Getting across--bacterial type III effector proteins on their way to the plant cell

Abstract

Pathogenicity of most Gram-negative bacterial plant pathogens depends on hrp (hypersensitive response and pathogenicity) genes, which control the ability to cause disease and to elicit specific defense responses in resistant plants. hrp genes encode a specialized type III secretion (TTS) system that mediates the vectorial delivery of bacterial effector proteins across both bacterial membranes as well as across the eukaryotic plasma membrane into the host cell cytosol. One well-studied effector protein is AvrBs3 from Xanthomonas campestris pv. vesicatoria, the causal agent of bacterial spot in pepper and tomato. AvrBs3 induces hypertrophy symptoms in susceptible plants and triggers a resistance gene-specific cell death reaction in resistant plants. Intriguingly, AvrBs3 has characteristic features of eukaryotic transcription factors, suggesting that it modulates the host's transcriptome. Here, we discuss the TTS system of X.campestris pv. vesicatoria in the light of current knowledge on type III-dependent protein secretion in plant pathogenic bacteria.

Fig. 1. Schematic overview of the hrp gene clusters and the left flanking regions from X.campestris pv. vesicatoria (group II) and P.syringae pv. tomato DC3000 (group I). The regions contain hrp, hrc and hpa genes (represented in blue, red and green, respectively). Arrows indicate the direction of transcription. Black dots and squares refer to the presence of PIP and hrp boxes, respectively. Hatched regions correspond to sequences with low G + C content; yellow regions refer to mobile genetic elements.

Fig. 2. Model for hrp gene regulation and type III secretion in X.campestris pv. vesicatoria. (A) A so far uncharacterized signal transduction system in the bacterial envelope (indicated by a question mark) senses environmental stimuli and transduces the signal to HrpG. HrpG activates the expression of hrpA and, via HrpX, the expression of hrpB–hrpF as well as of a number of xop genes. (B) Expression of hrp genes is essential for the formation of the TTS apparatus, which spans both bacterial membranes and mediates secretion of Hrp and effector proteins. The TTS apparatus is associated with the Hrp pilus, which presumably spans the cell wall (200 nm thick; not drawn to scale). The major subunit of the Hrp pilus is HrpE1. Translocation of effector proteins across the plant plasma membrane requires HrpF, the putative pore-forming component of the type III translocon. Effector proteins are targeted to different locations in the plant cell and presumably modulate cellular processes leading to disease symptom formation in susceptible plants. In resistant plants, effector proteins (designated Avr proteins) can be recognized and trigger the activation of specific defense responses. CW, cell wall; IM, inner membrane; OM, outer membrane; PM, plasma membrane.

Fig. 3. Proposed model for the molecular mechanisms underlying virulence and avirulence activity of AvrBs3 from X.campestris pv. vesicatoria. Characteristic features of AvrBs3 are the central 17.5 nearly identical 34 amino acid repeats, two functional C-terminal nuclear localization signals (NLSs) and an acidic activation domain (AAD). Delivery of AvrBs3 into the host cell is mediated by the TTS system. In the plant cell, the NLSs bind to importin α, which together with importin β targets AvrBs3 to the plant cell nucleus. Direct or indirect (via a target protein X) interaction of AvrBs3 with the plant DNA leads to the modulation of the host’s transcriptome and presumably results in hypertrophy, a disease symptom in susceptible plants. In resistant plants, specific plant defense responses are induced upon recognition of AvrBs3 by the R protein Bs3 (Bs, bacterial spot).