Structural composition and evolution of jujube centromere reveal a dominant role for LTR retrotransposon

Donghui Lin , Yunxin Lan , Zhongchen Zhang , Jingjing Guo , Jian Shen , Guoliang Wang , Shufeng Zhang , Yihan Yang , Jiao Li , Guiming Liu , Zhiguo Liu , Mengjun Liu , Meng Yang

Horticulture Research ›› 2025, Vol. 12 ›› Issue (11) : 244

PDF (12011KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (11) :244 DOI: 10.1093/hr/uhaf244
Article
research-article
Structural composition and evolution of jujube centromere reveal a dominant role for LTR retrotransposon
Author information +
History +
PDF (12011KB)

Abstract

Centromeres are essential for centromere-specific histone H3 (CENH3) recruitment and kinetochore assembly, ensuring accurate chromosome segregation and maintaining genome stability in plants. Although extensively studied in model species, the structural organization of centromeres in nonmodel plants, such as fruit trees, remains poorly explored. Our previous study revealed that jujube centromeres lack the typical tandem repeat (TR)-rich structure, complicating their precise identification. In this study, we updated the genome assembly of jujube (Ziziphus jujuba Mill. ‘Dongzao’) to a haplotype-resolved T2T version, enabling accurate mapping and comparison of centromeres between haplotypes using CENH3 ChIP-seq. These centromeres, ranging from 0.75 to 1.40 Mb, are largely conserved between haplotypes, except for a localized inversion on chromosome 10. Unlike the TR-rich centromeres found in many plant species, jujube centromeres are predominantly composed of Gypsy-type long-terminal repeat retrotransposons (LTR-RTs). Among these, we identified a centromere-enriched LTR family, centromeric retrotransposons of jujube (CRJ), which is particularly abundant in terminal LTRs compared to the internal transposon regions. Comparative analysis across plant species revealed that centromeric retrotransposons primarily fall into three subfamilies—CRM, Tekay, and Athila—highlighting strong subfamily specificity. Notably, early insertions of CRJ-derived LTR segments contributed to the formation of TR-like structures, suggesting a mechanistic link between transposable elements and the evolution of centromeric tandem repeats. This work provides the first in-depth characterization of a TE-dominated centromere architecture in a fruit tree, offering new insights into the diversity and evolution of plant centromeres.

Cite this article

Download citation ▾
Donghui Lin, Yunxin Lan, Zhongchen Zhang, Jingjing Guo, Jian Shen, Guoliang Wang, Shufeng Zhang, Yihan Yang, Jiao Li, Guiming Liu, Zhiguo Liu, Mengjun Liu, Meng Yang. Structural composition and evolution of jujube centromere reveal a dominant role for LTR retrotransposon. Horticulture Research, 2025, 12(11): 244 DOI:10.1093/hr/uhaf244

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgments

We thank Dr. Wei Huang (College of Agronomy and Biotechnology, China Agricultural University) for providing technical support in the FISH experiments. This work was supported by the National Natural Science Foundation of China (grant no. 32171817), the Natural Science Foundation of Hebei Province (grant no. C2022204030), and the Special Research Project for New Talent of Hebei Agricultural University (grant no. YJ2020025).

Author contributions

M.Y. conceived the project; D.L., Y.L., J.G., J.S., G.L., and Z.L. prepared samples and performed the experiments; D.L., M.Y, Z.Z., S.Z., Y.Y., J.L., and G.W. performed the data analysis; D.L. and M.Y. draft the manuscript; M.Y. revised the manuscript; M.L. supervised the work. All authors have reviewed and approved the manuscript.

Data availability

The raw data of ChIP-seq are deposited in the National Genomics Data Center with BioProject: PRJCA039671. The haplotype-resolved genome and annotation file have been shared in the figshare repository at https://figshare.com/s/e040dc92e6ceb9ec232d.

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Henikoff S, Ahmad K, Malik HS. The centromere paradox: sta-ble inheritance with rapidly evolving DNA. Science. 2001; 293: 1098-102

[2]

Furuyama S, Biggins S. Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci. 2007; 104:14706-11

[3]

Smirnova JB, McFarlane RJ. The unique Centromeric chromatin structure of Schizosaccharomyces pombe is maintained during meiosis. JBiolChem. 2002; 277:19817-22

[4]

Presting GG. Centromeric retrotransposons and centromere function. Curr Opin Genet Dev. 2018; 49:79-84

[5]

Malik HS, Henikoff S. Major evolutionary transitions in cen-tromere complexity. Cell. 2009; 138:1067-82

[6]

Naish M, Henderson IR. The structure, function, and evolution of plant centromeres. Genome Res. 2024; 34:161-78

[7]

Melters DP, Bradnam KR, Young HA. et al. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 2013; 14:1-20

[8]

Naish M, Alonge M, Wlodzimierz P. et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science. 2021;374:eabi7489

[9]

Liu Y, Yi C, Fan C. et al. Pan-centromere reveals widespread centromere repositioning of soybean genomes. Proc Natl Acad Sci. 2023; 120:e2310177120

[10]

Zhang L, Liang J, Chen H. et al. A near-complete genome assem-bly of Brassica rapa provides new insights into the evolution of centromeres. Plant Biotechnol J. 2023; 21:1022-32

[11]

Ahmed HI, Heuberger M, Schoen A. et al. Einkorn genomics sheds light on history of the oldest domesticated wheat. Nature. 2023; 620:830-8

[12]

Liu Q, Yi C, Zhang Z. et al. Non-B-form DNA tends to form in centromeric regions and has undergone changes in polyploid oat subgenomes. Proc Natl Acad Sci. 2023; 120:e2211683120

[13]

LiuC, FuS, YiC. et al. Unveiling the distinctive traits of functional rye centromeres: minisatellites, retrotransposons, and R-loop formation. Sci China Life Sci. 2024; 67:1989-2002

[14]

Yang X, Zhang L, Guo X. et al. The gap-free potato genome assem-bly reveals large tandem gene clusters of agronomical impor-tance in highly repeated genomic regions. Mol Plant. 2023; 16: 314-7

[15]

Chen W, Wang X, Sun J. et al. Two telomere-to-telomere gapless genomes reveal insights into capsicum evolution and capsaici-noid biosynthesis. Nat Commun. 2024; 15:4295

[16]

Chen W, Yan M, Chen S. et al. The complete genome assembly of Nicotiana benthamiana reveals the genetic and epigenetic land-scape of centromeres. Nat Plants. 2024; 10:1928-43

[17]

Pélissier T, Tutois S, Deragon J. et al. Athila, a new retroelement from Arabidopsis thaliana. Plant Mol Biol. 1995; 29:441-52

[18]

Han J, Masonbrink RE, Shan W. et al. Rapid proliferation and nucleolar organizer targeting centromeric retrotransposons in cotton. Plant J. 2016; 88:992-1005

[19]

Sharma A, Wolfgruber TK, Presting GG. Tandem repeats derived from centromeric retrotransposons. BMC Genomics. 2013; 14:1-11

[20]

Gong Z, Wu Y, Koblízková A. et al. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell. 2012; 24:3559-74

[21]

Zhang H, Koblížková A, Wang K. et al. Boom-bust turnovers of Megabase-sized Centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell. 2014; 26:1436-47

[22]

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

[23]

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

[24]

Zhou J, Liu Y, Guo X. et al. Centromeres: from chromosome biology to biotechnology applications and synthetic genomes in plants. Plant Biotechnol J. 2022; 20:2051-63

[25]

Li K, Chen R, Abudoukayoumu A. et al. Haplotype-resolved T2T reference genomes for wild and domesticated accessions shed new insights into the domestication of jujube. Hortic Res. 2024;11:uhae071

[26]

Hu H, Wang J, Nie S. et al. Plant pangenomics, current practice and future direction. Agric Commun. 2024; 2:100039

[27]

Huang Y, Ding W, Zhang M. et al. The formation and evolution of centromeric satellite repeats in Saccharum species. Plant J. 2021; 106:616-29

[28]

Bao Z, Li C, Li G. et al. Genome architecture and tetrasomic inheritance of autotetraploid potato. Mol Plant. 2022; 15:1211-26

[29]

Wolfgruber TK, Sharma A, Schneider KL. et al. Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic loci shaped primarily by retrotransposons. PLoS Genet. 2009; 5:e1000743

[30]

Zhang Y, Fan C, Li S. et al. The diversity of sequence and chromosomal distribution of new transposable element-related segments in the rye genome revealed by FISH and lineage anno-tation. Front Plant Sci. 2017; 8:1706

[31]

Wang Y, Zhou F, Li Y. et al. Characterization of the CsCENH3 protein and centromeric DNA profiles reveal the structures of centromeres in cucumber. Hortic Res. 2024;11, uhae127

[32]

Zwirglmaier K. Fluorescence in situ hybridisation (FISH) - the next generation. FEMS Microbiol Lett. 2005; 246:151-8

[33]

Tsukahara S, Bousios A, Perez-Roman E. et al. Centrophilic retro-transposon integration via CENH3 chromatin in Arabidopsis. Nature. 2025; 637:744-8

[34]

Wlodzimierz P, Rabanal FA, Burns R. et al. Cycles of satellite and transposon evolution in Arabidopsis centromeres. Nature. 2023; 618:557-65

[35]

Shimizu KK. Robustness and the generalist niche of polyploid species: genome shock or gradual evolution? Curr Opin Plant Biol. 2022; 69:102292

[36]

Parisod C, Alix K, Just J. et al. Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol. 2010; 186:37-45

[37]

Cheng H, Concepcion GT, Feng X. et al. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021; 18:170-5

[38]

Guan D, McCarthy SA, Wood J. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinfor-matics. 2020; 36:2896-8

[39]

Ou S, Jiang N. LTR_retriever: a highly accurate and sensitive pro-gram for identification of long terminal repeat retrotransposons. Plant Physiol. 2018; 176:1410-22

[40]

Zhang R-G, Li G-Y, Wang X-L. et al. TEsorter: an accurate and fast method to classify LTR-retrotransposons in plant genomes. Hortic Res. 2022;9:uhac017

[41]

Simao FA, Waterhouse RM, Ioannidis P. et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31:3210-2

[42]

Wang Y, Tang H, DeBarry JD. et al. MCScanX: a toolkit for detec-tion and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40:e49-9

[43]

Zhou Z-W, Yu Z-G, Huang X-M. et al. GenomeSyn: a bioin-formatics tool for visualizing genome synteny and structural variations. J Genet Genomics. 2022; 49:1174-6

[44]

Krzywinski M, Schein J, Birol I. et al. Circos: an information aes-thetic for comparative genomics. Genome Res. 2009; 19:1639-45

[45]

Cui J, Zhu C, Shen L. et al. The gap-free genome of Forsythia suspensa illuminates the intricate landscape of centromeres. Hortic Res. 2024;11:uhae185

[46]

Chen S, Zhou Y, Chen Y. et al. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884-90

[47]

Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012; 9:357-9

[48]

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

[49]

Ramírez F, Ryan DP, Grüning B. et al. deepTools2: a next genera-tion web server for deep-sequencing data analysis. Nucleic Acids Res. 2016;44:W160-5

[50]

Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013; 14:178-92

[51]

Lopez-Delisle L, Rabbani L, Wolff J. et al. pyGenomeTracks: repro-ducible plots for multivariate genomic datasets. Bioinformatics. 2021; 37:422-3

[52]

Xie Y, Li H, Luo X. et al. IBS 2.0: an upgraded illustrator for the visualization of biological sequences. Nucleic Acids Res. 2022;50:W420-6

[53]

Huang Y, Huang W, Meng Z. et al. Megabase-scale presence-absence variation with Tripsacum origin was under selec-tion during maize domestication and adaptation. Genome Biol. 2021; 22:237

[54]

Guo L, Wang X, Ayhan DH. et al. Super pangenome of Vitis empowers identification of downy mildew resistance genes for grapevine improvement. Nat Genet. 2025; 57:741-53

[55]

Feng J, Zhang W, Chen C. et al. The pineapple reference genome: telomere-to-telomere assembly, manually curated annotation, and comparative analysis. J Integr Plant Biol. 2024; 66:2208-25

[56]

Chen J, Wang Z, Tan K. et al. A complete telomere-to-telomere assembly of the maize genome. Nat Genet. 2023; 55:1221-31

[57]

Song J-M, Xie W-Z, Wang S. et al. Two gap-free reference genomes and a global view of the centromere architecture in rice. Mol Plant. 2021; 14:1757-67

[58]

Yang Y, Wu Z, Wu Z. et al. A near-complete assembly of aspara-gus bean provides insights into anthocyanin accumulation in pods. Plant Biotechnol J. 2023; 21:2473-89

[59]

Wang L, Zhang M, Li M. et al. A telomere-to-telomere gap-free assembly of soybean genome. Mol Plant. 2023; 16:1711-4

[60]

Minh BQ, Schmidt HA, Chernomor O. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020; 37:1530-4

[61]

Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293-6

PDF (12011KB)

306

Accesses

0

Citation

Detail

Sections
Recommended

/