甜樱桃Tieton v3.0的单倍型解析端粒到端粒参考基因组鉴定了与黄色果皮品种相关的大片段缺失

doi:10.1016/j.jia.2025.07.022

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (11): 4271-4281.DOI: 10.1016/j.jia.2025.07.022

甜樱桃Tieton v3.0的单倍型解析端粒到端粒参考基因组鉴定了与黄色果皮品种相关的大片段缺失

收稿日期:2024-08-20 修回日期:2025-07-21 接受日期:2025-06-09 出版日期:2025-11-20 发布日期:2025-10-13

Haplotype-resolved telomere-to-telomere reference genome of sweet cherry ‘Tieton’ v3.0 characterized the large fragment deletion associated with yellow-skinned variety

Ting Yu^1*, Ke Lin^{1, 2*}, Dongzi Zhu¹, Xingyan Li¹, Qian Qiao¹, Po Hong¹, Shibo Lin³, Quanfu Zhang³, Qingzhong Liu^1#, Jiawei Wang^1#

¹Shandong Institute of Pomology, Tai’an 271000, China
²School of Biology and Brewing Engineering, Taishan University, Tai’an 271000, China
³Yantai Yaohua Agricultural Technology Limited Company, Yantai 264003, China

Received:2024-08-20 Revised:2025-07-21 Accepted:2025-06-09 Online:2025-11-20 Published:2025-10-13
About author:#Correspondence Jiawei Wang, Tel: +86-538-8266605, E-mail: wangjw-sdip@qq.com; Qingzhong Liu, Tel: +86-538-8266663, E-mail: qzliu001@126.com * These authors contributed equally to this study.
Supported by:
This work was supported by the Shandong Provincial Natural Science Foundation, China (ZR2021MC117) and the Key R&D Program of Shandong Province, China (2022TZXD006).

摘要/Abstract

摘要：

甜樱桃（Prunus avium）是温带地区的重要核果树种之一。自第一个甜樱桃基因组发布以来，甜樱桃的分子育种取得了重大进展。已发表甜樱桃的基因组中存在的缺口较多，且嵌合序列无法区分单倍型等位基因信息，大大限制了对一些重要农艺性状的遗传研究。在本研究中，我们获得了甜樱桃“美早”单倍型解析端粒到端粒的参考基因组。在“美早”两个单倍型基因组中共有653.03 Mb的序列挂载到16个染色体，共预测了67,012个编码基因，其中，在hapA中包含33,777个基因，hapB中包含33,235个基因。该基因组的单碱基准确率的质量值超过44，conting N50超过17.94 Mb，有胚植物单拷贝同源基因基集（BUSCO）完整性达到98.7%，长末端重复序列组装指数(LAI)超过20,达到了金标准的水平。该基因组提供了单倍型解析的染色体组，全面解析了甜樱桃杂合二倍体基因组的结构差异。此外，利用该参考基因组，我们鉴定了与甜樱桃“13-33”黄色果皮性状相关的一个大片段缺失。期望该基因组能够为甜樱桃育种工作和遗传学研究的提供帮助。

Abstract:

Sweet cherry (Prunus avium) represents a significant stone fruit crop in temperate regions worldwide. While molecular breeding has progressed substantially following the initial sweet cherry genome release, existing genome assemblies contain unresolved gaps and comprise consensus chimeric sequences that fail to differentiate haplotype alleles, significantly constraining research on important agronomic trait inheritance. This study presents a phased-resolved telomere-to-telomere reference genome of sweet cherry ‘Tieton’. The assembly anchors 653.03 Mb of sequence onto 16 pseudochromosomes representing two haplotypes, with 67,012 coding genes identified (33,777 in hapA and 33,235 in hapB). The genome demonstrates superior quality metrics, including a consensus accuracy exceeding QV44, contig N50 above 17.94 Mb, Benchmarking Universal Single-Copy Orthologs completeness of 98.7%, and a long terminal repeat (LTR) assembly index exceeding 20. This genome provides phased and annotated chromosome pairs, offering a comprehensive view of sweet cherry’s diploid genome organization. Utilizing this reference genome, we identified a large fragment deletion associated with yellow-skinned fruit in sweet cherry ‘13-33’. This resource will significantly enhance breeding efforts and genetic research in sweet cherries.

Key words: sweet cherry , nanopore , Hi-C , genomic , chromosomal assembly

Ting Yu, Ke Lin, Dongzi Zhu, Xingyan Li, Qian Qiao, Po Hong, Shibo Lin, Quanfu Zhang, Qingzhong Liu, Jiawei Wang. 甜樱桃Tieton v3.0的单倍型解析端粒到端粒参考基因组鉴定了与黄色果皮品种相关的大片段缺失[J]. Journal of Integrative Agriculture, 2025, 24(11): 4271-4281.

Ting Yu, Ke Lin, Dongzi Zhu, Xingyan Li, Qian Qiao, Po Hong, Shibo Lin, Quanfu Zhang, Qingzhong Liu, Jiawei Wang. Haplotype-resolved telomere-to-telomere reference genome of sweet cherry ‘Tieton’ v3.0 characterized the large fragment deletion associated with yellow-skinned variety[J]. Journal of Integrative Agriculture, 2025, 24(11): 4271-4281.

参考文献

Alioto T, Alexiou K G, Bardil A, Barteri F, Castanera R, Cruz F, Dhingra A, Duval H, Martí A F I, Frias L, Galán B, García J L, Howad W, Gómez-Garrido J, Gut M, Julca I, Morata J, Puigdomènech P, Ribeca P, Cabetas M J R, et al. 2020. Transposons played a major role in the diversification between the closely related almond and peach genomes: Results from the almond genome sequence. Plant Journal, 101, 455–472.

Blazek J, Zeleny L, Suran P. 2022. Sweet cherry research world overview 2015–2017. Horticultural Science, 49, 121–146.

Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C. 2012. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell, 24, 1242–1255.

Calle A, Wünsch A. 2020. Multiple-population QTL mapping of maturity and fruit-quality traits reveals LG4 region as a breeding target in sweet cherry (Prunus avium L.). Horticulture Research, 7, 127.

Cao K, Yang X, Li Y, Zhu G, Fang W, Chen C, Wang X, Wu J, Wang L. 2021. New high-quality peach (Prunus persica L. Batsch) genome assembly to analyze the molecular evolutionary mechanism of volatile compounds in peach fruits. Plant Journal, 108, 281–295.

Castillejo C, Waurich V, Wagner H, Ramos R, Oiza N, Muñoz P, Triviño J C, Caruana J, Liu Z, Cobo N, Hardigan M A, Knapp S J, Vallarino J G, Osorio S, Martín-Pizarro C, Posé D, Toivainen T, Hytönen T, Oh Y, Barbey C R, et al. 2020. Allelic variation of MYB10 is the major force controlling natural variation in skin and flesh color in strawberry (Fragaria spp.) fruit. Plant Cell, 32, 3723–3749.

Chagné D, Kui L W, Espley R V, Volz R K, How N M, Rouse S, Brendolise C, Carlisle C M, Kumar S, De Silva N, Micheletti D, McGhie T, Crowhurst R N, Storey R D, Velasco R, Hellens R P, Gardiner S E, Allan A C. 2013. An ancient duplication of apple MYB transcription factors is responsible for novel red fruit-flesh phenotypes. Plant Physiology, 161, 225–239.

Cheng H, Concepcion G T, Feng X, Zhang H, Li H. 2021. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nature Methods, 18, 170–175.

Da necek P, Bonfield J K, Liddle J, Marshall J, Ohan V, Pollard M O, Whitwham A, Keane T, McCarthy S A, Davies R M, Li H. 2021. Twelve years of SAMtools and BCFtools. Gigascience, 10, giab008.

Dong Y X, Qi X L, Liu C L, Song L L, Ming L. 2022. A sweet cherry AGAMOUS-LIKE transcription factor PavAGL15 affects fruit size by directly repressing the PavCYP78A9 expression. Scientia Horticulturae, 297, 110947.

Donkpegan A S, Bernard A, Barreneche T, Quero-García J, Bonnet H, Fouché M, Le Dantec L, Wenden B, Dirlewanger E. 2023. Genome-wide association mapping in a sweet cherry germplasm collection (Prunus avium L.) reveals candidate genes for fruit quality traits. Horticulture Research, 10, uhad191.

Dudchenko O, Batra S S, Omer A D, Nyquist S K, Hoeger M, Durand N C, Shamim M S, Machol I, Lander E S, Aiden A P, Aiden E L. 2017. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science, 356, 92–95.

Durand N C, Shamim M S, Machol I, Rao S S, Huntley M H, Lander E S, Aiden E L. 2016. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems, 3, 95–98.

Edger P P, Poorten T J, VanBuren R, Hardigan M A, Colle M, McKain M R, Smith R D, Teresi S J, Nelson D L, Wai C M, Alger E I, Bird K A, Yocca A E, Pumplin N, Ou S, Ben-Zvi G, Brodt A, Baruch K, Swale T, Shiue L, et al. 2019. Origin and evolution of the octoploid strawberry genome. Nature Genetics, 51, 541–547.

Emms D M, Kelly S. 2019. OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biology, 20, 238.

Espley R V, Brendolise C, Chagné D, Kutty-Amma S, Green S, Volz R, Putterill J, Schouten H J, Gardiner S E, Hellens R P, Allan A C. 2009. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell, 21, 168–183.

Fiol A, García-Gómez B E, Jurado-Ruiz F, Alexiou K, Howad W, Aranzana M J. 2021. Characterization of Japanese plum (Prunus salicina) PsMYB10 alleles reveals structural variation and polymorphisms correlating with fruit skin color. Frontiers in Plant Science, 12, 655267.

Foster T M, Celton J M, Chagné D, Tustin D S, Gardiner S E. 2015. Two quantitative trait loci, Dw1 and Dw2, are primarily responsible for rootstock-induced dwarfing in apple. Horticulture Research, 2, 15001.

Fu A, Zheng Y, Guo J, Grierson D, Zhao X, Wen C, Liu Y, Li J, Zhang X, Yu Y, Ma H, Wang Q, Zuo J. 2022. Telomere-to-telomere genome assembly of bitter melon (Momordica charantia L. var. abbreviata Ser.) reveals fruit development, composition and ripening genetic characteristics. Horticulture Research, 10, uhac228.

Hoff K J, Stanke M. 2019. Predicting genes in single genomes with AUGUSTUS. Current Protocols in Bioinformatics, 65, e57.

Holusova K, Cmejlova J, Suran P, Cmejla R, Sedlak J, Zeleny L, Bartos J. 2023. High-resolution genome-wide association study of a large Czech collection of sweet cherry (Prunus avium L.) on fruit maturity and quality traits. Horticulture Research, 10, uhac233.

Huang D, Wang X, Tang Z, Yuan Y, Xu Y, He J, Jiang X, Peng S A, Li L, Butelli E, Deng X, Xu Q. 2018. Subfunctionalization of the Ruby2-Ruby1 gene cluster during the domestication of citrus. Nature Plants, 4, 930–941.

Hubley R, Finn R D, Clements J, Eddy S R, Jones T A, Bao W, Smit A F, Wheeler T J. 2016. The Dfam database of repetitive DNA families. Nucleic Acids Research, 44, D81–D89.

Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund S K, Cook H, Mende D R, Letunic I, Rattei T, Jensen L J, von Mering C, Bork P. 2019. eggNOG 5.0: A hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47, D309–D314.

Jin W, Wang H, Li M, Wang J, Yang Y, Zhang X, Yan G, Zhang H, Liu J, Zhang K. 2016. The R2R3 MYB transcription factor PavMYB10.1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry (Prunus avium L.). Plant Biotechnology Journal, 14, 2120–2133.

Korf I. 2004. Gene finding in novel genomes. BMC Bioinformatics, 5, 59.

Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J, Marra M A. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.

Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. BMC Bioinformatics, 26, 589–595.

Kui L W, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie T K, Espley R V, Hellens RP, Allan A C. 2010. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology, 10, 50.

Lin Y, Ye C, Li X, Chen Q, Wu Y, Zhang F, Pan R, Zhang S, Chen S, Wang X, Cao S, Wang Y, Yue Y, Liu Y, Yue J. 2023. quarTeT: A telomere-to-telomere toolkit for gap-free genome assembly and centromeric repeat identification. Horticulture Research, 10, uhad127.

Liu C, Qi X, Song L, Chen L, Dong Y, Pan F, Zheng W, Li Y, Zhao B, Guo W, Li M, Wang Z. 2023. Large-fragment deletion encompasses the R2R3 MYB transcription factor, PavMYB10.1, causes yellow fruits in sweet cherry (Prunus avium L.). Scientia Horticulturae, 309, 111648.

Lomsadze A, Ter-Hovhannisyan V, Chernoff Y O, Borodovsky M. 2005. Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Research, 33, 6494–6506.

Majoros W H, Pertea M, Salzberg S L. 2004. TigrScan and GlimmerHMM: Two open source ab initio eukaryotic gene-finders. BMC Bioinformatics, 20, 2878–2879.

Ou S, Chen J, Jiang N. 2018. Assessing genome assembly quality using the LTR Assembly Index (LAI). Nucleic Acids Research, 46, e126.

Rautiainen M, Nurk S, Walenz B P, Logsdon G A, Porubsky D, Rhie A, Eichler E E, Phillippy A M, Koren S. 2023. Telomere-to-telomere assembly of diploid chromosomes with Verkko. Nature Biotechnology, 41, 1474–1482.

Rhie A, Walenz B P, Koren S, Phillippy A M. 2020. Merqury: Reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biology, 21, 245.

Seppey M, Manni M, Zdobnov E M. 2019. BUSCO: Assessing genome assembly and annotation completeness. Methods in Molecular Biolgy, 1962, 227–245.

Shen T J, Wen X P, Wen Z, Qiu Z L, Hou Q D, Li Z C, Mei L N, Yu H H, Qiao G. 2021. Genome-wide identification and expression analysis of bHLH transcription factor family in response to cold stress in sweet cherry (Prunus avium L.). Scientia Horticulturae, 279, 109905.

Shirasawa K, Isuzugawa K, Ikenaga M, Saito Y, Yamamoto T, Hirakawa H, Isobe S. 2017. The genome sequence of sweet cherry (Prunus avium) for use in genomics-assisted breeding. DNA Research, 24, 499–508.

Sooriyapathirana S S, Khan A, Sebolt A M, Wang D, Bushakra J M, Kui L W, Allan A C, Gardiner S E, Chagné D, Iezzoni A F. 2010. QTL analysis and candidate gene mapping for skin and flesh color in sweet cherry fruit (Prunus avium L.). Tree Genetics & Genomes, 6, 821–832.

Sun C, Wang C, Zhang W, Liu S, Wang W, Yu X, Song T, Yu M, Yu W, Qu S. 2021. The R2R3-type MYB transcription factor MdMYB90-like is responsible for the enhanced skin color of an apple bud sport mutant. Horticulture Research, 8, 156.

Sun X, Jiao C, Schwaninger H, Chao C T, Ma Y, Duan N, Khan A, Ban S, Xu K, Cheng L, Zhong G Y, Fei Z. 2020. Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication. Nature Genetics, 52, 1423–1432.

Tang H, Bowers J E, Wang X, Ming R, Alam M, Paterson A H. 2008. Synteny and collinearity in plant genomes. Science, 320, 486–488.

Testa A C, Hane J K, Ellwood S R, Oliver R P. 2015. CodingQuarry: Highly accurate hidden Markov model gene prediction in fungal genomes using RNA-seq transcripts. BMC Genomics, 16, 170.

Verde I, Jenkins J, Dondini L, Micali S, Pagliarani G, Vendramin E, Paris R, Aramini V, Gazza L, Rossini L, Bassi D, Troggio M, Shu S, Grimwood J, Tartarini S, Dettori M T, Schmutz J. 2017. The Peach v2.0 release: High-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics, 18, 225.

Walker A R, Lee E, Bogs J, McDavid D A, Thomas M R, Robinson S P. 2007. White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant Journal, 49, 772–785.

Wan T, Feng Y, Liang C L, Pan L Y, He L, Cai Y L. 2021. Metabolomics and transcriptomics analyses of two contrasting cherry rootstocks in response to drought stress. Biology-Basel, 10, 201.

Wang J, Liu W, Zhu D, Hong P, Zhang S, Xiao S, Tan Y, Chen X, Xu L, Zong X, Zhang L, Wei H, Yuan X, Liu Q. 2020. Chromosome-scale genome assembly of sweet cherry (Prunus avium L.) cv. Tieton obtained using long-read and Hi-C sequencing. Horticulture Research, 7, 122.

Wang J Y, Sun W X, Wang L, Liu X J, Xu Y, Sabir I A, Jiu S T, Wang S P, Zhang C X. 2022. FRUITFULL is involved in double fruit formation at high temperature in sweet cherry. Environmental and Experimental Botany, 201, 104986.

Wang L, Feng Y, Wang Y, Zhang J, Chen Q, Liu Z, Liu C, He W, Wang H, Yang S, Zhang Y, Luo Y, Tang H, Wang X. 2022. Accurate chromosome identification in the Prunus Subgenus Cerasus (Prunus pseudocerasus) and its relatives by Oligo-FISH. International Journal of Molecular Sciences, 23, 13213.

Wang Z, Meng D, Wang A, Li T, Jiang S, Cong P, Li T. 2013. The methylation of the PcMYB10 promoter is associated with green-skinned sport in Max Red Bartlett pear. Plant Physiology, 162, 885–896.

Wei H, Chen X, Zong X, Shu H, Gao D, Liu Q. 2015. Comparative transcriptome analysis of genes involved in anthocyanin biosynthesis in the red and yellow fruits of sweet cherry (Prunus avium L.). PLoS ONE, 10, e0121164.

Xu M, Guo L, Gu S, Wang O, Zhang R, Peters B A, Fan G, Liu X, Xu X, Deng L, Zhang Y. 2020. TGS-GapCloser: A fast and accurate gap closer for large genomes with low coverage of error-prone long reads. Gigascience, 9, giaa094.

Yue J, Chen Q, Wang Y, Zhang L, Ye C, Wang X, Cao S, Lin Y, Huang W, Xian H, Qin H, Wang Y, Zhang S, Wu Y, Wang S, Yue Y, Liu Y. 2023. Telomere-to-telomere and gap-free reference genome assembly of the kiwifruit Actinidia chinensis. Horticulture Research, 10, uhac264.

Zhang L, Hu J, Han X, Li J, Gao Y, Richards C M, Zhang C, Tian Y, Liu G, Gul H, Wang D, Tian Y, Yang C, Meng M, Yuan G, Kang G, Wu Y, Wang K, Zhang H, Wang D, et al. 2019. A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nature Communications, 10, 1494.

Zhou Q, Tang D, Huang W, Yang Z, Zhang Y, Hamilton J P, Visser R G F, Bachem C W B, Robin Buell C, Zhang Z, Zhang C, Huang S. 2020. Haplotype-resolved genome analyses of a heterozygous diploid potato. Nature Genetics, 52, 1018–1023.

Zhou Y H, Xiong J S, Shu Z Q, Dong C, Gu T T, Sun P C, He S, Jiang M, Xia Z Q, Xue J Y, Khan W U, Chen F, Cheng Z M. 2023. The telomere-to-telomere genome of Fragaria vesca reveals the genomic evolution of Fragaria and the origin of cultivated octoploid strawberry. Horticulture Research, 10, uhad027.

甜樱桃Tieton v3.0的单倍型解析端粒到端粒参考基因组鉴定了与黄色果皮品种相关的大片段缺失

Haplotype-resolved telomere-to-telomere reference genome of sweet cherry ‘Tieton’ v3.0 characterized the large fragment deletion associated with yellow-skinned variety

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics