Phased-genome assemblies of saltgrass reveal structural dynamics and genomic basis for extreme salt tolerance and dioecy

The climate crisis poses a critical challenge to agriculture, with freshwater scarcity becoming a major constraint on crop production. Harnessing halophytic adaptations for growth in saline environments offers a promising path for neodomestication of salt-tolerant crops. Distichlis spp. (saltgrass)-a genus of dioecious, halophytic C4 grasses in the PACMAD clade-thrives in extreme saline conditions, making it a compelling species to understand salinity tolerance and adaptation. Here, we present high-quality phased genome assemblies of four Distichlis genets, revealing an allotetraploid genome (576-610 Mb) with two highly syntenic but degenerate subgenomes, each exhibiting over 30% gene loss across orthologous pairs. Comparative genomic analyses uncovered a novel chromosome fusion event differentiating D. spicata (2n=40) and D. stricta (2n=38), highlighting a chromosomal rearrangement differentiating the species. Population genomic analysis of 364 genets across 35 populations demonstrated strong geographic differentiation and confirmed D. stricta as a distinct species. Additionally, we identified a 7 Mb B chromosome in two genets, displaying common features shared with B chromosomes in other species. Using k-mer analyses of sex-typed populations, we identified an 8 Mb sex-determining region in female genets with 24 candidate genes, confirming that Distichlis has a ZW-type sex determination. Expression profiling of plants under extreme (seawater-level) salinity revealed key salt-tolerance genes that are also implicated in drought resilience, suggesting an overlapping genetic basis for these stress responses. These genomic resources establish a foundation for neodomestication of saltgrass as a climate-resilient crop for saline agroecosystems and enhance our understanding of genome evolution in halophytic grasses.