.…”

Section: Export Signalsmentioning

confidence: 99%

Type III secretion systems: the bacterial flagellum and the injectisome

Diepold

Armitage

2015

Phil. Trans. R. Soc. B

185

175

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One contribution of 12 to a theme issue 'The bacterial cell envelope'. The flagellum and the injectisome are two of the most complex and fascinating bacterial nanomachines. At their core, they share a type III secretion system (T3SS), a transmembrane export complex that forms the extracellular appendages, the flagellar filament and the injectisome needle. Recent advances, combining structural biology, cryo-electron tomography, molecular genetics, in vivo imaging, bioinformatics and biophysics, have greatly increased our understanding of the T3SS, especially the structure of its transmembrane and cytosolic components, the transcriptional, post-transcriptional and functional regulation and the remarkable adaptivity of the system. This review aims to integrate these new findings into our current knowledge of the evolution, function, regulation and dynamics of the T3SS, and to highlight commonalities and differences between the two systems, as well as their potential applications.

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“…There is little consensus between secretion signals of different bacteria, and it is thought that the protein sequence of these N-terminal secretion signals possesses a common secondary structure that allows proteins to be recruited to the T3SS (Stebbins, 2005). However, the fact that frameshift mutations of the DNA sequence corresponding to the first 15 amino acids of certain effectors still allow protein secretion has led others to propose an RNA-mediated secretion signal for transcripts of effectors to be recruited and effectors to be translated and secreted simultaneously (Ramamurthi & Schneewind, 2003;Sorg et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…delivery outside the bacterial cell) or translocation (i.e. delivery into host cells) in animal bacterial pathogens is accomplished in part by a short N-terminal secretion signal often located within the first 15-20 amino acids of type III (T3)-secreted proteins (Lilic et al, 2006;Lloyd et al, 2002;Sorg et al, 2005). The exact means by which this N-terminal signal targets proteins for secretion and translocation is unclear.…”

Section: Introductionmentioning

confidence: 99%

Secretion and translocation signals and DspB/F-binding domains in the type III effector DspA/E of Erwinia amylovora

Carpenter

Hayes

et al. 2010

Microbiology

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DspA/E is a type III effector of Erwinia amylovora, the bacterial pathogen that causes fire blight disease in roseaceous plants. This effector is indispensable for disease development, and it is translocated into plant cells. A DspA/E-specific chaperone, DspB/F, is necessary for DspA/E secretion and possibly for its translocation. In this work, DspB/F-binding sites and secretion and translocation signals in the DspA/E protein were determined. Based on yeast two-hybrid assays, DspB/F was found to bind DspA/E within the first 210 amino acids of the protein. Surprisingly, both DspB/F and OrfA, the putative chaperone of Eop1, also interacted with the C-terminal 1059 amino acids of DspA/E; this suggests another chaperone-binding site. Secretion and translocation assays using serial N-terminal lengths of DspA/E fused with the active form of AvrRpt2 revealed that at least the first 109 amino acids, including the first N-terminal chaperone-binding motif and DspB/F, were required for efficient translocation of DspA/E, although the first 35 amino acids were sufficient for its secretion and the presence of DspB/F was not required. These results indicate that secretion and translocation signals are present in the N terminus of DspA/E, and that at least one DspB/F-binding motif is required for efficient translocation into plant cells.

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Substrate recognition of type III secretion machines -testing the RNA signal hypothesis

Cited by 40 publications

References 87 publications

Positive Selection of the Hrp Pilin HrpE of the Plant Pathogen Xanthomonas

Positive Selection of the Hrp Pilin HrpE of the Plant Pathogen Xanthomonas

Type III secretion systems: the bacterial flagellum and the injectisome

Secretion and translocation signals and DspB/F-binding domains in the type III effector DspA/E of Erwinia amylovora

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