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

Abstract

AbstractTo complete its parasitic lifecycle,Salmacisia buchloëana, a biotrophic fungus, manipulates reproductive organ development, meristem determinacy, and resource allocation in its dioecious plant host, buffalograss (Bouteloua dactyloides;Poaceae). To gain insight intoS. buchloëana’sability to manipulate its host, we sequenced and assembled the 20.1 Mb genome ofS. buchloëanainto 22 chromosome-level pseudomolecules. Phylogenetic analysis suggests thatS. buchloëanais nested within the genusTilletiaand diverged fromT. cariesandT. walkeri ∼40 million years ago. We find thatS. buchloëanahas a novel chromosome arm with no syntenic relationship to other publicly availableTilletiagenomes and that genes on the novel arm are upregulated upon infection, suggesting that this unique chromosomal segment may have played a critical role inS. buchloëana’sevolution and host specificity.Salmacisia buchloëanahas 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 thatS. buchloëanahas a unique bias for the serine codon UCG. Finally, we identify three inteins within theS. buchloëanagenome, 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.