Chromosome-scale nuclear and mitochondrial genome assemblies reveal extreme genome compartmentalization in the hazelnut pathogen Anisogramma anomala

Abstract

Anisogramma anomala is an obligate biotrophic ascomycete and the causal agent of Eastern filbert blight, the most economically important disease of hazelnut in the United States. Here, we generated a chromosome-scale reference genome for A. anomala isolate OR-Ennis-d and characterized its nuclear and mitochondrial genome architecture. The 344-Mb nuclear genome was resolved into 9 predicted chromosomes and is repeat-rich, with transposable elements comprising 88.8% of the assembly. Although transposable elements are abundant, their divergence landscape and low retention of conserved protein domains support a history of past extensive transposon proliferation followed by widespread degeneration. Repeat accumulation was highly uneven and generated pronounced genome compartmentalization. Approximately half of predicted genes occur in compact, TE-poor regions with short flanking intergenic regions that are enriched for conserved BUSCO orthologs. In contrast, genes in TE-rich, gene-sparse regions with long flanking intergenic regions are enriched for carbohydrate-active enzymes, secreted proteins, and candidate secreted effector proteins, consistent with a two-speed-like genome architecture. The 462-kb mitochondrial genome is among the largest reported for ascomycetes and contains 117 introns, including an intron adjacent to cob codon 143 that may prevent acquisition of the p.G143A substitution associated with resistance to quinone outside inhibitor fungicides. Finally, we identified mitochondrial DNA insertions at 20 nuclear loci totaling at least 616.9 kb, an unusually extensive amount for a fungal genome. This chromosome-scale genome resource reveals the extreme nuclear and mitochondrial genome architecture in A. anomala and provides a foundation for investigating genome evolution and adaptation to hazelnut resistance.