Lifestyles of the effector-rich: genome-enabled characterization of bacterial plant pathogens

Authors: COLLMER, ALAN - Cornell University; Schneider, David; LINDEBERG, MAGDALEN - Cornell University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/26/2009
Publication Date: 6/10/2009
Citation: Collmer, A., Schneider, D.J., Lindeberg, M. 2009. Lifestyles of the effector-rich: genome-enabled characterization of bacterial plant pathogens. Plant Physiology. 150:1623-1630.

Interpretive Summary: Genome sequencing of bacterial plant pathogens has made it possible to create substantially complete lists of proteins that are secreted by the bacteria, thus are capable of direct interaction with plant cells. These proteins, referred to collectively as effectors, interact with plant cells in diverse ways but share a surprising number of important properties. First, they are collectively essential, along with the underlying secretion system. Deleting the entire set of effector-encoding genes leads to loss of virulence. Second, they are individually dispensable. It is uncommon for deletion of individual effectors to have a detectable effect on virulence, thus they are not detectable by genetic screens for virulence factors and can only be identified by genome-scale analysis. Third, genome sequencing has revealed that genes encoding characteristic sets of closely related effectors tend to be amplified in each pathogen strain. This amplification of related genes leads to functional redundancy and the robustness of the system as a whole and the observed dispensability of individual members within an amplified set. Finally, these amplified classes of effectors target critical plant defense pathways. As a result, the bacterial effectors become valuable tools for the study of plant defense mechanisms.

Technical Abstract: Genome sequencing of bacterial plant pathogens is providing transformative insights into the complex network of molecular plant-microbe interactions mediated by extracellular effectors during pathogenesis. Bacterial pathogens sequenced to completion are phylogenetically diverse and vary significantly in host-range, tissue specificity, and mechanisms of pathogenicity. Genomic sequences have made it possible to identify complete effector repertoires, aided by pattern-based searches with effector-associated sequence motifs. Among the hemibiotrophic proteobacteria – Pseudomonas, Xanthomonas, and Ralstonia – functional characterization of type III substrates supports an emerging model wherein effectors are collectively essential but individually dispensable as a consequence of redundant targeting by multiple effectors of high level defense-related processes in the host. Amplification of functionally related effectors is similarly evident for cell wall-degrading enzymes deployed by the nectrotrophic proteobacteria Pectobacterium atrosepticum and is suggested by the numerous homologs of a virulence-associated serine protease encoded by gram-positive actinobacterial pathogens in the genus Clavibacter. As more pathogen genomes are obtained, systematic identification of redundant effector groups represents a potentially powerful tool for revealing plant processes of particular importance to the outcome of the pathogenic interaction.