A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens

Abstract

Plant disease resistance is often conferred by genes with nucleotide binding site (NBS) and leucine-rich repeat (LRR) or serine/threonine protein kinase (S/TPK) domains. Much less is known about mechanisms of susceptibility, particularly to necrotrophic fungal pathogens. The pathogens that cause the diseases tan spot and Stagonospora nodorum blotch on wheat produce effectors (host-selective toxins) that induce susceptibility in wheat lines harboring corresponding toxin sensitivity genes. The effector ToxA is produced by both pathogens, and sensitivity to ToxA is governed by the Tsn1 gene on wheat chromosome arm 5BL. Here, we report the cloning of Tsn1 , which was found to have disease resistance gene-like features, including S/TPK and NBS-LRR domains. Mutagenesis revealed that all three domains are required for ToxA sensitivity, and hence disease susceptibility. Tsn1 is unique to ToxA-sensitive genotypes, and insensitive genotypes are null. Sequencing and phylogenetic analysis indicated that Tsn1 arose in the B-genome diploid progenitor of polyploid wheat through a gene-fusion event that gave rise to its unique structure. Although Tsn1 is necessary to mediate ToxA recognition, yeast two-hybrid experiments suggested that the Tsn1 protein does not interact directly with ToxA. Tsn1 transcription is tightly regulated by the circadian clock and light, providing further evidence that Tsn1 -ToxA interactions are associated with photosynthesis pathways. This work suggests that these necrotrophic pathogens may thrive by subverting the resistance mechanisms acquired by plants to combat other pathogens.

Sensitivity to three Parastagonospora nodorum necrotrophic effectors in current Australian wheat cultivars and the presence of further fungal effectors

“…The fungus is responsible for yield losses estimated at AU $108 million per year in Australia (Murray and Brennan 2009;Oliver et al 2012). SNB is quantitatively governed by the interaction of fungal necrotrophic effectors (NEs) with the products of host dominant sensitivity genes (Faris et al 2010;Tan et al 2010). A compatible interaction results in host tissue necrosis, which promotes infection by the pathogen.…”

“…Genetic evidence suggests that PtrToxA was acquired from P. nodorum via horizontal gene transfer (Friesen et al 2006). ToxA encodes a small, secreted protein that causes necrosis and promotes infection in wheat carrying the Tsn1 gene (Tan et al 2012), which is located on chromosome 5B and encodes a protein with distinct NBS-LRR (nucleotide-binding site-leucine-rich repeat) and protein kinase domains (Faris et al 2010). SnTox3 encodes a small, secreted protein (Liu et al 2009); Snn3-B1 and Snn3-D1 are key SnTox3 sensitivity genes that mapped to the short arm of chromosome 5B and 5D, respectively (Zhang et al 2011).…”

Reconstructing the Fungal Tree of Life Using Phylogenomics and a Preliminary Investigation of the Distribution of Yeast Prion-Like Proteins in the Fungal Kingdom

“…This enables us to use fungi to study evolutionary mechanisms associated with eukaryotic genome structure, organization, and content. Furthermore it permits us to undertake comparative analysis into fungal virulence (Butler et al 2009;Faris et al 2010), evolution (Fitzpatrick et al 2008), metabolic capabilities (Fitzpatrick et al 2010), and fate of genes that have arisen through duplication (Scannell et al 2006). However to fully understand fungal evolution and associated biological processes it is essential we have a reliable fungal tree of life (FTOL).…”

The wheat NB‐LRR gene TaRCR1 is required for host defence response to the necrotrophic fungal pathogen Rhizoctonia cerealis

“…The majority of the reported NB‐LRR proteins positively contribute to plant immunity to diverse biotrophic pathogens. In more recent documents, three distinct NB‐LRR proteins have been implicated in host susceptibility to necrotrophic fungal pathogens (Faris et al ., 2010; Lorang et al ., 2007; Nagy and Bennetzen, 2008). Here, to our knowledge, this study is the first to uncover the positive regulation of an NB‐LRR protein in plant resistance responses to the necrotrophic fungal pathogens.…”

“…However, in certain plant‐necrotrophic fungus pathosystems, the recognition of pathogen‐produced effectors by NB‐LRR proteins leads to effector‐triggered susceptibility (Faris et al ., 2010; Lorang et al ., 2007; Nagy and Bennetzen, 2008). For example, the wheat Tns1 governs effector‐triggered susceptibility to two necrotrophic fungi Stagonospora nodorum and Pyrenophora tritici‐repentis (Faris et al ., 2010). To our knowledge, no study about NB‐LRR genes involved positively in plant resistance responses to necrotrophic fungal pathogens has been reported yet.…”