The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut

Authors: COHEN, ALANNA - Rutgers University; Cai, Guohong; PRICE, DANA - Rutgers University; MOLNAR, THOMAS - Rutgers University; ZHANG, NING - Rutgers University; HILLMAN, BRADLEY - Rutgers University

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/7/2024
Publication Date: 4/5/2024
Citation: Cohen, A., Cai, G., Price, D.C., Molnar, T., Zhang, N., Hillman, B. 2024. The massive 340 megabase genome of Anisogramma anomala, a biotrophic ascomycete that causes eastern filbert blight of hazelnut. BMC Genomics. https://doi.org/10.1186/s12864-024-10198-1.
DOI: https://doi.org/10.1186/s12864-024-10198-1

Interpretive Summary: The ascomycete Anisogramma anomala causes Eastern Filbert Blight (EFB) on hazelnut trees. It’s a minor disease on its native host, the American hazelnut (C. americana). However, it is life threatening on the commercially important European hazelnut (C. avellana). EFB limits commercial production of hazelnut to west of the Rocky Mountains in the United States. A. anomala is an obligate fungus and only sexual stage has been observed. There is a 15-months latency before symptoms showing up on infected hazelnut trees. Despite its economic importance, the life cycle of this fungus presents great obstacle for studying it. Here we report the sequencing, annotation and characterization of its genome. This study reveals the genomic structure, composition, and putative gene function of the important pathogen A. anomala. It provides insight into the molecular basis of the pathogen’s life cycle and a solid foundation for studying EFB.

Technical Abstract: Background: The ascomycete fungus Anisogramma anomala causes Eastern Filbert Blight (EFB) on hazelnut (Corylus spp.) trees. It is a minor disease on its native host, the American hazelnut (C. americana), but is highly destructive on the commercially important European hazelnut (C. avellana). In North America, EFB has historically limited commercial production of hazelnut to west of the Rocky Mountains. A. anomala is an obligately biotrophic fungus that has not been grown in continuous culture, rendering its study challenging. There is a 15-month latency before symptoms appear on infected hazelnut trees, and only a sexual reproductive stage has been observed. Here we report the sequencing, annotation, and characterization of its genome. Results: The genome of A. anomala was assembled into 112 scaffolds totaling 342,525,599 nt with a GC content of 34.46%. Scaffold N50 was 33.3 Mb and L50 was 5. Nineteen scaffolds with lengths over 1 Mb constituted 99% of the assembly. Telomere sequences were identified on both ends of four scaffolds and on one end of another 10 scaffolds. Flow cytometry estimated the genome size of A. anomala at 370 Mb. The genome exhibits two-speed evolution, with 93% of the assembly as AT-rich regions (32.9% GC) and the other 7% as GC-rich (57.1% GC). The AT-rich regions consist predominantly of repeats with low gene content, while 90% of predicted protein coding genes were identified in GC-rich regions. Copia-like retrotransposons accounted for more than half of the genome. Evidence of repeat-induced point mutation (RIP) was identified throughout the AT-rich regions, and two copies of the rid gene, the key gene in the RIP mutation pathway, were identified in the genome. Consistent with its homothallic sexual reproduction cycle, both MAT1-1 and MAT1-2 idiomorphs were found. We identified a large suite of genes likely involved in pathogenicity, including 456 carbohydrate active enzymes, 762 secreted proteins and 165 effectors. Conclusions: This study reveals the genomic structure, composition, and putative gene function of the important pathogen A. anomala. It provides insight into the molecular basis of the pathogen’s life cycle and a solid foundation for studying EFB.