Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Haplotype-resolved genomes of wild octoploid progenitors illuminate genomic diversifications from wild relatives to cultivated strawberry

Nature Plants volume 9, pages 1252–1266 (2023)Cite this article

Subjects

Abstract

Strawberry is an emerging model for studying polyploid genome evolution and rapid domestication of fruit crops. Here we report haplotype-resolved genomes of two wild octoploids (Fragaria chiloensis and Fragaria virginiana), the progenitor species of cultivated strawberry. Substantial variation is identified between species and between haplotypes. We redefine the four subgenomes and track the genetic contributions of diploid species by additional sequencing of the diploid F. nipponica genome. We provide multiple lines of evidence that F. vesca and F. iinumae, rather than other described extant species, are the closest living relatives of these wild and cultivated octoploids. In response to coexistence with quadruplicate gene copies, the octoploid strawberries have experienced subgenome dominance, homoeologous exchanges and coordinated expression of homoeologous genes. However, some homoeologues have substantially altered expression bias after speciation and during domestication. These findings enhance our understanding of the origin, genome evolution and domestication of strawberries.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Hi-C-based anchoring of the wild octoploid strawberry genomes.
Fig. 2: Subgenome assignments of the octoploids and tracing the potential diploid ancestors.
Fig. 3: Static and dynamic pattern of HEB among quadruplets of the wild and cultivated octoploid strawberries.

Data availability

All the raw genome sequencing data have been submitted to the National Genomics Data Center (https://ngdc.cncb.ac.cn/), and the accession number is CRA005392. All the genome assemblies reported in this paper have been deposited in the Genome Warehouse of the National Genomics Data Center (https://ngdc.cncb.ac.cn/gwh), and the accession numbers are GWHDEDQ00000000 (F. chiloensis), GWHDEDR00000000 (F. virginiana) and GWHDEDN00000000 (F. nipponica). All the genome assembly and annotation files are also available in the Genome Database for Rosaceae (GDR) (https://www.rosaceae.org/Analysis/16216791,16216792,16216793).

Code availability

The scripts used for HEB category analysis for each quadruplet in this paper are available on GitHub (https://github.com/jinxin112233/HEB_categories). Bash commands for studying wild strawberry genomes have been uploaded on GitHub (https://github.com/jinxin112233/WSG).

References

  1. Soltis, P. S. & Soltis, D. E. Polyploidy and Genome Evolution (Springer, 2012).

  2. Chen, J. Z. & Birchler, J. A. Polyploid and Hybrid Genomics (Wiley-Blackwell, 2013).

  3. Ye, C. Y. et al. The genomes of the allohexaploid Echinochloa crus-galli and its progenitors provide insights into polyploidization-driven adaptation. Mol. Plant 13, 1298–1310 (2020).

    Article  CAS  PubMed  Google Scholar 

  4. Osborn, T. C. et al. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19, 141–147 (2003).

    Article  CAS  PubMed  Google Scholar 

  5. Comai, L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836–846 (2005).

    Article  CAS  PubMed  Google Scholar 

  6. Michael, T. P. & VanBuren, R. Building near-complete plant genomes. Curr. Opin. Plant Biol. 54, 26–33 (2020).

    Article  CAS  PubMed  Google Scholar 

  7. Koren, S. et al. De novo assembly of haplotype-resolved genomes with trio binning. Nat. Biotechnol. 36, 1174–1182 (2018).

    Article  CAS  Google Scholar 

  8. Campoy, J. A. et al. Gamete binning: chromosome-level and haplotype-resolved genome assembly enabled by high-throughput single-cell sequencing of gamete genomes. Genome Biol. 21, 306 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wenger, A. M. et al. Highly-accurate long-read sequencing improves variant detection and assembly of a human genome. Nat. Biotechnol. 37, 1155–1162 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Hon, T. et al. Highly accurate long-read HiFi sequencing data for five complex genomes. Sci. Data 7, 399 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mascher, M. et al. Long-read sequence assembly: a technical evaluation in barley. Plant Cell 33, 1888–1906 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Zhou, Q. et al. Haplotype-resolved genome analyses of a heterozygous diploid potato. Nat. Genet. 52, 1018–1023 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sun, X. et al. Phased diploid genome assemblies and pan-genomes provide insights into the genetic history of apple domestication. Nat. Genet. 52, 1423–1432 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chen, H. et al. Allele-aware chromosome-level genome assembly and efficient transgene-free genome editing for the autotetraploid cultivated alfalfa. Nat. Commun. 11, 2494 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Folta, K. M. & Davis, T. M. Strawberry genes and genomics. Crit. Rev. Plant Sci. 25, 399–415 (2006).

    Article  CAS  Google Scholar 

  16. Hummer, K. E. & Hancock, J. Strawberry genomics: botanical history, cultivation, traditional breeding, and new technologies. In Genetics and genomics of Rosaceae (eds Folta, K. M. & Gardiner, S. E.) 413–435 (Springer, 2009).

  17. Qiao, Q. et al. Evolutionary history and pan-genome dynamics of strawberry (Fragaria spp.). Proc. Natl Acad. Sci. USA 118, e2105431118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Liston, A., Cronn, R. & Ashman, T. L. Fragaria: a genus with deep historical roots and ripe for evolutionary and ecological insights. Am. J. Bot. 101, 1686–1699 (2014).

    Article  PubMed  Google Scholar 

  19. Njuguna, W., Liston, A., Cronn, R., Ashman, T. L. & Bassil, N. Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. Mol. Phylogenet. Evol. 66, 17–29 (2013).

    Article  PubMed  Google Scholar 

  20. Whitaker, V. M. et al. A roadmap for research in octoploid strawberry. Hortic. Res. 7, 33 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Moyano-Cañete, E. et al. FaGAST2, a strawberry ripening-related gene, acts together with FaGAST1 to determine cell size of the fruit receptacle. Plant Cell Physiol. 54, 218–236 (2013).

    Article  PubMed  Google Scholar 

  22. Gaston, A. et al. The FveFT2 florigen/FveTFL1 antiflorigen balance is critical for the control of seasonal flowering in strawberry while FveFT3 modulates axillary meristem fate and yield. N. Phytol. 232, 372–387 (2021).

    Article  CAS  Google Scholar 

  23. Hirakawa, H. et al. Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res. 21, 169–181 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Hirsch, C. N. & Buell, C. R. Tapping the promise of genomics in species with complex, nonmodel genomes. Annu. Rev. Plant Biol. 64, 89–110 (2013).

    Article  CAS  PubMed  Google Scholar 

  25. Hardigan, M. A. et al. Genome synteny has been conserved among the octoploid progenitors of cultivated strawberry over millions of years of evolution. Front. Plant Sci. 10, 1789 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Edger, P. P. et al. Origin and evolution of the octoploid strawberry genome. Nat. Genet. 51, 541–547 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Liston, A. et al. Revisiting the origin of octoploid strawberry. Nat. Genet. 52, 2–4 (2020).

    Article  CAS  PubMed  Google Scholar 

  28. Feng, C. et al. Tracing the diploid ancestry of the cultivated octoploid strawberry. Mol. Biol. Evol. 38, 478–485 (2021).

    Article  CAS  PubMed  Google Scholar 

  29. Zhang, X., Zhang, S., Zhao, Q., Ming, R. & Tang, H. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nat. Plants 5, 833–845 (2019).

    Article  CAS  PubMed  Google Scholar 

  30. Edger, P. P. et al. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. GigaScience 7, 1–7 (2018).

    Article  CAS  PubMed  Google Scholar 

  31. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Abou, Saada et al. nPhase: an accurate and contiguous phasing method for polyploids. Genome Biol. 22, 126 (2021).

    Article  Google Scholar 

  33. Hardigan, M. A. et al. Unraveling the complex hybrid ancestry and domestication history of cultivated strawberry. Mol. Biol. Evol. 38, 2285–2305 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Tennessen, J. A., Govindarajulu, R., Ashman, T. L. & Liston, A. Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol. Evol. 6, 3295–3313 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Session, A. M. & Rokhsar, D. S. Transposon signatures of allopolyploid genome evolution. Nat. Commun. 14, 3180 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mitros, T. et al. Genome biology of the paleotetraploid perennial biomass crop Miscanthus. Nat. Commun. 11, 5442 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Edger, P. P. et al. Reply to: Revisiting the origin of octoploid strawberry. Nat. Genet. 52, 5–7 (2020).

    Article  CAS  PubMed  Google Scholar 

  38. Zhang, J. et al. The high-quality genome of diploid strawberry (Fragaria nilgerrensis) provides new insights into anthocyanin accumulation. Plant Biotechnol. J. 18, 1908–1924 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wei, N., Tennessen, J. A., Liston, A. & Ashman, T. L. Present-day sympatry belies the evolutionary origin of a high-order polyploid. N. Phytol. 216, 279–290 (2017).

    Article  Google Scholar 

  40. Zhang, X., Wu, R., Wang, Y., Yu, J. & Tang, H. Unzipping haplotypes in diploid and polyploid genomes. Comput. Struct. Biotechnol. J. 18, 66–72 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Della Coletta, R., Qiu, Y., Ou, S., Hufford, M. B. & Hirsch, C. N. How the pan-genome is changing crop genomics and improvement. Genome Biol. 22, 3 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hancock, J. F. & Bringhurst, R. S. Evolution of California populations of diploid and octoploid Fragaria (Rosaceae): a comparison. Am. J. Bot. 68, 1–5 (1981).

    Article  Google Scholar 

  43. Harrison, R. E., Luby, J. J., Furnier, G. R. & Hancock, J. F. Morphological and molecular variation among populations of octoploid Fragaria virginiana and F. chiloensis (Rosaceae) from North America. Am. J. Bot. 84, 612–620 (1997).

    Article  CAS  PubMed  Google Scholar 

  44. Qu, M. et al. Karyotypic stability of Fragaria (strawberry) species revealed by cross-species chromosome painting. Chromosome Res. 29, 285–300 (2021).

    Article  CAS  PubMed  Google Scholar 

  45. Chen, Z. J. et al. Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement. Nat. Genet. 52, 525–533 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hancock, J. F. et al. Reconstruction of the strawberry, Fragaria × ananassa, using genotypes of F. virginiana and F. chiloensis. HortScience 45, 1006–1013 (2010).

    Article  Google Scholar 

  47. Nakashima, K. & Yamaguchi-Shinozaki, K. ABA signaling in stress-response and seed development. Plant Cell Rep. 32, 959–970 (2013).

    Article  CAS  PubMed  Google Scholar 

  48. Li, J. et al. Research advances of MYB transcription factors in plant stress resistance and breeding. Plant Signal. Behav. 14, 1613131 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Marçais, G. & Kingsford, C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27, 764–770 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Vurture, G. W. et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics 33, 2202–2204 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Ranallo-Benavidez, T. R. et al. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 11, 1432 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cheng, H. et al. Haplotype-resolved assembly of diploid genomes without parental data. Nat. Biotechnol. 40, 1332–1335 (2022).

    Article  CAS  PubMed  Google Scholar 

  53. Alonge, M. et al. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20, 224 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3, 99–101 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 27, 737–746 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Burton, J. N. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat. Biotechnol. 31, 1119–1125 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dierckxsens, N., Mardulyn, P. & Smits, G. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 45, e18 (2017).

    PubMed  Google Scholar 

  61. Nurk, S. et al. HiCanu: accurate assembly of segmental duplications, satellites, and allelic variants from high-fidelity long reads. Genome Res. 30, 1291–1305 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Rhie, A. et al. Towards complete and error-free genome assemblies of all vertebrate species. Nature 592, 737–746 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  64. 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).

    Article  CAS  PubMed  Google Scholar 

  65. Ou, S. & Jiang, N. LTR_FINDER_parallel: parallelization of LTR_FINDER enabling rapid identification of long terminal repeat retrotransposons. Mob. DNA 10, 48 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinform. 9, 18 (2008).

    Article  Google Scholar 

  67. Langdon, Q. K., Peris, D., Kyle, B. & Hittinger, C. T. sppIDer: a species identification tool to investigate hybrid genomes with high-throughput sequencing. Mol. Biol. Evol. 35, 2835–2849 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Guan, D. et al. Identifying and removing haplotypic duplication in primary genome assemblies. Bioinformatics 36, 2896–2898 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

    Article  PubMed  Google Scholar 

  72. Tarailo‐Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinform. 25, 4.10.1–4.10.14 (2009).

    Article  Google Scholar 

  73. Hoff, K. J., Lomsadze, A., Borodovsky, M. & Stanke, M. Whole-genome annotation with BRAKER. Methods Mol. Biol. 1962, 65–95 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  75. Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).

    Article  CAS  PubMed  Google Scholar 

  76. Cheng, C. Y. et al. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 89, 789–804 (2017).

    Article  CAS  PubMed  Google Scholar 

  77. Li, Y., Pi, M., Gao, Q., Liu, Z. & Kang, C. Updated annotation of the wild strawberry Fragaria vesca V4 genome. Hort. Res. 6, 61 (2019).

    Article  Google Scholar 

  78. Raymond, O. et al. The Rosa genome provides new insights into the domestication of modern roses. Nat. Genet. 50, 772–777 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Zhang, L. et al. A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat. Commun. 10, 1494 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinform. 12, 491 (2011).

    Article  Google Scholar 

  81. Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Marçais, G. et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput. Biol. 14, e1005944 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  83. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  84. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing nextgeneration DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Price, M. N. et al. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641–1650 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Jia, K. H. et al. SubPhaser: a robust allopolyploid subgenome phasing method based on subgenome-specific k-mers. N. Phytol. 235, 801–809 (2022).

    Article  CAS  Google Scholar 

  89. Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Buti, M. et al. The genome sequence and transcriptome of Potentilla micrantha and their comparison to Fragaria vesca (the woodland strawberry). GigaScience 7, 1–14 (2018).

    Article  PubMed  Google Scholar 

  91. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540–552 (2000).

    Article  CAS  PubMed  Google Scholar 

  94. Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    Article  CAS  PubMed  Google Scholar 

  95. Mirarab, S. et al. ASTRAL: genome-scale coalescent-based species tree estimation. Bioinformatics 30, i541–i548 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Fan, H., Ives, A. R., Surget-Groba, Y. & Cannon, C. H. An assembly and alignment-free method of phylogeny reconstruction from next-generation sequencing data. BMC Genomics 16, 522 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Ramírez-González, R. H. et al. The transcriptional landscape of polyploid wheat. Science 361, eaar6089 (2018).

    Article  PubMed  Google Scholar 

  100. Cantalapiedra, C. P. et al. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol. Biol. Evol. 38, 5825–5829 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the National Key Research and Development Program of China (grant no. 2018YFD1000107), CAS Pioneer Hundred Talents, and the open research project of the ‘Cross-Cooperative Team’ of the Germplasm Bank of Wild Species to A.Z., by the University of Nebraska–Lincoln to J.P.M, and by the National Science Foundation of China (grant no. 31860534) to J.R.

Author information

Authors and Affiliations

  1. Germplasm Bank of Wild Species, Yunnan Key Laboratory of Crop Wild Relatives Omics, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China

    Xin Jin, Haiyuan Du, Chumeng Zhu, Fang Liu & Andan Zhu

  2. University of Chinese Academy of Sciences, Beijing, China

    Xin Jin, Haiyuan Du & Chumeng Zhu

  3. Horticultural Research Institute, Yunnan Academy of Agricultural Sciences, Kunming, China

    Hong Wan

  4. Flower Research Institute, Yunnan Academy of Agricultural Sciences, Kunming, China

    Jiwei Ruan

  5. Center for Plant Science Innovation, University of Nebraska, Lincoln, NE, USA

    Jeffrey P. Mower

  6. Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE, USA

    Jeffrey P. Mower

Authors
  1. Xin Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haiyuan Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chumeng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiwei Ruan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jeffrey P. Mower
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.Z. and J.R. conceived the project. A.Z., J.P.M. and J.R. designed the research. J.R., H.W. and H.D. collected and cared for the plant materials. H.D., C.Z. and F.L. sampled the plant tissues for genome and transcriptome sequencing. X.J., A.Z. and H.D. performed the computational analyses. X.J., J.P.M. and A.Z. wrote the manuscript with input from all authors.

Corresponding authors

Correspondence to Jiwei Ruan, Jeffrey P. Mower or Andan Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Plants thanks Andrew H. Paterson, John Lovell and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Morphological identification of the sequenced Fragaria species.

(a) Morphological features of F. chiloensis, F. virginiana, F. nipponica, and the cultivar ‘Camarosa’. Scale bar, 1 cm. (b) Seedings of F. chiloensis, F. virginiana, F. nipponica in the greenhouse.

Extended Data Fig. 2 Ploidy level estimation.

Smudge plots showing the ploidy level estimation for the sequenced F. chiloensis, F. virginiana and F. nipponica plants.

Extended Data Fig. 3 Hi-C interaction maps of the haplotype2 of the octoploid F. chiloensis.

(a), F. virginiana (b) and diploid F. nipponica (c). Note: Low to high densities of interaction signals were scaled with colours from orange to deep red.

Extended Data Fig. 4 Graphical alignment of F. vesca genome with F. chiloensis genome, the F. virginiana genome, and the F. nipponica genome.

Macrosynteny between the F. vesca genome and the F. chiloensis (a) and the F. virginiana genome (b). Syntenic gene pairs are denoted by black points. (c) Macrosynteny between the F. nipponica genome and the F. vesca genome. Syntenic gene pairs are denoted by gray line.

Extended Data Fig. 5 Mapping-based subgenome assignments of the F. chiloensis and F. virginiana chromosomes.

Note: The top and bottom line of box plot represent 25th and 75th percentiles, the centre line is the median and whiskers are the full data range. Different lowercase letters indicate the significance of differences in mapping rates among subgenomes, using one-way ANOVA with Duncan’s multiple range test (df = 27; P < 0.05).

Extended Data Fig. 6 Identification of specific subgenome k-mers (K = 13 and frequency = 50) F. virginiana (hap1) based on the subgenomic assignment originally proposed in the ‘Camarosa’ genome by Edger et al., (2019) and Hardigan et al., (2021).

The difference of chromosome assignments (2 C, 2D, 5 C, 5D, 6 C, 6D) are shown. Note: n = number of specific k-mer on each subgenome.

Extended Data Fig. 7 Identification of F. chiloensis(hap1), F. chiloensis(hap2), F. virginiana(hap1) and F. virginiana(hap2) subgenome specific LTR-RTs based on new subgenome assignment and subgenome assignment by Edger et al., (2019) and Hardigan et al., (2021).

Note: n = number of specific LTR-RTs on each subgenome.

Extended Data Fig. 8 Genetic distance matrix between diploid species and each subgenome based on 21 k-mer calculation.

(homoeologous exchange regions were filtered).

Extended Data Fig. 9 Phylogenomic analysis of the octoploid subgenomes.

(a) Total of 6345 single copy gene were identified and 122 single copy gene located in homoeologous exchange regions (HEs) were filtered. (b) Coalescent-based analysis of 6223 genes from four diploid species and each subgenome of the F. virginiana genome. (c) Summary of phylogenetic positions of the four octoploid subgenomes. Different colour indicates the number of kept homologous gene clade with diploid species.

Extended Data Fig. 10 Expression dominance.

The distribution of HEB between all gene pairs in the red fruits of F. chiloensis, F. virginiana and ‘Camarosa’.

Supplementary information

Supplementary Information

Supplementary Figs. 1–43.

Reporting Summary

Supplementary Table 1

Supplementary Tables 1–16.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jin, X., Du, H., Zhu, C. et al. Haplotype-resolved genomes of wild octoploid progenitors illuminate genomic diversifications from wild relatives to cultivated strawberry. Nat. Plants 9, 1252–1266 (2023). https://doi.org/10.1038/s41477-023-01473-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-023-01473-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing