The haplotype-resolved T2T genome of teinturier cultivar Yan73 reveals the genetic basis of anthocyanin biosynthesis in grapes

Kekun Zhang , Mengrui Du , Hongyan Zhang , Xiaoqian Zhang , Shuo Cao , Xu Wang , Wenrui Wang , Xueqiang Guan , Penghui Zhou , Jin Li , Wenguang Jiang , Meiling Tang , Qiuling Zheng , Muming Cao , Yongfeng Zhou , Keqin Chen , Zhongjie Liu , Yulin Fang

Horticulture Research ›› 2023, Vol. 10 ›› Issue (11) : 205

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (11) :205 DOI: 10.1093/hr/uhad205
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The haplotype-resolved T2T genome of teinturier cultivar Yan73 reveals the genetic basis of anthocyanin biosynthesis in grapes
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Abstract

Teinturier grapes are characterized by the typical accumulation of anthocyanins in grape skin, flesh, and vegetative tissues, endowing them with high utility value in red wine blending and nutrient-enriched foods developing. However, due to the lack of genome information, the mechanism involved in regulating teinturier grape coloring has not yet been elucidated and their genetic utilization research is still insufficient. Here, the cultivar ‘Yan73’ was used for assembling the telomere-to-telomere (T2T) genome of teinturier grapes by combining the High Fidelity (HiFi), Hi-C and ultralong Oxford Nanopore Technologies (ONT) reads. Two haplotype genomes were assembled, at the sizes of 501.68 Mb and 493.38 Mb, respectively. In the haplotype 1 genome, the transposable elements (TEs) contained 32.77% of long terminal repeats (LTRs), while in the haplotype 2 genome, 31.53% of LTRs were detected in TEs. Furthermore, obvious inversions were identified in chromosome 18 between the two haplotypes. Transcriptome profiling suggested that the gene expression patterns in ‘Cabernet Sauvignon’ and ‘Yan73’ were diverse depending on tissues, developmental stages, and varieties. The transcription program of genes in the anthocyanins biosynthesis pathway between the two cultivars exhibited high similarity in different tissues and developmental stages, whereas the expression levels of numerous genes showed significant differences. Compared with other genes, the expression levels of VvMYBA1 and VvUFGT4 in all samples, VvCHS2 except in young shoots and VvPAL9 except in the E-L23 stage of ‘Yan73’ were higher than those of ‘Cabernet Sauvignon’. Further sequence alignments revealed potential variant gene loci and structure variations of anthocyanins biosynthesis related genes and a 816 bp sequence insertion was found in the promoter of VvMYBA1 of ‘Yan73’ haplotype 2 genome. The ‘Yan73’ T2T genome assembly and comparative analysis provided valuable foundations for further revealing the coloring mechanism of teinturier grapes and the genetic improvement of grape coloring traits.

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Kekun Zhang, Mengrui Du, Hongyan Zhang, Xiaoqian Zhang, Shuo Cao, Xu Wang, Wenrui Wang, Xueqiang Guan, Penghui Zhou, Jin Li, Wenguang Jiang, Meiling Tang, Qiuling Zheng, Muming Cao, Yongfeng Zhou, Keqin Chen, Zhongjie Liu, Yulin Fang. The haplotype-resolved T2T genome of teinturier cultivar Yan73 reveals the genetic basis of anthocyanin biosynthesis in grapes. Horticulture Research, 2023, 10 (11) : 205 DOI:10.1093/hr/uhad205

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Acknowledgements

This work was supported by grants from the Major Innovation Project of Shandong Province (2022CXGC010605), the National Natural Science Foundation of China (32002023 and 32172518), the Regional Joint Key Innovation Project of NSFC (U22A20491), and Shaanxi Key R&D Plan Project (2023-ZDLNY-21).

Author contributions

Y.F., Y.Z., K.C., and K.Z. conceived and designed the project. M.D., Z.L., W.W., S.C., and X.W. performed the genome assembly and gene annotation. K.Z., Z.L., and K.C. performed transcriptome analysis. H.Z., X.Z., P.Z., J.L., and W.J. assisted in grape culture and sample collection. X.G., M.T., Q.Z., and M.C. assisted in bioinformatics analyses and data visualization. K.Z., M.D., K.C., and Y.F. wrote and purified the manuscript.

Data availability

All the raw sequencing data generated for this project have been deposited in the National Genomics Data Center (NGDC) Genome Sequence Archive (GSA) (https://ngdc.cncb.ac.cn/gsa/) with BioProject number PRJCA018686, and in the NCBI Sequence Read Archive under project number PRJNA1000119. The assembly and annotation as well as the sequences of centromeres and heterozygous regions have been deposited in Zenodo.

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Gouot JC, Smith JP, Holzapfel BP, et al. Grape berry flavonoids: a review of their biochemical responses to high and extreme high temperatures. J Exp Bot. 2019; 70: 397-423

[2]

Zhao J, Pang Y, Dixon RA . The mysteries of proanthocyanidin transport and polymerization. Plant Physiol. 2010; 153: 437-43

[3]

Francisco RM, Regalado A, Ageorges A, et al. ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-glucosides. Plant Cell. 2013; 25: 1840-54

[4]

Kobayashi S, Goto-Yamamoto N, Hirochika H . Retrotransposon-induced mutations in grape skin color. Science. 2004; 304: 982

[5]

Walker AR, Lee E, Bogs J, et al. White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J. 2007; 49: 772-85

[6]

Rinaldo AR, Cavallini E, Jia Y, et al. A grapevine anthocyanin acyltransferase, transcriptionally regulated by VvMYBA, can produce most acylated anthocyanins present in grape skins. Plant Physiol. 2015; 169: 1897-916

[7]

Sun T, Xu L, Sun H, et al. VvVHP1;2 is transcriptionally activated by VvMYBA1 and promotes anthocyanin accumulation of grape berry skins via glucose signal . Front Plant Sci. 2017; 8: 1811

[8]

Jiu S, Guan L, Leng X, et al. The role of VvMYBA2r and VvMYBA2w alleles of the MYBA2 locus in the regulation of anthocyanin biosynthesis for molecular breeding of grape (Vitis spp.) skin coloration . Plant Biotechnol J. 2021; 19: 1216-39

[9]

Deluc L, Barrieu F, Marchive C, et al. Characterization of a grapevine R2R3-MYB transcription factor that regulates the phenylpropanoid pathway. Plant Physiol. 2006; 140: 499-511

[10]

Deluc L, Bogs J, Walker AR, et al. The transcription factor VvMYB5b contributes to the regulation of anthocyanin and proanthocyanidin biosynthesis in developing grape berries. Plant Physiol. 2008; 147: 2041-53

[11]

Matus JT, Cavallini E, Loyola R, et al. A group of grapevine MYBA transcription factors located in chromosome 14 control anthocyanin synthesis in vegetative organs with different specificities compared with the berry color locus. Plant J. 2017; 91: 220-36

[12]

Matus JT, Poupin MJ, Canon P, et al. Isolation of WDR and bHLH genes related to flavonoid synthesis in grapevine (Vitis vinifera L.). Plant Mol Biol. 2010; 72: 607-20

[13]

Hichri I, Heppel SC, Pillet J, et al. The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in grapevine. Mol Plant. 2010; 3: 509-23

[14]

Tirumalai V, Swetha C, Nair A, et al. miR828 and miR858 regulate VvMYB114 to promote anthocyanin and flavonol accumulation in grapes. J Exp Bot. 2019; 70: 4775-92

[15]

Ageorges A, Fernandez L, Vialet S, et al. Four specific iso-genes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci. 2006; 170: 372-83

[16]

He JJ, Liu YX, Pan QH, et al. Different anthocyanin profiles of the skin and the pulp of Yan7 (Muscat Hamburg x Alicante Bouschet) grape berries. Molecules. 2010; 15: 1141-53

[17]

Guan L, Li JH, Fan PG, et al. Anthocyanin accumulation in various organs of a Teinturier cultivar (Vitis vinifera L.) during the growing season . Am J Enol Vitic. 2012; 63: 177-84

[18]

Kong J, Wu J, Guan L, et al. Metabolite analysis reveals distinct spatio-temporal accumulation of anthocyanins in two teinturier variants of cv. ’Gamay’ grapevines (Vitis vinifera L.). Planta. 2021; 253: 84

[19]

Xie S, Lei Y, Chen H, et al. R2R3-MYB transcription factors regulate anthocyanin biosynthesis in grapevine vegetative tissues. Front Plant Sci. 2020; 11: 527

[20]

Xie S, Qiao X, Chen H, et al. Coordinated regulation of grape berry flesh color by transcriptional activators and repressors. J Agric Food Chem. 2019; 67: 11815-24

[21]

Röckel F, Moock C, Braun U, et al. Color intensity of the red-fleshed berry phenotype of Vitis vinifera Teinturier grapes varies due to a 408 bp duplication in the promoter of VvmybA1. Genes (Basel). 2020; 11: 891

[22]

Shi X, Cao S, Wang X, et al. The complete reference genome for grapevine (Vitis vinifera L.) genetics and breeding . Hortic Res. 2023; 10: uhad061

[23]

Zhou Y, Minio A, Massonnet M, et al. The population genetics of structural variants in grapevine domestication. Nat Plants. 2019; 5: 965-79

[24]

Xiao H, Liu Z, Wang N, et al. Adaptive and maladaptive introgression in grapevine domestication. Proc Natl Acad Sci U S A. 2023; 120: e2222041120

[25]

Giani AM, Gallo GR, Gianfranceschi L, et al. Long walk to genomics: history and current approaches to genome sequencing and assembly. Comput Struct Biotechnol J. 2020; 18: 9-19

[26]

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

[27]

Miga KH, Koren S, Rhie A, et al. Telomere-to-telomere assembly of a complete human X chromosome. Nature. 2020; 585: 79-84

[28]

Li F, Xu S, Xiao Z, et al. Gap-free genome assembly and comparative analysis reveal the evolution and anthocyanin accumulation mechanism of Rhodomyrtus tomentosa. Hortic Res. 2023; 10: uhad005

[29]

Song JM, 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

[30]

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

[31]

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

[32]

Minio A, Cochetel N, Vondras AM, et al. Assembly of complete diploid-phased chromosomes from draft genome sequences. G3 (Bethesda). 2022; 12: jkac143

[33]

Roach MJ, Johnson DL, Bohlmann J, et al. Population sequencing reveals clonal diversity and ancestral inbreeding in the grapevine cultivar chardonnay. PLoS Genet. 2018; 14: e1007807

[34]

Massonnet M, Cochetel N, Minio A, et al. The genetic basis of sex determination in grapes. Nat Commun. 2020; 11: 2902

[35]

Minio A, Cantu D . Grapegenomics.com: a web portal with genomic data and analysis tools for wild and cultivated grapevines. Zenodo. 2022

[36]

Coghlan A, Eichler EE, Oliver SG, et al. Chromosome evolution in eukaryotes: a multi-kingdom perspective. Trends Genet. 2005; 21: 673-82

[37]

Santiago JL, Gonzalez I, Gago P, et al. Identification of and relationships among a number of teinturier grapevines that expanded across Europe in the early 20th century. Aust J Grape Wine Res. 2008; 14: 223-9

[38]

Chen WK, Wang Y, Gao XT, et al. Flavonoid and aromatic profiles of two Vitis vinifera L. teinturier grape cultivars . Aust J Grape Wine Res. 2018; 24: 379-89

[39]

This P, Lacombe T, Cadle-Davidson M, et al. Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1. Theor Appl Genet. 2007; 114: 723-30

[40]

Ismail A, Gajjar P, Park M, et al. A recessive mutation in muscadine grapes causes berry color-loss without influencing anthocyanin pathway. Commun Biol. 2022; 5: 1012

[41]

Espley RV, Brendolise C, Chagne D, et al. Multiple repeats of a promoter segment causes transcription factor autoregulation in red apples. Plant Cell. 2009; 21: 168-83

[42]

Wen P, Chen J, Kong W, et al. Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci. 2005; 169: 928-34

[43]

Tian L, Wan S, Pan Q, et al. A novel plastid localization of chalcone synthase in developing grape berry. Plant Sci. 2008; 175: 431-6

[44]

Coombe BG . Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res. 1995; 1: 104-10

[45]

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

[46]

Manni M, Berkeley MR, Seppey M, et al. 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: 4647-54

[47]

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

[48]

Zhang K, Chen L, Wei M, et al. Metabolomic profile combined with transcriptomic analysis reveals the value of UV-C in improving the utilization of waste grape berries. Food Chem. 2021; 363: 130288

[49]

Zhong H, Liu Z, Zhang F, et al. Metabolomic and transcriptomic analyses reveal the effects of self- and hetero-grafting on anthocyanin biosynthesis in grapevine. Hortic Res. 2022; 9: uhac103

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