Phylogenetics of Fragaria, Rubus and Related Taxa

  • Maria Kinga SobczykEmail author
Part of the Compendium of Plant Genomes book series (CPG)


Fragaria L. and Rubus L. are two Rosaceae genera with strikingly different levels of taxonomic diversity (20 vs. ~500 species, respectively), yet with similar processes likely at play in their evolution—polyploidisation, hybridisation and apomixis. Each genus contains important soft fruit crops—garden strawberry in Fragaria, red raspberry and blackberries in Rubus. Furthermore, congeneric wild species have been used as a source of agronomically beneficial alleles. Both Rubus and Fragaria display well-supported monophyly, but resolution below the subgenus level in Rubus and beyond the two main clades in Fragaria is limited. More comprehensive sampling of plant genomes at a population level combined with more sophisticated models of phylogenetic inference is required for complete detangling of the reticulate genealogies in Fragaria and Rubus.


  1. Alice LA, Campbell CS (1999) Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Am J Bot 86:81–97CrossRefPubMedGoogle Scholar
  2. Alice LA, Dodson TM, Sutherland BL (2008) Diversity and relationships of Bhutanese Rubus (Rosaceae). Acta Hortic 777:63–69.
  3. Alice LA, Eriksson T, Eriksen B et al (2001) Hybridization and gene flow between distantly related species of Rubus (Rosaceae): evidence from nuclear ribosomal DNA internal transcribed spacer region sequences. Syst Bot 26:769–778Google Scholar
  4. Amsellem L, Noyer J-L, Hossaert-McKey M (2001) Evidence for a switch in the reproductive biology of Rubus alceifolius (Rosaceae) towards apomixis, between its native range and its area of introduction. Am J Bot 88:2243–2251CrossRefPubMedGoogle Scholar
  5. Bors RH, Sullivan JA (2005a) Interspecific hybridization of Fragaria moschata with two diploid species, F. nubicola and F. viridis. Euphytica 143:201–207CrossRefGoogle Scholar
  6. Bors RH, Sullivan JA (2005b) Interspecific hybridization of Fragaria vesca subspecies with F. nilgerrensis, F. nubicola, F. pentaphylla, and F. viridis. J Am Soc Hortic Sci 130:418–423Google Scholar
  7. Briggs JB, Danek J, Lyth M et al (1982) Resistance to the raspberry beetle, Byturus tomentosus, in Rubus species and their hybrid derivatives with R. idaeus. J Hort Sci 57:73–78CrossRefGoogle Scholar
  8. Bringhurst RS (1990) Cytogenetics and evolution in American Fragaria. HortScience 25:879–881Google Scholar
  9. Bringhurst RS, Gill T (1970) Origin of Fragaria polyploids. II. Unreduced and doubled-unreduced gametes. Am J Bot 57:969–976CrossRefGoogle Scholar
  10. Bringhurst RS, Khan DA (1963) Natural pentaploid Fragaria chiloensis-F. vesca hybrids in coastal California and their significance in polyploid Fragaria evolution. Am J Bot 50:658–661CrossRefGoogle Scholar
  11. Caplan JS, Yeakley JA (2010) Water relations advantages for invasive Rubus armeniacus over two native ruderal congeners. Plant Ecol 210:169–179CrossRefGoogle Scholar
  12. Clark LV, Jasieniuk M (2012) Spontaneous hybrids between native and exotic Rubus in the Western United States produce offspring both by apomixis and by sexual recombination. Heredity 109:320–328CrossRefPubMedPubMedCentralGoogle Scholar
  13. Clark JR, Stafne ET, Hall HK et al (2011) Blackberry breeding and genetics. Fruit Veg Cereal Sci Biotechnol 5:27–43Google Scholar
  14. Clark LV, Evans KJ, Jasieniuk M (2013) Origins and distribution of invasive Rubus fruticosus L. agg. (Rosaceae) clones in the Western United States. Biol Invasions 15:1331–1342CrossRefGoogle Scholar
  15. Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24:332–340CrossRefPubMedGoogle Scholar
  16. DeVore ML, Pigg KB (2007) A brief review of the fossil history of the family Rosaceae with a focus on the Eocene Okanogan Highlands of eastern Washington State, USA, and British Columbia, Canada. Plant Syst Evol 266:45–57CrossRefGoogle Scholar
  17. Dickinson TA, Lo E, Talent N (2007) Polyploidy, reproductive biology, and Rosaceae: understanding evolution and making classifications. Plant Syst Evol 266:59–78CrossRefGoogle Scholar
  18. DiMeglio LM, Staudt G, Yu H et al (2014) A phylogenetic analysis of the genus Fragaria (strawberry) using intron-containing sequence from the ADH-1 gene. PLoS ONE 9:e102237CrossRefPubMedPubMedCentralGoogle Scholar
  19. Eriksson T, Donoghue MJ, Hibbs MS (1998) Phylogenetic analysis of Potentilla using DNA sequences of nuclear ribosomal internal transcribed spacers (ITS), and implications for the classification of Rosoideae (Rosaceae). Plant Syst Evol 211:155–179CrossRefGoogle Scholar
  20. Evans KJ, Symon DE, Whalen MA et al (2007) Systematics of the Rubus fruticosus aggregate (Rosaceae) and other exotic Rubus taxa in Australia. Aust Syst Bot 20:187–251CrossRefGoogle Scholar
  21. Focke WO (1914) Species Ruborum. Monographiae Generis Rubi Prodromus part I. Schweizerbart, StuttgartGoogle Scholar
  22. Folta KM, Davis TM (2006) Strawberry genes and genomics. Crit Rev Plant Sci 25:399–415CrossRefGoogle Scholar
  23. Govindarajulu R, Parks M, Tennessen JA et al (2015) Comparison of nuclear, plastid, and mitochondrial phylogenies and the origin of wild octoploid strawberry species. Am J Bot 102:544–554CrossRefPubMedGoogle Scholar
  24. Gu Y, Wang C, Zhao C et al (1995) Evaluation of Rubus genetic resources. J Plant Resour Environ 5:6–13Google Scholar
  25. Harrison RE, Luby JJ, Furnier GR (1997) Chloroplast DNA restriction fragment variation among strawberry (Fragaria spp.) taxa. J Am Soc Hortic Sci 122:63–68Google Scholar
  26. Hokanson KE, Smith MJ, Connor AM et al (2006) Relationships among subspecies of New World octoploid strawberry species, Fragaria virginiana and Fragaria chiloensis, based on simple sequence repeat marker analysis. Can J Bot 84:1829–1841CrossRefGoogle Scholar
  27. Howarth DG, Gardner DE, Morden CW (1997) Phylogeny of Rubus subgenus Idaeobatus (Rosaceae) and its implications toward colonization of the Hawaiian Islands. Syst Bot 22:433–441CrossRefGoogle Scholar
  28. Hummer KE (2012) A new species of Fragaria (Rosaceae) from Oregon. J Bot Res Inst Texas 6:9–15Google Scholar
  29. Hummer KE, Nathewet P, Yanagi T (2009) Decaploidy in Fragaria iturupensis (Rosaceae). Am J Bot 96:713–716CrossRefPubMedGoogle Scholar
  30. Hummer KE, Bassil N, Njuguna W (2011) Genomic and breeding resources. In: Kole C (ed) Wild crop relatives. Springer, Berlin, pp 17–44CrossRefGoogle Scholar
  31. Illa E, Sargent DJ, Girona EL et al (2011) Comparative analysis of rosaceous genomes and the reconstruction of a putative ancestral genome for the family. BMC Evol Biol 11:9CrossRefPubMedPubMedCentralGoogle Scholar
  32. Jennings DL (1988) Raspberries and blackberries: their breeding, diseases and growth. Academic Press, LondonGoogle Scholar
  33. Kalkman C (2004) Flowering plants—dicotyledons. The families and genera of vascular plants, vol 6. Springer, Berlin, pp 343–386Google Scholar
  34. Kamneva OK, Syring J, Liston A et al (2017) Evaluating allopolyploid origins in strawberries (Fragaria) using haplotypes generated from target capture sequencing. BMC Evol Biol 17:180CrossRefPubMedPubMedCentralGoogle Scholar
  35. Keep E, Knight VH, Parker JH (1977) Rubus coreanus as donor of resistance to cane diseases and mildew in red raspberry breeding. Euphytica 26:505–510CrossRefGoogle Scholar
  36. Korpelainen H, Antonius-Klemola K, Werlemark G (1999) Clonal structure of Rubus chamaemorus populations: comparison of different molecular methods. Plant Ecol 143:123–128CrossRefGoogle Scholar
  37. Kraft T, Nybom H, Werlemark G (1995) Rubus vestervicensis (Rosaceae)—its hybrid origin revealed by DNA fingerprinting. Nord J Bot 15:237–242CrossRefGoogle Scholar
  38. Lin J, Davis TM (2000) S1 analysis of long PCR heteroduplexes: detection of chloroplast indel polymorphisms in Fragaria. Theor Appl Genet 101:415–420CrossRefGoogle Scholar
  39. Liston A, Cronn R, Ashman TL (2014) Fragaria: a genus with deep historical roots and ripe for evolutionary and ecological insights. Am J Bot 101:1686–1699CrossRefPubMedGoogle Scholar
  40. Lu LD (1983) A study on the genus Rubus of China. J Syst Evol 21:13–25Google Scholar
  41. Lu LD, Boufford DE (2003) Rosaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 9. Missouri Botanical Garden Press, St. Louis, pp 195–285Google Scholar
  42. Lundberg M, Töpel M, Eriksen B et al (2009) Allopolyploidy in Fragariinae (Rosaceae): comparing four DNA sequence regions, with comments on classification. Mol Phylogenet Evol 51:269–280CrossRefPubMedGoogle Scholar
  43. Mahoney LL, Quimby ML, Shields ME et al (2009) Mitochondrial DNA transmission, ancestry, and sequences in Fragaria. Acta Hort 859:301–308Google Scholar
  44. Meng R, Finn C (2002) Determining ploidy level and nuclear DNA content in Rubus by flow cytometry. J Am Soc Hort Sci 127:767–775Google Scholar
  45. Mimura M, Mishima M, Lascoux M et al (2014) Range shift and introgression of the rear and leading populations in two ecologically distinct Rubus species. BMC Evol Biol 14:1CrossRefGoogle Scholar
  46. Miyashita T, Kunitake H, Yotsukura N et al (2015) Assessment of genetic relationships among cultivated and wild Rubus accessions using AFLP markers. Sci Hort 193:165–173CrossRefGoogle Scholar
  47. Morden CW, Gardner DE, Weniger DA (2003) Phylogeny and biogeography of Pacific Rubus subgenus Idaeobatus (Rosaceae) species: investigating the origin of the endemic Hawaiian raspberry R. macraei. Pacific Sci 57:181–197CrossRefGoogle Scholar
  48. Morgan R (1994) Systematic and evolutionary implications of rbcl sequence variation in Rosaceae. Am J Bot 81:890–903CrossRefGoogle Scholar
  49. Morrison DA (2014) Is the tree of life the best metaphor, model, or heuristic for phylogenetics? Syst Biol 63:628–638CrossRefPubMedGoogle Scholar
  50. Naruhashi N, Iwatsubo Y, Peng C-I (2002) Chromosome numbers in Rubus (Rosaceae) of Taiwan. Bot Bull Acad Sin 43:193–201Google Scholar
  51. Njuguna W, Liston A, Cronn R et al (2013) Insights into phylogeny, sex function and age of Fragaria based on whole chloroplast genome sequencing. Mol Phylogenet Evol 66:17–29CrossRefPubMedGoogle Scholar
  52. Noguchi Y, Mochizuki T, Sone K (2002) Breeding of a new aromatic strawberry by interspecific hybridization Fragaria × ananassa × F. nilgerrensis. J Jpn Soc Hortic Sci 71:208–213CrossRefGoogle Scholar
  53. Nybom H, Schaal BA (1990) DNA‘ fingerprints’ reveal genotypic distributions in natural populations of blackberries and raspberries (Rubus, Rosaceae). Am J Bot 77:883–888CrossRefGoogle Scholar
  54. Potter D, Luby JJ, Harrison RE (2000) Phylogenetic relationships among species of Fragaria (Rosaceae) inferred from non-coding nuclear and chloroplast DNA sequences. Syst Bot 25:337CrossRefGoogle Scholar
  55. Potter D, Gao F, Bortiri EP et al (2002) Phylogenetic relationships in Rosaceae inferred from chloroplast matK and trnL-trnF nucleotide sequence data. Plant Syst Evol 231:77–89CrossRefGoogle Scholar
  56. Potter D, Eriksson T, Evans RC et al (2007) Phylogeny and classification of Rosaceae. Plant Syst Evol 266:5–43CrossRefGoogle Scholar
  57. Qiao Q, Xue Li, Wang Q et al (2016) Comparative transcriptomics of strawberries (Fragaria spp.) provides insights into evolutionary patterns. Front Plant Sci 7:1–10Google Scholar
  58. Rousseau-Gueutin M, Lerceteau-Köhler E, Barrot L et al (2008) Comparative genetic mapping between octoploid and diploid Fragaria species reveals a high level of colinearity between their genomes and the essentially disomic behavior of the cultivated octoploid strawberry. Genetics 179:2045–2060CrossRefPubMedPubMedCentralGoogle Scholar
  59. Rousseau-Gueutin M, Gaston A, Aïnouche A et al (2009) Tracking the evolutionary history of polyploidy in Fragaria L. (strawberry): new insights from phylogenetic analyses of low-copy nuclear genes. Mol Phylogenet Evol 51:515–530CrossRefPubMedGoogle Scholar
  60. Sargent DJ (2005) A genetic investigation of diploid Fragaria. University of ReadingGoogle Scholar
  61. Sargent DJ, Geibel M, Hawkins JA et al (2004) Quantitative and qualitative differences in morphological traits revealed between diploid Fragaria species. Ann Bot 94:787–796CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sargent DJ, Yang Y, Šurbanovski N et al (2015) HaploSNP affinities and linkage map positions illuminate subgenome composition in the octoploid, cultivated strawberry (Fragaria × ananassa). Plant Sci 242:140–150CrossRefPubMedGoogle Scholar
  63. Šarhanová P, Sharbel TF, Sochor M et al (2017) Hybridization drives evolution of apomicts in Rubus subgenus Rubus: evidence from microsatellite markers. Ann Bot 120:317–328CrossRefPubMedPubMedCentralGoogle Scholar
  64. Schulze-Menz GK (1964) Rosaceae. Gebru der Borntraeger, StuttgartGoogle Scholar
  65. Sochor M, Vašut RJ, Sharbel TF et al (2015) How just a few makes a lot: Speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae). Mol Phylogenet Evol 89:13–27CrossRefPubMedGoogle Scholar
  66. Staudt G (2008) Strawberry biogeography, genetics and systematics. Acta Hort 842:71–84Google Scholar
  67. Staudt G, Dickoré WB (2001) Notes on Asiatic Fragaria species: Fragaria pentaphylla Losinsk. and Fragaria tibetica spec. nov. Bot Jahrbücher 123:341–354Google Scholar
  68. Staudt G, Olbricht K (2008) Notes on Asiatic Fragaria species V: F. nipponica and F. iturupensis. Bot Jahrbücher 127:317–341CrossRefGoogle Scholar
  69. Tennessen JA, Govindarajulu R, Ashman T-L et al (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol Evol 6:3295–3313CrossRefPubMedPubMedCentralGoogle Scholar
  70. Thompson MM (1995) Chromosome numbers of Rubus species at the national clonal germplasm repository. HortScience 30:1447–1452Google Scholar
  71. Thompson MM (1997) Survey of chromosome numbers in Rubus (Rosaceae: Rosoideae). Ann Missouri Bot Gard 84:128–164CrossRefGoogle Scholar
  72. Vamosi JC, Dickinson TA (2006) Polyploidy and diversification: a phylogenetic investigation in Rosaceae. Int J Plant Sci 167:349–358CrossRefGoogle Scholar
  73. Wang X-R, Tang H-R, Duan J et al (2008) A comparative study on karyotypes of 28 taxa in Rubus sect. Idaeobatus and sect. Malachobatus (Rosaceae) from China. J Syst Evol 46:505–515Google Scholar
  74. Wang X, Liu Y, Zhong B et al (2010) Cytological and RAPD data revealed genetic relationships among nine selected populations of the wild bramble species, Rubus parvifolius and R. coreanus (Rosaceae). Genet Resour Crop Evol 57:431–441CrossRefGoogle Scholar
  75. Wang Y, Wang X, Chen Q et al (2015) Phylogenetic insight into subgenera Idaeobatus and Malachobatus (Rubus, Rosaceae) inferring from ISH analysis. Mol Cytogenet 8:11CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wang Y, Chen Q, Chen T et al (2016) Phylogenetic insights into Chinese Rubus (Rosaceae) from multiple chloroplast and nuclear DNAs. Front Plant Sci 7:1–13PubMedPubMedCentralGoogle Scholar
  77. Weber HE (1996) Former and modern taxonomic treatment of the apomictic Rubus complex. Folia Geobot 31:373–380CrossRefGoogle Scholar
  78. Wei N, Tennessen JA, Liston A et al (2017) Present-day sympatry belies the evolutionary origin of a high-order polyploid. New Phytol 216:279–290CrossRefPubMedPubMedCentralGoogle Scholar
  79. Xiang Y, Huang C-H, Hu Y et al (2017) Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Mol Biol Evol 34:262–281PubMedGoogle Scholar
  80. Yang Y, Davis TM (2017) A new perspective on polyploid Fragaria (strawberry) genome composition based on large-scale, multi-locus phylogenetic analysis. Genome Biol EvolCrossRefPubMedPubMedCentralGoogle Scholar
  81. Yang JY, Pak J-H (2006) Phylogeny of Korean Rubus (Rosaceae) based on ITS (nrDNA) and trnL/F intergenic region (cpDNA). J Plant Biol 49:44–54CrossRefGoogle Scholar
  82. Yü DJ, Lu LD, Gu CZ et al (1985) Rosaceae. In: Flora Republicae Popularis Sinicae, vol 38. Science Press, pp 10–218Google Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.NIAB EMREast MallingUK

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