A pangenome reveals LTR repeat dynamics as a major driver of genome evolution in Chenopodium

The genus Chenopodium L. is characterized by its wide geographic distribution and ecological adaptability. Species such as quinoa (Chenopodium quinoa Willd.) have served as domesticated staple crops for centuries. Wild Chenopodium species exhibit diverse niche adaptations and are important genetic reservoirs for beneficial agronomic traits, including disease resistance and climate hardiness. To harness the potential of the wild taxa for crop improvement, we developed a Chenopodium pangenome through the assembly and comparative analyses of 12 Chenopodium species that encompass the eight known genome types (A-H). Six of the species are new chromosome-scale assemblies, and many are polyploids; thus, a total of 20 genomes were included in the pangenome analyses. We show that the genomes vary dramatically in size with the D genome being the smallest (∼370 Mb) and the B genome being the largest (∼700 Mb) and that genome size was correlated with independent expansions of the Copia and Gypsy LTR retrotransposon families, suggesting that transposable elements have played a critical role in the evolution of the Chenopodium genomes. We annotated a total of 33,457 pan-Chenopodium gene families, of which ∼65% were classified as shell (2% private). Phylogenetic analysis clarified the evolutionary relationships among the genome lineages, notably resolving the taxonomic placement of the F genome while highlighting the uniqueness of the A genome in the Western Hemisphere. These genomic resources are particularly important for understanding the secondary and tertiary gene pools available for the improvement of the domesticated chenopods while furthering our understanding of the evolution and complexity within the genus.