Telomere-to-telomere assembly of cassava genome reveals the evolution of cassava and divergence of allelic expression

Xin-Dong Xu , Ru-Peng Zhao , Liang Xiao , Liuying Lu , Min Gao , Yu-Hong Luo , Zu-Wen Zhou , Si-Ying Ye , Yong-Qing Qian , Bing-Liang Fan , Xiaohong Shang , Pingli Shi , Wendan Zeng , Sheng Cao , Zhengdan Wu , Huabing Yan , Ling-Ling Chen , Jia-Ming Song

Horticulture Research ›› 2023, Vol. 10 ›› Issue (11) : 200

PDF (7074KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (11) :200 DOI: 10.1093/hr/uhad200
Article
research-article
Telomere-to-telomere assembly of cassava genome reveals the evolution of cassava and divergence of allelic expression
Author information +
History +
PDF (7074KB)

Abstract

Cassava is a crucial crop that makes a significant contribution to ensuring human food security. However, high-quality telomere-to-telomere cassava genomes have not been available up to now, which has restricted the progress of haploid molecular breeding for cassava. In this study, we constructed two nearly complete haploid resolved genomes and an integrated, telomere-to-telomere gap-free reference genome of an excellent cassava variety, ‘Xinxuan 048’, thereby providing a new high-quality genomic resource. Furthermore, the evolutionary history of several species within the Euphorbiaceae family was revealed. Through comparative analysis of haploid genomes, it was found that two haploid genomes had extensive differences in linear structure, transcriptome features, and epigenetic characteristics. Genes located within the highly divergent regions and differentially expressed alleles are enriched in the functions of auxin response and the starch synthesis pathway. The high heterozygosity of cassava ‘Xinxuan 048’ leads to rapid trait segregation in the first selfed generation. This study provides a theoretical basis and genomic resource for molecular breeding of cassava haploids.

Cite this article

Download citation ▾
Xin-Dong Xu, Ru-Peng Zhao, Liang Xiao, Liuying Lu, Min Gao, Yu-Hong Luo, Zu-Wen Zhou, Si-Ying Ye, Yong-Qing Qian, Bing-Liang Fan, Xiaohong Shang, Pingli Shi, Wendan Zeng, Sheng Cao, Zhengdan Wu, Huabing Yan, Ling-Ling Chen, Jia-Ming Song. Telomere-to-telomere assembly of cassava genome reveals the evolution of cassava and divergence of allelic expression. Horticulture Research, 2023, 10 (11) : 200 DOI:10.1093/hr/uhad200

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32100526, 32270712), the Guangxi Natural Science Foundation (AD23026047), the Young Elite Scientists Sponsorship Program by CAST (2022QNRC001), the State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources (SKLCUSA-a202205, SKLCUSA-a03), Ba-Gui Scholar Program of Guangxi (To Z.G. H), the Project of Bama County for Talents in Science and Technology (20220008), Chief Expert of Tuberous Crops Innovation Team in Guangxi Province (nycytxgxcxtd-2023-11-01) and the starting research grant for High-level Talents and Innovation and development multiplication plan from Guangxi University (2022BZRC015).

Author contributions

J.M.S., L.L.C., and H.B.Y. conceived and designed the study. L.L., X.H.S., P.S., W.Z., S.C., and Z.D.W. contributed to sample preparation. X.D.X., R.P.Z., L.X., M.G., Y.H.L., Z.W.Z., S.Y.Y., Y.Q.Q., and B.L.F. participated in data analysis and substantively revised the manuscript. All authors read and approved the final manuscript.

Data availability

The original sequencing and assembly of the cassava variety XX048 genome is available from the National Genomics Data Center [77] under project number PRJCA016162.

Conflict of interest

The authors declare that they have no conflict of interest.

References

[1]

Parmar A, Sturm B, Hensel O . Crops that feed the world: production and improvement of cassava for food, feed, and industrial uses. Food Sec. 2017; 9: 907-27

[2]

Xiao L, Lu L, Zeng W. et al. DNA methylome and LncRNAome analysis provide insights into mechanisms of genome-dosage effects in autotetraploid cassava. Front Plant Sci. 2022; 13: 915056

[3]

Hu W, Ji C, Shi H. et al. Allele-defined genome reveals biallelic differentiation during cassava evolution. Mol Plant. 2021; 14: 851-4

[4]

Halsey ME, Olsen KM, Taylor NJ. et al. Reproductive biology of cassava (Manihot esculenta Crantz) and isolation of experimental field trials . Crop Sci. 2008; 48: 49-58

[5]

Lyons JB, Bredeson JV, Mansfeld BN. et al. Current status and impending progress for cassava structural genomics. Plant Mol Biol. 2022; 109: 177-91

[6]

Qi W, Lim YW, Patrignani A. et al. The haplotype-resolved chromosome pairs of a heterozygous diploid African cassava cultivar reveal novel pan-genome and allele-specific transcriptome features. GigaScience. 2022; 11: giac028

[7]

Kuon J-E, Qi W, Schläpfer P. et al. Haplotype-resolved genomes of geminivirus-resistant and geminivirus-susceptible African cassava cultivars. BMC Biol. 2019; 17: 75

[8]

Mao Y, Zhang G . A complete, telomere-to-telomere human genome sequence presents new opportunities for evolutionary genomics. Nat Methods. 2022; 19: 635-8

[9]

Song J-M, Xie WZ, 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

[10]

Nurk S, Koren S, Rhie A. et al. The complete sequence of a human genome. Science. 2022; 376: 44-53

[11]

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

[12]

Ma B, Wang H, Liu J. et al. The gap-free genome of mulberry elucidates the architecture and evolution of polycentric chromosomes. Hortic Res. 2023; 10: uhad111

[13]

Wang T, Wang B, Hua X. et al. A complete gap-free diploid genome in Saccharum complex and the genomic footprints of evolution in the highly polyploid Saccharum genus . Nat Plants. 2023; 9: 554-71

[14]

Zhou Y, Xiong J, Shu Z. et al. The telomere-to-telomere genome of Fragaria vesca reveals the genomic evolution of Fragaria and the origin of cultivated octoploid strawberry . Hortic Res. 2023; 10: uhad027

[15]

Luo X. Selection and application of new cassava variety Xinxuan048. Chin Agron Bull. 2009; 25: 501-5

[16]

Ou S, Chen J, Jiang N . Assessing genome assembly quality using the LTR assembly index (LAI). Nucleic Acids Res. 2018; 46: e126

[17]

Bredeson JV, Lyons JB, Prochnik SE. et al. Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nat Biotechnol. 2016; 34: 562-70

[18]

Lu J, Pan C, Fan W. et al. A chromosome-level genome assembly of wild castor provides new insights into its adaptive evolution in tropical desert. Genomics Proteomics Bioinformatics. 2022; 20: 42-59

[19]

Jalali S, Kancharla N, Yepuri V. et al. Exploitation of Hi-C sequencing for improvement of genome assembly and in-vitro validation of differentially expressing genes in Jatropha curcas L. 3 Biotech. 2020; 10: 91

[20]

Liu J, Shi C, Shi CC. et al. The chromosome-based rubber tree genome provides new insights into spurge genome evolution and rubber biosynthesis. Mol Plant. 2020; 13: 336-50

[21]

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

[22]

Navrátilová P, Toegelová H, Tulpová Z. et al. Prospects of telomere-to-telomere assembly in barley: analysis of sequence gaps in the MorexV3 reference genome. Plant Biotechnol J. 2022; 20: 1373-86

[23]

Kawahara Y, de la Bastide M, Hamilton JP. et al. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data . Rice. 2013; 6: 4

[24]

Theologis A, Ecker JR, Palm CJ. et al. Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature. 2000; 408: 816-20

[25]

Song J-M, Guan Z, Hu J. et al. Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat Plants. 2020; 6: 34-45

[26]

Li H, Feng X, Chu C . The design and construction of reference pangenome graphs with minigraph. Genome Biol. 2020; 21: 265

[27]

Hu G, Feng J, Xiang X. et al. Two divergent haplotypes from a highly heterozygous lychee genome suggest independent domestication events for early and late-maturing cultivars. Nat Genet. 2022; 54: 73-83

[28]

Niederhuth CE, Bewick AJ, Ji L. et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 2016; 17: 194

[29]

Zhong Z, Feng S, Mansfeld BN. et al. Haplotype-resolved DNA methylome of African cassava genome. Plant Biotechnol J. 2023; 21: 247-9

[30]

Della Coletta R, Qiu Y, Ou S. et al. How the pan-genome is changing crop genomics and improvement. Genome Biol. 2021; 22: 3

[31]

Wang S, Qian Y-Q, Zhao R-P. et al. Graph-based pan-genomes: increased opportunities in plant genomics. J Exp Bot. 2023; 74: 24-39

[32]

Wang T, Antonacci-Fulton L, Howe K. et al. The human pangenome project: a global resource to map genomic diversity. Nature. 2022; 604: 437-46

[33]

Qin P, Lu H, du H. et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell. 2021; 184: 3542-3558.e16

[34]

Hufford MB, Seetharam AS, Woodhouse MR. et al. De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science. 2021; 373: 655-62

[35]

Zhang X, Liu T, Wang J. et al. Pan-genome of Raphanus highlights genetic variation and introgression among domesticated, wild, and weedy radishes . Mol Plant. 2021; 14: 2032-55

[36]

Marçais G, Kingsford C . A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011; 27: 764-70

[37]

Ranallo-Benavidez TR, Jaron KS, Schatz MC . GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 2020; 11: 1432

[38]

Simpson JT, Durbin R . Efficient construction of an assembly string graph using the FM-index. Bioinformatics. 2010; 26: i367-73

[39]

Cheng H, Jarvis ED, Fedrigo O. et al. Haplotype-resolved assembly of diploid genomes without parental data. Nat Biotechnol. 2022; 40: 1332-5

[40]

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

[41]

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

[42]

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: 95-8

[43]

Xu G-C, Xu TJ, Zhu R. et al. LR_Gapcloser: a tiling path-based gap closer that uses long reads to complete genome assembly. GigaScience. 2019; 8: giy157

[44]

Vaser R, Sović I, Nagarajan N. et al. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 2017; 27: 737-46

[45]

Alonge M, Lebeigle L, Kirsche M. et al. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol. 2022; 23: 258

[46]

Xu M, Guo L, Gu S. et al. TGS-GapCloser: a fast and accurate gap closer for large genomes with low coverage of error-prone long reads. GigaScience. 2020; 9: giaa094

[47]

Walker BJ, Abeel T, Shea T. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014; 9: e112963

[48]

Rhie A, Walenz BP, Koren S. et al. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 2020; 21: 245

[49]

Marçais G, Delcher AL, Phillippy AM. et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol. 2018; 14: e1005944

[50]

Goel M, Sun H, Jiao W-B. et al. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 2019; 20: 277

[51]

Cingolani P, Platts A, Wang LL. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3 . Fly (Austin). 2012; 6: 80-92

[52]

Yin L, Zhang H, Tang Z. et al. rMVP: a memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. Genomics Proteomics Bioinformatics. 2021; 19: 619-28

[53]

Zhou Z-W, Yu ZG, Huang XM. et al. GenomeSyn: a bioinformatics tool for visualizing genome synteny and structural variations. J Genet Genomics. 2022; 49: 1174-6

[54]

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

[55]

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

[56]

Li H . A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011; 27: 2987-93

[57]

Robinson JT, Thorvaldsdottir H, Turner D. et al. Igv.Js: an embeddable JavaScript implementation of the Integrative Genomics Viewer (IGV). Bioinformatics. 2023; 39: btac830

[58]

Wolff J, Rabbani L, Gilsbach R. et al. Galaxy HiCExplorer 3: a web server for reproducible Hi-C, capture Hi-C and single-cell Hi-C data analysis, quality control and visualization. Nucleic Acids Res. 2020; 48: W177-84

[59]

Wu TD, Watanabe CK . GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics. 2005; 21: 1859-75

[60]

Emms DM, Kelly S . OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019; 20: 238

[61]

Emms DM, Kelly S . OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015; 16: 157

[62]

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30: 1312-3

[63]

De Bie T, Cristianini N, Demuth JP. et al. CAFE: a computational tool for the study of gene family evolution. Bioinformatics. 2006; 22: 1269-71

[64]

Yang Z . PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24: 1586-91

[65]

Tang H, Bowers JE, Wang X. et al. Synteny and collinearity in plant genomes. Science. 2008; 320: 486-8

[66]

Sun P, Jiao B, Yang Y. et al. WGDI: a user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Mol Plant. 2022; 15: 1841-51

[67]

Liu P-L, Zhang X, Mao JF. et al. The Tetracentron genome provides insight into the early evolution of eudicots and the formation of vessel elements . Genome Biol. 2020; 21: 291

[68]

Zhang Y, Park C, Bennett C. et al. Rapid and accurate alignment of nucleotide conversion sequencing reads with HISAT-3N. Genome Res. 2021; 31: 1290-5

[69]

Liao Y, Smyth GK, Shi W . featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014; 30: 923- 30

[70]

Love MI, Huber W, Anders S . Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15: 550

[71]

Wu T, Hu E, Xu S. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation (Camb). 2021; 2: 100141

[72]

Yu G, Wang L-G, Han Y. et al. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012; 16: 284-7

[73]

Bardou P, Mariette J, Escudié F. et al. jvenn: an interactive Venn diagram viewer. BMC Bioinformatics. 2014; 15: 293

[74]

Wick RR, Schultz MB, Zobel J. et al. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics. 2015; 31: 3350-2

[75]

Xi Y, Li W . BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics. 2009; 10: 232

[76]

Servant N, Varoquaux N, Lajoie BR. et al. HiC-pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 2015; 16: 259

[77]

CNCB-NGDC Members and Partners. Database resources of the National Genomics Data Center, China National Center for Bioinformation in 2023. Nucleic Acids Res. 2023; 51: D18-28

PDF (7074KB)

77

Accesses

0

Citation

Detail

Sections
Recommended

/