A chromosome‐level Amaranthus cruentus genome assembly highlights gene family evolution and biosynthetic gene clusters that may underpin the nutritional value of this traditional crop

Summary Traditional crops have historically provided accessible and affordable nutrition to millions of rural dwellers but have been neglected, with most modern agricultural systems over‐reliant on a small number of internationally traded crops. Traditional crops are typically well‐adapted to local agro‐ecological conditions and many are nutrient‐dense. They can play a vital role in local food systems through enhanced nutrition (particularly where diets are dominated by starch crops), food security and livelihoods for smallholder farmers, and a climate‐resilient and biodiverse agriculture. Using short‐read, long‐read and phased sequencing technologies, we generated a high‐quality chromosome‐level genome assembly for Amaranthus cruentus, an under‐researched crop with micronutrient‐ and protein‐rich leaves and gluten‐free seed, but lacking improved varieties, with respect to productivity and quality traits. The 370.9 Mb genome demonstrates a shared whole genome duplication with a related species, Amaranthus hypochondriacus. Comparative genome analysis indicates chromosomal loss and fusion events following genome duplication that are common to both species, as well as fission of chromosome 2 in A. cruentus alone, giving rise to a haploid chromosome number of 17 (versus 16 in A. hypochondriacus). Genomic features potentially underlying the nutritional value of this crop include two A. cruentus‐specific genes with a likely role in phytic acid synthesis (an anti‐nutrient), expansion of ion transporter gene families, and identification of biosynthetic gene clusters conserved within the amaranth lineage. The A. cruentus genome assembly will underpin much‐needed research and global breeding efforts to develop improved varieties for economically viable cultivation and realization of the benefits to global nutrition security and agrobiodiversity. Significance Statement Our chromosomal‐level Amaranthus cruentus genome assembly will drive genetic improvement of this traditional crop. Amaranthus cruentus can play a key role in enhancing dietary diversity and nutrition world‐wide, as well as increased food security, climate resilience and livelihoods in low‐input smallholder agricultural systems. The genome sequence facilitates improvement of grain and leafy vegetable traits and our analysis identifies gene family expansion and biosynthetic gene clusters that may underlie the nutritional value of this underutilized crop. ​