Genomic data provides insights into the evolutionary history and adaptive differentiation of two tetraploid strawberries

Abstract

Over the decades, evolutionists and ecologists have shown intense interest in the role of polyploidization in plant evolution. Without clear knowledge of the diploid ancestor(s) of polyploids, we would not be able to answer fundamental ecological questions such as the evolution of niche differences between them or its underlying genetic basis. Here, we explored the evolutionary history of two Fragaria tetraploids, Fragaria corymbosa and Fragaria moupinensis. We de novo assembled five genomes including these two tetraploids and three diploid relatives. Based on multiple lines of evidence, we found no evidence of subgenomes in either of the two tetraploids, suggesting autopolyploid origins. We determined that Fragaria chinensis was the diploid ancestor of F. corymbosa while either an extinct species affinitive to F. chinensis or an unsampled population of F. chinensis could be the progenitor of F. moupinensis. Meanwhile, we found introgression signals between F. chinensis and Fragaria pentaphylla, leading to the genomic similarity between these two diploids. Compared to F. chinensis, gene families related to high ultraviolet (UV)-B and DNA repair were expanded, while those that responded towards abiotic and biotic stresses (such as salt stress, wounding, and various pathogens) were contracted in both tetraploids. Furthermore, the two tetraploids tended to down-regulate defense response genes but up-regulate UV-B response, DNA repairing, and cell division gene expression compared to F. chinensis. These findings may reflect adaptions toward high-altitude habitats. In summary, our work provides insights into the genome evolution of wild Fragaria tetraploids and opens up an avenue for future works to answer deeper evolutionary and ecological questions regarding the strawberry genus.

Acknowledgements

This work was funded by the National Natural Science Foundation of China (No. 31261120580 to M.D. and J.L.) and the National Science Foundation (DEB 12410006 to T.-L.A.; DEB 1241217 to A.L.). The authors thank Lingsong Chen, Minghua Song, Tong Chen, Xiaoyan Wang, Beifen Yang, Jinzhi Li, and Zhaokui Du for the collection of samples.

Author contributions

M.D., J.L., T.-L.A., and A.L. initiated the project. H.L. and J.L. wrote and finalized the manuscript. H.L., L.C., C.C., and J.M. designed and performed most of the experiments. T.-L.A., A.L., and M.D. provided assistance and suggestions. All authors discussed the results and commented on the manuscript.

Data availability

The assembled genome sequences and annotation files are available from the figshare repository (https://doi.org/10.6084/m9.figshare.25999996).

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1] Soltis PS, Marchant DB, Van de Peer Y. et al. Curr Opin Genet Dev. Polyploidy and genome evolution in plants. 2015; 35:119-25

[2] Jiao Y, Wickett NJ, Ayyampalayam S. et al. Ancestral polyploidy in seed plants and angiosperms. Nature. 2011; 473:97-100

[3] Van de Peer Y, Mizrachi E, Marchal K. The evolutionary significance of polyploidy. Nat Rev Genet. 2017; 18:411-24

[4] Alix K, Gérard PR, Schwarzacher T. et al. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot. 2017; 120:183-94

[5] Ge S. A review of recent studies of plant systematics and evolution in China. Biodivers Sci. 2022; 30:22385

[6] Van de Peer Y, Ashman T-L, Soltis PS. et al. Polyploidy: an evolutionary and ecological force in stressful times. Plant Cell. 2021; 33:11-26

[7] Arrigo N, Barker MS. Rarely successful polyploids and their legacy in plant genomes. Curr Opin Plant Biol. 2012; 15:140-6

[8] Mayrose I, Zhan SH, Rothfels CJ. et al. Recently formed polyploid plants diversify at lower rates. Science. 2011; 333:1257-7

[9] Soltis DE, Segovia-Salcedo MC, Jordon-Thaden I. et al. Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytol. 2014; 202:1105-17

[10] Abbott RJ, Brochmann C. History and evolution of the arctic flora: in the footsteps of Eric Hultén. Mol Ecol. 2003; 12:299-313

[11] Baniaga AE, Marx HE, Arrigo N. et al. Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives. Ecol Lett. 2020; 23:68-78

[12] Pandit MK, Pocock MJO, Kunin WE. Ploidy influences rarity and invasiveness in plants. J Ecol. 2011; 99:1108-15

[13] Rice A, Šmarda P, Novosolov M. et al. The global biogeography of polyploid plants. Nat Ecol Evol. 2019; 3:265-73

[14] Paterson AH, Wendel JF, Gundlach H. et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature. 2012; 492:423-7

[15] Wang T, Wang B, Hua X. et al. A complete gap-free diploid genome in Saccharum complex and the genomic footprints of evolution in the highly polyploid Saccharum genus. Nat Plants. 2023; 9:554-71

[16] Li X, Yu S, Cheng Z. et al. Origin and evolution of the triploid cultivated banana genome. Nat Genet. 2024; 56:136-42

[17] Lei JJ, Xue L, Guo RX. et al. The Fragaria species native to China and their geographical distribution. Acta Hortic. 2017; 1156:37-46

[18] Liston A, Cronn R, Ashman T. Fragaria: a genus with deep historical roots and ripe for evolutionary and ecological insights. Am J Bot. 2014; 101:1686-99

[19] Edger PP, McKain MR, Yocca AE. et al. Reply to: revisiting the origin of octoploid strawberry. Nat Genet. 2020; 52:5-7

[20] Edger PP, Poorten TJ, VanBuren R. et al. Origin and evolution of the octoploid strawberry genome. Nat Genet. 2019; 51:541-7

[21] Feng C, Wang J, Harris AJ. et al. Tracing the diploid ancestry of the cultivated octoploid strawberry. Mol Biol Evol. 2021; 38:478-85

[22] 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. 2023; 9:1252-66

[23] Liston A. On the origin of strawberries. Nat Plants. 2023; 9:1176-7

[24] Liston A, Wei N, Tennessen JA. et al. Revisiting the origin of octoploid strawberry. Nat Genet. 2020; 52:2-4

[25] Session AM, Rokhsar DS. Transposon signatures of allopolyploid genome evolution. Nat Commun. 2023; 14:3180

[26] Zhou Y, Xiong J, Shu Z. et al. The telomere-to-telomere genome of Fragaria vesca reveals the genomic evolution of Fragaria and the origin of cultivated octoploid strawberry. Hortic Res. 2023;10:uhad027

[27] Kamneva OK, Syring J, Liston A. et al. Evaluating allopolyploid origins in strawberries (Fragaria) using haplotypes generated from target capture sequencing. BMC Evol Biol. 2017; 17:180

[28] Feng C, Wang J, Liston A. et al. Recombination variation shapes phylogeny and introgression in wild diploid strawberries. Mol Biol Evol. 2023;40:msad049

[29] Staudt G. Strawberry biogeography, genetics and systematics. Acta Hortic. 2009; 842:71-84

[30] Johnson AL, Govindarajulu R, Ashman T-L. Bioclimatic evaluation of geographical range in Fragaria (Rosaceae): consequences of variation in breeding system, ploidy and species age. Bot J Linn Soc. 2014; 176:99-114

[31] Wan J-Z, Chen L-X, Gao S. et al. Ecological niche shift between diploid and tetraploid plants of Fragaria (Rosaceae) in China. South African J Bot. 2019; 121:68-75

[32] Qiao Q, Edger PP, Xue L. et al. Evolutionary history and pan-genome dynamics of strawberry (Fragaria spp.). Proc Natl Acad Sci. 2021; 118:e2105431118

[33] Liu B, Davis TM. Conservation and loss of ribosomal RNA gene sites in diploid and polyploid Fragaria (Rosaceae). BMC Plant Biol. 2011; 11:157

[34] Zhang L, Han Y, Li Z. Advances in cytogenetics of Fragaria. J Jiangsu Norm Univ Sci Ed. 2020; 38:65-9

[35] Qiao Q, Cao Q, Zhang R. et al. Genomic analyses provide insights into sex differentiation of tetraploid strawberry (Fragaria moupinensis). Plant Biotechnol J. 2024; 22:1552-65

[36] Wu S, Wang Y, Wang Z. et al. Species divergence with gene flow and hybrid speciation on the Qinghai-Tibet plateau. New Phytol. 2022; 234:392-404

[37] Hu R, Li X, Hu Y. et al. Adaptive evolution of the enigmatic Takakia now facing climate change in Tibet. Cell. 2023; 186:3558-3576.e17

[38] Tsukaya H, Tsuge T. Morphological adaptation of inflorescences in plants that develop at low temperatures in early spring: the convergent evolution of “downy plants”. Plant Biol. 2001; 3:536-43

[39] Kumar S, Suyal DC, Yadav A. et al. Microbial diversity and soil physiochemical characteristic of higher altitude. PLoS One. 2019; 14:e0213844

[40] Pellissier L, Roger A, Bilat J. et al. High elevation Plantago lanceolata plants are less resistant to herbivory than their low elevation conspecifics: is it just temperature? Ecography. 2014; 37:950-9

[41] Rasmann S, Buri A, Gallot-Lavallée M. et al. Differential allocation and deployment of direct and indirect defences by Vicia sepium along elevation gradients. J Ecol. 2014; 102:930-8

[42] Zhu Y, Zhang Y, Yan S. et al. Viral community structure and functional potential vary with lifestyle and altitude in soils of Mt. Everest. Environ Int. 2023; 178:108055

[43] Zhang X, Kuang T, Dong W. et al. Genomic convergence underlying high-altitude adaptation in alpine plants. J Integr Plant Biol. 2023; 65:1620-35

[44] Nathewet P, Yanagi T, Hummer KE. et al. Karyotype analysis in wild diploid, tetraploid and hexaploid strawberries, Fragaria (Rosaceae). Cytologia. 2009; 74:355-64

[45] 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

[46] Chin C-S, Peluso P, Sedlazeck FJ. et al. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods. 2016; 13:1050-4

[47] Hu J, Fan J, Sun Z. et al. NextPolish: a fast and efficient genome polishing tool for long-read assembly. Bioinformatics. 2020; 36:2253-5

[48] Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012; 9:357-9

[49] Zhang X, Zhang S, Zhao Q. et al. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on Hi-C data. Nat Plants. 2019; 5:833-45

[50] Robinson JT, Turner D, Durand NC. et al. Juicebox.Js provides a cloud-based visualization system for hi-C data. Cell Syst. 2018; 6:256-258.e1

[51] Manni M, Berkeley MR, Seppey M. et al. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021; 38:4647-54

[52] Wang Y, Tang H, DeBarry JD. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40:e49-9

[53] Ranallo-Benavidez TR, Jaron KS, Schatz MC. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 2020; 11:1432

[54] Wang L, Sun X, Peng Y. et al. Genomic insights into the origin, adaptive evolution, and herbicide resistance of Leptochloa chinensis, a devastating tetraploid weedy grass in rice fields. Mol Plant. 2022; 15:1045-58

[55] R Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing, 2021

[56] Hibrand Saint-Oyant L, Ruttink T, Hamama L. et al. A high-quality genome sequence of Rosa chinensis to elucidate ornamental traits. Nat Plants. 2018; 4:473-84

[57] VanBuren R, Wai CM, Colle M. et al. A near complete, chromosome-scale assembly of the black raspberry (Rubus occidentalis) genome. Gigascience. 2018;7:giy094

[58] Ireland HS, Wu C, Deng CH. et al. The Gillenia trifoliata genome reveals dynamics correlated with growth and reproduction in Rosaceae. Hortic Res. 2021; 8:233

[59] Khan A, Carey SB, Serrano A. et al. A phased, chromosome-scale genome of ‘Honeycrisp’ apple (Malus domestica). Gigabyte. 2022; 2022:1-15

[60] Zheng T, Li P, Zhuo X. et al. The chromosome-level genome provides insight into the molecular mechanism underlying the tortuous-branch phenotype of Prunus mume. New Phytol. 2022; 235:141-56

[61] Zhang A, Zhou H, Jiang X. et al. The draft genome of a flat peach ( ‘ 124 pan’) provides insights into its good fruit flavor traits. Plan Theory. 2021; 10:538

[62] Linsmith G, Rombauts S, Montanari S. et al. Pseudo-chromosome-length genome assembly of a double haploid “Bartlett” pear (Pyrus communis L.). Gigascience. 2019;8:giz138

[63] Cheng C, Krishnakumar V, Chan AP. et al. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 2017; 89:789-804

[64] Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019; 20:238

[65] Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015; 12:59-60

[66] Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30:772-80

[67] Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009; 25:1972-3

[68] Hoang DT, Chernomor O, von Haeseler A. et al. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018; 35:518-22

[69] Minh BQ, Schmidt HA, Chernomor O. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020; 37:1530-4

[70] Kalyaanamoorthy S, Minh BQ, Wong TKF. et al. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017; 14:587-9

[71] Zhang C, Rabiee M, Sayyari E. et al. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics. 2018; 19:153

[72] Langdon QK, Peris D, Kyle B. et al. sppIDer: a species identification tool to investigate hybrid genomes with high-throughput sequencing. Mol Biol Evol. 2018; 35:2835-49

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

[74] Patterson N, Moorjani P, Luo Y. et al. Ancient admixture in human history. Genetics. 2012; 192:1065-93

[75] Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics. 2009; 25:1754-60

[76] Danecek P, Bonfield JK, Liddle J. et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10:giab008

[77] Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011; 27:2987-93

[78] Danecek P, Auton A, Abecasis G. et al. The variant call format and VCFtools. Bioinformatics. 2011; 27:2156-8

[79] Mendes FK, Vanderpool D, Fulton B. et al. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics. 2021; 36:5516-8

[80] Sanderson MJ. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics. 2003; 19:301-2

[81] Shen W, Le S, Li Y. et al. SeqKit: a cross-platform and ultra-fast toolkit for fasta/q file manipulation. PLoS One. 2016; 11:e0163962

[82] Bu D, Luo H, Huo P. et al. KOBAS-i: intelligent prioritization and exploratory visualization of biological functions for gene enrichment analysis. Nucleic Acids Res. 2021;49:W317-25

[83] Kim D, Paggi JM, Park C. et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37:907-15

[84] Pertea M, Kim D, Pertea GM. et al. Transcript-level expression analysis of RNA-seq experiments with HISAT. StringTie and Ballgown. Nat Protoc. 2016; 11:1650-67

[85] Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15:550