Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria

Genes of plant-pathogenic bacteria controlling hypersensitive response (HR) elicitation and pathogenesis were designated ‘hrp’ by Lindgren et al. in 1986 (J Bacteriol 168: 512–522). hrp genes have been characterized in several species of the four major genera of Gramnegative plant pathogens, Erwinia, Pseudomonas, Ralstonia (a new proposed genus including Pseudomonas solanacearum) and Xanthomonas. To date, hrp genes have been found mainly in large clusters, and they have been shown to be conserved physically and, in many cases, functionally among different bacteria. Hybridization studies and genetic analyses have revealed the presence of functional hrp genes even in species that are not typically observed to elicit an HR, such as Erwinia chrysanthemi and Erwinia stewartii, suggesting that hrp genes may be common to all Gram-negative plant pathogens, possibly excluding Agrobacterium spp. Current knowledge of hrp genes has been reviewed by Bonas (1994, Curr Top Microbiol Immunol 192: 79–98) and by Van Gijsegem et al. (1995, In Pathogenesis and Host–Parasite Specificity in Plant Diseases: Histopathological, Biochemical, Genetic and Molecular Basis. Volume 1. (Kohmoto et al., eds); Oxford: Pergamon Press, pp. 273–292). The nucleotide sequences of four hrp gene clusters, those of Ralstonia solanacearum (previously P. solanacearum) (Genin et al., 1992, Mol Microbiol 6: 3065–3076; Gough et al., 1992, Mol Plant–Microbe Interact 5: 384–389; Gough et al., 1993, Mol Gen Genet 239: 378–392; Van Gijsegem et al., 1995, Mol Microbiol 15: 1095–1114), Erwinia amylovora (Bogdanove et al., 1996, J Bacteriol 178: 1720– 1730; Wei and Beer, 1993, J Bacteriol 175: 7958–7967; Wei and Beer, 1995, J Bacteriol 177: 6201–6210; Wei et al., 1992, Science 257: 85–88; S. V. Beer, unpublished), Pseudomonas syringae pv. syringae (Huang et al., 1992, J Bacteriol 174: 6878–6885; Huang et al., 1993, Mol Plant–Microbe Interact 6: 515–520; Huang et al., 1995, Mol Plant–Microbe Interact 8: 733–746; Lidell and Hutcheson, 1994, Mol Plant–Microbe Interact 7: 488–497; Preston et al., 1995, Mol Plant–Microbe Interact 8: 717–732; Xiao et al., 1994, J Bacteriol 176: 1025–1036), and Xanthomonas campestris pv. vesicatoria (Fenselau et al., 1992, Mol Plant–Microbe Interact 5: 390–396; Fenselau and Bonas, 1995, Mol Plant–Microbe Interact 8: 845–854; U. Bonas, unpublished), have been largely determined. These clusters each contain more than twenty genes, many of which encode components of a novel proteinsecretion pathway designated ‘type III’. It has been shown directly that various extracellular proteins involved in pathogenesis and defence elicitation by plantpathogenic bacteria utilize this pathway (Arlat et al., 1994, EMBO J 13: 543–553; He et al., 1993, Cell 73: 1255–1266; Wei and Beer, 1993, ibid.), and the pathway is known to function in the export of virulence factors from the animal pathogens Salmonella typhimurium, Shigella flexneri, and Yersinia entercolitica, Yersinia pestis, and Yersinia pseudotuberculosis (for reviews, see Salmond and Reeves, 1993, Trends Biochem Sci 18: 7–12; and Van Gijsegem et al., 1993, Trends Microbiol 1: 175– 180). Nine type III secretion genes are conserved among all four of the plant pathogens listed above and among the animal pathogens. Based on sequence analysis and some experimental evidence, they are believed to encode one outer-membrane protein, one outer-membrane-associated lipoprotein, five inner-membrane proteins, and two cytoplasmic proteins, one of which is a putative ATPase. All of the predicted gene products, except the outer-membrane protein, show significant similarity to components of the flagellar biogenesis complex (for reviews see Blair, 1995, Annu Rev Microbiol 49: 489–522; and Bischoff and Ordal, 1992, Mol Microbiol 6: 23–28). We herein refer to the hrp-encoded type III pathway as the ‘Hrp pathway’. Because hrp genes have been characterized independently in diverse plant-pathogenic bacteria, hrp gene nomenclature differs in different species, and it is not always consistent even within the same organism. Different designations are used for homologous genes, and, even worse, the same designation is used for different genes in different organisms. For example, hrpI of E. amylovora is homologous with hrpC2 of X. campestris pv. vesicatoria and hrpO of R. solanacearum, and the homologue in P. syringae pv. syringae appears in the literature both as hrpI and as hrpJ2. Also, ‘hrpN ’ in R. solanacearum designates a secretion-pathway gene, whereas in E. amylovora, ‘hrpN ’ designates the gene encoding the elicitor harpin. Furthermore, in many bacteria the number of known hrp genes approaches 26. In anticipation of exhausting the alphabet, some authors chose to designate hrp genes with a letter and a number, creating the potential for confusion of distinct genes with alleles of the same gene. For hrp gene researchers, the current nomenclature is at best inconvenient; for other scientists, it is bewildering. Another problem exists: accumulation of knowledge about the structure of hrp loci has outpaced the accumulation of Molecular Microbiology (1996) 20(3), 681–683