Abstract
The γ-proteobacterial plant pathogen Pseudomonas syringae pv. tomato DC3000 uses the type III secretion system to inject ca. 28 Avr/Hop effector proteins into plants, which enables the bacterium to grow from low inoculum levels to produce bacterial speck symptoms in tomato, Arabidopsis thaliana, and (when lacking hopQ1-1) Nicotiana benthamiana. The effectors are collectively essential but individually dispensable for the ability of the bacteria to defeat defenses, grow, and produce symptoms in plants. Eighteen of the effector genes are clustered in six genomic islands/islets. Combinatorial deletions involving these clusters and two of the remaining effector genes revealed a redundancy-based structure in the effector repertoire, such that some deletions diminished growth in N. benthamiana only in combination with other deletions. Much of the ability of DC3000 to grow in N. benthamiana was found to be due to five effectors in two redundant-effector groups (REGs), which appear to separately target two high-level processes in plant defense: perception of external pathogen signals (AvrPto and AvrPtoB) and deployment of antimicrobial factors (AvrE, HopM1, HopR1). Further support for the membership of HopR1 in the same REG as AvrE was gained through bioinformatic analysis, revealing the existence of an AvrE/DspA/E/HopR effector superfamily, which has representatives in virtually all groups of proteobacterial plant pathogens that deploy type III effectors.
Highlights
Many bacterial pathogens of plants and animals disarm and remodel host cells by injecting large repertoires of effectors via the type III secretion system (T3SS) [1,2]
The DC3000 genome has been fully sequenced [8]; the DC3000 T3SS, which is encoded by hrp/hrc genes, is being intensively investigated [9,10,11,12]; multiple approaches have been used to firmly establish the effector repertoire [13,14,15]; the molecular function of several of these effectors in plants has been determined [16,17,18]; DC3000 can infect the experimentally tractable plants Arabidopsis thaliana and Nicotiana benthamiana [19,20]; and this strain has become the pathogen of choice for plant biologists probing the plant defense systems thought to be targeted by the effectors
Pseudomonas syringae is a Gram-negative plant pathogen that defeats plant defenses through effector proteins that are injected into plant cells via the type III secretion system
Summary
Many bacterial pathogens of plants and animals disarm and remodel host cells by injecting large repertoires of effectors via the type III secretion system (T3SS) [1,2]. The potential extent of such redundancy is highlighted by recent reports that enterohemorrhagic Escherichia coli 0157:H7 may inject 39 effectors into animal cells via the T3SS and that fungal and oomycete pathogens, using alternative protein translocation pathways, may deliver hundreds of effectors into plant cells [4,5,6,7]. Tomato DC3000, which causes bacterial speck of tomato, is an excellent model for investigating the possible operation of type III effector repertoires as systems. The DC3000 genome has been fully sequenced [8]; the DC3000 T3SS, which is encoded by hrp/hrc (hypersensitive response and pathogenicity or conserved) genes, is being intensively investigated [9,10,11,12]; multiple approaches have been used to firmly establish the effector repertoire [13,14,15]; the molecular function of several of these effectors in plants has been determined [16,17,18]; DC3000 can infect the experimentally tractable plants Arabidopsis thaliana and Nicotiana benthamiana [19,20]; and this strain has become the pathogen of choice for plant biologists probing the plant defense systems thought to be targeted by the effectors
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