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Necrotrophic effector epistasis in the Pyrenophora tritici-repentis-wheat interaction.

ABSTRACT: Pyrenophora tritici-repentis, the causal agent of tan spot disease of wheat, mediates disease by the production of host-selective toxins (HST). The known toxins are recognized in an 'inverse' gene-for-gene manner, where each is perceived by the product of a unique locus in the host and recognition leads to disease susceptibility. Given the importance of HSTs in disease development, we would predict that the loss of any of these major pathogenicity factors would result in reduced virulence and disease development. However, after either deletion of the gene encoding the HST ToxA or, reciprocally, heterologous expression of ToxA in a race that does not normally produce the toxin followed by inoculation of ToxA-sensitive and insensitive wheat cultivars, we demonstrate that ToxA symptom development can be epistatic to other HST-induced symptoms. ToxA epistasis on certain ToxA-sensitive wheat cultivars leads to genotype-specific increases in total leaf area affected by disease. These data indicate a complex interplay between host responses to HSTs in some genotypes and underscore the challenge of identifying additional HSTs whose activity may be masked by other toxins. Also, through mycelial staining, we acquire preliminary evidence that ToxA may provide additional benefits to fungal growth in planta in the absence of its cognate recognition partner in the host.

SUBMITTER: Manning VA

PROVIDER: S-EPMC4386829 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Necrotrophic effector epistasis in the Pyrenophora tritici-repentis-wheat interaction.

Manning Viola A VA Ciuffetti Lynda M LM

PloS one 20150406 4

Pyrenophora tritici-repentis, the causal agent of tan spot disease of wheat, mediates disease by the production of host-selective toxins (HST). The known toxins are recognized in an 'inverse' gene-for-gene manner, where each is perceived by the product of a unique locus in the host and recognition leads to disease susceptibility. Given the importance of HSTs in disease development, we would predict that the loss of any of these major pathogenicity factors would result in reduced virulence and di ...[more]

PMID: 25845019

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Project description:Tan spot is a destructive foliar wheat disease worldwide and caused by the ascomycete fungus Pyrenophora tritici-repentis (Ptr); it has become more frequent in Tunisia over the last decade. In this study, the virulence of 73 single-spore isolates, collected from durum and bread wheat fields during 2017-2018 growing season, was evaluated on four differential wheat genotypes. This was followed by polymerase chain reaction tests with specific primers for the effector genes ToxA, ToxB, and toxb (ToxB-homolog). Sequence analysis to validate the identity of the amplified genes was followed, and ToxA amplicons from a subset of 22 isolates were analyzed to determine its haplotype identity. Ptr isolates from Tunisia were grouped in races 2, 4, 5, and 7, and 44% of the tested isolates did not fit under any known race, and were denoted here as atypical. These atypical isolates induced the same symptoms as race 7 isolates, extensive necrosis, and chlorosis on susceptible genotypes, but lacked the ToxA gene. ToxA is the only identified necrosis-inducing effector in Ptr, and was amplified in 51% of tested isolates, and shared identical sequence to previously identified haplotype (H15). ToxB and its homolog toxb were present in 97% and 93% of tested isolates, respectively. Ptr in Tunisia lacked Ptr ToxC activity, and none of the tested isolates induced the specific symptoms of that effector. Race 7 and the atypical isolates dominated the Tunisian Ptr population, while races 2, 4, and 5 were found at low percentages. In conclusion, ToxB and its homolog were the most dominant genes in Ptr from Tunisia, and the majority of the isolates induced necrosis and chlorosis on Ptr ToxA and Ptr ToxB susceptible wheat genotypes. However, only about half of that necrosis can be attributed to ToxA presence, this result necessitates further research to investigate the prevalence of additional necrotic effector(s). Terminology: in this paper, Pyrenophora tritici-repentis abbreviated as Ptr, the effectors are referred to by Ptr ToxA, Ptr ToxB and Ptr ToxC, and the genes coding for them are written in italic as ToxA, ToxB, and ToxC, respectively.

Project description:BackgroundIn fungal plant pathogens, genome rearrangements followed by selection pressure for adaptive traits have facilitated the co-evolutionary arms race between hosts and their pathogens. Pyrenophora tritici-repentis (Ptr) has emerged recently as a foliar pathogen of wheat worldwide and its populations consist of isolates that vary in their ability to produce combinations of different necrotrophic effectors. These effectors play vital roles in disease development. Here, we sequenced the genomes of a global collection (40 isolates) of Ptr to gain insights into its gene content and genome rearrangements.ResultsA comparative genome analysis revealed an open pangenome, with an abundance of accessory genes (~ 57%) reflecting Ptr's adaptability. A clear distinction between pathogenic and non-pathogenic genomes was observed in size, gene content, and phylogenetic relatedness. Chromosomal rearrangements and structural organization, specifically around effector coding genes, were detailed using long-read assemblies (PacBio RS II) generated in this work in addition to previously assembled genomes. We also discovered the involvement of large mobile elements associated with Ptr's effectors: ToxA, the gene encoding for the necrosis effector, was found as a single copy within a 143-kb 'Starship' transposon (dubbed 'Horizon') with a clearly defined target site and target site duplications. 'Horizon' was located on different chromosomes in different isolates, indicating mobility, and the previously described ToxhAT transposon (responsible for horizontal transfer of ToxA) was nested within this newly identified Starship. Additionally, ToxB, the gene encoding the chlorosis effector, was clustered as three copies on a 294-kb element, which is likely a different putative 'Starship' (dubbed 'Icarus') in a ToxB-producing isolate. ToxB and its putative transposon were missing from the ToxB non-coding reference isolate, but the homolog toxb and 'Icarus' were both present in a different non-coding isolate. This suggests that ToxB may have been mobile at some point during the evolution of the Ptr genome which is contradictory to the current assumption of ToxB vertical inheritance. Finally, the genome architecture of Ptr was defined as 'one-compartment' based on calculated gene distances and evolutionary rates.ConclusionsThese findings together reflect on the highly plastic nature of the Ptr genome which has likely helped to drive its worldwide adaptation and has illuminated the involvement of giant transposons in facilitating the evolution of virulence in Ptr.

Project description:Key messageGenetic mapping of sensitivity to the Pyrenophora tritici-repentis effector ToxB allowed development of a diagnostic genetic marker, and investigation of wheat pedigrees allowed transmission of sensitive alleles to be tracked. Tan spot, caused by the necrotrophic fungal pathogen Pyrenophora tritici-repentis, is a major disease of wheat (Triticum aestivum). Secretion of the P. tritici-repentis effector ToxB is thought to play a part in mediating infection, causing chlorosis of plant tissue. Here, genetic analysis using an association mapping panel (n = 480) and a multiparent advanced generation intercross (MAGIC) population (n founders = 8, n progeny = 643) genotyped with a 90,000 feature single nucleotide polymorphism (SNP) array found ToxB sensitivity to be highly heritable (h2 ≥ 0.9), controlled predominantly by the Tsc2 locus on chromosome 2B. Genetic mapping of Tsc2 delineated a 1921-kb interval containing 104 genes in the reference genome of ToxB-insensitive variety 'Chinese Spring'. This allowed development of a co-dominant genetic marker for Tsc2 allelic state, diagnostic for ToxB sensitivity in the association mapping panel. Phenotypic and genotypic analysis in a panel of wheat varieties post-dated the association mapping panel further supported the diagnostic nature of the marker. Combining ToxB phenotype and genotypic data with wheat pedigree datasets allowed historic sources of ToxB sensitivity to be tracked, finding the variety 'Maris Dove' to likely be the historic source of sensitive Tsc2 alleles in the wheat germplasm surveyed. Exploration of the Tsc2 region gene space in the ToxB-sensitive line 'Synthetic W7984' identified candidate genes for future investigation. Additionally, a minor ToxB sensitivity QTL was identified on chromosome 2A. The resources presented here will be of immediate use for marker-assisted selection for ToxB insensitivity and the development of germplasm with additional genetic recombination within the Tsc2 region.

Dataset Information

Necrotrophic effector epistasis in the Pyrenophora tritici-repentis-wheat interaction.

Publications

Necrotrophic effector epistasis in the Pyrenophora tritici-repentis-wheat interaction.

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