Identification of Rust Fungi Avirulence Elicitors

Rust fungi (Basidiomycetes of the order Uredinales) are obligate biotrophs that grow and reproduce only in living plant tissue. There are on the order of 5000 or more species of rust fungi that collectively cause disease on most crops, ornamentals, and many other plants. For example, rusts caused by Puccinia species are some of the most important diseases of wheat and other small grain crops worldwide. A new wheat rust epidemic is currently building in East Africa with the appearance of a highly virulent strain of Puccinia graminis tritici called Ug99, which is perceived as a threat to global wheat production and has led to the establishment of a Global Rust Initiative (http://www. globalrust.org/index.html). Common maize rust caused by Puccinia sorghi is a major disease problem of maize, particularly in tropical and subtropical regions such as South Africa and India. The Asian soybean rust caused by Phakopsora pachyrhizi has recently spread to Africa and the western hemisphere, including the U.S., and is now a major concern in most of the soybeangrowing regions of the world. Rust fungi have extremely complex life cycles, involving up to five different sporeproducing stages. Many rusts are heteroecious, requiring two phylogenetically distinct host plants to complete their life cycle. For example, the wheat rust Puccinia graminis alternates between wheat as the primary host and barberry as the alternate host, and Melampsora epitea willow-conifer rusts alternate between a coniferous primary host, such as hemlock or tamarack, and a willow alternate host. Some rusts, such as the flax rust Melampsora lini, are autoecious and complete their life cycle on a single host plant. Rust fungi are host specific and will develop compatible or incompatible associations with their host plants in a gene-forgene manner, depending on the presence or absence of avirulence (Avr) genes in the pathogen and corresponding resistance (R) genes in the host. The interaction of M. lini with flax (Linum usitatissimum) has a central place in the history of plant pathology, as studies with this pathosystem led to the development of the genefor-gene hypothesis of plant–pathogen interactions, one of the most important principles of plant pathology (Flor, 1942, 1955). During infection of a host plant, rust fungi form haustoria, specialized infection structures that penetrate the plant cell wall and form invaginations in the plasma membrane that are believed to form the major sites of nutrient uptake from the host cell (Hahn and Mendgen, 2001). It is also thought that signals emanating from haustoria suppress host defense responses and facilitate disease in sensitive host plants (Panstruga, 2003; Vogele and Mendgen, 2003) or trigger a hypersensitive response (HR) leading to disease resistance in resistant hosts (i.e., interaction between Avr factors and host R gene products; Heath, 1997). In this issue of The Plant Cell, Catanzariti et al. (pages 243–256) identify a number of avirulence elicitors (Avr proteins) encoded by genes expressed in haustoria of the flax rust M. lini (see figure). The previously identified AvrL567 proteins from flax rust are expressed in haustoria and contain secretory pathway signal peptides, suggesting that they are secreted into the extrahaustorial matrix (Dodds et al., 2004). In addition, all 19 of the flax R genes identified to date encode predicted cytoplasmic TIR-NBSLRR proteins, suggesting that the corresponding rust Avr genes encode secreted proteins that somehow gain entry into the