Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Molecular systematics of Rosoideae (Rosaceae)

Abstract

The four-subfamily subdivision of Rosaceae has been recently replaced by a three-subfamily scheme. The re-circumscribed Rosoideae lacks a solid and well-resolved phylogeny on which a classification can be based. In this study, we sampled 56 genera presumably belonging to Rosoideae and 10 genera belonging to other subfamilies or families and used 12 chloroplast regions (matK, rbcL, trnL, trnL–F, ndhF, ycf1, trnC–ycf6, trnS–G, trnS, psbA–trnH, rpoC1 and trnS–ycf9) to reconstruct their phylogeny. Our results confirmed (1) the exclusion of Rhodotypos and Kerria from Rosoideae and their inclusion in the subfamily Amygdaloideae and (2) the exclusion of Chamaebatia, Cercocarpus, Dryas and Purshia (including Cowania) from Rosoideae and their inclusion in Dryadoideae, the sister subfamily of Rosoideae. Within Rosoideae, there are six strongly supported lineages that correspond to six tribes: Ulmarieae, Colurieae, Rubeae, Roseae, Agrimonieae and Potentilleae. We dated the divergence of Rosoideae back to approximately 69.77 million years ago (Mya; 95% HPD = 61.28–78.33 Mya) and that of the tribes within Rosoideae to from 10.42 to 40.02 million years ago (Mya; 95% HPD = 4.73–59.08 Mya). The subfamily is probably of North American and Asian origin and thrives in the northern hemisphere, especially in Asia. After re-circumscriptions of several genera, there are 36 genera recognized in Rosoideae.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Chin SW, Shaw J, Haberle R, Wen J, Potter D (2014) Diversification of almonds, peaches, plums and cherries—molecular systematics and biogeographic history of Prunus (Rosaceae). Molec Phylogen Evol 76:34–48. https://doi.org/10.1016/j.ympev.2014.02.024

  2. 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. Pl Syst Evol 266:45–57. https://doi.org/10.1007/s00606-007-0540-3

  3. Dobes C, Paule J (2010) A comprehensive chloroplast DNA-based phylogeny of the genus Potentilla (Rosaceae): Implications for its geographic origin, phylogeography and generic circumscription. Molec Phylogen Evol 56:156–175. https://doi.org/10.1016/j.ympev.2010.03.005

  4. Dong W, Liu J, Yu J, Wang L, Zhou S (2012) Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS ONE 7:e35071. https://doi.org/10.1371/journal.pone.0035071

  5. Dong W, Cheng T, Li C, Xu C, Long P, Chen C, Zhou S (2014) Discriminating plants using the DNA barcode rbcLb: an appraisal based on a large data set. Molec Ecol Resources 14:336–343. https://doi.org/10.1111/1755-0998.12185

  6. Dong W, Xu C, Li C, Sun J, Zuo Y, Shi S, Cheng T, Guo J, Zhou S (2015) ycf1, the most promising plastid DNA barcode of land plants. Sci Rep 5:8348. https://doi.org/10.1038/srep08348

  7. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molec Biol Evol 29:1969–1973. https://doi.org/10.1093/molbev/mss075

  8. Edelman DW (1975) The Eocene Germer Basin flora of south-central Idaho. MSc Thesis, University of Idaho, Moscow

  9. 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). Pl Syst Evol 211:155–179. https://doi.org/10.1007/bf00985357

  10. Eriksson T, Hibbs MS, Yoder AD, Delwiche CF, Donoghue MJ (2003) The phylogeny of Rosoideae (Rosaceae) based on sequences of the internal transcribed spacers (ITS) of nuclear ribosomal DNA and the trnL/F region of chloroplast DNA. Int J Pl Sci 164:197–211. https://doi.org/10.1086/346163

  11. Eriksson T, Lundberg M, Töpel M, Östensson P, Smedmark JEE (2014) Sibbaldia: a molecular phylogenetic study of a remarkably polyphyletic genus in Rosaceae. Pl Syst Evol 301:171–184. https://doi.org/10.1007/s00606-014-1063-3

  12. Evanhoff E, Gregory-Wodzicki KM, Johnson KR (2001) Fossil flora and stratigraphy of the Florissant Formation, Colorado. Denver Museum of Nature & Science, Denver

  13. Gardens RB (2007) DNA barcoding. Available at: http://www.kew.org/barcoding/protocols.html. Accessed 21 Apr 2014

  14. Gehrke B, Brauchler C, Romoleroux K, Lundberg M, Heubl G, Eriksson T (2008) Molecular phylogenetics of Alchemilla, Aphanes and Lachemilla (Rosaceae) inferred from plastid and nuclear intron and spacer DNA sequences, with comments on generic classification. Molec Phylogen Evol 47:1030–1044. https://doi.org/10.1016/j.ympev.2008.03.004

  15. Hillis DM (1998) Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst Biol 47:3–8. https://doi.org/10.1080/106351598260987

  16. Hutchinson J (1964) The genera of flowering plants. Clarendon Press, Oxford

  17. Kalkman C (2004) Rosaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer, Berlin, pp 343–386. https://doi.org/10.1007/978-3-662-07257-8

  18. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molec Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

  19. Lavin M, Luckow M (1993) Origins and relationships of tropical North America in the context of the boreotropics hypothesis. Amer J Bot 80:1–14. https://doi.org/10.1002/j.1537-2197.1993.tb13761.x

  20. Li H-L (1952) Floristic relationships between eastern Asia and eastern North. Trans Amer Philos Soc 42:371–429. https://doi.org/10.2307/1005654

  21. Li J, Wang S, Yu J, Wang L, Zhou S (2013) A modified CTAB protocol for Plant DNA extraction. Chin Bull Bot 48:72–78. https://doi.org/10.3724/SP.J.1259.2013.00072

  22. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

  23. Lu L, Gu C, Li C, Alexander C, Bartholomew B, Brach AR, Boufford DE, Ikeda H, Ohba H, Robertson KR, Spongberg SA (2003) Rosaceae. In: Wu Z, Raven PH, Hong D (eds) Flora of China. Science Press/Missouri Botanical Garden Press, Beijing/St.Louis, pp 46–434

  24. MacGinite HD (1953) Fossil plants of the Florissant beds of Colorado. Carnegie Institute of Washington, Washington, DC

  25. McInerney FA, Wing SL (2011) The Paleocene-Eocene Thermal Maximum: a perturbation of carbon cycle, climate, and biosphere with implications for the future. Annual Rev Earth Planet Sci 39:489–516. https://doi.org/10.1146/annurev-earth-040610-133431

  26. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE). IEEE, New Orleans, pp 1–8

  27. Morgan DR, Soltis DE, Robertson KR (1994) Systematic and evolutionary implications of rbcL sequence variation in Rosaceae. Amer J Bot 81:890–903. https://doi.org/10.1002/j.1537-2197.1994.tb15570.x

  28. Morley RJ (1999) Origin and evolution of tropical rain forests. Wiley, Chichester

  29. Paule J, Soják J (2009) Taxonomic comments on the genus Sibbaldiopsis Rydb. (Rosaceae). J Natl Mus (Pragus) Nat Hist Ser 178:15–16

  30. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. https://doi.org/10.1080/10635150490522304

  31. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. https://doi.org/10.1093/bioinformatics/14.9.817

  32. Potter D, Gao F, Bortiri PE, Oh SH, Baggett S (2002) Phylogenetic relationships in Rosaceae inferred from chloroplast matK and trnL-trnF nucleotide sequence data. Pl Syst Evol 231:77–89. https://doi.org/10.1007/s006060200012

  33. Potter D, Eriksson T, Evans RC, Oh S, Smedmark JEE, Morgan DR, Kerr M, Robertson KR, Arsenault M, Dickinson TA, Campbell CS (2007) Phylogeny and classification of Rosaceae. Pl Syst Evol 266:5–43. https://doi.org/10.1007/s00606-007-0539-9

  34. Rambaut A (2002) Se-Al, sequence alignment editor v2.0a ll [online]. Available at: http://tree.bio.ed.ac.uk/software/seal/

  35. Rambaut A, Drummond AJ (2009) Tracer: MCMC trace analysis tool, version 1.5.0. Available at: http://tree.bio.ed.ac.uk/software/tracer/. Accessed 19 May 2014

  36. Rambaut A, Drummond AJ (2010a) LogCombiner: MCMC output combiner, version 1.5.4. University of Edinburgh, Institute of Evolutionary Biology

  37. Rambaut A, Drummond AJ (2010b) TreeAnnotator: MCMC output analysis, version 1.5.4. University of Edinburgh, Institute of Evolutionary Biology

  38. Raven PH (1972) Plant species disjunctions: a summary. Ann Missouri Bot Gard 59:234–246. https://doi.org/10.2307/2394756

  39. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

  40. Schulze-Menz GK (1964) Rosaceae. In: Melchior H (ed) In Engler’s Syllabus der Pflanzenfamilien Gebruder. Borntraeger, Berlin, pp 209–218

  41. Smedmark JEE, Eriksson T (2002) Phylogenetic relationships of Geum (Rosaceae) and relatives inferred from the nrITS and trnL-trnF regions. Syst Bot 27:303–317. https://doi.org/10.1043/0363-6445-27.2.303

  42. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

  43. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland. https://doi.org/10.1002/0471650129.dob0522

  44. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152

  45. Takhtajan A (1997) Diversity and classification of flowering plants. Columbia University Press, New York

  46. Thorne RF (1972) Major disjunctions in the geographic ranges of seed plants. Quatern Rev Biol 47:365–411. https://doi.org/10.2307/2820737

  47. Tiffney BH (1985a) The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. J Arnold Arbor 66:243–273. https://doi.org/10.5962/bhl.part.13183

  48. Tiffney BH (1985b) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J Arnold Arbor 66:73–94. https://doi.org/10.5962/bhl.part.13179

  49. Tiffney BH, Manchester SR (2001) The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere Tertiary. Int J Pl Sci 162:S3–S17. https://doi.org/10.1086/323880

  50. Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, Davis CC, Latvis M, Manchester SR, Soltis DE (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106:3853–3858. https://doi.org/10.1073/pnas.0813376106

  51. Wen J (1998) Evolution of the eastern Asian and eastern North American disjunct pattern: insights from phylogenetic studies. Korean J Pl Tax 28:63–81. https://doi.org/10.11110/kjpt.1998.28.1.063

  52. Wen J (1999) Evolution of eastern Asian and eastern North America disjunct pattern in flowering plants. Annual Rev Ecol Syst 30:421–455. https://doi.org/10.2307/221691

  53. Wen J, Ickert-Bond S, Nie ZL, Li R (2010) Timing and modes of evolution of eastern Asian—North America biogeographic disjunctions in seed plants. In: Long M, Gu H, Zhou Z (eds) Darwin’s heritage today—proceedings of the Darwin 200 Beijing international conference. Higher Education Press, Beijing, pp 252–269

  54. Wolfe JA (1975) Some aspects of plant geography of the Northern hemisphere during the late cretaceous and tertiary. Ann Missouri Bot Gard 62:264–279. https://doi.org/10.2307/2395198

  55. Xiang Q-Y, Soltis DE (2001) Dispersal-vicariance analyses of intercontinental disjuncts: historical biogeographical implications for angiosperms in the Northern hemisphere. Int J Pl Sci 162:S29–S39. https://doi.org/10.1086/323332

  56. Xiang QY, Soltis DE, Soltis PS, Manchester SR, Crawford DJ (2000) Timing the eastern Asian–eastern North American floristic disjunction: molecular clock corroborates paleontological estimates. Molec Phylogen Evol 15:462–472. https://doi.org/10.1006/mpev.2000.0766

  57. Xiang Y, Huang CH, Hu Y, Wen J, Li S, Yi T, Chen H, Xiang J, Ma H (2017) Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Molec Biol Evol 34:262–281. https://doi.org/10.1093/molbev/msw242

  58. Yu Y, Harris AJ, He X (2010) S-DIVA (statistical dispersal-vicariance analysis): a tool for inferring biogeographic histories. Molec Phylogen Evol 56:848–850. https://doi.org/10.1016/j.ympev.2010.04.011

  59. Yu J, Xue J-H, Zhou S-L (2011) New universal matK primers for DNA barcoding angiosperms. J Syst Evol 49:176–181. https://doi.org/10.1111/j.1759-6831.2011.00134.x

  60. Yu Y, Harris AJ, Blair C, He X (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Molec Phylogen Evol 87:46–49. https://doi.org/10.1016/j.ympev.2015.03.008

  61. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693. https://doi.org/10.1126/science.1059412

  62. Zhang SD, Jin JJ, Chen SY, Chase MW, Soltis DE, Li HT, Yang JB, Li DZ, Yi TS (2017) Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics. New Phytol 214:1355–1367. https://doi.org/10.1111/nph.14461

Download references

Acknowledgements

We thank Dr. Guojin Zhang and Dr. Bao Nie for their help in the molecular dating and historical biogeography analyses. This study was partly supported by funds from National Natural Science Foundation of China (NSFC31872679), Chinese Academy of Sciences (CAS) Biodiversity Conservation and the Collaborative Innovation Plan, Institute of Forensic Science, Ministry of Public Security, China (2016XTCX01).

Author information

Correspondence to Xueying Yang or Ling Wang or Shiliang Zhou.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests.

Additional information

Publisher's Note

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

Handling Editor: Christian Parisod.

Electronic supplementary material

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Material list and newly produced sequences in this study.

Online Resource 2. Primers and procedures used to amplify DNA fragments.

Online Resource 3. Taxa and GenBank accessions used in this study.

Online Resource 4. Detailed Fig. 2 of chronogram of Rosaceae based on partition of 12 cpDNA regions derived from BEAST. Numbers at nodes are divergence time of clades.

Online Resource 5. Geographical distributions of extant species in Rosoideae used in this study.

Online Resource 6. Detailed Fig. 1 of maximum likelihood phylogram of Rosoideae based on 12 cpDNA regions of all taxa. Numeric values at nodes indicate 23 maximum likelihood bootstrap values.

Online Resource 7. Detailed Fig. 1 of BI tree of Rosoideae based on 12 cpDNA regions of all taxa. Numbers at the nodes are Bayesian posterior probabilities and PP values ≥0.50 are shown

Online Resource 8. Detailed Fig. 1 of maximum parsimony tree of Rosoideae based on 12 cpDNA regions of all taxa. Numbers at the nodes are bootstrap values, and BP values ≥50 are shown.

Online Resource 9. Detailed Fig. 3 of ancestral area reconstruction of Rosoideae inferred by S-DIVA. Numbers at the nodes are Bayesian posterior probabilities obtained from the BEAST tree.

Online Resource 10. Sequence matrix A containing 12 chloroplast regions of 169 taxa for phylogenetic analyses.

Online Resource 11. Sequence matrix B containing 12 chloroplast regions of 130 taxa for molecular dating and biogeographical analyses.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, X., Li, J., Cheng, T. et al. Molecular systematics of Rosoideae (Rosaceae). Plant Syst Evol 306, 9 (2020). https://doi.org/10.1007/s00606-020-01629-z

Download citation

Keywords

  • Biogeography
  • Divergence times
  • Phylogeny
  • Rosoideae