BACKGROUND: Tartary buckwheat (Fagopyrum tataricum) is a nutritionally balanced and flavonoid-rich crop plant that has been in cultivation for 4000 years and is now grown globally. Despite its nutraceutical and agricultural value, the characterization of its genetics and its domestication history is limited. RESULTS: Here, we report a comprehensive database of Tartary buckwheat genomic variation based on whole-genome resequencing of 510 germplasms. Our analysis suggests that two independent domestication events occurred in southwestern and northern China, resulting in diverse characteristics of modern Tartary buckwheat varieties. Genome-wide association studies for important agricultural traits identify several candidate genes, including FtUFGT3 and FtAP2YT1 that significantly correlate with flavonoid accumulation and grain weight, respectively. CONCLUSIONS: We describe the domestication history of Tartary buckwheat and provide a detailed resource of genomic variation to allow for genomic-assisted breeding in the improvement of elite cultivars.

Agricultural Institute of Slovenia Hacquetova ulica Ljubljana Slovenia

BGI Genomics BGI Shenzhen Shenzhen 58083 Guangdong China

Biotechnical Faculty University of Ljubljana Jamnikarjeva 101 SI 1000 Ljubljana Slovenia

Center of Plant Systems Biology and Biotechnology Plovdiv Bulgaria

College of Horticulture China Agricultural University Beijing 100083 China

Department of Botany North Eastern Hill University Shillong 793022 India

Department of Crop Science Chungbuk National University Cheong ju Republic of Korea

Department of Plant Breeding and Seed Production University of Warmia and Mazury in Olsztyn Plac Łódzki 3 10 724 Olsztyn Poland

Gene Bank Crop Research Institute Drnovská 507 Prague 6 Czech Republic

Group of Plant Cell Biotechnology and Metabolomics The Stephan Angeloff Institute of Microbiology Bulgarian Academy of Sciences Plovdiv Bulgaria

Groupe de Recherche en Physiologie Végétale Université catholique de Louvain Croix du Sud 45 boîte L7 07 13 B 1348 Louvain la Neuve Belgium

Institute of Crop Sciences Chinese Academy of Agricultural Sciences Room 107 Ziyuan North Building Xueyuan South Road No 80 Haidian District Beijing 100081 China

Kyushu Okinawa Agricultural Research Center National Agriculture and Food Research Organization Suya 2421 Koshi Kumamoto 861 1192 Japan

N 1 Vavilov All Russian Institute of Plant Genetic Resources Bol'shaya Morskaya 42 44 St Petersburg Russia 190000

Research Station of Alpine Crop Xichang Institute of Agricultural Sciences Liangshan 616150 Sichuan China

Zobrazit více v PubMed

Joshi DC, Zhang K, Wang C, Chandora R, Khurshid M, Li J, et al. Strategic enhancement of genetic gain for nutraceutical development in buckwheat: a genomics-driven perspective. Biotechnol Adv 2020;39:107479. PubMed

Joshi DC, Chaudhari GV, Sood S, Kant L, Pattanayak A, Zhang K, et al. Revisiting the versatile buckwheat: reinvigorating genetic gains through integrated breeding and genomics approach. Planta. 2019;250:783–801. doi: 10.1007/s00425-018-03080-4. PubMed DOI

Hunt HV, Shang X, Jones MK. Buckwheat: a crop from outside the major Chinese domestication centres? A review of the archaeobotanical, palynological and genetic evidence. Veget Hist Archaeobot. 2018;27:493–506. PubMed PMC

Bonafaccia G, Fabjan N. Nutritional comparison of tartary buckwheat with common buckwheat and minor cereals. Zb Bioteh Fak Univ Ljublj Kmet. 2003;81:349–355.

Xu P, Wang S, Yu X, Su Y, Wang T, Zhou W, et al. Rutin improves spatial memory in Alzheimer’s disease transgenic mice by reducing Aβ oligomer level and attenuating oxidative stress and neuroinflammation. Behav Brain Res. 2014;264:173–180. doi: 10.1016/j.bbr.2014.02.002. PubMed DOI

Pan RY, Ma J, Kong XX, Wang XF, Li SS, Qi XL, et al. Sodium rutin ameliorates Alzheimer’s disease-like pathology by enhancing microglial amyloid-β clearance. Sci Adv. 2019;5:eaau6328. doi: 10.1126/sciadv.aau6328. PubMed DOI PMC

Ohnishi O. Search for the wild ancestor of buckwheat I. Description of new Fagopyrum (Polygonaceae) species and their distribution in China and the Himalayan hills. Fagopyrum. 1998;15:18–28.

Ohnishi O. Search for the wild ancestor of buckwheat III. The wild ancestor of cultivated common buckwheat, and of Tatary buckwheat. Econ Bot. 1998;52:123. doi: 10.1007/BF02861199. DOI

Ohnishi O, Konishi T. Cultivated and wild buckwheat species in eastern Tibet. Fagopyrum. 2001;18:3–8.

Yasui Y, Hirakawa H, Ueno M, Matsui K, Katsube-Tanaka T, Yang SJ, et al. Assembly of the draft genome of buckwheat and its application in identifying agronomically useful genes. DNA Res. 2016;23:215–224. doi: 10.1093/dnares/dsw012. PubMed DOI PMC

Zhang L, Li X, Ma B, Gao Q, Du H, Han Y, et al. The Tartary buckwheat genome provides insights into rutin biosynthesis and abiotic stress tolerance. Mol Plant. 2017;10:1224–1237. doi: 10.1016/j.molp.2017.08.013. PubMed DOI

Varshney RK, Saxena RK, Upadhyaya HD, Khan AW, Yu Y, Kim C, et al. Whole-genome resequencing of 292 pigeonpea accessions identifies genomic regions associated with domestication and agronomic traits. Nat Genet. 2017;49:1082–1088. doi: 10.1038/ng.3872. PubMed DOI

Varshney RK, Thudi M, Rookiwal M, He W, Upadhyaya HD, Yang W, et al. Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet. 2019;51:857–864. doi: 10.1038/s41588-019-0401-3. PubMed DOI

Fan W, Lu J, Pan C, Tan M, Lin Q, Liu W, et al. Sequencing of Chinese castor lines reveals genetic signatures of selection and yield-associated loci. Nat Commun. 2019;10:3418. doi: 10.1038/s41467-019-11228-3. PubMed DOI PMC

Zhou Z, Jiang Y, Wang Z, Gou Z, Lyu J, Li W, et al. Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean. Nat Biotechnol. 2015;33:408–414. doi: 10.1038/nbt.3096. PubMed DOI

Raizada A, Souframanien J. Transcriptome sequencing, de novo assembly, characterisation of wild accession of blackgram (Vigna mungo var. silvestris) as a rich resource for development of molecular markers and validation of SNPs by high resolution melting (HRM) analysis. BMC Plant Biol. 2019;19:358. doi: 10.1186/s12870-019-1954-0. PubMed DOI PMC

Bhardwaj A, Dhar YV, Asif MH, Bag SK. In silico identification of SNP diversity in cultivated and wild tomato species: insight from molecular simulations. Sci Rep. 2016;6:38715. doi: 10.1038/srep38715. PubMed DOI PMC

Batley J, Barker G, O'Sullivan H, Edwards KJ, Edwards D. Mining for single nucleotide polymorphisms and insertions/deletions in maize expressed sequence tag data. Plant Physiol. 2003;132:84–91. doi: 10.1104/pp.102.019422. PubMed DOI PMC

Yasui Y, Ohnishi O. Phylogenetic relationships among Fagopyrum species revealed by nucleotide sequence of the ITS region of the nuclear rRNA gene. Genes Genet Syst. 1998;73:201–210. doi: 10.1266/ggs.73.201. PubMed DOI

Honda Y, Mukasa Y, Suzuki T, Abe N. Stone buckwheat, genetic resources of buckwheat in Japan. In: “9th Int Symp Buckwheat”, Prague. 2004; pp.185–9.

Suzuki T, Morishita T, Mukasa Y, Takegawa S, Yokota S, Ishiguro K, et al. Discovery and genetic analysis of non-bitter Tartary buckwheat (Fagopyrum tataricum Gaertn.) with trace-rutinosidase activity. Breeding Sci. 2014;64:339–343. doi: 10.1270/jsbbs.64.339. PubMed DOI PMC

Sano M, Nakagawa M, Oishi A, Yasui Y, Katsube-Tanaka T. Diversification of 13S globulins, allergenic seed storage proteins, of common buckwheat. Food Chem. 2014;155:192–198. doi: 10.1016/j.foodchem.2014.01.047. PubMed DOI

Huang C, Zhang R, Gui J, Zhong Y, Li L. The receptor-like kinase AtVRLK1 regulates secondary cell wall thickening. Plant Physiol. 2018;177:671–683. doi: 10.1104/pp.17.01279. PubMed DOI PMC

Feng H, Chen Q, Feng J, Zhang J, Yang X, Zuo J. Functional characterization of the Arabidopsis eukaryotic translation initiation factor 5A-2 that plays a crucial role in plant growth and development by regulating cell division, cell growth, and cell death. Plant Physiol. 2007;144:1531–1545. doi: 10.1104/pp.107.098079. PubMed DOI PMC

Zhou J, Li CL, Gao F, Luo XP, Zhao HX, Yao HP, et al. Characterization of three glucosyltransferase genes in Tartary buckwheat and their expression after cold stress. J Agric Food Chem. 2016;64:6930–6938. doi: 10.1021/acs.jafc.6b02064. PubMed DOI

Sun Y, Li H, Huang J. Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Mol Plant. 2012;5:387–400. doi: 10.1093/mp/ssr110. PubMed DOI

Liu Y, Jiang H, Zhao Y, Li X, Dai X, Zhuang J, et al. Three Camellia sinensis glutathione S-transferases are involved in the storage of anthocyanins, flavonols, and proanthocyanidins. Planta. 2019;250:1163–1175. doi: 10.1007/s00425-019-03206-2. PubMed DOI

Zhao Y, Dong W, Zhu Y, Allan AC, Lin-Wang K, Xu C. PpGST1, an anthocyanin-related glutathione S-transferase gene, is essential for fruit coloration in peach. Plant Biotechnol J. 2019. 10.1111/pbi.13291. PubMed PMC

Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell. 2001;13:2099–2114. doi: 10.1105/TPC.010098. PubMed DOI PMC

Riechmann JL, Meyerowitz EM. The AP2/EREBP family of plant transcription factors. Bio Chem. 1998;379:633–646. PubMed

Kakei Y, Yamamoto M, Ishida Y, Yamazaki C, Sato A, Narukawa-Nara M, et al. Biochemical and chemical biology study of rice OsTAR1 revealed that tryptophan aminotransferase is involved in auxin biosynthesis: identification of a potent OsTAR1 inhibitor, pyruvamine2031. Plant Cell Physiol. 2017;58:598–606. PubMed

Shao A, Ma W, Zhao X, Hu M, He X, Teng W, et al. The auxin biosynthetic TRYPTOPHAN AMINOTRANSFERASE RELATED TaTAR2.1-3A increases grain yield of wheat. Plant Physiol. 2017;174:2274–2288. doi: 10.1104/pp.17.00094. PubMed DOI PMC

Suvorova G, Zhou M. Distribution of cultivated buckwheat resources in the world. In: Zhou M, Kreft I, Suvorova G, Tang Y, Woo SH, editors. Buckwheat germplasm in the world. London: Academic; 2018. pp. 21–35.

Li C, Zhou A, Sang T. Rice domestication by reducing shattering. Science. 2006;311:1936–1939. doi: 10.1126/science.1123604. PubMed DOI

Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, et al. The origin of the naked grains of maize. Nature. 2005;436:714–719. doi: 10.1038/nature03863. PubMed DOI PMC

Tan L, Li X, Liu F, Sun X, Li C, Zhu Z, et al. Control of a key transition from prostrate to erect growth in rice domestication. Nat Genet. 2008;40:1360–1364. doi: 10.1038/ng.197. PubMed DOI

Wang M, Li W, Fang C, Xu F, Liu Y, Wang Z, et al. Parallel selection on a dormancy gene during domestication of crops from multiple families. Nat Genet. 2018;50:1435–1441. doi: 10.1038/s41588-018-0229-2. PubMed DOI

Liu PL, Du L, Huang Y, Gao SM, Yu M. Origin and diversification of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in plants. BMC Evol Biol. 2017;17:47. doi: 10.1186/s12862-017-0891-5. PubMed DOI PMC

Li H et al. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997v2, 2013.

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27:2987–2993. doi: 10.1093/bioinformatics/btr509. PubMed DOI PMC

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–1303. doi: 10.1101/gr.107524.110. PubMed DOI PMC

Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38:e164. doi: 10.1093/nar/gkq603. PubMed DOI PMC

Xue AT, Hickerson MJ. The aggregate site frequency spectrum for comparative population genomic inference. Mol Ecol. 2015;24:6223–6240. doi: 10.1111/mec.13447. PubMed DOI PMC

Li H. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res. 2006;34:D572–D580. doi: 10.1093/nar/gkj118. PubMed DOI PMC

Zheng X, Levine D, Shen J, Gogarten S, Laurie C, Weir B. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics. 2012;28:3326–3328. doi: 10.1093/bioinformatics/bts606. PubMed DOI PMC

Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics. 2008;24:1403–1405. doi: 10.1093/bioinformatics/btn129. PubMed DOI

Raj A, Stephens M, Pritchard JK. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics. 2014;197:573–589. doi: 10.1534/genetics.114.164350. PubMed DOI PMC

Chen H, Patterson N, Reich D. Population differentiation as a test for selective sweeps. Genome Res. 2010;20:393–402. doi: 10.1101/gr.100545.109. PubMed DOI PMC

Ma Y, Ding X, Qanbari S, Weigend S, Zhang Q, Simianer H. Properties of different selection signature statistics and a new strategy for combining them. Heredity. 2015;115:426–436. doi: 10.1038/hdy.2015.42. PubMed DOI PMC

Pfeifer B, Wittelsbürger U, Ramos-Onsins SE, Lercher MJ. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol. 2014;31(7):1929–1936. doi: 10.1093/molbev/msu136. PubMed DOI PMC

Kang HM, Sul JH, Service SK. Zaitlen NA, Kong S, Freimer NB, et al. Variance component model to account for sample structure in genome-wide association studies. Nat Genet. 2010;42:348–354. doi: 10.1038/ng.548. PubMed DOI PMC

Lippert C, Listgarten J, Liu Y, Kadie CM, Davidson RI, Heckerman D. FaST linear mixed models for genome-wide association studies. Nat Methods. 2011;8:833–835. doi: 10.1038/nmeth.1681. PubMed DOI

Walker IH, Hsieh P, Riggs PD. Mutations in maltose-binding protein that alter affinity and solubility properties. Appl Microbiol Biotechnol. 2010;88:187–197. doi: 10.1007/s00253-010-2696-y. PubMed DOI PMC

Zhou M, Sun Z, Ding M, Logacheva MD, Kreft I, Wang Dm, et al. FtSAD2 and FtJAZ1 regulate activity of the FtMYB11 transcription repressor of the phenylpropanoid pathway in Fagopyrum tataricum. New Phytol 2017;216(3):814–828. PubMed

Zhang K, Logacheva MD, Meng Y, Hu J, Wan D, Li L, et al. Jasmonate-responsive MYB factors spatially repress rutin biosynthesis in Fagopyrum tataricum. J Exp Bot. 2018;69(8):1955–1966. doi: 10.1093/jxb/ery032. PubMed DOI PMC

Li J, Zhang K, Meng Y, Li Q, Ding M, Zhou M. FtMYB16 interacts with Ftimportin-α1 to regulate rutin biosynthesis in Tartary buckwheat. Plant Biotechnol J. 2019;17(8):1479–1481. doi: 10.1111/pbi.13121. PubMed DOI PMC

Zhang K, He M, Fan Y, Zhao H, Gao B, Yang K, Li F, Tang Y, Gao Q, Lin T, Quinet M, Janovská D, Meglič V, Kwiatkowski J, Romanova O, Chrungoo N, Suzuki T, Luthar Z, Germ M, Woo SH, Georgiev MI, Zhou M. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Raw data sets for genetic diversity analysis and GWAS (PRJNA600676) https://www.ncbi.nlm.nih.gov/bioproject/PRJNA600676 /. Accessed 5 Aug 2020.

Zhang K, He M, Fan Y, Zhao H, Gao B, Yang K, Li F, Tang Y, Gao Q, Lin T, Quinet M, Janovská D, Meglič V, Kwiatkowski J, Romanova O, Chrungoo N, Suzuki T, Luthar Z, Germ M, Woo SH, Georgiev MI, Zhou M. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Github 2020, https://github.com/rahello/tartary_population. Accessed 5 Aug 2020. PubMed PMC

Zhang K, He M, Fan Y, Zhao H, Gao B, Yang K, Li F, Tang Y, Gao Q, Lin T, Quinet M, Janovská D, Meglič V, Kwiatkowski J, Romanova O, Chrungoo N, Suzuki T, Luthar Z, Germ M, Woo SH, Georgiev MI, Zhou M. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Zenodo. 2020. 10.5281/zenodo.3972746. PubMed PMC

Genomic insight into the origin, domestication, dispersal, diversification and human selection of Tartary buckwheat

Agro-Morphological and Molecular Characterization Reveal Deep Insights in Promising Genetic Diversity and Marker-Trait Associations in Fagopyrum esculentum and Fagopyrum tataricum

Comparative and population genomics of buckwheat species reveal key determinants of flavor and fertility

Rewiring of the seed metabolome during Tartary buckwheat domestication

Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits