Mechanistic insights into host adaptation, virulence and epidemiology of the phytopathogen Xanthomonas

Abstract

Xanthomonas is a well-studied genus of bacterial plant pathogens whose members cause a variety of diseases in economically important crops worldwide. Genomic and functional studies of these phytopathogens have provided significant understanding of microbial-host interactions, bacterial virulence and host adaptation mechanisms including microbial ecology and epidemiology. In addition, several strains of Xanthomonas are important as producers of the extracellular polysaccharide, xanthan, used in the food and pharmaceutical industries. This polymer has also been implicated in several phases of the bacterial disease cycle. In this review, we summarise the current knowledge on the infection strategies and regulatory networks controlling virulence and adaptation mechanisms from Xanthomonas species and discuss the novel opportunities that this body of work has provided for disease control and plant health.

Keywords: adaptation; biofilm; extracellular polysaccharides; plant disease; regulatory circuits; type III effectors.

Figure 1.

Life cycle and disease symptoms of Xanthomonas. (A), Model illustrating the life cycle of the black rot pathogen Xanthomonas campestris pv. campestris (Xcc). Like most Xanthomonads, Xcc can survive in plant debris in soil for up to two years, but not more than six weeks in free soil. Xcc also has the ability to colonise plant seeds which represents a major route of disease transmission. Xcc can also be spread from infected plants to healthy plants by various environmental and mechanical means. After germination of colonised seeds, the seedling becomes infected. This may manifest as shrivelling and the blackening of the margins of the seedling. Xcc may also invade mature plants via the hydathodes, although leaf damage caused by insects and the root system also serve as portals of entry. These entry points usually provide a direct path to the plant vascular system leading to systemic host infection. V-shaped necrotic lesions extending from the leaf margins manifest as the infection develops. The disease draws its name from the blackened veins within the necrotic lesions. (B), Examples of disease symptoms caused by various Xanthomonas species. (i, ii) Black rot of cabbage caused by Xanthomonas campestris pv. campestris. (iii, iv) Citrus canker of citrus caused by Xanthomonas citri pv. citri. (v, vi) Bacterial leaf streak of rice caused by Xanthomonas oryzae pv. oryzicola. (vii, viii) Bacterial blight of rice caused by Xanthomonas oryzae pv. oryzae.

Figure 2.

Phylogenetic tree of the Xanthomonas genus based on the NCBI taxonomy. The list of taxonomic names obtained from the NCBI Taxonomy Browser filtered using ‘has genome sequences’. The tree was annotated and visualized using iTOL (Interactive Tree Of Life) software.

Figure 3.

Xanthomonas employs multiple systems to link sensing of diverse environmental signals to regulation of appropriate responses. The Xcc genome encodes a number of two-component and other systems thought to be involved in environmental sensing and regulation. In a relatively small number of cases the signals that activate these pathways have been established, to include the DSF cell–cell signal, oxygen tension, iron and other metal ions, cytokinin and other plant-derived molecules to include sucrose and light. In addition to two-component regulators, a number of transcription factors have been implicated in downstream signalling pathways that lead to activation of functions associated with virulence and other environmental adaptations. These include the cyclic di-GMP responsive Clp, the type III secretion regulators Zur, FhrR PhoP, HpaR, HrpX, HrpG and HpaR1. Interestingly, VgrR although be shown to be involved in iron uptake also contributes to type III secretion regulation. Code Blue sensor proteins, Green regulatory proteins

Figure 4.

Polysaccharide biosynthesis and selected lipopolysaccharide structures in xanthomonads. (A), An overview indicates how the biosynthesis of polysaccharides and glycoconjugates is embedded in the Xanthomonas metabolism. Main stages of polysaccharide biosynthesis are marked in red. (B), In an inlay, the structure of a pentasaccharide repeat unit of the exopolysaccharide xanthan is given. Two glucose residues contribute to the xanthan main chain, with a trisaccharide side chain attached to every second glucose residue. The mannose residues of the side chains can be modified at varying degrees. The proxymal mannose close to the main chain is depicted with an acetyl group, while the terminal mannose carries a pyruvyl group. Alternatively, this mannose can be acetylated. (C), LPS structures are indicated for X. campestris pv. campestris 8004, which have been partly confirmed for strain B100, for X. translucens pv. translucens DSM-18 974, for X. oryzae pv. oryzicola BLS303, and for X. fragariae NCPPB 1469. Main constituents are identified in the graphical legend. In several cases, side chains are linked non-stoichiometrically. Such non-stoichiometric linkages are marked in red. For X. fragariae NCPPB 1469, part of the monosaccharide side chains were linked in irregular intervals to the main chain.