Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia

Genome Center and Department of Plant Sciences, University of California, Davis, California 95616, USA.
Plant physiology (Impact Factor: 6.84). 08/2009; 150(4):1733-49. DOI: 10.1104/pp.109.140251
Source: PubMed


Bacterial plant pathogens manipulate their hosts by injection of numerous effector proteins into host cells via type III secretion systems. Recognition of these effectors by the host plant leads to the induction of a defense reaction that often culminates in a hypersensitive response manifested as cell death. Genes encoding effector proteins can be exchanged between different strains of bacteria via horizontal transfer, and often individual strains are capable of infecting multiple hosts. Host plant species express diverse repertoires of resistance proteins that mediate direct or indirect recognition of bacterial effectors. As a result, plants and their bacterial pathogens should be considered as two extensive coevolving groups rather than as individual host species coevolving with single pathovars. To dissect the complexity of this coevolution, we cloned 171 effector-encoding genes from several pathovars of Pseudomonas and Ralstonia. We used Agrobacterium tumefaciens-mediated transient assays to test the ability of each effector to induce a necrotic phenotype on 59 plant genotypes belonging to four plant families, including numerous diverse accessions of lettuce (Lactuca sativa) and tomato (Solanum lycopersicum). Known defense-inducing effectors (avirulence factors) and their homologs commonly induced extensive necrosis in many different plant species. Nonhost species reacted to multiple effector proteins from an individual pathovar more frequently and more intensely than host species. Both homologous and sequence-unrelated effectors could elicit necrosis in a similar spectrum of plants, suggesting common effector targets or targeting of the same pathways in the plant cell.

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    • "Toward this goal, a collection of cloned R3bv2 effectors was previously used in Agrobacterium-mediated expression to identify potential sources of resistance among tomato, pepper, and lettuce accessions and N. benthamiana (Wroblewski et al. 2009). We extended the search here to two eggplant genotypes: MM853 found to be resistant to most R. solanacearum strains, including R3bv2 strains, and the susceptible MM738 genotype (Lebeau et al. 2011). "
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    ABSTRACT: Phylogeographic studies inform about routes of pathogen dissemination and are instrumental for improving import/export controls. Genomes of seventeen isolates of the bacterial wilt and potato brown rot pathogen Ralstonia solanacearum race 3 biovar 2 (R3bv2), a select agent in the USA, were thus analyzed to get insight into the phylogeography of this pathogen. Thirteen of fourteen isolates from Europe, Africa, and Asia were found to belong to a single clonal lineage while isolates from South America were genetically diverse and carried ancestral alleles at the analyzed genomic loci consistent with a South American origin of R3bv2. The R3bv2 isolates share a core repertoire of thirty-one type III-secreted effector genes representing excellent candidates to be targeted with resistance genes in breeding programs to develop durable disease resistance. Towards this goal, 27 R3bv2 effectors were tested in eggplant, tomato, pepper, tobacco, and lettuce for induction of a hypersensitive-like response indicative of recognition by cognate resistance receptors. Fifteen effectors, eight of them core effectors, triggered a response in one or more plant species. These genotypes may harbor resistance genes that could be identified and mapped, cloned and expressed in tomato or potato, for which sources of genetic resistance to R3bv2 are extremely limited.
    Phytopathology 02/2015; 105(5). DOI:10.1094/PHYTO-12-14-0373-R · 3.12 Impact Factor
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    • "The efficient plant defense strategy, hypersensitive cell death, is induced when HopQ1 is transiently expressed in tobacco (Fig. 8A), in contrast to the severe chloroses triggered by the effector in N. benthamiana leaves (Wroblewski et al., 2009). To determine whether modification of the 14-3-3 binding site is critical for HopQ1 recognition by the plant immune system, tobacco leaves were infiltrated with Agrobacterium tumefaciens "
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    ABSTRACT: HopQ1, a type III effector secreted by Pseudomonas syringae pv. phaseolicola, is widely conserved among diverse genera of plant bacteria. It promotes the development of halo blight in common bean. However, when this same effector is injected into Nicotiana benthamiana cells, it is recognized by the immune system and prevents infection. Although the ability to synthesize HopQ1 determines host specificity, the role it plays inside plant cells remains unexplored. Following transient expression in planta, HopQ1 was shown to co-purify with host 14-3-3 proteins. The physical interaction between HopQ1 and 14-3-3a was confirmed in planta using FRET-FLIM techniques. Moreover, mass spectrometric (LC-MS-MS/MS) analyses detected specific phosphorylation of the canonical 14-3-3 binding site (RSXpSXP, pS denotes phosphoserine) located in the N-terminal region of HopQ1. Amino acid substitution within this motif abrogated the association and led to altered subcellular localization of HopQ1. In addition, the mutated HopQ1 protein showed reduced stability in planta. These data suggest that the association between host 14-3-3 proteins and HopQ1 is important for modulating the properties of this bacterial effector.
    Plant physiology 02/2013; 161(4). DOI:10.1104/pp.112.209023 · 6.84 Impact Factor
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    • "Both PTI and ETI can limit the growth of P. syringae across a wide variety of hosts (Ferrante et al. 2009; Ham et al. 2007; Li et al. 2005; Lin and Martin 2007; Perchepied et al. 2006; Takeuchi et al. 2003; Wen et al. 2010; Wroblewski et al. 2009). For example, transfer of the EFR receptor from Arabidopsis to Nicotiana benthamiana can restrict the growth of previously pathogenic strains (Lacombe et al. 2010), while diversity in flagellar proteins across strains contributes to immune evasion (Li et al. 2005; Takeuchi et al. 2003). "
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    ABSTRACT: Biotrophic phytopathogens are typically limited to their adapted host range. In recent decades, investigations have teased apart the general molecular basis of intraspecific variation for innate immunity of plants, typically involving receptor proteins that enable perception of pathogen-associated molecular patterns or avirulence elicitors from the pathogen as triggers for defense induction. However, general consensus concerning evolutionary and molecular factors that alter host range across closely related phytopathogen isolates has been more elusive. Here, through genome comparisons and genetic manipulations, we investigate the underlying mechanisms that structure host range across closely related strains of Pseudomonas syringae isolated from different legume hosts. Although type III secretion-independent virulence factors are conserved across these three strains, we find that the presence of two genes encoding type III effectors (hopC1 and hopM1) and the absence of another (avrB2) potentially contribute to host range differences between pathovars glycinea and phaseolicola. These findings reinforce the idea that a complex genetic basis underlies host range evolution in plant pathogens. This complexity is present even in host-microbe interactions featuring relatively little divergence among both hosts and their adapted pathogens.
    Molecular Plant-Microbe Interactions 03/2012; 25(7):877-88. DOI:10.1094/MPMI-08-11-0218 · 3.94 Impact Factor
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