Playing the “Harp”: Evolution of Our Understanding of hrp/hrc Genes

Abstract

With the advent of recombinant DNA techniques, the field of molecular plant pathology witnessed dramatic shifts in the 1970s and 1980s. The new and conventional methodologies of bacterial molecular genetics put bacteria center stage. The discovery in the mid-1980s of the hrp/hrc gene cluster and the subsequent demonstration that it encodes a type III secretion system (T3SS) common to Gram negative bacterial phytopathogens, animal pathogens, and plant symbionts was a landmark in molecular plant pathology. Today, T3SS has earned a central role in our understanding of many fundamental aspects of bacterium-plant interactions and has contributed the important concept of interkingdom transfer of effector proteins determining race-cultivar specificity in plant-bacterium pathosystems. Recent developments in genomics, proteomics, and structural biology enable detailed and comprehensive insights into the functional architecture, evolutionary origin, and distribution of T3SS among bacterial pathogens and support current research efforts to discover novel antivirulence drugs.

Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic

“…For the two functional T3SSs described to date in P. syringae (Clarke et al, 2010;Tampakaki et al, 2010), our observations suggest an exclusivity of the type of T3SS harbored in the genomes of P. syringae. Similarly in P. viridiflava, strains harbor only one of the two types of T3SS identified by Bergelson and colleagues (Araki et al, 2006).…”

A Career on Both Sides of the Atlantic: Memoirs of a Molecular Plant Pathologist

“…Historical accounts of the discovery and characterization of hrp genes in phytopathogenic bacteria are provided in past and more recent reviews, including one that I coauthored in 2010 (108). Here, I have chosen, arbitrarily, to revisit only some areas of my involvement in this journey.…”

“…These reports are not cited here for reasons of economy but are well detailed in various reviews (7,8,21,67,108,125). In all cases that were studied in sufficient detail, hrp-type mutations were clustered in largely contiguous chromosomal or megaplasmid regions, which were later shown to have the molecular footprints of "pathogenicity islands," i.e., evolutionarily mobile genetic elements.…”

“…First, sequence comparisons established the occurrence of hrp genes in all gram-negative phytopathogen lineages beyond what Southern blot hybridizations were able to show initially. Second, several groups reported significant sequence similarities between several Hrp proteins and structural proteins of bacterial flagella as well as virulence gene clusters found in gram-negative mammalian pathogens, thus establishing a link between virulence-related genes across pathogens of the plant and animal kingdoms (7,12,19,45,49,108). Third, some Yersinia virulence proteins that were secreted in culture [Yersinia outer proteins (Yops)] did not possess a canonical signal peptide necessary for secretion via the main bacterial protein secretion system (Sec) known at that time; however, they could be detected intracellularly in cultured mammalian cells after contact with the pathogen.…”

Shigella

“…T3SS are encoded by large operons, usually 20-40 kb long, that are found on pathogenicity islands. 63 The virulence of Shigella is defined by a virulence plasmid allowing the expression of the T3SS components. 8 T3SS is a multicomponent apparatus spanning both bacterial membranes with a needle-like extracellular appendage that delivers effectors.…”