Multiple Avirulence Paralogues in Cereal Powdery Mildew Fungi May Contribute to Parasite Fitness and Defeat of Plant Resistance

Abstract

Powdery mildews, obligate biotrophic fungal parasites on a wide range of important crops, can be controlled by plant resistance (R) genes, but these are rapidly overcome by parasite mutants evading recognition. It is unknown how this rapid evolution occurs without apparent loss of parasite fitness. R proteins recognize avirulence (AVR) molecules from parasites in a gene-for-gene manner and trigger defense responses. We identify AVR a10 and AVR k1 of barley powdery mildew fungus, Blumeria graminis f sp hordei (Bgh), and show that they induce both cell death and inaccessibility when transiently expressed in Mla10 and Mlk1 barley (Hordeum vulgare) varieties, respectively. In contrast with other reported fungal AVR genes, AVR a10 and AVR k1 encode proteins that lack secretion signal peptides and enhance infection success on susceptible host plant cells. AVR a10 and AVR k1 belong to a large family with >30 paralogues in the genome of Bgh, and homologous sequences are present in other formae speciales of the fungus infecting other grasses. Our findings imply that the mildew fungus has a repertoire of AVR genes, which may function as effectors and contribute to parasite virulence. Multiple copies of related but distinct AVR effector paralogues might enable populations of Bgh to rapidly overcome host R genes while maintaining virulence.

Host-Induced Gene Silencing in Barley Powdery Mildew Reveals a Class of Ribonuclease-Like Effectors

“…Likewise, in B. graminis, we have found a superfamily of 491 genes encoding small proteins, predicted to be secreted and with features typical of effectors ). These candidate secreted effector proteins (CSEP) differ from previously identified B. graminis avirulence proteins AVR A10 and AVR K1 , which do not contain a predicted signal peptide (Ridout et al 2006;Sacristán et al 2009). The CSEP superfamily includes many of the genes and proteins previously identified as specifically expressed in haustoria ) and in infected epidermis (Bindschedler et al 2009(Bindschedler et al , 2011.…”

“…hordei has been driven by the identification of i) genes specifically upregulated during infection (Both et al 2005), ii) RNAs specifically associated with haustoria Spanu et al 2010), iii) proteins found specifically in haustoria (Bindschedler et al 2009(Bindschedler et al , 2011, iv) genes predicted to encode small secreted proteins with no evident homologs in other fungi by means of a bioinformatic survey of the B. graminis f. sp. hordei genome , and v) characterization of avirulence genes in the fungus that confer race-specific incompatibility on barley genotypes with corresponding resistance genes (Ridout et al 2006;Sacristán et al 2009). …”

Blufensin1Negatively Impacts Basal Defense in Response to Barley Powdery Mildew

“…Pathogen recognition in barley-Bgh interactions is triggered in a pathogen race-specific manner by genes designated Ml (for Mildew resistance locus; Jørgensen, 1994). Approximately 30 distinct resistance specificities have been identified at the Mla locus; all cloned Mla alleles isolated so far encode coiled-coil, nucleotide-binding site, Leu-rich repeat (CC-NBS-LRR) resistance proteins (Wei et al, 2002;Shen et al, 2003;Halterman and Wise, 2004) that recognize, either directly or indirectly, corresponding fungal effector (AVR) proteins (Ridout et al, 2006). Programmed cell death mediated by MLA proteins occurs after fungal penetration, when primordial haustoria are presumed to secrete AVR a proteins.…”

Genetics and molecular mechanisms of resistance to powdery mildews in tomato (Solanum lycopersicum) and its wild relatives

“…For few of this type of genes, the interacting pathogen effector is also identified and further verifies that these genes perceive a pathogen's effector and trigger ETI. For example barley MLA10 recognizes AVR A10 effector from Bgh (Ridout et al 2006). PTI: race-non-specific resistance conferred by PAMP-receptors Among the genes that have been discussed above, some do not encode NBS-LRR proteins and confer race nonspecific resistance.…”

“…These genes were isolated by map-based cloning from Bgh, and their products are recognized by barley R proteins MLA10 and MLK1, respectively (Ridout et al 2006). With the available PM genomes, plenty of genes encoding for putative effectors, i.e., genes encoding for proteins that have a secretion signal and have no match in organisms outside the PMs, have been identified.…”