Telomere-to-telomere Citrullus super-pangenome provides direction for watermelon breeding.


Journal

Nature genetics
ISSN: 1546-1718
Titre abrégé: Nat Genet
Pays: United States
ID NLM: 9216904

Informations de publication

Date de publication:
08 Jul 2024
Historique:
received: 26 08 2023
accepted: 04 06 2024
medline: 9 7 2024
pubmed: 9 7 2024
entrez: 8 7 2024
Statut: aheadofprint

Résumé

To decipher the genetic diversity within the cucurbit genus Citrullus, we generated telomere-to-telomere (T2T) assemblies of 27 distinct genotypes, encompassing all seven Citrullus species. This T2T super-pangenome has expanded the previously published reference genome, T2T-G42, by adding 399.2 Mb and 11,225 genes. Comparative analysis has unveiled gene variants and structural variations (SVs), shedding light on watermelon evolution and domestication processes that enhanced attributes such as bitterness and sugar content while compromising disease resistance. Multidisease-resistant loci from Citrullus amarus and Citrullus mucosospermus were successfully introduced into cultivated Citrullus lanatus. The SVs identified in C. lanatus have not only been inherited from cordophanus but also from C. mucosospermus, suggesting additional ancestors beyond cordophanus in the lineage of cultivated watermelon. Our investigation substantially improves the comprehension of watermelon genome diversity, furnishing comprehensive reference genomes for all Citrullus species. This advancement aids in the exploration and genetic enhancement of watermelon using its wild relatives.

Identifiants

pubmed: 38977857
doi: 10.1038/s41588-024-01823-6
pii: 10.1038/s41588-024-01823-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Renner, S. S. et al. A chromosome-level genome of a Kordofan melon illuminates the origin of domesticated watermelons. Proc. Natl Acad. Sci. USA 118, e2101486118 (2021).
pubmed: 34031154 pmcid: 8201767 doi: 10.1073/pnas.2101486118
Levi, A. et al. Genetic diversity in the desert watermelon Citrullus colocynthis and its relationship with Citrullus species as determined by high-frequency oligonucleotides-targeting active gene markers. J. Am. Soc. Hortic. Sci. 142, 47–56 (2017).
doi: 10.21273/JASHS03834-16
Yuan, P. et al. Watermelon domestication was shaped by stepwise selection and regulation of the metabolome. Sci. China Life Sci. 66, 579–594 (2023).
pubmed: 36346547 doi: 10.1007/s11427-022-2198-5
Nkoana, D. K., Mashilo, J., Shimelis, H. & Ngwepe, R. M. Nutritional, phytochemical compositions and natural therapeutic values of citron watermelon (Citrullus lanatus var. citroides): a review. S. Afr. J. Bot. 145, 65–77 (2022).
doi: 10.1016/j.sajb.2020.12.008
Volino-Souza, M. et al. Current evidence of watermelon (Citrullus lanatus) ingestion on vascular health: a food science and technology perspective. Nutrients 14, 2913 (2022).
pubmed: 35889869 pmcid: 9318495 doi: 10.3390/nu14142913
Guo, S. et al. Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits. Nat. Genet. 51, 1616–1623 (2019).
pubmed: 31676863 doi: 10.1038/s41588-019-0518-4
Deng, 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 15, 1268–1284 (2022).
pubmed: 35746868 doi: 10.1016/j.molp.2022.06.010
Zhou, Y. et al. Graph pangenome captures missing heritability and empowers tomato breeding. Nature 606, 527–534 (2022).
pubmed: 35676474 doi: 10.1038/s41586-022-04808-9
Tang, D. et al. Genome evolution and diversity of wild and cultivated potatoes. Nature 606, 535–541 (2022).
pubmed: 35676481 pmcid: 9200641 doi: 10.1038/s41586-022-04822-x
Shang, L. et al. A super pan-genomic landscape of rice. Cell Res. 32, 878–896 (2022).
pubmed: 35821092 pmcid: 9525306 doi: 10.1038/s41422-022-00685-z
Li, N. et al. Super-pangenome analyses highlight genomic diversity and structural variation across wild and cultivated tomato species. Nat. Genet. 55, 852–860 (2023).
pubmed: 37024581 pmcid: 10181942 doi: 10.1038/s41588-023-01340-y
Bohra, A. et al. Reap the crop wild relatives for breeding future crops. Trends Biotechnol. 40, 412–431 (2022).
pubmed: 34629170 doi: 10.1016/j.tibtech.2021.08.009
Liu, Y. et al. Pan-genome of wild and cultivated soybeans. Cell 182, 162–176 (2020).
pubmed: 32553274 doi: 10.1016/j.cell.2020.05.023
Wu, S. et al. Citrullus genus super-pangenome reveals extensive variations in wild and cultivated watermelons and sheds light on watermelon evolution and domestication. Plant Biotechnol. J. 21, 1926–1928 (2023).
pubmed: 37490004 pmcid: 10502741 doi: 10.1111/pbi.14120
Wellenreuther, M., Mérot, C., Berdan, E. & Bernatchez, L. Going beyond SNPs: the role of structural genomic variants in adaptive evolution and species diversification. Mol. Ecol. 28, 1203–1209 (2019).
pubmed: 30834648 doi: 10.1111/mec.15066
Ren, Y. et al. Genetic analysis and chromosome mapping of resistance to Fusarium oxysporum f. sp. niveum (FON) race 1 and race 2 in watermelon (Citrullus lanatus L.). Mol. Breed. 35, 183 (2015).
pubmed: 26347205 doi: 10.1007/s11032-015-0375-5
Ren, Y. et al. A high resolution genetic map anchoring scaffolds of the sequenced watermelon genome. PLoS ONE 7, e29453 (2012).
pubmed: 22247776 pmcid: 3256148 doi: 10.1371/journal.pone.0029453
Wang, J. et al. The NAC transcription factor ClNAC68 positively regulates sugar content and seed development in watermelon by repressing ClINV and ClGH3.6. Hortic. Res. 8, 214 (2021).
pubmed: 34593776 pmcid: 8484586 doi: 10.1038/s41438-021-00649-1
Wang, Y. et al. CRISPR/Cas9-mediated mutagenesis of ClBG1 decreased seed size and promoted seed germination in watermelon. Hortic. Res. 8, 70 (2021).
pubmed: 33790265 pmcid: 8012358 doi: 10.1038/s41438-021-00506-1
Rieseberg, L. H. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351–358 (2001).
pubmed: 11403867 doi: 10.1016/S0169-5347(01)02187-5
Hawkins, L. K. et al. Linkage mapping in a watermelon population segregating for fusarium wilt resistance. J. Am. Soc. Hortic. Sci. 126, 344–350 (2001).
doi: 10.21273/JASHS.126.3.344
Sain, R. S. & Joshi, P. Pollen fertility of interspecific F1 hybrids in genus Citrullus (Cucurbitaceae). Curr. Sci. 85, 431–434 (2003).
Sandlin, K. C. et al. Comparative mapping in watermelon [Citrullus lanatus (Thunb.) Matsum. et Nakai]. Theor. Appl. Genet. 125, 1603–1618 (2012).
pubmed: 22875176 doi: 10.1007/s00122-012-1938-z
McGregor, C. E. & Waters, V. Pollen viability of F1 hybrids between watermelon cultivars and disease-resistant, infraspecific crop wild relatives. Hortscience 48, 1428–1432 (2013).
doi: 10.21273/HORTSCI.48.12.1428
Ren, Y. et al. An integrated genetic map based on four mapping populations and quantitative trait loci associated with economically important traits in watermelon (Citrullus lanatus). BMC Plant Biol. 14, 33 (2014).
pubmed: 24443961 pmcid: 3898567 doi: 10.1186/1471-2229-14-33
Ni, L. et al. Pan-3D genome analysis reveals structural and functional differentiation of soybean genomes. Genome Biol. 24, 12 (2023).
pubmed: 36658660 pmcid: 9850592 doi: 10.1186/s13059-023-02854-8
Monforte, A. et al. The genetic basis of fruit morphology in horticultural crops: lessons from tomato and melon. J. Exp. Bot. 65, 4625–4637 (2014).
pubmed: 24520021 doi: 10.1093/jxb/eru017
Paudel, L., Clevenger, J. & McGregor, C. Chromosomal locations and interactions of four loci associated with seed coat color in watermelon. Front. Plant Sci. 10, 788 (2019).
pubmed: 31293604 pmcid: 6603093 doi: 10.3389/fpls.2019.00788
Guo, S. et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat. Genet. 45, 51–58 (2013).
pubmed: 23179023 doi: 10.1038/ng.2470
Zhang, J. et al. High‐level expression of a novel chromoplast phosphate transporter ClPHT4;2 is required for flesh color development in watermelon. New Phytol. 213, 1208–1221 (2017).
pubmed: 27787901 doi: 10.1111/nph.14257
Chomicki, G., Schaefer, H. & Renner, S. S. Origin and domestication of Cucurbitaceae crops: insights from phylogenies, genomics and archaeology. New Phytol. 226, 1240–1255 (2020).
pubmed: 31230355 doi: 10.1111/nph.16015
Zhou, Y. et al. Convergence and divergence of bitterness biosynthesis and regulation in Cucurbitaceae. Nat. Plants 2, 16183 (2016).
pubmed: 27892922 pmcid: 5449191 doi: 10.1038/nplants.2016.183
Zhong, Y. et al. Root-secreted bitter triterpene modulates the rhizosphere microbiota to improve plant fitness. Nat. Plants 8, 887–896 (2022).
pubmed: 35915145 doi: 10.1038/s41477-022-01201-2
Gong, C. et al. Multi-omics integration to explore the molecular insight into the volatile organic compounds in watermelon. Food Res. Int. 166, 112603 (2023).
pubmed: 36914327 doi: 10.1016/j.foodres.2023.112603
Ren, Y. et al. Localization shift of a sugar transporter contributes to phloem unloading in sweet watermelons. New Phytol. 227, 1858–1871 (2020).
pubmed: 32453446 doi: 10.1111/nph.16659
Ren, Y. et al. Evolutionary gain of oligosaccharide hydrolysis and sugar transport enhanced carbohydrate partitioning in sweet watermelon fruits. Plant Cell 33, 1554–1573 (2021).
pubmed: 33570606 pmcid: 8254481 doi: 10.1093/plcell/koab055
Liu, S. et al. Nucleotide variation in the phytoene synthase (ClPsy1) gene contributes to golden flesh in watermelon (Citrullus lanatus L.). Theor. Appl. Genet. 135, 185–200 (2022).
pubmed: 34633472 doi: 10.1007/s00122-021-03958-0
Dou, J. et al. Genome-wide analysis of IQD proteins and ectopic expression of watermelon ClIQD24 in tomato suggests its important role in regulating fruit shape. Front. Genet. 13, 993218 (2022).
pubmed: 36186419 pmcid: 9515400 doi: 10.3389/fgene.2022.993218
Li, N. et al. A 13.96-kb chromosomal deletion of two genes is responsible for the tomato seed size in watermelon (Citrullus lanatus). Plant Breed. 140, 944–952 (2021).
doi: 10.1111/pbr.12954
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
pubmed: 30423086 pmcid: 6129281 doi: 10.1093/bioinformatics/bty560
Belton, J.-M. et al. Hi–C: a comprehensive technique to capture the conformation of genomes. Methods 58, 268–276 (2012).
pubmed: 22652625 doi: 10.1016/j.ymeth.2012.05.001
Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764–770 (2011).
pubmed: 21217122 pmcid: 3051319 doi: 10.1093/bioinformatics/btr011
Vurture, G. W. et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202–2204 (2017).
pubmed: 28369201 pmcid: 5870704 doi: 10.1093/bioinformatics/btx153
Cheng, H., Concepcion, G. T., Feng, X., Zhang, H. & Li, H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat. Methods 18, 170–175 (2021).
pubmed: 33526886 pmcid: 7961889 doi: 10.1038/s41592-020-01056-5
Cheng, H. et al. Haplotype-resolved assembly of diploid genomes without parental data. Nat. Biotechnol. 40, 1332–1335 (2022).
pubmed: 35332338 doi: 10.1038/s41587-022-01261-x
Hu, J. et al. NextDenovo: an efficient error correction and accurate assembly tool for noisy long reads. Genome Biol. 25, 107 (2024).
pubmed: 38671502 pmcid: 11046930 doi: 10.1186/s13059-024-03252-4
Li, K. et al. Gapless indica rice genome reveals synergistic contributions of active transposable elements and segmental duplications to rice genome evolution. Mol. Plant 14, 1745–1756 (2021).
pubmed: 34171481 doi: 10.1016/j.molp.2021.06.017
Bankevich, A. et al. Multiplex de Bruijn graphs enable genome assembly from long, high-fidelity reads. Nat. Biotechnol. 40, 1075–1081 (2022).
pubmed: 35228706 doi: 10.1038/s41587-022-01220-6
Servant, N. et al. HiC-Pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 16, 259 (2015).
pubmed: 26619908 pmcid: 4665391 doi: 10.1186/s13059-015-0831-x
Wang, S. et al. EndHiC: assemble large contigs into chromosome-level scaffolds using the Hi-C links from contig ends. BMC Bioinformatics 23, 528 (2022).
pubmed: 36482318 pmcid: 9730666 doi: 10.1186/s12859-022-05087-x
Akdemir, K. C. & Chin, L. HiCPlotter integrates genomic data with interaction matrices. Genome Biol. 16, 198 (2015).
pubmed: 26392354 pmcid: 4576377 doi: 10.1186/s13059-015-0767-1
Alonge, M. et al. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol. 23, 258 (2022).
pubmed: 36522651 pmcid: 9753292 doi: 10.1186/s13059-022-02823-7
Rhie, A. et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature 592, 737–746 (2021).
pubmed: 33911273 pmcid: 8081667 doi: 10.1038/s41586-021-03451-0
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242 pmcid: 6137996 doi: 10.1093/bioinformatics/bty191
Mc Cartney, A. M. et al. Chasing perfection: validation and polishing strategies for telomere-to-telomere genome assemblies. Nat. Methods 19, 687–695 (2022).
pubmed: 35361931 pmcid: 9812399 doi: 10.1038/s41592-022-01440-3
Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 (1999).
pubmed: 9862982 pmcid: 148217 doi: 10.1093/nar/27.2.573
Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152 (2012).
pubmed: 23060610 pmcid: 3516142 doi: 10.1093/bioinformatics/bts565
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690 pmcid: 3603318 doi: 10.1093/molbev/mst010
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
pubmed: 20224823 pmcid: 2835736 doi: 10.1371/journal.pone.0009490
Manni, M., Berkeley, M. R., Seppey, M., Simão, F. A. & Zdobnov, E. M. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol. 38, 4647–4654 (2021).
pubmed: 34320186 pmcid: 8476166 doi: 10.1093/molbev/msab199
Rhie, A., Walenz, B. P., Koren, S. & Phillippy, A. M. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 21, 245 (2020).
pubmed: 32928274 pmcid: 7488777 doi: 10.1186/s13059-020-02134-9
Ou, S., Chen, J. & Jiang, N. Assessing genome assembly quality using the LTR assembly index (LAI). Nucleic Acids Res. 21, e126 (2018).
Ou, S. & Jiang, N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 176, 1410–1422 (2018).
pubmed: 29233850 doi: 10.1104/pp.17.01310
Ou, S. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20, 275 (2019).
pubmed: 31843001 pmcid: 6913007 doi: 10.1186/s13059-019-1905-y
Tarailo‐Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics 25, 4.10.1–4.10.14 (2009).
doi: 10.1002/0471250953.bi0410s25
Stanke, M., Tzvetkova, A. & Morgenstern, B. AUGUSTUS at EGASP: using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biol. 7, S11.1–S11.8 (2006).
pubmed: 16925833 doi: 10.1186/gb-2006-7-s1-s11
Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).
pubmed: 15145805 doi: 10.1093/bioinformatics/bth315
Brůna, T., Hoff, K. J., Lomsadze, A., Stanke, M. & Borodovsky, M. BRAKER2: automatic eukaryotic genome annotation with GeneMark-EP+ and AUGUSTUS supported by a protein database. NAR Genom. Bioinformatics 3, lqaa108 (2021).
doi: 10.1093/nargab/lqaa108
Li, Q. et al. A chromosome-scale genome assembly of cucumber (Cucumis sativus L.). GigaScience 8, giz072 (2019).
pubmed: 31216035 pmcid: 6582320 doi: 10.1093/gigascience/giz072
Castanera, R., Ruggieri, V., Pujol, M., Garcia-Mas, J. & Casacuberta, J. M. An improved melon reference genome with single-molecule sequencing uncovers a recent burst of transposable elements with potential impact on genes. Front. Plant Sci. 10, 1815 (2020).
pubmed: 32076428 pmcid: 7006604 doi: 10.3389/fpls.2019.01815
Bairoch, A. & Apweiler, R. The SWISS-PROT protein sequence data bank and its supplement TrEMBL. Nucleic Acids Res. 25, 31–36 (1997).
pubmed: 9016499 pmcid: 146382 doi: 10.1093/nar/25.1.31
Slater, G. & Birney, E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics 6, 31 (2005).
pubmed: 15713233 pmcid: 553969 doi: 10.1186/1471-2105-6-31
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 21572440 pmcid: 3571712 doi: 10.1038/nbt.1883
Pertea, M., Kim, D., Pertea, G. M., Leek, J. T. & Salzberg, S. L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 11, 1650–1667 (2016).
pubmed: 27560171 pmcid: 5032908 doi: 10.1038/nprot.2016.095
Kovaka, S. et al. Transcriptome assembly from long-read RNA-seq alignments with StringTie2. Genome Biol. 20, 278 (2019).
pubmed: 31842956 pmcid: 6912988 doi: 10.1186/s13059-019-1910-1
Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 9, R7 (2008).
pubmed: 18190707 pmcid: 2395244 doi: 10.1186/gb-2008-9-1-r7
Chan, P. P., Lin, B. Y., Mak, A. J. & Lowe, T. M. tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes. Nucleic Acids Res. 49, 9077–9096 (2021).
pubmed: 34417604 pmcid: 8450103 doi: 10.1093/nar/gkab688
Lagesen, K. et al. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100–3108 (2007).
pubmed: 17452365 pmcid: 1888812 doi: 10.1093/nar/gkm160
Nawrocki, E. P. & Eddy, S. R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933–2935 (2013).
pubmed: 24008419 pmcid: 3810854 doi: 10.1093/bioinformatics/btt509
Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 36, D281–D288 (2007).
pubmed: 18039703 pmcid: 2238907 doi: 10.1093/nar/gkm960
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
pubmed: 24451626 pmcid: 3998142 doi: 10.1093/bioinformatics/btu031
Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A. C. & Kanehisa, M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, W182–W185 (2007).
pubmed: 17526522 doi: 10.1093/nar/gkm321
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825–5829 (2021).
pubmed: 34597405 pmcid: 8662613 doi: 10.1093/molbev/msab293
Jin, J.-J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 241 (2020).
pubmed: 32912315 pmcid: 7488116 doi: 10.1186/s13059-020-02154-5
Danecek, P. et al. Twelve years of SAMtools and BCFtools. GigaScience 10, giab008 (2021).
pubmed: 33590861 pmcid: 7931819 doi: 10.1093/gigascience/giab008
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021).
pubmed: 33885785 pmcid: 8265157 doi: 10.1093/nar/gkab301
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).
pubmed: 31727128 doi: 10.1186/s13059-019-1832-y
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147 pmcid: 390337 doi: 10.1093/nar/gkh340
Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).
pubmed: 27004904 pmcid: 8210823 doi: 10.1093/molbev/msw054
Qin, P. et al. Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell 184, 3542–3558 (2021).
pubmed: 34051138 doi: 10.1016/j.cell.2021.04.046
Tang, H. et al. Synteny and collinearity in plant genomes. Science 320, 486–488 (2008).
pubmed: 18436778 doi: 10.1126/science.1153917
Goel, M., Sun, H., Jiao, W.-B. & Schneeberger, K. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 20, 277 (2019).
pubmed: 31842948 pmcid: 6913012 doi: 10.1186/s13059-019-1911-0
Song, B. et al. AnchorWave: sensitive alignment of genomes with high sequence diversity, extensive structural polymorphism, and whole-genome duplication. Proc. Natl Acad. Sci. USA 119, e2113075119 (2022).
pubmed: 34934012 doi: 10.1073/pnas.2113075119
Servant, N. et al. HiTC: exploration of high-throughput ‘C’ experiments. Bioinformatics 28, 2843–2844 (2012).
pubmed: 22923296 doi: 10.1093/bioinformatics/bts521
Mendes, F. K., Vanderpool, D., Fulton, B. & Hahn, M. W. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 36, 5516–5518 (2021).
pubmed: 33325502 doi: 10.1093/bioinformatics/btaa1022
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
pubmed: 17483113 doi: 10.1093/molbev/msm088
Kumar, S. et al. TimeTree 5: an expanded resource for species divergence times. Mol. Biol. Evol. 39, msac174 (2022).
pubmed: 35932227 pmcid: 9400175 doi: 10.1093/molbev/msac174
Calle García, J. et al. PRGdb 4.0: an updated database dedicated to genes involved in plant disease resistance process. Nucleic Acids Res. 50, D1483–D1490 (2022).
pubmed: 34850118 doi: 10.1093/nar/gkab1087
Osuna-Cruz, C. M. et al. PRGdb 3.0: a comprehensive platform for prediction and analysis of plant disease resistance genes. Nucleic Acids Res. 46, D1197–D1201 (2018).
pubmed: 29156057 doi: 10.1093/nar/gkx1119
Paysan-Lafosse, T. et al. InterPro in 2022. Nucleic Acids Res. 51, D418–D427 (2023).
pubmed: 36350672 doi: 10.1093/nar/gkac993
Sibbesen, J. A. & Maretty, L. The Danish Pan-Genome Consortium Accurate genotyping across variant classes and lengths using variant graphs. Nat. Genet. 50, 1054–1059 (2018).
pubmed: 29915429 doi: 10.1038/s41588-018-0145-5
Bang, H., Kim, S., Leskovar, D. & King, S. Development of a codominant CAPS marker for allelic selection between canary yellow and red watermelon based on SNP in lycopene β-cyclase (LCYB) gene. Mol. Breed. 20, 63–72 (2007).
doi: 10.1007/s11032-006-9076-4
Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008).
pubmed: 19114008 pmcid: 2631488 doi: 10.1186/1471-2105-9-559
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2
pubmed: 11846609 doi: 10.1006/meth.2001.1262
Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45 (2001).
pubmed: 11328886 doi: 10.1093/nar/29.9.e45
Li, H., Feng, X. & Chu, C. The design and construction of reference pangenome graphs with minigraph. Genome Biol. 21, 265 (2020).
pubmed: 33066802 pmcid: 7568353 doi: 10.1186/s13059-020-02168-z
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Zhang, Y. & Huang, M. Codes for the watermelon pangenome project in 2023. Zenodo https://doi.org/10.5281/zenodo.10693455 (2024).

Auteurs

Yilin Zhang (Y)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.
State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing, China.

Mingxia Zhao (M)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Jingsheng Tan (J)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Minghan Huang (M)

State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing, China.

Xiao Chu (X)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Yan Li (Y)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Xue Han (X)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Taohong Fang (T)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Yao Tian (Y)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Robert Jarret (R)

Plant Genetic Resource Unit, Griffin, GA, USA.

Dongdong Lu (D)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Yijun Chen (Y)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Lifang Xue (L)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Xiaoni Li (X)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Guochen Qin (G)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Bosheng Li (B)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.

Yudong Sun (Y)

Vegetable Research and Development Center, Huaiyin Institute of Agricultural Sciences of Xuhuai Region in Jiangsu, Huai'an, China.

Xing Wang Deng (XW)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China.
State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing, China.

Yun Deng (Y)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China. yun.deng@pku-iaas.edu.cn.

Xingping Zhang (X)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China. xingping.zhang@pku-iaas.edu.cn.

Hang He (H)

National Key Laboratory of Wheat Improvement, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China. hang.he@pku-iaas.edu.cn.
State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing, China. hang.he@pku-iaas.edu.cn.

Classifications MeSH