Haustorially Expressed Secreted Proteins from Flax Rust Are Highly Enriched for Avirulence Elicitors

Abstract

Rust fungi, obligate biotrophs that cause disease and yield losses in crops such as cereals and soybean (Glycine max), obtain nutrients from the host through haustoria, which are specialized structures that develop within host cells. Resistance of flax (Linum usitatissimum) to flax rust (Melampsora lini) involves the induction of a hypersensitive cell death response at haustoria formation sites, governed by gene-for-gene recognition between host resistance and pathogen avirulence genes. We identified genes encoding haustorially expressed secreted proteins (HESPs) by screening a flax rust haustoriumspecific cDNA library. Among 429 unigenes, 21 HESPs were identified, one corresponding to the AvrL567 gene. Three other HESPs cosegregated with the independent AvrM, AvrP4, and AvrP123 loci. Expression of these genes in flax induced resistance gene-mediated cell death with the appropriate specificity, confirming their avirulence activity. AvrP4 and AvrP123 are Cys-rich proteins, and AvrP123 contains a Kazal Ser protease inhibitor signature, whereas AvrM contains no Cys residues. AvrP4 and AvrM induce cell death when expressed intracellularly, suggesting their translocation into plant cells during infection. However, secreted AvrM and AvrP4 also induce necrotic responses, with secreted AvrP4 more active than intracellular AvrP4, possibly as a result of enhanced formation of endoplasmic reticulum-dependent disulfide bonds. Addition of an endoplasmic reticulum retention signal inhibited AvrM-induced necrosis, suggesting that both AvrM and AvrP4 can reenter the plant cell after secretion in the absence of the pathogen.

Blufensin1Negatively Impacts Basal Defense in Response to Barley Powdery Mildew

“…To acquire nutrients from host cells, obligate biotrophic fungi have evolved mechanisms to secrete effectors to suppress host defenses (Dodds et al, 2004;Catanzariti et al, 2006;Wang et al, 2007) and to induce host susceptibility genes (Schulze-Lefert and Panstruga, 2003;Hü ckelhoven, 2005). In Arabidopsis (Arabidopsis thaliana) and barley, several host susceptibility factors have been identified for powdery mildew, but how pathogens utilize these host genes remains unclear (Schultheiss et al, 2002(Schultheiss et al, , 2003Hü ckelhoven et al, 2003;Hü ckelhoven, 2005).…”

Insights into Nonhost Disease Resistance: Can They Assist Disease Control in Agriculture?

“…Virulent Bgh strains induce susceptibility to host cell penetration and haustorium formation by the normally avirulent strain (Lyngkjaer et al, 2001), consistent with the idea that the first strain delivers effector molecules that induce a susceptible state. Studies of genes expressed in rust haustoria are beginning to provide insights into proteins delivered from these pathogens to infected host cells (Kemen et al, 2005;Catanzariti et al, 2006), and intensive genomics studies of Bgh now in progress could identify mildew effectors (Both et al, 2005;Zhang et al, 2005). Characterization of fungal pathogen effectors and their host targets is now a research priority.…”

Two modes of pathogen recognition by plants

“…These Avr proteins are small (150 aa) and contain a signal sequence that is removed (giving rise to a 127-aa mature peptide). They are presumably delivered across the haustorial membrane, through the extrahaustorial matrix, and into the plant cell (15,16). Importantly, AvrL567 proteins contain particular amino acid residues that are under selection for sequence divergence.…”