Structure and Function of RXLR Effectors of Plant Pathogenic Oomycetes

Abstract

A diverse number of plant pathogens, including bacteria, fungi, oomycetes and nematodes, secrete effector proteins to different cellular compartments of their hosts to modulate plant defense circuitry and enable parasitic colonization (Birch et al., 2006; Chisholmet al., 2006;Kamoun, 2006;O?Connell and Panstruga, 2006). The current paradigm in the study of plant–microbe interactions is that unravel- ing the molecular function of effectors is central to a mechanistic understanding of pathogenicity. Indeed, significant progress has been made in elucidating the viru- lence functions of bacterial effectors and the biochemical activities that enable these proteins to perturb host defense processes and facilitate pathogenicity (Chisholm et al., 2006). In contrast, little is known about the biology of effectors of eukaryotic plant pathogens. Nonetheless, this area of research is to function as inhibitors of host enzymes, such as proteases and glucanases (Rose et al., 2002; Tian et al., 2005; 2004). They are thought to contribute to counter- defense by disabling host enzymes that accumulate in response to pathogen infec- tion. In contrast, the biochemical activities of cytoplasmic effectors remain poorly understood. Oomycete cytoplasmic effectors have been discovered first through their avirulence (Avr) function, i.e. their ability to trigger hypersensitive cell death on specific host genotypes that carry particular disease resistance (R) genes (Allen et al., 2004; Armstrong et al., 2005; Rehmany et al., 2005; Shan et al., 2004). The function of these effectors in plants that do not carry the cognate R genes remains largely unknown (Kamoun, 2006). This review summarizes recent findings on the structure and function of the RXLR class of oomycete effectors (Birch et al., 2006;Kamoun, 2006). These effec- tors function inside host cells and are characterized by a highly conserved region defined by the invariant sequence RXLR. This review will cover two main topics of RXLR effector research: trafficking and function. progressing rapidly as illus- trated by the recent identification of effectors from the flax rust and barley powdery mildew fungi (Catanzariti et al., 2006; Dodds et al., 2004; Ridout et al., 2006), the oomycetes Phytophthora and Hyaloperonospora (Allen et al., 2004; Armstrong et al., 2005;Rehmany et al., 2005; Shan et al., 2004), aswell as root-knot nematodes (Huang et al., 2006a; Huang et al., 2006b). Oomycetes form a distinct group of eukaryotic microorganisms that includes some of the most notorious pathogens of plants (Kamoun, 2003). Research on oomycete effectors has accelerated in recent years due in great part to the avail- ability of resources stemmed from genomics. The emerging picture is complex and fascinating. Oomycetes are now thought to secrete hundreds of effector pro- teins belonging to two classes that target distinct sites in the host plant (Birch et al., 2006; Kamoun, 2006; Tyler et al., 2006). Apoplastic effectors are secreted into the plant extracellular space, whereas cytoplasmic effectors are translocated inside the plant cell, where they target different subcellular compartments (Birch et al., 2006; Kamoun, 2006). Several apoplastic effectors have been determined