Top panels (left to right): bacterial speck of tomato caused by Pseudomonas syringae pathovar (pv.) tomato; crown gall of grape caused by Agrobacterium tumefaciens; blackleg of potato caused by Erwinia carotovora subspecies atroseptica; and bacterial wilt of tomato caused by Ralstonia solanacearum. Bottom panels (left to right): P. syringae pv. tomato enters the leaf apoplastic space through stomata or wounds, and uses a type III secretion system to inject a large number of virulence (effector) proteins into the plant cell. Agrobacterium tumefaciens uses a type IV secretion system to inject a tumour-inducing transfer DNA (tDNA) into the plant cell cytoplasm. This tDNA is integrated into the plant genome and leads to the development of crown gall disease. Erwinia carotovora subspecies atroseptica uses a type II secretion system to deliver cell wall-degrading enzymes (for example, cellulases and pectinases) to the plant cell wall. Ralstonia solanacearum enters plant roots through wounds and multiplies in the xylem vessels in which it produces exopolysaccharides that are believed both to interfere with recognition and to inhibit water transport through the vascular system. Each of these four pathogens also uses other virulence mechanisms (Supplementary information 1 (table)). Ti, tumour inducing. Photo credits for top panels, left to right: G.B.M., T. Burr, A. Charkowski and P. Frey.

Plants have evolved resistance (R) proteins to detect the presence of type III effectors and to signal hypersensitive response (HR)-based defences in response to effectors. Several effectors have been shown to suppress HR-based defences in plants21,26,27,90,91. Here we present a speculative model of how AvrPtoB suppresses HR-based defences. In tomato, the AvrPtoB N terminus is recognized by the R protein Rsb in a Prf-dependent manner to signal the HR. The AvrPtoB C terminus encodes E3 ubiquitin (Ub) ligase activity24,25, which includes a conserved E2 Ub-conjugating enzyme binding site. AvrPtoB might function as a scaffold to bind both to a tomato E2 Ub-conjugating enzyme and a positive regulator of HR-based programmed cell death (PCD). The E2 Ub-conjugating enzyme might then ubiquitylate the substrate to target it for degradation or alter the substrate’s localization, therefore interfering with HR-based signalling.

Plants possess plasma-membrane-localized pattern recognition receptors (PRRs) that consist of an extracellular leucine-rich repeat (LRR) domain and a cytoplasmic serine/threonine kinase domain. In Arabidopsis, FLS2 and elongation factor Tu (EF-Tu) receptor (EFR) are PRRs that recognize the flg22 peptide of flagellin or the elf18 peptide of EF-Tu, respectively 47,49,54,59,119. Other bacterial elicitors such as lipopolysaccharide (LPS), harpins, and cold-shock protein have been identified11,45,48,120. PRR activation triggers signalling events that lead to the upregulation of over 300 plant genes51,52,56,57. A complete mitogen-activated protein kinase (MAPK) pathway and several WRKY transcription factors that function downstream of FLS2 and induce the expression of genes such as FRK1 and NHO1 have been identified51. Phenotypes that are associated with activated basal defences include cell wall fortifications and the production of reactive oxygen species (ROS) and nitrogen species (NO). Delivery of effector proteins through the type III secretion system (T3SS) into plant cells is one strategy that is used by bacteria to suppress PRR-mediated defences. As many as 16 effectors have been identified that suppress basal defences42,65–68,110. The model highlights the effector AvrPto that is required for suppressing the recognition of flg22 and other pathogen-associated molecular patterns (PAMPs)42,87. In Arabidopsis, AvrPto functions upstream of MAPK kinase kinase (MAPKKK), indicating that it targets components that function early on in the PRR pathway42. The residue I96, which resides within an extended Ω-loop, is required for the basal defence suppression of AvrPto in Arabidopsis. See text for more details.

The outcome of plant–pathogen interactions might be dependent on the complement of four important factors: pathogen-associated molecular patterns (PAMPS); pattern recognition receptors (PRRs); resistance (R) proteins; and effectors. If the host can recognize the PAMPS or effectors of the pathogen, then non-host or hypersensitive response (HR)-based resistance might be elicited. If the pathogen can vary PAMPS to avoid detection or has the correct complement of effectors to suppress PRR- or R-protein-mediated resistance then disease might be observed. LRR, leucine-rich repeats; NBS, nucleotide-binding site.