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DOI: 10.1101/2023.05.24.542141

The genome of Salmacisia buchloëana, the parasitic puppetmaster pulling strings of sexual phenotypic monstrosities in buffalograss

C. W.Benson M. R. Sheltra D. R. Huff
To complete its parasitic lifecycle, Salmacisia buchloeana, a biotrophic fungus, manipulates reproductive organ development, meristem determinacy, and resource allocation in its dioecious plant host, buffalograss (Bouteloua dactyloides; Poaceae). To gain insight into S. buchloeana's ability to manipulate its host, we sequenced and assembled the 20.1 Mb genome of S. buchloeana into 22 chromosome-level pseudomolecules. Phylogenetic analysis suggests that S. buchloeana is nested within the genus Tilletia and diverged from T. caries and T. walkeri ~40 million years ago. We find that S. buchloeana has a novel chromosome arm with no syntenic relationship to other publicly available Tilletia genomes and that genes on the novel arm are upregulated upon infection, suggesting that this unique chromosomal segment may have played a critical role in S. buchloeana's evolution and host specificity. Salmacisia buchloeana has one of the largest fractions of serine peptidases (1.53% of the proteome) and one of the highest GC contents (62.3%) in all classified fungi. Analysis of codon base composition indicated that GC content is controlled more by selective constraints than directional mutation and that S. buchloeana has a unique bias for the serine codon UCG. Finally, we identify three inteins within the S. buchloeana genome, two of which are located in a gene often used in fungal taxonomy. The genomic and transcriptomic resources generated here will aid plant pathologists and breeders by providing insight into the extracellular components contributing to sex determination in dioecious grasses.