The <i>Xenopyricularia zizaniicola</i> exhibits a genome architecture distinct to the two-speed genome

The fungal pathogens exhibit diverse genome architecture, which facilitates the host adaptation. Although increasing high-quality genomic data enable insights into the genome architecture of many fungal pathogens during the last decades, genomic features of many fungal species are still not fully characterized. Here, we identified a <i>Pyriculariaceae</i> family fungal strain <i>Xenopyricularia zizaniicola</i> JB-1 causing the leaf spot disease on <i>Zizania latifolia</i> and revealed its distinct genome compartment features. The fungal strain JB-1 was identified as <i>X. zizaniicola</i> based on the Koch's postulate, conidial morphology, and phylogenetic analysis. Using 2.51 Gb PacBio HiFi sequencing data, the JB-1 genome was assembled into nine contigs, five of which contain telomeric repeats at both ends. The genome size is 40,888,459 bp with an N50 of 6,431,016 bp, and a total of 9,894 protein-coding genes were predicted. BUSCO assessment demonstrated high completeness, with 754 (99.47%) of the 758 BUSCO orthologs identified as complete. The absence of both repeat-rich regions at chromosome ends and preferential residing of pathogenicity-associated genes (PAGs) in the repeat-rich regions indicated a genome compartment dissimilar to the "two-speed genome" commonly observed in <i>Pyricularia oryzae</i>, indicating a distinct evolution drive of the PAGs in <i>X. zizaniicola</i> strain JB-1. Additionally, the JB-1 genome encodes fewer PAGs compared to other members of family <i>Pyriculariaceae</i>. These findings provide valuable genomic resources of family <i>Pyriculariaceae</i> and will facilitate future studies on host-pathogen interactions and the development of effective disease management strategies for <i>X. zizaniicola</i>.IMPORTANCEThe family <i>Pyriculariaceae</i> includes notorious pathogens that annually result in significant agricultural losses. The genome architecture of plant fungal pathogens reflects their evolutionary adaptation to host-pathogen interactions. However, limited knowledge exists regarding the genomic features of other species within family <i>Pyriculariaceae</i>, particularly those associated with the economically important crop <i>Zizania latifolia</i>. In this study, we assembled the first high-quality genome of <i>Xenopyricularia zizaniicola</i> strain JB-1, which infects <i>Z. latifolia</i>, and revealed its distinct genome architecture. We provide evidence that the distribution pattern of pathogenicity-associated genes in <i>X. zizaniicola</i> strain JB-1 closely resembles the "one-speed genome" structure, which contrasts with <i>Pyricularia oryzae</i>. Our findings provide valuable resources for genomic studies within family <i>Pyriculariaceae</i> and contribute to our understanding of the adaptive evolution of pathogens to their hosts.