Pangenome-guided breeding restores high-altitude adaptation and improves yield in Tartary buckwheat

Highlights

•

Structural variations are diverse between wild buckwheat and landraces

•

The presence of FtRNH in wild accessions is associated with high-altitude adaptability

•

Structural variations in FtPLATZ are linked to seed-size variations

•

An ideal highland buckwheat is developed by integrating superior alleles

Summary

Tartary buckwheat is a nutritionally important crop of the Himalayas and is crucial for local economies and food security. However, key genes and superior alleles for high-altitude adaptability and yield remain poorly defined, constraining the breeding of high-altitude buckwheat varieties. Here, we generated a telomere-to-telomere reference genome and a 16-accession pangenome spanning Himalayan wild populations and globally distributed landraces. We identified 123,131 non-redundant structural variations in 16 accessions, including gene copy-number variations. The graph-based pangenome revealed FtRNH, a wild-specific gene that enhances high-altitude adaptability. We also identified a copy-number variation at the FtPLATZ locus and a 28-bp insertion in the FtPLATZ3 promoter that together contribute to seed-size variation across wild buckwheat and landraces. Leveraging these superior FtRNH and FtPLATZ alleles, we developed buckwheat lines with enhanced high-altitude adaptability and improved yields across sites. These findings establish a pangenome-guided strategy for recovering wild alleles and combining stress adaptation with yield improvement in crops.

Graphical abstract

Keywords

1. buckwheat
2. pangenome
3. genetic breeding
4. high-altitude adaptation
5. Himalayan region

Get full text access

Log in, subscribe or purchase for full access.

References

International Centre, Integrated, Mountain, Development

The Hindu Kush Himalaya Assessment: Mountains, Climate Change, Sustainability and People

Cham (Switzerland): Springer, 2019

He, Y. ∙ Zhang, K. ∙ Shi, Y. ...

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

Genome Biol. 2024; 25, 61

Zhang, K. ∙ He, M. ∙ Fan, Y. ...

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

Genome Biol. 2021; 22, 23

Kumari, A. ∙ Chaudhary, H.K.

Nutraceutical crop buckwheat: a concealed wealth in the lap of Himalayas

Crit. Rev. Biotechnol. 2020; 40:539-554

Zeng, X. ∙ Guo, Y. ∙ Xu, Q. ...

Origin and evolution of qingke barley in Tibet

Nat. Commun. 2018; 9, 5433

Jha, R. ∙ Zhang, K. ∙ He, Y. ...

Global nutritional challenges and opportunities: Buckwheat, a potential bridge between nutrient deficiency and food security

Trends Food Sci. Technol. 2024; 145, 104365

Joshi, D.C. ∙ Zhang, K. ∙ Wang, C. ...

Strategic enhancement of genetic gain for nutraceutical development in buckwheat: A genomics-driven perspective

Biotechnol. Adv. 2020; 39, 107479

Huda, M.N. ∙ Lu, S. ∙ Jahan, T. ...

Treasure from garden: Bioactive compounds of buckwheat

Food Chem. 2021; 335, 127653

Bao, H. ∙ Yuan, L. ∙ Luo, Y. ...

The transcription factor WRKY41-FLAVONOID 3′-HYDROXYLASE module fine-tunes flavonoid metabolism and cold tolerance in potato

Plant Physiol. 2025; 197, kiaf070

Bulut, M. ∙ Tohge, T. ∙ Chen, W. ...

Learning from nature: phytochemical strategies to protect against UV-B damage

Nat. Commun. 2025; 16, 9927

He, J. ∙ Yao, L. ∙ Pecoraro, L. ...

Cold stress regulates accumulation of flavonoids and terpenoids in plants by phytohormone, transcription process, functional enzyme, and epigenetics

Crit. Rev. Biotechnol. 2023; 43:680-697

Hunt, H.V. ∙ Shang, X. ∙ Jones, M.K.

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

Zhao, H. ∙ He, Y. ∙ Zhang, K. ...

Rewiring of the seed metabolome during Tartary buckwheat domestication

Plant Biotechnol. J. 2023; 21:150-164

Lin, H. ∙ Yao, Y. ∙ Sun, P. ...

Haplotype-resolved genomes of two buckwheat crops provide insights into their contrasted rutin concentrations and reproductive systems

BMC Biol. 2023; 21, 87

Lai, D. ∙ Zhang, K. ∙ He, Y. ...

Multi-omics identification of a key glycosyl hydrolase gene FtGH1 involved in rutin hydrolysis in Tartary buckwheat (Fagopyrum tataricum)

Plant Biotechnol. J. 2024; 22:1206-1223

He, Y. ∙ Zhang, K. ∙ Li, S. ...

Multiomics 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

Du, H. ∙ Liang, C.

Assembly of chromosome-scale contigs by efficiently resolving repetitive sequences with long reads

Nat. Commun. 2019; 10, 5360

Kang, M. ∙ Wu, H. ∙ Liu, H. ...

The pan-genome and local adaptation of Arabidopsis thaliana

Nat. Commun. 2023; 14, 6259

Yan, H. ∙ Sun, M. ∙ Zhang, Z. ...

Pangenomic analysis identifies structural variation associated with heat tolerance in pearl millet

Nat. Genet. 2023; 55:507-518

Gao, L. ∙ Gonda, I. ∙ Sun, H. ...

The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor

Nat. Genet. 2019; 51:1044-1051

Yang, W. ∙ Duan, H. ∙ Yu, K. ...

Integrative dissection of lignin composition in Tartary buckwheat seed hulls for enhanced dehulling efficiency

Adv. Sci. (Weinh). 2024; 11, e2400916

Fawcett, J.A. ∙ Takeshima, R. ∙ Kikuchi, S. ...

Genome sequencing reveals the genetic architecture of heterostyly and domestication history of common buckwheat

Nat. Plants. 2023; 9:1236-1251

Závodník, M. ∙ Fajkus, P. ∙ Franek, M. ...

Telomerase RNA gene paralogs in plants - the usual pathway to unusual telomeres

New Phytol. 2023; 239:2353-2366

He, M. ∙ He, Y. ∙ Zhang, K. ...

Comparison of buckwheat genomes reveals the genetic basis of metabolomic divergence and ecotype differentiation

New Phytol. 2022; 235:1927-1943

Zhang, N. ∙ McHale, L.K. ∙ Finer, J.J.

Changes to the core and flanking sequences of G-box elements lead to increases and decreases in gene expression in both native and synthetic soybean promoters

Plant Biotechnol. J. 2019; 17:724-735

Chinnusamy, V. ∙ Ohta, M. ∙ Kanrar, S. ...

ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis

Genes Dev. 2003; 17:1043-1054

Li, W. ∙ Wen, Y. ∙ Quan, J. ...

Regulation of jasmonic acid signalling in tomato cold stress response: Insights into the MYB15-LOXD and MYB15-MYC2-LOXD regulatory modules

Plant Biotechnol. J. 2025; 23:4246-4260

Liu, Y. ∙ Patra, B. ∙ Pattanaik, S. ...

GATA and phytochrome interacting factor transcription factors regulate light-induced vindoline biosynthesis in Catharanthus roseus

Plant Physiol. 2019; 180:1336-1350

Wang, G. ∙ Xu, X. ∙ Lu, H. ...

The bZIP transcription factor BcbZIP72 positively regulates cold tolerance through CBF-dependent pathways in non-heading Chinese cabbage

Plant Physiol. Biochem. 2025; 229, 110522

Chen, S. ∙ Dong, X. ∙ Yang, Z. ...

Regulation of the development in Physcomitrium (Physcomitrella) patens implicates the functional differentiation of plant RNase H1s

Plant Sci. 2021; 313, 111070

Cheng, L. ∙ Wang, W. ∙ Yao, Y. ...

Mitochondrial RNase H1 activity regulates R-loop homeostasis to maintain genome integrity and enable early embryogenesis in Arabidopsis

PLoS Biol. 2021; 19, e3001357

Kuciński, J. ∙ Chamera, S. ∙ Kmera, A. ...

Evolutionary history and activity of RNase H1-like proteins in Arabidopsis thaliana

Plant Cell Physiol. 2020; 61:1107-1119

Wang, W. ∙ Li, K. ∙ Yang, Z. ...

RNase H1C collaborates with ssDNA binding proteins WHY1/3 and recombinase RecA1 to fulfill the DNA damage repair in Arabidopsis chloroplasts

Nucleic Acids Res. 2021; 49:6771-6787

Yang, Z. ∙ Hou, Q. ∙ Cheng, L. ...

RNase H1 cooperates with DNA gyrases to restrict R-loops and maintain genome integrity in Arabidopsis chloroplasts

Plant Cell. 2017; 29:2478-2497

Hideg, E. ∙ Jansen, M.A.K. ∙ Strid, A.

UV-B exposure, ROS, and stress: inseparable companions or loosely linked associates?

Trends Plant Sci. 2013; 18:107-115

Li, R. ∙ Chen, Z. ∙ Zheng, R. ...

QTL mapping and candidate gene analysis for yield and grain weight/size in Tartary buckwheat

BMC Plant Biol. 2023; 23, 58

Li, J. ∙ Feng, S. ∙ Zhang, Y. ...

Genome-wide identification and expression analysis of the plant-specific PLATZ gene family in Tartary buckwheat (Fagopyrum tataricum)

BMC Plant Biol. 2022; 22, 160

Wang, A. ∙ Hou, Q. ∙ Si, L. ...

The PLATZ transcription factor GL6 affects grain length and number in rice

Plant Physiol. 2019; 180:2077-2090

Zhou, S.R. ∙ Xue, H.W.

The rice PLATZ protein SHORT GRAIN6 determines grain size by regulating spikelet hull cell division

J. Integr. Plant Biol. 2020; 62:847-864

Stratmann, J.

Ultraviolet-B radiation co-opts defense signaling pathways

Trends Plant Sci. 2003; 8:526-533

Shi, C. ∙ Liu, H.

How plants protect themselves from ultraviolet-B radiation stress

Plant Physiol. 2021; 187:1096-1103

Liang, T. ∙ Shi, C. ∙ Peng, Y. ...

Brassinosteroid-activated BRI1-EMS-SUPPRESSOR 1 inhibits flavonoid biosynthesis and coordinates growth and UV-B stress responses in plants

Plant Cell. 2020; 32:3224-3239

Hu, S. ∙ Chen, Y. ∙ Qian, C. ...

Nuclear accumulation of rice UV-B photoreceptors is UV-B- and OsCOP1-independent for UV-B responses

Nat. Commun. 2024; 15, 6396

Guo, H. ∙ Gao, S. ∙ Li, H. ...

Natural variation of CTB5 confers cold adaptation in plateau japonica rice

Nat. Commun. 2025; 16, 1032

Zeng, R. ∙ Shi, Y. ∙ Guo, L. ...

A natural variant of COOL1 gene enhances cold tolerance for high-latitude adaptation in maize

Cell. 2025; 188:1315-1329.e13

Shi, J. ∙ Lai, J.

Patterns of genomic changes with crop domestication and breeding

Curr. Opin. Plant Biol. 2015; 24:47-53

Tao, Y. ∙ Luo, H. ∙ Xu, J. ...

Extensive variation within the pan-genome of cultivated and wild sorghum

Nat. Plants. 2021; 7:766-773

He, Q. ∙ Tang, S. ∙ Zhi, H. ...

A graph-based genome and pan-genome variation of the model plant Setaria

Nat. Genet. 2023; 55:1232-1242

Chen, J. ∙ Liu, Y. ∙ Liu, M. ...

Pangenome analysis reveals genomic variations associated with domestication traits in broomcorn millet

Nat. Genet. 2023; 55:2243-2254

Wang, Y. ∙ Chen, W. ∙ Xing, M. ...

Wild rice GL12 synergistically improves grain length and salt tolerance in cultivated rice

Nat. Commun. 2024; 15, 9453

Zhang, X. ∙ Meng, W. ∙ Liu, D. ...

Enhancing rice panicle branching and grain yield through tissue-specific brassinosteroid inhibition

Science. 2024; 383, eadk8838

Zsögön, A. ∙ Čermák, T. ∙ Naves, E.R. ...

De novo domestication of wild tomato using genome editing

Nat. Biotechnol. 2018; 36:1211-1216

Yu, H. ∙ Lin, T. ∙ Meng, X. ...

A route to de novo domestication of wild allotetraploid rice

Cell. 2021; 184:1156-1170.e14

Cheng, H. ∙ Jarvis, E.D. ∙ Fedrigo, O. ...

Haplotype-resolved assembly of diploid genomes without parental data

Nat. Biotechnol. 2022; 40:1332-1335

Zhang, H. ∙ Song, L. ∙ Wang, X. ...

Fast alignment and preprocessing of chromatin profiles with Chromap

Nat. Commun. 2021; 12, 6566

Zhou, C. ∙ McCarthy, S.A. ∙ Durbin, R.

YaHS: yet another Hi-C scaffolding tool

Bioinformatics. 2023; 39, btac808

Manni, M. ∙ Berkeley, M.R. ∙ Seppey, M. ...

BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes

Mol. Biol. Evol. 2021; 38:4647-4654

Ou, S. ∙ Su, W. ∙ Liao, Y. ...

Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline

Genome Biol. 2019; 20, 275

Birney, E. ∙ Clamp, M. ∙ Durbin, R.

Genewise and genomewise

Genome Res. 2004; 14:988-995

Stanke, M. ∙ Steinkamp, R. ∙ Waack, S. ...

AUGUSTUS: a web server for gene finding in eukaryotes

Nucleic Acids Res. 2004; 32:W309-W312

Majoros, W.H. ∙ Pertea, M. ∙ Salzberg, S.L.

TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders

Bioinformatics. 2004; 20:2878-2879

Kim, D. ∙ Paggi, J.M. ∙ Park, C. ...

Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype

Nat. Biotechnol. 2019; 37:907-915

Haas, B.J. ∙ Delcher, A.L. ∙ Mount, S.M. ...

Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies

Nucleic Acids Res. 2003; 31:5654-5666

Haas, B.J. ∙ Salzberg, S.L. ∙ Zhu, W. ...

Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments

Genome Biol. 2008; 9, R7

Lin, Y. ∙ Ye, C. ∙ Li, X. ...

quarTeT: a telomere-to-telomere toolkit for gap-free genome assembly and centromeric repeat identification

Hortic. Res. 2023; 10, uhad127

Tang, H. ∙ Krishnakumar, V. ∙ Zeng, X. ...

JCVI: A versatile toolkit for comparative genomics analysis

Imeta. 2024; 3, e211

Shen, W. ∙ Sipos, B. ∙ Zhao, L.

SeqKit2: A Swiss army knife for sequence and alignment processing

Imeta. 2024; 3, e191

Chao, K.H. ∙ Heinz, J.M. ∙ Hoh, C. ...

Combining DNA and protein alignments to improve genome annotation with LiftOn

Genome Res. 2025; 35:311-325

Bolger, A.M. ∙ Lohse, M. ∙ Usadel, B.

Trimmomatic: a flexible trimmer for Illumina sequence data

Bioinformatics. 2014; 30:2114-2120

Langmead, B. ∙ Salzberg, S.L.

Fast gapped-read alignment with Bowtie 2

Nat. Methods. 2012; 9:357-359

Li, H. ∙ Handsaker, B. ∙ Wysoker, A. ..., 1000 Genome Project Data Processing Subgroup

The sequence alignment/map format and SAMtools

Bioinformatics. 2009; 25:2078-2079

McKenna, A. ∙ Hanna, M. ∙ Banks, E. ...

The genome analysis Toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data

Genome Res. 2010; 20:1297-1303

Zhang, Y. ∙ Liu, T. ∙ Meyer, C.A. ...

Model-based analysis of ChIP-Seq (MACS)

Genome Biol. 2008; 9, R137

Vasimuddin, M. ∙ Misra, S. ∙ Li, H. ...

Efficient architecture-aware acceleration of BWA-MEM for multicore systems

IPDPS

Institute of Electrical and Electronics Engineers, 2019; 314-324

Wang, K. ∙ Li, M. ∙ Hakonarson, H.

ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data

Nucleic Acids Res. 2010; 38, e164

Purcell, S. ∙ Neale, B. ∙ Todd-Brown, K. ...

PLINK: a tool set for whole-genome association and population-based linkage analyses

Am. J. Hum. Genet. 2007; 81:559-575

Vilella, A.J. ∙ Severin, J. ∙ Ureta-Vidal, A. ...

Ensemblcompara genetrees: complete, duplication-aware phylogenetic trees in vertebrates

Genome Res. 2009; 19:327-335

Letunic, I. ∙ Bork, P.

Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation

Nucleic Acids Res. 2021; 49:W293-W296

Alexander, D.H. ∙ Novembre, J. ∙ Lange, K.

Fast model-based estimation of ancestry in unrelated individuals

Genome Res. 2009; 19:1655-1664

Yang, J. ∙ Lee, S.H. ∙ Goddard, M.E. ...

GCTA: a tool for genome-wide complex trait analysis

Am. J. Hum. Genet. 2011; 88:76-82

Zhang, C. ∙ Dong, S.S. ∙ Xu, J.Y. ...

PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files

Bioinformatics. 2019; 35:1786-1788

Buchfink, B. ∙ Xie, C. ∙ Huson, D.H.

Fast and sensitive protein alignment using DIAMOND

Nat. Methods. 2015; 12:59-60

Emms, D.M. ∙ Kelly, S.

OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy

Genome Biol. 2015; 16, 157

Edgar, R.C.

MUSCLE: a multiple sequence alignment method with reduced time and space complexity

BMC Bioinform. 2004; 5, 113

Wu, T. ∙ Hu, E. ∙ Xu, S. ...

clusterProfiler 4.0: A universal enrichment tool for interpreting omics data

Innovation (Camb.). 2021; 2, 100141

Sun, P. ∙ Jiao, B. ∙ Yang, Y. ...

WGDI: A user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes

Mol. Plant. 2022; 15:1841-1851

Marçais, G. ∙ Delcher, A.L. ∙ Phillippy, A.M. ...

MUMmer4: A fast and versatile genome alignment system

PLOS Comput. Biol. 2018; 14, e1005944

Goel, M. ∙ Sun, H. ∙ Jiao, W.B. ...

SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies

Genome Biol. 2019; 20, 277

Jeffares, D.C. ∙ Jolly, C. ∙ Hoti, M. ...

Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast

Nat. Commun. 2017; 8, 14061

Garrison, E. ∙ Sirén, J. ∙ Novak, A.M. ...

Variation graph toolkit improves read mapping by representing genetic variation in the reference

Nat. Biotechnol. 2018; 36:875-879

Chen, H. ∙ Patterson, N. ∙ Reich, D.

Population differentiation as a test for selective sweeps

Genome Res. 2010; 20:393-402

Jones, P. ∙ Binns, D. ∙ Chang, H.Y. ...

InterProScan 5: genome-scale protein function classification

Bioinformatics. 2014; 30:1236-1240

Katoh, K. ∙ Standley, D.M.

MAFFT multiple sequence alignment software version 7: improvements in performance and usability

Mol. Biol. Evol. 2013; 30:772-780

Capella-Gutiérrez, S. ∙ Silla-Martínez, J.M. ∙ Gabaldón, T.

trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses

Bioinformatics. 2009; 25:1972-1973

Nguyen, L.T. ∙ Schmidt, H.A. ∙ von Haeseler, A. ...

IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies

Mol. Biol. Evol. 2015; 32:268-274

Zhou, X. ∙ Stephens, M.

Genome-wide efficient mixed-model analysis for association studies

Nat. Genet. 2012; 44:821-824

Chen, S. ∙ Zhou, Y. ∙ Chen, Y. ...

**fastp: an ultra-fast all-in-one