The genome of Chenopodium ficifolium: developing genetic resources and a diploid model system for allotetraploid quinoa.

High-quality nuclear, chloroplast, and preliminary mitochondrial genomes have been assembled and annotated for the B genome diploid (BB: 2n = 2x = 18) figleaf goosefoot (Chenopodium ficifolium). The primary objective was to advance a simplified model system for genetic characterization and improvement of allotetraploid (AABB: 2n = 4x = 36) quinoa (Chenopodium quinoa), a nutritionally valuable, halophytic orphan crop. In addition to its diploidy and favorably small genome size, the C. ficifolium model provides a shorter generational period and smaller overall plant size as compared to C. quinoa, while displaying relevant agronomic trait variations amenable to gene-trait association studies. The C. ficifolium "Portsmouth" nuclear genome was sequenced using PacBio HiFi long-read technology and assembled using Hifiasm. After manual adjustments, the final ChenoFicP_1.0 assembly consisted of 9 pseudochromosomes spanning 730 Mbp, while 22,617 genes were identified and annotated. BUSCO analyses indicated a nuclear genome completeness of 97.5% and a proteome and transcriptome completeness of 98.4%. The chloroplast genome assembly detected 2 equally represented structural haplotypes differing in the orientation of the short single copy region relative to the long single copy region. Phylogenetic and parentage analyses pointed to an unspecified AA diploid species and away from C. ficifolium as the likely maternal chloroplast and mitochondrial genome donor(s) during the initial tetraploidization event in the C. quinoa lineage. Using the new ChenoFicP_1.0 reference genome, a genome-wide association study was performed on a previously studied C. ficifolium F2 population to further define region(s) implicated in the control of 3 key agronomic traits: days to flowering, plant height, and branch number. This analysis localized control of all 3 traits to a 7-Mb interval on pseudochromosome Cf4. This region contains ∼770 genes, including the FTL1 locus, thus confirming and extending our prior, single-marker analysis showing association of these 3 traits with an FTL1 amplicon length polymorphism. The use of these data to further develop C. ficifolium as a model species for genetics and breeding of quinoa serves to expand knowledge and germplasm resources for quinoa improvement.