Acquisition and Evolution of Plant Pathogenesis–Associated Gene Clusters and Candidate Determinants of Tissue-Specificity in Xanthomonas

Abstract

Background Xanthomonas is a large genus of plant-associated and plant-pathogenic bacteria. Collectively, members cause diseases on over 392 plant species. Individually, they exhibit marked host- and tissue-specificity. The determinants of this specificity are unknown.Methodology/Principal FindingsTo assess potential contributions to host- and tissue-specificity, pathogenesis-associated gene clusters were compared across genomes of eight Xanthomonas strains representing vascular or non-vascular pathogens of rice, brassicas, pepper and tomato, and citrus. The gum cluster for extracellular polysaccharide is conserved except for gumN and sequences downstream. The xcs and xps clusters for type II secretion are conserved, except in the rice pathogens, in which xcs is missing. In the otherwise conserved hrp cluster, sequences flanking the core genes for type III secretion vary with respect to insertion sequence element and putative effector gene content. Variation at the rpf (regulation of pathogenicity factors) cluster is more pronounced, though genes with established functional relevance are conserved. A cluster for synthesis of lipopolysaccharide varies highly, suggesting multiple horizontal gene transfers and reassortments, but this variation does not correlate with host- or tissue-specificity. Phylogenetic trees based on amino acid alignments of gum, xps, xcs, hrp, and rpf cluster products generally reflect strain phylogeny. However, amino acid residues at four positions correlate with tissue specificity, revealing hpaA and xpsD as candidate determinants. Examination of genome sequences of xanthomonads Xylella fastidiosa and Stenotrophomonas maltophilia revealed that the hrp, gum, and xcs clusters are recent acquisitions in the Xanthomonas lineage.Conclusions/SignificanceOur results provide insight into the ancestral Xanthomonas genome and indicate that differentiation with respect to host- and tissue-specificity involved not major modifications or wholesale exchange of clusters, but subtle changes in a small number of genes or in non-coding sequences, and/or differences outside the clusters, potentially among regulatory targets or secretory substrates.

Two New Complete Genome Sequences Offer Insight into Host and Tissue Specificity of Plant Pathogenic Xanthomonas spp

“…raphani 756C contains only three of these (xopF1, xopP, and xopR) and four other T3E genes that are less broadly conserved (Table 3). All the T3S genes themselves, including the hpa and hrpW accessory protein genes, are intact (52). Bordering the hrp gene cluster, a novel candidate T3E gene, xopAT, was identified on the basis of the presence of a plant-inducible promoter (PIP) box and a properly positioned Ϫ10 box-like sequence upstream of the coding sequence (Table 3; see Table S2 in the supplemental material).…”

Host and Pathogen Factors Controlling the Rice-Xanthomonas oryzae Interaction

“…The genomic sequences are available for three strains of Xoo and one strain of Xoc (Lee et al, 2005;Ochiai et al, 2005;Lu et al, 2008;Salzberg et al, 2008). The full complement of TAL T3 effectors are now known for two strains of Xoo and one strain of Xoc, and both pathogens are unusual due to the high number of TAL effector genes within their individual genomes.…”

Underexplored Niches in Research on Plant Pathogenic Bacteria

“…Similar analyses can find conserved hypothetical proteins specific to epiphytes, xylem dwellers, bacteria attacking only monocots, etc. An analysis of plant pathogenic Xanthomonas genomes used this idea to identify genes potentially linked to infecting specific tissues (Lu et al, 2008). However, the next steps require a better understanding of the hidden lives of bacterial pathogens than we currently have, highlighting the need for a greater overlap with bioinformatics and natural history.…”