Chapter 14 : Role of the Type III Protein Secretion System in Bacterial Infection of Plants

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In the past two decades, research into the molecular basis of bacterial pathogenesis has led to the conclusion that although different bacteria may use unique mechanisms to subvert hosts, a few strategies are common. One striking example is the discovery that many plant and animal bacterial pathogens contain members of a family of protein secretion systems classified as type III. The type III secretion system (TTSS) supramolecular structures in both mammalian and plant pathogenic bacteria have been characterized. The central importance of the TTSSs in mammalian and plant bacterial pathogenesis is underscored by the finding that a defect in this system often leads to a complete loss of bacterial pathogenicity. Plant pathogenic bacteria encounter a unique eukaryotic cell type that is enveloped by a cell wall; they multiply predominantly in the intercellular space outside of the plant cell wall and are therefore extracellular pathogen. Plant basal defense is associated with the induction of certain general defense genes, the production of antimicrobial phytoalexins, and the fortification of plant cell walls, which involves the localized deposition of callose (β-1,3-glucan) and other compounds in the plant cell wall. Recent studies show that certain virulent strains have found ways to break down gene-for-gene resistance and expand the host range at the cultivar level. TTSS effectors appear to be highly evolved microbial molecules that have adapted to carry out precise functions on specific host proteins.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
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Image of FIGURE 1

Model for the activation and inactivation of basal defenses during subsp. DC3000 infection of susceptible plants. PAMPs from TTSS-defective mutants activate basal defense in an SA-independent manner. In the case of flagellin, perception is mediated by the FLS2 receptor, the signal is transduced via the MAPK3/6 pathway, and basal defense is activated ( ). In the ΔCEL mutant, the AvrPto class of effectors inactivates the SA-independent basal defense. However, the host cell partially overcomes the AvrPto-mediated inactivation of SA-independent basal defense and activates an SA-dependent basal defense pathway ( ). The bacterial factors involved in this SA-dependent activation are not known, but they may be type III effectors or the type III secretion process per se. In subsp. DC3000, HopM1 and AvrE inactivate the SA-dependent basal defense and promote disease-associated host cell death (necrosis). MAPKK, MAPK kinase; MAPKKK, MAPK kinase kinase. Plus and minus signs indicate degrees of effectiveness of host defense and bacterial virulence. Reprinted from ( ) with permission of the publisher.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
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Image of FIGURE 2

Model for the virulence and avirulence functions of AvrRpt2, AvrRpm1, and RIN4 in In a susceptible plant (left), RIN4 negatively regulates basal defense (line 1), which is activated by PAMPs via the corresponding receptors (e.g., FLS2 for flagellin). The effector AvrRpm1 or AvrRpt2 is injected into an cell via the TTSS. The binding of AvrRpm1 to RIN4 induces RIN4 phosphorylation (P), which may augment the ability of RIN4 to suppress basal defense, via an unknown mechanism (line 2). AvrRpt2 cleaves RIN4. It is not known how the cleavage of RIN4 would enhance the suppressor function, unless the cleavage products are more potent as suppressors (line 3). AvrRpt2 targets multiple host proteins ( ), so its defense suppression function may be exerted via additional mechanisms ( ). In a resistant plant (right), besides its role in suppressing basal defense (data not shown), RIN4 is guarded by RPS2 and/or RPM1, which is in an inactive state ( ). The virulence action of AvrRpt2 (proteolysis) or AvrRpm1 (phosphorylation) on RIN4 activates the cognate resistance proteins and subsequent R protein-mediated resistance (arrows 4). In the presence of both AvrRpt2 and AvrRpm1, AvrRpm1/RPM1-dependent resistance is prevented because of the AvrRpt2-mediated removal of RIN4. At present, the molecular interplay between RIN4, Avr-Rpt2/Avr-Rpm1, and RPM1/RPS2 provides the most crucial evidence for the so-called guard hypothesis ( ), in which plant disease resistance proteins (e.g., RPM1 and RPS2) activate gene-for-gene resistance by monitoring host proteins (e.g., RIN4) that are targeted by cognate pathogen effector proteins (e.g., AvrRpm1 and AvrRPt2). Reprinted from ( ) with permission of the publisher.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
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Image of FIGURE 3

Schematic diagram depicting a putative polarized vesicle-trafficking pathway, in which AtMIN7 is a key component. The AtMIN7-dependent pathway is associated with localized plant immune responses, including the formation of callose deposits and probably the release of antimicrobial phytoalexins (dots in the papilla and plant cell wall) and cell wall thickening. DC3000 and presumably other strains inject HopM1 into the host cell ( ). Once inside the host cell, HopM1 is associated with an endomembrane compartment, binds to AtMIN7 through the N terminus, and promotes the ubiquitination and proteasome-dependent degradation of AtMIN7 and presumably other AtMIN proteins. BFA may mimic the effect of HopM1 by inhibiting the guanosine nucleotide exchange factor activity of the Sec7 protein family, of which AtMIN7 is a member. Golgi, Golgi apparatus; ER, endoplasmic reticulum; Ub, ubiquitin. Reprinted from ( ) with permission of the publisher.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
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