Two divergent haplotypes from a highly heterozygous lychee genome suggest independent domestication events for early and late-maturing cultivars.

Guibing Hu, Junting Feng, Xu Xiang, Jiabao Wang, Jarkko Salojärvi, Chengming Liu, Zhenxian Wu, Jisen Zhang, Xinming Liang, Zide Jiang, Wei Liu, Liangxi Ou, Jiawei Li, Guangyi Fan, Yingxiao Mai, Chengjie Chen, Xingtan Zhang, Jiakun Zheng, Yanqing Zhang, Hongxiang Peng, Lixian Yao, Ching Man Wai, Xinping Luo, Jiaxin Fu, Haibao Tang, Tianying Lan, Biao Lai, Jinhua Sun, Yongzan Wei, Huanling Li, Jiezhen Chen, Xuming Huang, Qian Yan, Xin Liu, Leah K McHale, William Rolling, Romain Guyot, David Sankoff, Chunfang Zheng, Victor A Albert, Ray Ming, Houbin Chen, Rui Xia, Jianguo Li
Author Information
  1. Guibing Hu: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  2. Junting Feng: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  3. Xu Xiang: Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China.
  4. Jiabao Wang: Danzhou Scientific Observing and Experimental Station of Agro-Environment, Ministry of Agriculture and Rural Affairs, Environment and Plant Protection Institute, Chinese Academy of Tropical Agriculture Sciences, Haikou, China.
  5. Jarkko Salojärvi: School of Biological Sciences, Nanyang Technological University, Singapore, Singapore. ORCID
  6. Chengming Liu: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  7. Zhenxian Wu: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China. ORCID
  8. Jisen Zhang: Center for Genomics and Biotechnology, Haixia Institute of Science and Technology Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  9. Xinming Liang: BGI-Shenzhen, Shenzhen, Guangdong, China.
  10. Zide Jiang: Guangdong Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural University, Guangzhou, China.
  11. Wei Liu: Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China.
  12. Liangxi Ou: Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China.
  13. Jiawei Li: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  14. Guangyi Fan: BGI-Shenzhen, Shenzhen, Guangdong, China.
  15. Yingxiao Mai: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  16. Chengjie Chen: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  17. Xingtan Zhang: Center for Genomics and Biotechnology, Haixia Institute of Science and Technology Fujian Agriculture and Forestry University, Fuzhou, China.
  18. Jiakun Zheng: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  19. Yanqing Zhang: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  20. Hongxiang Peng: Horticultural Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, China.
  21. Lixian Yao: College of Natural Resources and Environment, South China Agricultural University, Guangzhou, China.
  22. Ching Man Wai: Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
  23. Xinping Luo: Institute of Tropical and Subtropical Cash Crops, Yunnan Academy of Agricultural Sciences, Baoshan, China.
  24. Jiaxin Fu: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  25. Haibao Tang: Center for Genomics and Biotechnology, Haixia Institute of Science and Technology Fujian Agriculture and Forestry University, Fuzhou, China. ORCID
  26. Tianying Lan: Department of Biological Sciences, University at Buffalo, Buffalo, NY, USA.
  27. Biao Lai: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  28. Jinhua Sun: Danzhou Scientific Observing and Experimental Station of Agro-Environment, Ministry of Agriculture and Rural Affairs, Environment and Plant Protection Institute, Chinese Academy of Tropical Agriculture Sciences, Haikou, China.
  29. Yongzan Wei: Key Laboratory for Tropical Fruit Biology of Ministry of Agriculture and Rural Affair, South Subtropical Crops Research Institute, Chinese Academy of Tropical Agriculture Sciences, Zhanjiang, China. ORCID
  30. Huanling Li: Danzhou Scientific Observing and Experimental Station of Agro-Environment, Ministry of Agriculture and Rural Affairs, Environment and Plant Protection Institute, Chinese Academy of Tropical Agriculture Sciences, Haikou, China.
  31. Jiezhen Chen: Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China.
  32. Xuming Huang: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China.
  33. Qian Yan: Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China.
  34. Xin Liu: BGI-Shenzhen, Shenzhen, Guangdong, China. ORCID
  35. Leah K McHale: Department of Horticulture and Crop Sciences and Center for Applied Plant Sciences, The Ohio State University, Columbus, OH, USA. ORCID
  36. William Rolling: Center for Applied Plant Sciences, The Ohio State University, Columbus, OH, USA.
  37. Romain Guyot: IRD, UMR DIADE, EVODYN, Montpellier, France.
  38. David Sankoff: Department of Mathematics and Statistics, University of Ottawa, Ottawa, Ontario, Canada. ORCID
  39. Chunfang Zheng: Department of Mathematics and Statistics, University of Ottawa, Ottawa, Ontario, Canada.
  40. Victor A Albert: School of Biological Sciences, Nanyang Technological University, Singapore, Singapore. vaalbert@buffalo.edu. ORCID
  41. Ray Ming: Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA. rayming@illinois.edu. ORCID
  42. Houbin Chen: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China. hbchen@scau.edu.cn. ORCID
  43. Rui Xia: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China. rxia@scau.edu.cn. ORCID
  44. Jianguo Li: State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Laboratory for Lingnan Modern Agriculture, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, Guangdong Litchi Engineering Research Center, College of Horticulture, South China Agricultural University, Guangzhou, China. jianli@scau.edu.cn. ORCID

Abstract

Lychee is an exotic tropical fruit with a distinct flavor. The genome of cultivar 'Feizixiao' was assembled into 15 pseudochromosomes, totaling ~470 Mb. High heterozygosity (2.27%) resulted in two complete haplotypic assemblies. A total of 13,517 allelic genes (42.4%) were differentially expressed in diverse tissues. Analyses of 72 resequenced lychee accessions revealed two independent domestication events. The extremely early maturing cultivars preferentially aligned to one haplotype were domesticated from a wild population in Yunnan, whereas the late-maturing cultivars that mapped mostly to the second haplotype were domesticated independently from a wild population in Hainan. Early maturing cultivars were probably developed in Guangdong via hybridization between extremely early maturing cultivar and late-maturing cultivar individuals. Variable deletions of a 3.7 kb region encompassed by a pair of CONSTANS-like genes probably regulate fruit maturation differences among lychee cultivars. These genomic resources provide insights into the natural history of lychee domestication and will accelerate the improvement of lychee and related crops.

References

  1. Li, C. et al. De novo assembly and characterization of fruit transcriptome in Litchi chinensis Sonn and analysis of differentially regulated genes in fruit in response to shading. BMC Genomics 14, 552 (2013). pubmed:23941440; pmcid:3751308; doi:10.1186/1471-2164-14-552
  2. Liu, C. & Mei, M. Classification of lychee cultivars with RAPD analysis. Acta Hortic. 665, 149–160 (2005). doi:10.17660/ActaHortic.2005.665.17
  3. Liu, W. et al. Identifying Litchi (Litchi chinensis Sonn.) cultivars and their genetic relationships using single nucleotide polymorphism (SNP) markers. PLoS ONE 10, e0135390 (2015). pubmed:26261993; pmcid:4532366; doi:10.1371/journal.pone.0135390
  4. VanBuren, R. et al. Longli is not a hybrid of longan and lychee as revealed by genome size analysis and trichome morphology. Trop. Plant Biol. 4, 228–236 (2011). doi:10.1007/s12042-011-9084-3
  5. Huang, S., Kang, M. & Xu, A. HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly. Bioinformatics 33, 2577–2579 (2017). pubmed:28407147; pmcid:5870766; doi:10.1093/bioinformatics/btx220
  6. Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463–467 (2007). pubmed:17721507; doi:10.1038/nature06148
  7. Lam, H.-M. et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053 (2010). pubmed:21076406; doi:10.1038/ng.715
  8. Cao, K. et al. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol. 15, 415 (2014). pubmed:25079967; pmcid:4174323
  9. Alexander, D. H. & Lange, K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinf. 12, 246 (2011). doi:10.1186/1471-2105-12-246
  10. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012). pubmed:22960212; pmcid:3522152; doi:10.1534/genetics.112.145037
  11. Julca, I. et al. Genomic evidence for recurrent genetic admixture during the domestication of Mediterranean olive trees (Olea europaea L.). BMC Biol. 18, 148 (2020). pubmed:33100219; pmcid:7586694; doi:10.1186/s12915-020-00881-6
  12. Edge, P., Bafna, V. & Bansal, V. HapCUT2: robust and accurate haplotype assembly for diverse sequencing technologies. Genome Res. 27, 801–812 (2017). pubmed:27940952; pmcid:5411775; doi:10.1101/gr.213462.116
  13. Combes, M.-C., Dereeper, A., Severac, D., Bertrand, B. & Lashermes, P. Contribution of subgenomes to the transcriptome and their intertwined regulation in the allopolyploid Coffea arabica grown at contrasted temperatures. N. Phytol. 200, 251–260 (2013). doi:10.1111/nph.12371
  14. Payne, J. L. & Wagner, A. The causes of evolvability and their evolution. Nat. Rev. Genet. 20, 24–38 (2019). pubmed:30385867; doi:10.1038/s41576-018-0069-z
  15. Lee, J. H. et al. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev. 21, 397–402 (2007). pubmed:17322399; pmcid:1804328; doi:10.1101/gad.1518407
  16. Swaminathan, K., Peterson, K. & Jack, T. The plant B3 superfamily. Trends Plant Sci. 13, 647–655 (2008). pubmed:18986826; doi:10.1016/j.tplants.2008.09.006
  17. Levy, Y. Y., Mesnage, S., Mylne, J. S., Gendall, A. R. & Dean, C. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243–246 (2002). pubmed:12114624; doi:10.1126/science.1072147
  18. Suárez-López, P. et al. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116–1120 (2001). pubmed:11323677; doi:10.1038/35074138
  19. Lin, W. L. Exploring on the source of Pearl River. Front. Lit. 3, 51–52 (2008).
  20. Qian, S. Volcanic activity and magma evolution in the north of the Hainan Island. PhD Thesis, Institute of Geology. China Earthquake Administration. (2003).
  21. Chen, L., Zhang, Y. F., Li, T. J., Yang, W. F. & Chen, J. Sedimentary environment and its evolution of Qiongzhou Strait and nearby seas since last ten thousand years. Earth Sci. J. China Univ. Geosci. 39, 696–704 (2014).
  22. Fan, Q. C., Sun, Q. & Sui, J. L. Periods of volcanic activity and magma evolution of Holocene in North Hainan Island. Acta Petrol. Sin. 20, 533–544 (2004).
  23. Nordborg, M. & Donnelly, P. The coalescent process with selfing. Genetics 146, 1185–1195 (1997). pubmed:9215919; pmcid:1208046; doi:10.1093/genetics/146.3.1185
  24. Bäurle, I. & Dean, C. The timing of developmental transitions in plants. Cell 125, 655–664 (2006). pubmed:16713560; doi:10.1016/j.cell.2006.05.005
  25. Andrés, F. & Coupland, G. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627–639 (2012). pubmed:22898651; doi:10.1038/nrg3291
  26. Li, H.-T. et al. Origin of angiosperms and the puzzle of the Jurassic gap. Nat. Plants 5, 461–470 (2019). pubmed:31061536; doi:10.1038/s41477-019-0421-0
  27. Zhang, L. et al. The water lily genome and the early evolution of flowering plants. Nature 577, 79–84 (2020). pubmed:31853069; doi:10.1038/s41586-019-1852-5
  28. Terhorst, J., Kamm, J. A. & Song, Y. S. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat. Genet. 49, 303–309 (2017). pubmed:28024154; doi:10.1038/ng.3748
  29. Manichaikul, A. et al. Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867–2873 (2010). pubmed:20926424; pmcid:3025716; doi:10.1093/bioinformatics/btq559
  30. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014). pubmed:24695404; pmcid:4103590; doi:10.1093/bioinformatics/btu170
  31. Xie, T. et al. De novo plant genome assembly based on chromatin interactions: a case study of Arabidopsis thaliana. Mol. Plant 8, 489–492 (2015). pubmed:25667002; doi:10.1016/j.molp.2014.12.015
  32. Salmela, L. & Rivals, E. LoRDEC: accurate and efficient long read error correction. Bioinformatics 30, 3506–3514 (2014). pubmed:25165095; pmcid:4253826; doi:10.1093/bioinformatics/btu538
  33. 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). pubmed:28298431; pmcid:5411767; doi:10.1101/gr.215087.116
  34. Huang, S., Kang, M. & Xu, A. HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly. Bioinformatics 33, 2577–2579 (2017). pubmed:28407147; pmcid:5870766; doi:10.1093/bioinformatics/btx220
  35. Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3, 95–98 (2016). pubmed:27467249; pmcid:5846465; doi:10.1016/j.cels.2016.07.002
  36. Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92–95 (2017). pubmed:28336562; pmcid:5635820; doi:10.1126/science.aal3327
  37. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009). pubmed:19451168; pmcid:2705234; doi:10.1093/bioinformatics/btp324
  38. Wolff, J. et al. Galaxy HiCExplorer: a web server for reproducible Hi-C data analysis, quality control and visualization. Nucleic Acids Res. 46, W11–W16 (2018). pubmed:29901812; pmcid:6031062; doi:10.1093/nar/gky504
  39. 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
  40. Poplin, R. et al. Scaling accurate genetic variant discovery to tens of thousands of samples. Preprint at bioRxiv https://doi.org/10.1101/201178 (2018).
  41. Edge, P., Bafna, V. & Bansal, V. HapCUT2: robust and accurate haplotype assembly for diverse sequencing technologies. Genome Res. 27, 801–812 (2017). pubmed:27940952; pmcid:5411775; doi:10.1101/gr.213462.116
  42. Marks, P. et al. Resolving the full spectrum of human genome variation using linked-reads. Genome Res. 29, 635–645 (2019). pubmed:30894395; pmcid:6442396; doi:10.1101/gr.234443.118
  43. Zhang, X. et al. Genomes of the banyan tree and pollinator wasp provide insights into fig–wasp coevolution. Cell 183, 875–889.e17 (2020). pubmed:33035453; doi:10.1016/j.cell.2020.09.043
  44. Alonge, M. et al. RaGOO: fast and accurate reference-guided scaffolding of draft genomes. Genome Biol. 20, 224 (2019). pubmed:31661016; pmcid:6816165; doi:10.1186/s13059-019-1829-6
  45. Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinf. 12, 491 (2011). doi:10.1186/1471-2105-12-491
  46. Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439 (2006). pubmed:16845043; pmcid:1538822; doi:10.1093/nar/gkl200
  47. Korf, I. Gene finding in novel genomes. BMC Bioinf. 5, 59 (2004). doi:10.1186/1471-2105-5-59
  48. Bairoch, A. & Apweiler, R. The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28, 45–48 (2000). pubmed:10592178; pmcid:102476; doi:10.1093/nar/28.1.45
  49. 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
  50. Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 9, R7–R7 (2008). pubmed:18190707; pmcid:2395244; doi:10.1186/gb-2008-9-1-r7
  51. Wu, T. D. & Watanabe, C. K. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21, 1859–1875 (2005). pubmed:15728110; doi:10.1093/bioinformatics/bti310
  52. 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). pubmed:26059717; doi:10.1093/bioinformatics/btv351
  53. Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265–W268 (2007). pubmed:17485477; pmcid:1933203; doi:10.1093/nar/gkm286
  54. Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinf. 9, 18 (2008). doi:10.1186/1471-2105-9-18
  55. 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
  56. Ou, S., Chen, J. & Jiang, N. Assessing genome assembly quality using the LTR assembly index (LAI). Nucleic Acids Res. 46, e126–e126 (2018). pubmed:30107434; pmcid:6265445
  57. Lin, Y. et al. Genome-wide sequencing of longan (Dimocarpus longan Lour.) provides insights into molecular basis of its polyphenol-rich characteristics. Gigascience 6, 1–14 (2017). pubmed:29099922; pmcid:5726476; doi:10.1093/gigascience/gix023
  58. Bi, Q. et al. Pseudomolecule-level assembly of the Chinese oil tree yellowhorn (Xanthoceras sorbifolium) genome. Gigascience 8, giz070 (2019).
  59. Xu, Q. et al. The draft genome of sweet orange (Citrus sinensis). Nat. Genet. 45, 59–66 (2013). pubmed:23179022; doi:10.1038/ng.2472
  60. Initiative, T. A. G. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000). doi:10.1038/35048692
  61. Ming, R. et al. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452, 991–996 (2008). pubmed:18432245; pmcid:2836516; doi:10.1038/nature06856
  62. Edger, P. P. Single-molecule sequencing and optical mapping yields an improved genome of woodland strawberry (Fragaria vesca) with chromosome-scale contiguity. Gigascience 7, gix124 (2017).
  63. Velasco, R. et al. The genome of the domesticated apple (Malus × domestica Borkh.). Nat. Genet. 42, 833–839 (2010). pubmed:20802477; doi:10.1038/ng.654
  64. Li, Q. A chromosome-scale genome assembly of cucumber (Cucumis sativus L.). Gigascience 8, giz072 (2019).
  65. Tang, H. et al. An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics 15, 312 (2014).
  66. Hosmani, P. S. et al. An improved de novo assembly and annotation of the tomato reference genome using single-molecule sequencing, Hi-C proximity ligation and optical maps. Preprint at bioRxiv https://doi.org/10.1101/767764 (2019).
  67. Yang, J. et al. De novo genome assembly of the endangered Acer yangbiense, a plant species with extremely small populations endemic to Yunnan Province, China. Gigascience 8, giz085 (2019).
  68. Chen, C. et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194–1202 (2020). pubmed:32585190; doi:10.1016/j.molp.2020.06.009
  69. Emms, D.M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019)
  70. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007). pubmed:17483113; doi:10.1093/molbev/msm088
  71. Wang, Y. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49–e49 (2012). pubmed:22217600; pmcid:3326336; doi:10.1093/nar/gkr1293
  72. Wickham, H. ggplot2: Elegant Graphics for Data Analysis. (Springer-Verlag, 2016).
  73. Chen, C. et al. sRNAanno—a database repository of uniformly annotated small RNAs in plants. Hortic. Res. 8, 45 (2021)
  74. Tang, H., Krishnakumar, V. & Li, J. jcvi: JCVI utility libraries https://doi.org/10.5281/zenodo.31631 (2015).
  75. Andrews, S. FastQC: a quality control tool for high throughput sequence data. (Barbraham Bioinformatics, 2010).
  76. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012). pubmed:22388286; pmcid:3322381; doi:10.1038/nmeth.1923
  77. Picard toolkit (Broad Institute, GitHub repository, 2019).
  78. Narasimhan, V. et al. BCFtools/RoH: a hidden Markov model approach for detecting autozygosity from next-generation sequencing data. Bioinformatics 32, 1749–1751 (2016). pubmed:26826718; pmcid:4892413; doi:10.1093/bioinformatics/btw044
  79. Chang, C. C. et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4, 7 (2015). pubmed:25722852; pmcid:4342193; doi:10.1186/s13742-015-0047-8
  80. Lee, T.-H., Guo, H., Wang, X., Kim, C. & Paterson, A. H. SNPhylo: a pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics 15, 162 (2014). pubmed:24571581; pmcid:3945939; doi:10.1186/1471-2164-15-162
  81. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014). pubmed:24451623; pmcid:3998144; doi:10.1093/bioinformatics/btu033
  82. Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinf. 15, 356 (2014). doi:10.1186/s12859-014-0356-4
  83. Salojärvi, J. et al. Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat. Genet. 49, 904–912 (2017). pubmed:28481341; doi:10.1038/ng.3862
  84. R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2017).
  85. Liu, X. & Fu, Y.-X. Stairway Plot 2: demographic history inference with folded SNP frequency spectra. Genome Biol. 21, 280 (2020). pubmed:33203475; pmcid:7670622; doi:10.1186/s13059-020-02196-9
  86. Li, H. & Durbin, R. Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011). pubmed:21753753; pmcid:3154645; doi:10.1038/nature10231
  87. Excoffier, L., Dupanloup, I., Huerta-Sánchez, E., Sousa, V. C. & Foll, M. Robust demographic inference from genomic and SNP data. PLoS Genet. 9, e1003905 (2013). pubmed:24204310; pmcid:3812088; doi:10.1371/journal.pgen.1003905
  88. Zhang, C., Dong, S.-S., Xu, J.-Y., He, W.-M. & Yang, T.-L. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786–1788 (2018). doi:10.1093/bioinformatics/bty875
  89. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011). pubmed:21653522; pmcid:3137218; doi:10.1093/bioinformatics/btr330
  90. Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984). pubmed:28563791
  91. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly (Austin) 6, 80–92 (2012). doi:10.4161/fly.19695
  92. Chen, J., Glémin, S. & Lascoux, M. Genetic diversity and the efficacy of purifying selection across plant and animal species. Mol. Biol. Evol. 34, 1417–1428 (2017). pubmed:28333215; doi:10.1093/molbev/msx088
  93. Salojärvi, J. jsalojar/PiNSiR: first release of PiNSiR https://doi.org/10.5281/zenodo.5136527 (2021).
  94. Bradbury, P. J. et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633–2635 (2007). pubmed:17586829; doi:10.1093/bioinformatics/btm308
  95. Rabah, S. et al. Plastome sequencing of ten nonmodel crop species uncovers a large insertion of mitochondrial DNA in cashew. Plant Genome 10 https://doi.org/10.3835/plantgenome2017.03.0020 (2017).
  96. Chevreux, B. et al. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14, 1147–1159 (2004). pubmed:15140833; pmcid:419793; doi:10.1101/gr.1917404
  97. Hahn, C., Bachmann, L. & Chevreux, B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res. 41, e129–e129 (2013). pubmed:23661685; pmcid:3711436; doi:10.1093/nar/gkt371
  98. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002). pubmed:12136088; pmcid:135756; doi:10.1093/nar/gkf436
  99. Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009). pubmed:19505945; pmcid:2712344; doi:10.1093/bioinformatics/btp348
  100. Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. Syst. Biol. 65, 997–1008 (2016). pubmed:27121966; pmcid:5066062; doi:10.1093/sysbio/syw037

MeSH Term

China
Crops, Agricultural
Domestication
Evolution, Molecular
Flowers
Genome, Plant
Haplotypes
Heterozygote
Litchi
Molecular Sequence Annotation
Polymorphism, Single Nucleotide
Sequence Analysis, DNA
Species Specificity