Haplotype-resolved T2T reference genomes for wild and domesticated accessions shed new insights into the domestication of jujube

Abstract

Chinese jujube ( Ziziphus jujuba Mill.) is one of the most important deciduous tree fruits in China, with substantial economic and nutritional value. Jujube was domesticated from its wild progenitor, wild jujube ( Z. jujuba var. spinosa ), and both have high medicinal value. Here we report the 767.81- and 759.24-Mb haplotype-resolved assemblies of a dry-eating ‘Junzao’ jujube (JZ) and a wild jujube accession (SZ), using a combination of multiple sequencing strategies. Each assembly yielded two complete haplotype-resolved genomes at the telomere-to-telomere (T2T) level, and ∼ 81.60 and 69.07 Mb of structural variations were found between the two haplotypes within JZ and SZ, respectively. Comparative genomic analysis revealed a large inversion on each of chromosomes 3 and 4 between JZ and SZ, and numerous genes were affected by structural variations, some of which were associated with starch and sucrose metabolism. A large-scale population analysis of 672 accessions revealed that wild jujube originated from the lower reaches of the Yellow River and was initially domesticated at local sites. It spread widely and was then independently domesticated at the Shanxi-Shaanxi Gorge of the middle Yellow River. In addition, we identified some new selection signals regions on genomes, which are involved in the tissue development, pollination, and other aspects of jujube tree morphology and fertilization domestication. In conclusion, our study provides high-quality reference genomes of jujube and wild jujube and new insights into the domestication history of jujube.

Acknowledgements

This work was supported by the earmarked fund of Xinjiang Jujube Industrial Technology System (XJCYTX-01), and the National Natural Science Foundation of China (grants 31870584 and 31860223).

Author contributions

J.H. and Q.H. conceived the project. K.L., R.C., and A.A. performed the experiments and wrote the manuscript. Q.W., Z.M., Z.W. collected the samples and analyzed the data. All authors read and approved the final manuscript.

Data availability

The raw sequence data of whole-genome sequencing and transcriptome sequencing in Z. jujuba Mill. and Z. jujuba var. spinosa, as well as the assemblies, have been deposited in NCBI project PRJNA974227 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA974227/). The whole-genome resequencing data were deposited in CNGB project PRJCA015614 (https://ngdc.cncb.ac.cn/gsa/s/VZxLq3Z8). The annotation files for protein-coding genes, along with other related files for genome assembly, have been stored in figshare, an online data repository, at https://figshare.com/s/ad5d747ccc2ccbb2b65b.

Conflict of interest

The authors declared that they have no conflict of interest in relation to this work.

Supplementary data

Supplementary data are available at Horticulture Research online.

References

[1] Liu M. Chinese jujube:botany and horticulture. In: Janick J,ed. Horticultural Reviews, Vol. 32. United States:Wiley, 2006, 229-98

[2] Liu M, Wang J, Wang L. et al. The historical and current research progress on jujube—a superfruit for the future. Hortic Res. 2020; 7 :119

[3] Zhang Z, Shi Q, Wang B. et al. Jujube metabolome selection determined the edible properties acquired during domestica- tion. Plant J. 2022; 109 :1116-33

[4] Huang J, Zhang C, Zhao X. et al. The jujube genome provides insights into genome evolution and the domestication of sweet- ness/acidity taste in fruit trees. PLoS Genet. 2016; 12 :e1006433

[5] Guo M, Zhang Z, Li S. et al. Genomic analyses of diverse wild and cultivated accessions provide insights into the evolutionary history of jujube. Plant Biotechnol J. 2021; 19 :517-31

[6] Guo MX, Zhang ZR, Cheng YW. et al. Comparative population genomics dissects the genetic basis of seven domestication traits in jujube. Hortic Res. 2020; 7 :89

[7] Deng Y, Liu S, Zhang Y. et al. A telomere-to-telomere gap- free reference genome of watermelon and its mutation library provide important resources for gene discovery and breeding. Mol Plant. 2022; 15 :1268-84

[8] Garg S. Computational methods for chromosome-scale haplo- type reconstruction. Genome Biol. 2021; 22 :101

[9] Han X, Zhang Y, Zhang Q. et al. Two haplotype-resolved, gap-free genome assemblies for Actinidia latifolia and Actinidia chinensis shed light on the regulatory mechanisms of vitamin C and sucrose metabolism in kiwifruit. Mol Plant. 2023; 16 :452-70

[10] Yue J, Chen Q, Wang Y. et al. Telomere-to-telomere and gap-free reference genome assembly of the kiwifruit Actinidia chinensis. Hortic Res. 2023; 10 :uhac264

[11] Xu XD, Zhao RP, Xiao L. et al. Telomere-to-telomere assembly of cassava genome reveals the evolution of cassava and divergence of allelic expression. Hortic Res. 2023; 10 :uhad200

[12] Bao Y, Zeng Z, Yao W. et al. A gap-free and haplotype-resolved lemon genome provides insights into flavor synthesis and huan- glongbing (HLB) tolerance. Hortic Res. 2023; 10 :uhad020

[13] Li G, Tang L, He Y. et al. The haplotype-resolved T2T reference genome highlights structural variation underlying agronomic traits of melon. Hortic Res. 2023; 10 :uhad182

[14] Liu MJ, Zhao J, Cai QL. et al. The complex jujube genome provides insights into fruit tree biology. Nat Commun. 2014; 5 :5315

[15] Yang M, Han L, Zhang S. et al. Insights into the evolu- tion and spatial chromosome architecture of jujube from an updated gapless genome assembly. Plant Commun. 2023; 4 : 100662

[16] Shen LY, Luo H, Wang XL. et al. Chromosome-scale genome assembly for Chinese sour jujube and insights into its genome evolution and domestication signature. Front Plant Sci. 2021; 12 :773090

[17] 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 :92-5

[18] Qu Z, Wang Y. Chinese Fruit Trees Record—Chinese Jujube. Beijing: China Forestry Publishing House, 1993

[19] Liu M, Wang M. Germplasm Resources of Chinese Jujube. Beijing: China Forestry Publishing House, 2009

[20] Julius BT, Leach KA, Tran TM. et al. Sugar transporters in plants: new insights and discoveries. Plant Cell Physiol. 2017; 58 :1442-60

[21] Wu H-C, Bulgakov VP, Jinn T-L. Pectin methylesterases: cell wall remodeling proteins are required for plant response to heat stress. Front Plant Sci. 2018; 9 :1612

[22] Sun XL, Yu QY, Tang LL. et al. GsSRK, a G-type lectin S- receptor-like serine/threonine protein kinase, is a positive reg- ulator of plant tolerance to salt stress. J Plant Physiol. 2013; 170 : 505-15

[23] Zhao C, Zayed O, Yu Z. et al. Leucine-rich repeat extensin pro- teins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci USA. 2018; 115 :13123-8

[24] Disch S, Anastasiou E, Sharma VK. et al. The E3 ubiquitin lig- ase BIG BROTHER controls arabidopsis organ size in a dosage- dependent manner. Curr Biol. 2006; 16 :272-9

[25] Köhler C, Weinhofer-Molisch I. Mechanisms and evolution of genomic imprinting in plants. Heredity. 2010; 105 :57-63

[26] Cirilli M, Bassi D, Ciacciulli A. Sugars in peach fruit: a breeding perspective. Hortic Res. 2016; 3 :15067

[27] Qu Z, Wang Y. Chinese Fruit Trees Record—Chinese Jujube. Beijing: China Forestry Publishing House, 1993

[28] SunB. Shanwang plant fossils. Jinan: Shandong Science and Tech- nology Press, 1999

[29] Liang Z, Duan S, Sheng J. et al. Whole-genome resequencing of 472 Vitis accessions for grapevine diversity and demographic history analyses. Nat Commun. 2019; 10 :1190

[30] Porebski S, Bailey LG, Baum BR. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Report. 1997; 15 :8-15

[31] Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018; 34 :3094-100

[32] Zhang X, Zhang S, Zhao Q. et al. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nat Plants. 2019; 5 :833-45

[33] Jain C, Rhie A, Zhang H. et al. Weighted minimizer sampling improves long read mapping. Bioinformatics. 2020; 36 :i111-8

[34] Danecek P, Bonfield JK, Liddle J. et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021; 10 :giab:0008

[35] Lin YZ, Ye C, Li XZ. et al. quarTeT: a telomere-to-telomere toolkit for gap-free genome assembly and centromeric repeat identifi- cation. Hortic Res. 2023; 10 :uhad127

[36] Li H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics. 2016; 32 :2103-10

[37] Kim D, Paggi JM, Park C. et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37 :907-15

[38] Kovaka S, Zimin AV, Pertea GM. et al. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 2019; 20 :278

[39] Slater GS, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 2005; 6 :31

[40] Camacho C, Coulouris G, Avagyan V. et al. BLAST + : architecture and applications. BMC Bioinformatics. 2009; 10 :421

[41] Delcher AL, Bratke KA, Powers EC. et al. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007; 23 :673-9

[42] Stanke M, Diekhans M, Baertsch R. et al. Using native and syn- tenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008; 24 :637-44

[43] Holt C, Yandell M. MAKER2: an annotation pipeline and genome- database management tool for second-generation genome projects. BMC Bioinformatics. 2011; 12 :491

[44] Apweiler R, Bairoch A, Wu CH. et al. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2004; 32 :115D-9

[45] Deng YY, Li QQ, Wu SF. et al. Integrated nr database in pro- tein annotation system and its localization. Comput Eng. 2006; 32 :2

[46] Ashburner M, Ball CA, Blake JA. et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25 :25-9

[47] Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000; 28 :27-30

[48] Blum M, Chang HY, Chuguransky S. et al. The InterPro protein families and domains database:20 years on. Nucleic Acids Res. 2021; 49 :D344-54

[49] Finn RD, Bateman A, Clements J. et al. Pfam: the protein families database. Nucleic Acids Res. 2014; 42 :D222-30

[50] Goel M, Schneeberger K. Plotsr: visualizing structural similar- ities and rearrangements between multiple genomes. Bioinfor- matics. 2022; 38 :2922-6

[51] Li H, Handsaker B, Wysoker A. et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25 : 2078-9

[52] Purcell S, Neale B, Todd-Brown K. et al. PLINK: a tool set for whole-genome association and population-based linkage anal- yses. Am J Hum Genet. 2007; 81 :559-75

[53] Bradbury PJ, Zhang Z, Kroon DE. et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioin- formatics. 2007; 23 :2633-5

[54] Alexander DH, Novembre J, Lange K. Fast model-based estima- tion of ancestry in unrelated individuals. Genome Res. 2009; 19 : 1655-64

[55] Zhou Q, Tang D, Huang W. et al. Haplotype-resolved genome analyses of a heterozygous diploid potato. Nat Genet. 2020; 52 : 1018-23

[56] Chen C, Chen H, Zhang Y. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020; 13 :1194-202