Genome variation and LTR-RT analyses of an ancient peach landrace reveal mechanism of blood-flesh fruit color formation and fruit maturity date advancement

Jiao Wang, Ke Cao, Yong Li, Jinlong Wu, Wenqing Li, Qi Wang, Gengrui Zhu, Weichao Fang, Changwen Chen, Xinwei Wang, Wenxuan Dong, Weisheng Liu, Lirong Wang

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (1) : 265. DOI: 10.1093/hr/uhad265
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Genome variation and LTR-RT analyses of an ancient peach landrace reveal mechanism of blood-flesh fruit color formation and fruit maturity date advancement

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Abstract

Peach (Prunus persica) landrace has typical regional characteristics, strong environmental adaptability, and contains many valuable genes that provide the foundation for breeding excellent varieties. Therefore, it is necessary to assemble the genomes of specific landraces to facilitate the localization and utilization of these genes. Here, we de novo assembled a high-quality genome from an ancient blood-fleshed Chinese landrace Tianjin ShuiMi (TJSM) that originated from the China North Plain. The assembled genome size was 243.5 Mb with a contig N50 of 23.7 Mb and a scaffold N50 of 28.6 Mb. Compared with the reported peach genomes, our assembled TJSM genome had the largest number of specific structural variants (SVs) and long terminal repeat-retrotransposons (LTR-RTs). Among the LTR-RTs with the potential to regulate their host genes, we identified a 6688 bp LTR-RT (named it blood TE) in the promoter of NAC transcription factor-encoding PpBL, a gene regulating peach blood-flesh formation. The blood TE was not only co-separated with the blood-flesh phenotype but also associated with fruit maturity date advancement and different intensities of blood-flesh color formation. Our findings provide new insights into the mechanism underlying the development of the blood-flesh color and determination of fruit maturity date and highlight the potential of the TJSM genome to mine more variations related to agronomic traits in peach fruit.

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Jiao Wang, Ke Cao, Yong Li, Jinlong Wu, Wenqing Li, Qi Wang, Gengrui Zhu, Weichao Fang, Changwen Chen, Xinwei Wang, Wenxuan Dong, Weisheng Liu, Lirong Wang. Genome variation and LTR-RT analyses of an ancient peach landrace reveal mechanism of blood-flesh fruit color formation and fruit maturity date advancement. Horticulture Research, 2024, 11(1): 265 https://doi.org/10.1093/hr/uhad265

References

[1.]
Faust M, Timon B. Origin and dissemination of peach. Hortic Rev. 1995;17:331-79
[2.]
Arús P, Verde I, Sosinski B. et al. The peach genome. Tree Genet Genomes. 2012;8:531-47
[3.]
Verde I, Abbott AG, Scalabrin S. et al. The high-quality draft genome of peach (Prunus persica.) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013;45:487-94
[4.]
Verde I, Jenkins J, Dondini L. et al. The Peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics. 2017;18:225
[5.]
Cao K, Zheng Z, Wang L. et al. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 2014;15:415
[6.]
Guo J, Cao K, Deng C. et al. An integrated peach genome struc-tural variation map uncovers genes associated with fruit traits. Genome Biol. 2020;21:258
[7.]
Li Y, Cao K, Li N. et al. Genomic analyses provide insights into peach local adaptation and responses to climate change. Genome Res. 2021;31:592-606
[8.]
Li Y, Cao K, Zhu G. et al. Genomic analyses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history. Genome Biol. 2019;20:36
[9.]
Yu Y, Fu J, Xu Y. et al. Genome re-sequencing reveals the evolu-tionary history of peach fruit edibility. Nat Commun. 2018;9:5404
[10.]
Liu Y, Du H, Li P. et al. Pan-genome of wild and cultivated soybeans. Cell. 2020;182:162-176.e113
[11.]
Sun X, Jiao C, Schwaninger H. et al. Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication. Nat Genet. 2020;52:1423-32
[12.]
Tao Y, Luo H, Xu J. et al. Extensive variation within the pan-genome of cultivated and wild sorghum. Nat Plants. 2021;7: 766-73
[13.]
Zhao J, Bayer PE, Ruperao P. et al. Trait associations in the pangenome of pigeon pea (Cajanus cajan). Plant Biotechnol J. 2020;18:1946-54
[14.]
Zhao Q, Feng Q, Lu H. et al. Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nat Genet. 2018;50:278-84
[15.]
Cao K, Yang X, Li Y. et al. New high-quality peach (Prunus persica L. Batsch) genome assembly to analyze the molecular evolution-ary mechanism of volatile compounds in peach fruits. Plant J. 2021;108:281-95
[16.]
Guan J, Xu Y, Yu Y. et al. Genome structure variation analyses of peach reveal population dynamics and a 1.67 Mb causal inversion for fruit shape. Genome Biol. 2021;22:13
[17.]
Yu Y, Guan J, Xu Y. et al. Population-scale peach genome analyses unravel selection patterns and biochemical basis underlying fruit flavor. Nat Commun. 2021;12:3604
[18.]
Wang Z, Zhuang E. Geographical distribution and cultivation regions of peach in China. In: PU F. (ed.) Fruit Trees of China. Beijing: China Forestry Publishing House, 2001, 49-51
[19.]
Ravaglia D, Espley RV, Henry-Kirk RA. et al. Transcriptional regu-lation of flavonoid biosynthesis in nectarine (Prunus persica)bya set of R2R3 MYB transcription factors. BMC Plant Biol. 2013;13:68
[20.]
Shomura A, Izawa T, Ebana K. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nat Genet. 2008;40:1023-8
[21.]
Zhang L, Hu J, Han X. et al. A high-quality apple genome assem-bly reveals the association of a retrotransposon and red fruit color. Nat Commun. 2019;10:1494
[22.]
Ding T, Cao K, Fang W. et al. The difference of anthocyanin accumulation pattern and related gene expression in two kinds of red flesh peach. Sci Agric Sin. 2017;50:2553-63
[23.]
Cao K, Ding T, Mao D. et al. Transcriptome analysis reveals novel genes involved in anthocyanin biosynthesis in the flesh of peach. Plant Physiol Biochem. 2018;123:94-102
[24.]
Zhou H, Lin-Wang K, Wang H. et al. Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. Plant J. 2015;82:105-21
[25.]
Rahim MA, Busatto N, Trainotti L. Regulation of anthocyanin biosynthesis in peach fruits. Planta. 2014;240:913-29
[26.]
Shen Z, Confolent C, Lambert P. et al. Characterization and genetic mapping of a new blood-flesh trait controlled by the single dominant locus DBF in peach. Tree Genet Genomes. 2013;9: 1435-46
[27.]
Hara-Kitagawa M, Unoki Y, Hihara S. et al. Development of simple PCR-based DNA marker for the red-fleshed trait of a blood peach ‘Tenshin-suimitsuto’. Mol Breed. 2020;40:5
[28.]
Hayashi K, Yoshida H. Refunctionalization of the ancient rice blast disease resistance gene pit by the recruitment of a retro-transposon as a promoter. Plant J. 2009;57:413-25
[29.]
Wang J, Cao K, Wang L. et al. Deciphering the genetic effect of a 483 bp deletion in the PpMYB10.1 promoter to determine intensities of the red-colored flesh peach. J Plant Genet Resour. 2023;24:758-66
[30.]
Dirlewanger E, Quero-García J, Le Dantec L. et al. Comparison of the genetic determinism of two key phenological traits, flower-ing and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity. 2012;109:280-92
[31.]
Eduardo I, Pacheco I, Chietera G. et al. QTL analysis of fruit qual-ity traits in two peach intraspecific populations and importance of maturity date pleiotropic effect. Tree Genet Genomes. 2011;7: 323-35
[32.]
Pirona R, Eduardo I, Pacheco I. et al. Fine mapping and identifica-tion of a candidate gene for a major locus controlling maturity date in peach. BMC Plant Biol. 2013;13:166
[33.]
Kou X, Liu C, Han L. et al. NAC transcription factors play an important role in ethylene biosynthesis, reception and signaling of tomato fruit ripening. Mol Gen Genomics. 2016;291:1205-17
[34.]
Blanquart F, Kaltz O, Nuismer SL. et al. A practical guide to measuring local adaptation. Ecol Lett. 2013;16:1195-205
[35.]
Fournier-Level A, Korte A, Cooper MD. et al. A map of local adaptation in Arabidopsis thaliana. Science. 2011;334:86-9
[36.]
Wang L, Zhu G, Fang W. et al. Genetic diversity of Chinese peach landraces and elite landrace cultivars. In: Xu J. (ed.) Peach Genetic Resource in China. China Agriculture Press: Beijing, 2012, 199-214
[37.]
Khanal BP, Knoche M. Mechanical properties of cuticles and their primary determinants. JExp Bot. 2017;68:5351-67
[38.]
Mamrutha HM, Mogili T, Jhansi Lakshmi K. et al. Leaf cuticu-lar wax amount and crystal morphology regulate post-harvest water loss in mulberry (Morus species). Plant Physiol Biochem. 2010;48:690-6
[39.]
Biémont C, Vieira C. Genetics: junk DNA as an evolutionary force. Nature. 2006;443:521-4
[40.]
Dorsett D. Distance-independent inactivation of an enhancer by the suppressor of hairy-wing DNA-binding protein of Drosophila. Genetics. 1993;134:1135-44
[41.]
Zhu M, Chen G, Zhou S. et al. A new tomato NAC (NAM/ATAF1/2/CUC2.) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol. 2014;55:119-35
[42.]
Gao Y, Wei W, Zhao X. et al. A NAC transcription factor. NOR-like1, is a new positive regulator of tomato fruit ripening. Hortic Res. 2018;5:75
[43.]
P, Yu S, Zhu N. et al. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nat Plants. 2018;4:784-91
[44.]
Tollis M, Boissinot S. The evolutionary dynamics of transposable elements in eukaryote genomes. Genome Dyn. 2012;7:68-91
[45.]
Leung DC, Lorincz MC. Silencing of endogenous retroviruses: when and why do histone marks predominate? Trends Biochem Sci. 2012;37:127-33
[46.]
Lisch D. Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol. 2009;60:43-66
[47.]
Lu C, Chen J, Zhang Y. et al. Miniature inverted-repeat transpos-able elements (MITEs.) have been accumulated through ampli-fication bursts and play important roles in gene expression and species diversity in Oryza sativa. Mol Biol Evol. 2012;29: 1005-17
[48.]
Mager S, Ludewig U. Massive loss of DNA methylation in nitrogen-, but not in phosphorus-deficient Zea mays roots is poorly correlated with gene expression differences. Front Plant Sci. 2018;9:497
[49.]
Mhiri C, Morel JB, Vernhettes S. et al. The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol. 1997;33:257-66
[50.]
Rodríguez-Negrete E, Lozano-Durán R, Piedra-Aguilera A. et al. Geminivirus rep protein interferes with the plant DNA methyla-tion machinery and suppresses transcriptional gene silencing. New Phytol. 2013;199:464-75
[51.]
Zhang M, Zhang X, Guo L. et al. Single-base resolution methy-lome of cotton cytoplasmic male sterility system reveals epige-nomic changes in response to high-temperature stress during anther development. JExp Bot. 2020;71:951-69
[52.]
Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980;8:4321-6
[53.]
Belton JM, Mccord RP, Gibcus JH. et al. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods. 2012;58:268-76
[54.]
Lieberman-Aiden E, van Berkum NL, Williams L. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326: 289-93
[55.]
Li R, Zhu H, Ruan J. et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 2010;20:265-72
[56.]
Nurk S, Walenz BP, Rhie A. et al. HiCanu: accurate assem-bly of segmental duplications, satellites, and allelic vari-ants from high-fidelity long reads. Genome Res. 2020;30: 1291-305
[57.]
Simão FA, Waterhouse RM, Ioannidis P. et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210-2
[58.]
Burton JN, Adey A, Patwardhan RP. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol. 2013;31:1119-25
[59.]
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357-9
[60.]
Chen N. Using repeat masker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics. 2004; Chapter 4:Unit 4.10.1-4.10.14
[61.]
Jurka J, Kapitonov VV, Pavlicek A. et al. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462-7
[62.]
Roberts A, Pimentel H, Trapnell C. et al. Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics. 2011;27:2325-9
[63.]
Birney E, Clamp M, Durbin R. Gene wise and genome wise. Genome Res. 2004;14:988-95
[64.]
Stanke M, Steinkamp R, Waack S. et al. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 2004;32: W309-12
[65.]
Ter-Hovhannisyan V, Lomsadze A, Chernoff YO. et al. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 2008;18: 1979-90
[66.]
Kanehisa M, Goto S, Sato Y. et al. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012;40:D109-14
[67.]
Griffiths-Jones S, Moxon S, Marshall M. et al. Rfam: annotat-ing non-coding RNAs in complete genomes. Nucleic Acids Res. 2005;33:D121-4
[68.]
Lowe TM, Eddy SR. tRNA scan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997;25:955-64
[69.]
Li L, Stoeckert CJ Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13: 2178-89
[70.]
De Bie T, Cristianini N, Demuth JP. et al. CAFE: a computa-tional tool for the study of gene family evolution. Bioinformatics. 2006;22:1269-71
[71.]
Ellinghaus D, Kurtz S, Willhoeft U. LTR harvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics. 2008;9:18
[72.]
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
[73.]
Li F. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094-100
[74.]
Mckenna A, Hanna M, Banks E. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297-303
[75.]
Wang L, Zhu G. Descriptors and Data Standard for Peach (Prunus persica.). Beijing: China Agriculture Press; 2005:74-5
[76.]
Huang D, Yuan Y, Tang Z. et al. Retrotransposon promoter of Ruby1 controls both light-and cold-induced accumulation of anthocyanins in blood orange. Plant Cell Environ. 2019;42: 3092-104
[77.]
Hellens RP, Allan AC, Friel EN. et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods. 2005;1:13
[78.]
LaSarre B, Federle MJ. EMSA analysis of DNA binding by Rgg proteins. Bio Protoc. 2013;3:e838
[79.]
Tong Z, Gao Z, Wang F. et al. Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol. 2009;10:71
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