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

. 2024 Feb 27 ; 25 (1) : 61. [epub] 20240227

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid38414075

Grantová podpora
2023YFF1002500 National Key R&D Program of China
32161143005 National Natural Science Foundation of China
Y2022QC02 the Youth Innovation Program of Chinese Academy of Agricultural Sciences
P4-0077 Slovenian Research and Innovation Agency program: Genetics and Modern Technologies of Crops
P1-0212 Slovenian Research and Innovation Agency program: Genetics and Modern Technologies of Crops
P3-0395 Slovenian Research and Innovation Agency program: Genetics and Modern Technologies of Crops

Odkazy

PubMed 38414075
PubMed Central PMC10898187
DOI 10.1186/s13059-024-03203-z
PII: 10.1186/s13059-024-03203-z
Knihovny.cz E-zdroje

BACKGROUND: Tartary buckwheat, Fagopyrum tataricum, is a pseudocereal crop with worldwide distribution and high nutritional value. However, the origin and domestication history of this crop remain to be elucidated. RESULTS: Here, by analyzing the population genomics of 567 accessions collected worldwide and reviewing historical documents, we find that Tartary buckwheat originated in the Himalayan region and then spread southwest possibly along with the migration of the Yi people, a minority in Southwestern China that has a long history of planting Tartary buckwheat. Along with the expansion of the Mongol Empire, Tartary buckwheat dispersed to Europe and ultimately to the rest of the world. The different natural growth environments resulted in adaptation, especially significant differences in salt tolerance between northern and southern Chinese Tartary buckwheat populations. By scanning for selective sweeps and using a genome-wide association study, we identify genes responsible for Tartary buckwheat domestication and differentiation, which we then experimentally validate. Comparative genomics and QTL analysis further shed light on the genetic foundation of the easily dehulled trait in a particular variety that was artificially selected by the Wa people, a minority group in Southwestern China known for cultivating Tartary buckwheat specifically for steaming as a staple food to prevent lysine deficiency. CONCLUSIONS: This study provides both comprehensive insights into the origin and domestication of, and a foundation for molecular breeding for, Tartary buckwheat.

Zobrazit více v PubMed

Liu X, Li L, Li Y, et al. Synergistic evolution theory of crop germplasm resources and cultural environments. In Chinese. J Plant Genet Resour. 2022;23:1–11.

Chen YH, Gols R, Benrey B. Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol. 2015;60:35–58. PubMed

Huang X, Huang S, Han B, Li J. The integrated genomics of crop domestication and breeding. Cell. 2022;185:2828–2839. PubMed

Wang Z, Miao L, Chen Y, Peng H, Ni Z, Sun Q, Guo W. Deciphering the evolution and complexity of wheat germplasm from a genomic perspective. J Genet Genomics. 2023;50:846–860. PubMed

Huda MN, Lu S, Jahan T, et al. Treasure from garden: Bioactive compounds of buckwheat. Food Chem. 2021;335:127653. PubMed PMC

Schenke D, Utami HP, Zhou Z, et al. Suppression of UV-B stress induced flavonoids by biotic stress: Is there reciprocal crosstalk? Plant Physiol. Biochem. 2019;134:53–63. PubMed

He Y, Zhang K, Li S, et al. Multi-omics analysis reveals the molecular mechanisms underlying virulence in Rhizoctonia and jasmonic acid-mediated resistance in Tartary buckwheat (Fagopyrum tataricum) Plant Cell. 2023;35:2773–2798. PubMed PMC

Zhang K, He M, Fan Y, et al. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. Genome Biol. 2021;22:1–23. PubMed PMC

Zhu F. Chemical composition and health effects of Tartary buckwheat. Food Chem. 2016;203:231–245. PubMed

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. Veg Hist Archaeobot. 2018;27:493–506. PubMed PMC

Alseekh S, Scossa F, Wen W, et al. Domestication of crop metabolomes: Desired and unintended consequences. Trends Plant Sci. 2021;26:650–661. PubMed

Zhao H, He Y, Zhang K, et al. Rewiring of the seed metabolome during Tartary buckwheat domestication. Plant Biotechnol J. 2023;21:150–164. PubMed PMC

De Candolle, A. (1883). Origine des Plantes Cultivées; G. Baillière et cie: Paris, France, Volume 43.

Tsuji K, Ohnishi O. Phylogenetic relationships among wild and cultivated Tartary buckwheat (Fagopyrum tataricum Gaert.) populations revealed by AFLP analyses. Genes Genet Syst. 2001;76:47–52. PubMed

Ohnishi O. Search for the wild ancestor of buckwheat III. The wild ancestor of cultivated common buckwheat, and of Tatary buckwheat. Econ Bot. 1998;52:123–133.

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

Fan Y, Ding M, Zhang K, et al. Overview and utilization of wild germplasm resources of the genus Fagopyrum Mill. In Chinese. J Plant Genet Resour. 2020;21:1395–1406.

Bradley D. Proto-Tibeto-Burman grain crops. Rice. 2011;4:134–141.

Weisskopf A, Fuller DQ. Buckwheat: origins and development. In: Smith Claire., editor. Encyclopedia of Global Archaeology. New York: Springer; 2014. pp. 1025–1028.

Tang, Y., Ding, M., Tang, Y., et al. Germplasm resources of buckwheat in China. In Molecular Breeding and Nutritional Aspects of Buckwheat, Meiliang Zhou et al., ed. (Academic Press), 2016. pp. 13–20.

Boivin N, Fuller DQ, Crowther A. Old world globalization and the columbian exchange: comparison and contrast. World Archaeol. 2012;44:452–469.

Hughes, D.H., and Henson, R.E. Crop production principles and practices. (The Macmillan Company). 1934.

Yao YF, Song XY, Xie G, et al. New insights into the origin of buckwheat cultivation in southwestern China from pollen data. New Phytol. 2023;237:2467–2477. PubMed

Smith BD. Documenting plant domestication: The consilience of biological and archaeological approaches. Proc Natl Acad Sci USA. 2001;98:1324–1326. PubMed PMC

Zeder MA, Emshwiller E, Smith BD, Bradley DG. Documenting domestication: the intersection of genetics and archaeology. Trends Genet. 2006;22:139–155. PubMed

Huang X, Kurata N, Wei X, et al. A map of rice genome variation reveals the origin of cultivated rice. Nature. 2012;490:497–501. PubMed PMC

van Andel TR, Meyer RS, Aflitos SA, et al. Tracing ancestor rice of Suriname Maroons back to its African origin. Nat Plants. 2016;2:16149. PubMed

Wang W, Mauleon R, Hu Z, et al. Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature. 2018;557:43–49. PubMed PMC

Hufford MB, Xu X, van Heerwaarden J, et al. Comparative population genomics of maize domestication and improvement. Nat Genet. 2012;44:808–811. PubMed PMC

Chen L, Luo J, Jin M, et al. Genome sequencing reveals evidence of adaptive variation in the genus Zea. Nat. Genet. 2022;54:1736–1745. PubMed

Kang L, Qian L, Zheng M, et al. Genomic insights into the origin, domestication and diversification of Brassica juncea. Nat Genet. 2021;53:1392–1402. PubMed PMC

Wei T, van Treuren R, Liu X, et al. Whole-genome resequencing of 445 Lactuca accessions reveals the domestication history of cultivated lettuce. Nat Genet. 2021;53:752–760. PubMed

Dong Y, Duan S, Xia Q, et al. Dual domestications and origin of traits in grapevine evolution. Science. 2023;379:892–901. PubMed

Bellucci E, Benazzo A, Xu C, et al. Selection and adaptive introgression guided the complex evolutionary history of the European common bean. Nat Commun. 2023;14:1901–1908. PubMed PMC

Varshney RK, Roorkiwal M, Sun S, et al. A chickpea genetic variation map based on the sequencing of 3,366 genomes. Nature. 2021;599:622–627. PubMed PMC

Suarez-Gonzalez A, Lexer C, Cronk Q. Adaptive introgression: a plant perspective. Biol Lett. 2018;14:20170688. PubMed PMC

Cai W, Hong J, Liu Z, et al. A receptor-like kinase controls the amplitude of secondary cell wall synthesis in rice. Curr Biol. 2023;33:498–506. PubMed

Wang P. Battle for survival: the role of plant thioredoxin in the war against Barley stripe mosaic virus. Plant Physiol. 2022;189:1199–1201. PubMed PMC

Breen S, Williams SJ, Outram M, et al. Emerging insights into the functions of pathogenesis-related protein 1. Trends Plant Sci. 2017;22:871–879. PubMed

Cheng GY, Yang ZT, Zhang H, et al. Remorin interacting with PCaP1 impairs Turnip mosaic virus intercellular movement but is antagonised by VPg. New Phytol. 2020;225:2122–2139. PubMed

Ji C, Xu L, Li Y, et al. The O2-ZmGRAS11 transcriptional regulatory network orchestrates the coordination of endosperm cell expansion and grain filling in maize. Mol Plant. 2022;15:468–487. PubMed

Botanga CJ, Bethke G, Chen Z, et al. Metabolite profiling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Mol Plant Microbe Interact. 2012;12:1628–1638. PubMed

Paciolla C, Fortunato S, Dipierro N, et al. Vitamin C in plants: From functions to biofortification. Antioxidants. 2019;8:511–519. PubMed PMC

Potok ME, Wang YF, Xu LH, et al. Arabidopsis SWR1-associated protein methyl-CpG-binding domain 9 is required for histone H2A.Z deposition. Nat Commun. 2019;10:3352. PubMed PMC

Baek D, Shin G, Kim MC, et al. Histone deacetylase HDA9 with ABI4 contributes to abscisic acid homeostasis in drought stress response. Front Plant Sci. 2020;11:143. PubMed PMC

Blankenagel S, Eggels S, Frey M, et al. Natural alleles of the abscisic acid catabolism gene ZmAbh4 modulate water use efficiency and carbon isotope discrimination in maize. Plant Cell. 2022;34:3860–3872. PubMed PMC

Jacob P, Hirt H, Bendahmane A. The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnol J. 2017;15:405–414. PubMed PMC

Liu L, Wang B. Protection of halophytes and their uses for cultivation of saline-alkali soil in China. Biology (Basel) 2021;10:353–355. PubMed PMC

Campbell C. Buckwheat crop improvement. Fagopyrum. 2003;20:1–6.

Peng Y, Yan H, Guo L, et al. Reference genome assemblies reveal the origin and evolution of allohexaploid oat. Nat Genet. 2022;54:1248–1258. PubMed PMC

Shi TX, Li RY, Zheng R, et al. Mapping QTLs for 1000-grain weight and genes controlling hull type using SNP marker in Tartary buckwheat (Fagopyrum tataricum) BMC Genomics. 2021;22:142. PubMed PMC

Li HY, Wu CX, Lv QY, et al. Comparative cellular, physiological and transcriptome analyses reveal the potential easy dehulling mechanism of rice-tartary buckwheat (Fagopyrum tararicum) BMC Plant Biol. 2020;20:505. PubMed PMC

Fierens E, Rombouts S, Gebruers K, et al. TLXI, a novel type of xylanase inhibitor from wheat (Triticum aestivum) belonging to the thaumatin family. Biochem J. 2007;403:583–591. PubMed PMC

Meyer RS, DuVal AE, Jensen HR. Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol. 2012;196:29–48. PubMed

Pandit MK. The Himalaya should be a nature reserve. Nature. 2020;583:7814–7819. PubMed

Ning C, Li T, Wang K, et al. Ancient genomes from northern China suggest links between subsistence changes and human migration. Nat. Commun. 2020;11:2700–2701. PubMed PMC

Zhu G, Wang S, Huang Z, et al. Rewiring of the fruit metabolome in tomato breeding. Cell. 2018;172:249–261. PubMed

Gasparini K, Moreira JDR, Peres LEP, Zsögön A. De novo domestication of wild species to create crops with increased resilience and nutritional value. Curr Opin Plant Biol. 2021;60:102006. PubMed

Zhu JK. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol. 2002;53:247–273. PubMed PMC

Zhou H, Shi H, Yang Y, Feng X, Chen X, Xiao F, Lin H, Guo Y. Insights into plant salt stress signaling and tolerance. J Genet Genomics. 2023;50:846–860. PubMed

Lai D, Zhang K, He Y, et al. Multi-omics identification of a key glycosyl hydrolase gene FtGH1 involved in rutin hydrolysis in Tartary buckwheat (Fagopyrum tataricum) Plant Biotechnol J. 2023 doi: 10.1111/pbi.14259. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. PubMed PMC

Du H, Liang C. Assembly of chromosome-scale contigs by efficiently resolving repetitive sequences with long reads. Nat Commun. 2019;10:5360. PubMed PMC

Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. preprint arXiv: 2013; 1303: 997.

McKenna A, Hanna M, Banks E, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–1303. PubMed PMC

Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19:1655–1664. PubMed PMC

Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–274. PubMed PMC

Chen H, Patterson N, Reich D. Population differentiation as a test for selective sweeps. Genome Res. 2010;20:393–402. PubMed 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 (Edinb) 2015;115:426–36. PubMed PMC

Li N, Zhang X, Sun X, et al. Genomic insights into the evolutionary history and diversification of bulb traits in garlic. Genome Biol. 2022;23:188. PubMed PMC

Li N, He Q, Wang J, et al. Super-pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nat Genet. 2023;55:852–860. PubMed PMC

Zhang H, Mi S, Brito L, Hu L, Wang L, Ma L, Xu Q, Guo G, Yu Y, Wang Y. Genomic and transcriptomic analyses enable the identification of important genes associated with subcutaneous fat deposition in Holstein cows. J Genet Genomics. 2023;50:385–397. PubMed

Kang HM, Sul JH, Service SK, et al. Variance component model to account for sample structure in genome-wide association studies. Nat Genet. 2010;42:348–354. PubMed PMC

Danecek P, Auton A, Abecasis G, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156–2158. PubMed PMC

Purcell S, Neale B, Todd-Brown K, et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–575. PubMed PMC

Patterson N, Moorjani P, Luo Y, et al. Ancient admixture in human history. Genetics. 2012;192:1065–1093. PubMed PMC

Feuerborn TR, Carmagnini A, Losey RJ, et al. Modern Siberian dog ancestry was shaped by several thousand years of Eurasian-wide trade and human dispersal. Proc Natl Acad Sci USA. 2021;118:e2100338118. PubMed PMC

Swarts K, Gutaker RM, Benz B, et al. Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America. Science. 2017;357:512–515. PubMed

Fitak RR. OptM: estimating the optimal number of migration edges on population trees using Treemix. Biol Methods Protoc. 2021;6:bpab017. PubMed PMC

Macqueen, J. Some methods for classification and analysis of multivariate observations. Proc. Symp. Math. Statist. and Probability, 5th, 1. 1967.

Durand EY, Patterson N, Reich D, Slatkin M. Testing for ancient admixture between closely related populations. Mol Biol Evol. 2011;28:2239–2252. PubMed PMC

Villa-Islas V, Izarraras-Gomez A, Larena M, et al. Demographic history and genetic structure in pre-Hispanic Central Mexico. Science. 2023;380:eadd6142. PubMed

Terhorst J, Kamm JA, Song YS. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat Genet. 2017;49:303–309. PubMed PMC

Feng X, Cheng H, Portik D, Li H. Metagenome assembly of high-fidelity long reads with hifiasm-meta. Nat Methods. 2022;19:671–674. PubMed PMC

Durand NC, Shamim MS, Machol I, et al. Juicer provides a One-Click system for analyzing Loop-Resolution Hi-C experiments. Cell Syst. 2016;3:95–98. PubMed PMC

Dudchenko O, Batra SS, Omer AD, et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017;356:92–95. PubMed PMC

Durand NC, Robinson JT, Shamim MS, et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 2016;3:99–101. PubMed PMC

Simao FA, Waterhouse RM, Ioannidis P, et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–3212. PubMed

Goel M, Sun H, Jiao WB, Schneeberger K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 2019;20:277. PubMed PMC

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–3100. PubMed PMC

Mansfeld BN, Grumet R. QTLseqr: An R package for bulk segregant analysis with next-generation sequencing. Plant Genome. 2018;11:180006. PubMed

Wang X, Prokhnevsky AI, Skarjinskaia M, et al. Facilitating viral vector movement enhances heterologous protein production in an established plant system. Plant Biotechnol J. 2023;21:635–645. PubMed PMC

Park DS, Sayler RJ, Hong YG, Nam MH, Yang Y. A method for inoculation and evaluation of rice sheath blight disease. Plant Dis. 2008;92:25–29. PubMed

Niu C, Jiang L, Cao F, et al. Methylation of a MITE insertion in the MdRFNR1-1 promoter is positively associated with its allelic expression in apple in response to drought stress. Plant Cell. 2022;34:3983–4006. PubMed PMC

Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–425. PubMed

Kumar S, Stecher G, Li M, et al. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–1549. PubMed PMC

Yan S, Chong P, Zhao M. Effect of salt stress on the photosynthetic characteristics and endogenous hormones, and: A comprehensive evaluation of salt tolerance in Reaumuria soongorica seedlings. Plant Signal Behav. 2022;17:2031782. PubMed PMC

Chen T, Chen X, Zhang S, et al. The genome sequence archive family: Toward explosive data growth and diverse data types. Genom Proteom Bioinform. 2021;19:578–583. PubMed PMC

CNCB-NGDC Members and Partners Database resources of the National Genomics Data Center, China National Center for Bioinformation in 2022. Nucleic Acids Res. 2022;50:D27–D38. PubMed PMC

He, Y., Zhang, K., Shi, Y., et al. Genomic insight into the origin, domestication, dispersal and diversification of Tartary buckwheat. PRJCA020346. Genome reseguencing of wild and foreign Tartary buckwheat. 2024. https://ngdc.cncb.ac.cn/bioproject/browse/PRJCA020346. PubMed PMC

Zhang, K., He, M., Fan, Y., et al. Resequencing of global Tartary buckwheat accessions reveals multiple domestication events and key loci associated with agronomic traits. PRJNA600676. Fagopyrum tataricum clean sequence reads. 2021. https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA600676. PubMed PMC

Shi, T., Li, R., Zheng, R., et al. Mapping QTLs for 1000-grain weight and genes controlling hull type using SNP marker in Tartary buckwheat (Fagopyrum tataricum). PRJCA003285. Construction Linkage Map of Tartary Buckwheat Based on RAD. 2021. https://ngdc.cncb.ac.cn/bioproject/browse/PRJCA003285. PubMed PMC

He, Y., Zhang, K., Shi, Y., et al. Genomic insight into the origin, domestication, dispersal and diversification of Tartary buckwheat. GitHub. 2024. https://github.com/Buckwheat-lab/Tartary_buckwheat_WGS. PubMed PMC

He Y, Zhang K, Shi Y, et al. Genomic insight into the origin, domestication, dispersal and diversification of Tartary buckwheat. 2024. Zenodo. 10.5281/zenodo.10663969. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...