Analyses of contiguous reference genomes of Amaranthus tuberculatus highlight the landscape of the sex-associated region and PEBP gene family diversity.

BACKGROUND

Amaranthus tuberculatus (waterhemp) is a troublesome agronomic weed species that is dioecious with an XY sex-determination system. The evolution of the sex-determining region (SDR), the contiguity of the region, genomic landscape, and the expression pattern of genes within the region remain poorly understood.

RESULTS

We assembled a high-quality, chromosome-level nuclear genome and chloroplast and mitochondrial genomes of a male A. tuberculatus. Combining the genomes with restriction site-associated DNA genome-wide association (RAD-GWA) analysis, comparative genomics, adaptive evolution analysis, and transcriptomic profiling, we identified a ~ 31.8 Mb region on chromosome 1 that is strongly associated with sex. This region is gene-poor, abundant in long terminal repeat (LTR) retrotransposons, and harbors two inversions and a 3.19 Mb haplotype-specific region. Synteny analysis revealed that chromosome 1 likely originated from the fusion of two ancestral chromosomes, and mRNA analysis indicated 76 genes out of the 528 protein-coding genes within the putative SDR of Hap1 were differentially expressed between mature male and female flowers, with several of the genes enriched for Gene Ontology (GO) terms involved in floral development. We further characterized the phosphatidylethanolamine binding protein (PEBP) family in A. tuberculatus and related species to gain insights into FLOWERING LOCUS T diversity, as well as identified nuclear insertions of organellar origin in the species.

CONCLUSION

Our results provide insight into the evolution of a sex-associated region in a weedy dioecious species, and the diversity of the PEBP protein family in amaranths. The genomic resources from this study will also be valuable for addressing further questions on adaptive trait evolution within the genus as well as questions surrounding dioecy in this and other plant species.