A comparative genomic analysis of the barley pathogen Pyrenophora teres f. teres identifies sub-telomeric regions as drivers of virulence

Authors: WYATT, NATHAN - North Dakota State University; RICHARDS, JONATHAN - North Dakota State University; BRUEGGEMAN, ROBERT - North Dakota State University; Friesen, Timothy

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2019
Publication Date: 1/28/2020
Citation: Wyatt, N.A., Richards, J.K., Brueggeman, R.S., Friesen, T.L. 2020. A comparative genomic analysis of the barley pathogen Pyrenophora teres f. teres identifies sub-telomeric regions as drivers of virulence. Molecular Plant-Microbe Interactions. 33:173-188. https://doi.org/10.1094/MPMI-05-19-0128-R.
DOI: https://doi.org/10.1094/MPMI-05-19-0128-R

Interpretive Summary: Net form net blotch (NFNB), caused by the fungal pathogen Pyrenophora teres f. teres, is a destructive disease of barley wherever barley is grown and is currently a major problem in malting barley production in the Northern Great Plains. More comprehensive genetic and genomic information is needed to investigate how the pathogen attacks barley in order to better breed for durable disease resistance. In the current work, we assembled, annotated, and compared five complete reference quality genome sequences. The five annotated sequences were then used to show that pathogen genes involved in disease induction (virulence) on barley were localized to evolutionarily active accessory regions of the genome that are highly variable between isolates. This variability shows the potential of these accessory regions to be important drivers of adaptation on local barley cultivars. This information is valuable to barley breeders and geneticist working on host resistance in that it shows the high potential of adaptation that the NFNB pathogen harbors. This potential for adaptation in the pathogen population directly impacts the durability of any locally deployed disease resistance.

Technical Abstract: Pyrenophora teres f. teres causes net form net blotch of barley and is an economically important pathogen throughout the world. However, P. teres f. teres is lacking in genomic resources necessary to characterize the mechanisms of virulence. Recently a high quality reference genome was generated for P. teres f. teres isolate 0-1. Here, we present the reference quality sequence and annotation of four new isolates and we use the five available P. teres f. teres genomes for an in-depth comparison resulting in the generation of hypotheses pertaining to the potential mechanisms and evolution of virulence. Comparative analyses were performed between all five P. teres f. teres genomes examining genomic organization, structural variations, and core and accessory genomic content, specifically focusing on the genomic characterization of known virulence loci and the localization of genes predicted to encode secreted and effector proteins. We showed that 14 of 15 currently published virulence QTL span accessory genomic regions consistent with these accessory regions being important drivers of host adaptation. Additionally, these accessory genomic regions were frequently found in sub-telomeric regions of chromosomes with 10 of the 14 accessory region QTL localizing to sub-telomeric regions. Comparative analysis of the sub-telomeric regions of P. teres f. teres chromosomes revealed disjointed synteny where homology was detected between non-homologous chromosomes at a significantly higher rate than the rest of the genome. These results indicate that the sub-telomeric accessory genomic compartments not only harbor most of the known virulence loci, but also that these regions have the capacity to rapidly evolve.