Common buckwheat (Fagopyrum esculentum) is an ancient crop with a world-wide distribution. Due to its excellent nutritional quality and high economic and ecological value, common buckwheat is becoming increasingly important throughout the world. The availability of a high-quality reference genome sequence and population genomic data will accelerate the breeding of common buckwheat, but the high heterozygosity due to the outcrossing nature has greatly hindered the genome assembly. Here we report the assembly of a chromosome-scale high-quality reference genome of F. esculentum var. homotropicum, a homozygous self-pollinating variant of common buckwheat. Comparative genomics revealed that two cultivated buckwheat species, common buckwheat (F. esculentum) and Tartary buckwheat (F. tataricum), underwent metabolomic divergence and ecotype differentiation. The expansion of several gene families in common buckwheat, including FhFAR genes, is associated with its wider distribution than Tartary buckwheat. Copy number variation of genes involved in the metabolism of flavonoids is associated with the difference of rutin content between common and Tartary buckwheat. Furthermore, we present a comprehensive atlas of genomic variation based on whole-genome resequencing of 572 accessions of common buckwheat. Population and evolutionary genomics reveal genetic variation associated with environmental adaptability and floral development between Chinese and non-Chinese cultivated groups. Genome-wide association analyses of multi-year agronomic traits with the content of flavonoids revealed that Fh05G014970 is a potential major regulator of flowering period, a key agronomic trait controlling the yield of outcrossing crops, and that Fh06G015130 is a crucial gene underlying flavor-associated flavonoids. Intriguingly, we found that the gene translocation and sequence variation of FhS-ELF3 contribute to the homomorphic self-compatibility of common buckwheat. Collectively, our results elucidate the genetic basis of speciation, ecological adaptation, fertility, and unique flavor of common buckwheat, and provide new resources for future genomics-assisted breeding of this economically important crop.

Agricultural Institute of Slovenia Hacquetova ulica Ljubljana Slovenia

Annoroad Gene Technology Co Ltd Beijing 100176 China

Biological Sciences University of Southampton Life Sciences Building 85 Highfield Campus Southampton SO17 1BJ UK

Biotechnical Faculty University of Ljubljana 1000 Ljubljana Slovenia

Biotechnical Faculty University of Ljubljana 1000 Ljubljana Slovenia; Nutrition Institute Tržaška 40 1000 Ljubljana Slovenia

College of Agriculture Institute of Agricultural Bioengineering Shanxi Agricultural University Taigu 030801 Shanxi China; Shanxi Key Laboratory of Minor Crops Germplasm Innovation and Molecular Breeding Shanxi Agricultural University Taiyuan 030031 Shanxi China

Gene Bank Crop Research Institute Drnovská 507 Prague 6 Czech Republic

Groupe de Recherche en Physiologie Végétale Université Catholique de Louvain Croix du Sud 4 5 boîte L7 07 13 B 1348 Louvain la Neuve Belgium

Institute of Crop Sciences Chinese Academy of Agricultural Sciences National Crop Genebank Building Zhongguancun South Street No 12 Haidian District Beijing 100081 China

Institute of Crop Sciences Chinese Academy of Agricultural Sciences National Crop Genebank Building Zhongguancun South Street No 12 Haidian District Beijing 100081 China; College of Agronomy Sichuan Agricultural University Chengdu 611130 China

Laboratory of Metabolomics Institute of Microbiology Bulgarian Academy of Sciences Plovdiv Bulgaria; Center of Plant Systems Biology and Biotechnology Plovdiv Bulgaria

Molecular Plant Breeding Institute of Agricultural Sciences ETH Zurich Universitaetstrasse 2 8092 Zurich Switzerland

Tongliao Institute Agricultural and Animal Husbandry Sciences Tongliao 028015 Inner Mongolia China

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