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

TL;DR

This study explores the genome of waterhemp, focusing on the sex-determination region and PEBP gene family, offering insights into its evolution and genetic diversity.

Contribution

The study provides a high-quality genome assembly and identifies a sex-associated region with unique genomic features and gene expression patterns.

Findings

A ~31.8 Mb sex-associated region on chromosome 1 was identified, rich in LTR retrotransposons and containing gene expression differences between male and female flowers.

Synteny analysis suggests chromosome 1 originated from the fusion of two ancestral chromosomes.

The PEBP gene family was characterized, shedding light on FLOWERING LOCUS T diversity in amaranths.

Abstract

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.

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.

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.

The online version contains supplementary material available at 10.1186/s12864-025-12181-w.

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