Pan-parastagonospora comparative genome analysis - effector prediction and genome evolution

Authors: SYME, ROBERT - Curtin University; TAN, KAR-CHUN - Curtin University; RYBAK, KASIA - Curtin University; Friesen, Timothy; MCDONALD, BRUCE - Swiss Federal Institute Of Technology Zurich; OLIVER, RICHARD - Curtin University; HANE, JAMES - Curtin University

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/3/2018
Publication Date: 9/4/2018
Citation: Syme, R.A., Tan, K., Rybak, K., Friesen, T.L., McDonald, B.A., Oliver, R.P., Hane, J.K. 2018. Pan-parastagonospora comparative genome analysis - effector prediction and genome evolution. Genome Biology and Evolution. 10(9):2443-2457. https://doi.org/10.1093/gbe/evy192.
DOI: https://doi.org/10.1093/gbe/evy192

Interpretive Summary: Parastagonospora nodorum causal agent of septoria nodorum blotch (SNB) has been a major problem for wheat growers worldwide. SNB results in both quality and yield losses due to the fungus infecting both the leaves and glumes. Here we compared the genomes of 21 isolates of P. nodorum, ten isolates of the grass infecting P. avenae as well as two additional Parastagonospora spp. isolates of an undefined sister species. High levels of polymorphism were identified within and between species including gene presence-absence variation suggesting chromosome variation as well as the potential of dispensable chromosomes that are present in only some of the isolates. The known necrotrophic effectors SnToxA, SnTox1, and SnTox3 showed presence-absence polymorphism among the P. nodorum isolates and both SnTox1 and SnTox3 were identified in different combinations in some of the P. avenae isolates. This Pan-genome analysis will be useful information for the identification of genes involved in virulence as well as providing testable hypotheses on various aspects of genome evolution contributing to changes in pathogen virulence that ultimately affects wheat quality and yield.

Technical Abstract: We report a fungal pan-genome study involving Parastagonospora spp., including 21 isolates of the wheat (Triticum aestivum) pathogen Parastagonospora nodorum, 10 of the grass-infecting Parastagonospora avenae, and 2 of a closely related undefined sister species. We observed substantial variation in the distribution of polymorphisms across the pan-genome, including repeat-induced point mutations, diversifying selection and gene gains and losses. We also discovered chromosome-scale inter and intraspecific presence/absence variation of some sequences, suggesting the occurrence of one or more accessory chromosomes or regions that may play a role in host–pathogen interactions. The presence of known pathogenicity effector loci SnToxA, SnTox1, and SnTox3 varied substantially among isolates. Three P. nodorum isolates lacked functional versions for all three loci, whereas three P. avenae isolates carried one or both of the SnTox1 and SnTox3 genes, indicating previously unrecognized potential for discovering additional effectors in the P. nodorum-wheat pathosystem. We utilized the pan-genomic comparative analysis to improve the prediction of pathogenicity effector candidates, recovering the three confirmed effectors among our top-ranked candidates. We propose applying this pan-genomic approach to identify the effector repertoire involved in other host–microbe interactions involving necrotrophic pathogens in the Pezizomycotina.