The Synchytrium endobioticum AvrSen1 triggers a Hypersensitive Response in Sen1 potatoes while natural variants evade detection
AbstractSynchytrium endobioticum is an obligate biotrophic fungus of the phylum Chytridiomycota. It causes potato wart disease, has a world-wide quarantine status and is included on the HHS and USDA Select Agent list. S. endobioticum isolates are grouped in pathotypes based on their ability to evade host-resistance in a set of differential potato varieties. So far, thirty-nine pathotypes are reported. A single dominant gene (Sen1) governs pathotype 1 resistance and we anticipated that the underlying molecular model would involve a pathogen effector (AvrSen1) that is recognized by the host. The S. endobioticum specific secretome of fourteen isolates representing six different pathotypes was screened for effectors specifically present in pathotype 1(D1) isolates but absent in others. We identified a single AvrSen1 candidate. Expression of this candidate in potato Sen1 plants showed a specific hypersensitive response, which co-segregated with the Sen1 resistance in potato populations. No HR was obtained with truncated genes found in pathotypes that evaded recognition by Sen1. These findings established that our candidate gene was indeed Avrsen1. The S. endobioticum AvrSen1 is a single copy gene and encodes a 376 amino acid protein without predicted function or functional domains, and is the first effector gene identified in Chytridiomycota, an extremely diverse yet underrepresented basal lineage of fungi.Author SummaryPlant pathogens can have a great social and economic impact, and are a continuous threat to food security. A clear example is Synchytrium endobioticum, the fungus causing potato wart disease. The impact of the pathogen, lack of effective chemical control agents and the longevity of resting spores produced by the pathogen led to a world-wide quarantine status for S. endobioticum. Strict phytosanitary measures and the use of resistance potato varieties are currently the only way to prevent the spread of the disease. The emergence of new pathotypes that overcome resistance urged to study the underlying molecular mechanisms of S. endobioticum recognition by the plant. Here we describe the identification of the first effector (AvrSen1) of S. endobioticum that is recognized by the Sen1 resistance gene product. Also, we report the loss of AvrSen1 in other pathotypes thus avoiding recognition by the plant and triggering immune responses. AvrSen1 represents the first effector to be identified in the basal fungal lineage Chytridiomycota. The discovery of AvrSen1 provides an important tool to manage potato wart disease. Moreover, knowledge about Chytridiomycota effectors will shed light on other (pathogenic) interactions and the co-evolution of Chytridiomycota species with their hosts.