Skip to main content
Log in

Non-monophyly of Primula subgenera Auganthus and Carolinella (Primlaceae) as confirmed by the nuclear DNA sequence variation

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

An earlier molecular phylogenetic analysis using cpDNA sequence data revealed the non-monophyly of Primula subgenera Auganthus and Carolinella, and the evolutionary implication of the infrageneric division of these two groups remains uncertain. In the present study, 130 new sequences were newly analyzed, with the combination of plastid genes and nrDNA ITS regions through maximum parsimony and Bayesian inference analyses. It confirms that neither subgenus Auganthus nor subgenus Carolinella is monophyletic in its current circumscription. The calyptrate capsule, a diagnostic character for subgenus Carolinella, may have evolved multiple times in Primula. Subgenus Auganthus would be a natural group only with inclusion of subgenus Carolinella and exclusion of P. aromatica. The positions of some infrageneric groups are clarified, but challenges remain regarding relevant morphological characters for sectional delimitations within subgenus Auganthus.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alvarez IA, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogen Evol 29:417–434

    Article  CAS  Google Scholar 

  • Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Missouri Bot Gard 82:247–277

    Article  Google Scholar 

  • Chemisquy MA, Morrone O (2012) Molecular phylogeny of Gavilea (Chloraeinae: Orchidaceae) using plastid and nuclear markers. Molec Phylogen Evol 62:889–897

    Article  Google Scholar 

  • Cunningham CW (1997) Is congruence between data partitions a reliable predictor of phylogenetic accuracy? Empirically testing an iterative procedure for choosing among phylogenetic methods. Syst Bot 46:464–478

    CAS  Google Scholar 

  • Darlu P, Lecointre G (2002) When does the incongruence length difference test fail? Molec Biol Evol 2:432–437

    Article  Google Scholar 

  • de Queiroz A (1993) For consensus (sometimes). Syst Biol 42:368–372

    Article  Google Scholar 

  • de Vos JM, Wüest RO, Conti E (2013) Small and ugly? Phylogenetic analyses of the “selfing syndrome” reveal complex evolutionary fates of monomorphic primrose flowers. Evolution 68:1042–1057

    Article  Google Scholar 

  • de Vos JM, Hughes CE, Schneeweiss GM, Moore BR, Conti E (2014) Heterostyly accelerates diversification via reduced extinction in primroses. Proc Roy Soc B 281:20140075

    Article  Google Scholar 

  • Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24:332–340

    Article  PubMed  Google Scholar 

  • Degtjareva GV, Valiejo-Roman CM, Samigullin TH, Guara-Requena M, Sokoloff DD (2012) Phylogenetics of Anthyllis (Leguminosae: Papilionoideae: Loteae): Partial incongruence between nuclear and plastid markers, a long branch problem and implications for morphological evolution. Molec Phylogen Evol 62:693–707

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation method for small quantities of fresh tissues. Phytochem Bull 19:11–15

    Google Scholar 

  • Fehrer J, Gemeinholzer B, Chrtek JC, Bräutigam S (2007) Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Molec Phylogen Evol 42:347–361

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gong X, Fang RC (2003) Primula calyptrata, a new species in section Carolinella (Primulaceae) from Yunnan, China. Novon 13:193–195

    Article  Google Scholar 

  • Hipp AL, Hall JC, Sytsma KJ (2004) Congruence versus phylogenetic accuracy: revisiting the incongruence length difference test. Syst Bot 53:81–89

    Google Scholar 

  • Hu CM (1990a) Primula. In: Chen FH, Hu CM (eds) Flora Reipublicae Popularis Sinicae, vol 59(2). Science Press, Beijing, pp 1–277

    Google Scholar 

  • Hu CM (1990b) A new species of Primula from Thailand with critical notes on the section Carolinella. Nord J Bot 10:399–401

    Article  Google Scholar 

  • Hu CM, Kelso S (1996) Primulaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 15. Science Press/Missouri Botanical Garden Press, Beijing/St. Louis, pp 99–185

    Google Scholar 

  • Källersjö M, Bergqvist G, Anderberg AA (2000) Generic realignment in Primuloid families of the Ericales s.l.: a phylogenetic analysis based on DNA sequences from three chloroplast genes and morphology. Amer J Bot 87:1325–1341

    Article  Google Scholar 

  • Kim ST, Donoghue MJ (2008) Incongruence between cpDNA and nrITS trees indicates extensive hybridization within Eupersicaria (Polygonaceae). Amer J Bot 95:1122–1135

    Article  CAS  Google Scholar 

  • Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50:913–925

    Article  CAS  PubMed  Google Scholar 

  • Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536

    Article  Google Scholar 

  • Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30

    Article  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2014) Mesquite: a modular system for evolutionary analysis. Version 3.01. Available at http://mesquiteproject.org

  • Mast AR, Richards AJ, Lang DJ, Feller DMS, Conti E (2001) Phylogenetic relationships in Primula L. and related genera (Primulaceae) based on noncoding chloroplast DNA. Int J Pl Sci 162:1381–1400

    Article  CAS  Google Scholar 

  • Mast AR, Kelso S, Conti E (2006) Are any primroses (Primula) primitively monomorphic? New Phytol 171:605–616

    Article  CAS  PubMed  Google Scholar 

  • Nylander JA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583

    Article  CAS  PubMed  Google Scholar 

  • Pelser PB, Kennedy AH, Tepe EJ, Shidler JB, Nordenstam B, Kadereit JW, Watson LE (2010) Patterns and causes of incongruence between plastid and nuclear Senecioneae (Asteraceae) phylogenies. Amer J Bot 97:856–873

    Article  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 9:817–818

    Article  Google Scholar 

  • 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 25:337–348

    Article  Google Scholar 

  • Rambaut A, Suchard M, Drummond A (2013) Tracer. Version 1.6. Available at http://tree.bio.ed.ac.uk/software/tracer/

  • Resetnik I, Satovic Z, Schneeweiss GM, Liber Z (2013) Phylogenetic relationships in Brassicaceae tribe Alysseae inferred from nuclear ribosomal and chloroplast DNA sequence data. Molec Phylogen Evol 69:772–786

    Article  Google Scholar 

  • Richards AJ (1993) Primula. B. T. Batsford Ltd., London, pp 1–299

    Google Scholar 

  • Richards AJ (2002) Primula, 2nd edn. B.T. Batsford Ltd, London, pp 1–346

    Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed Central  PubMed  Google Scholar 

  • Schmidt-Lebuhn AN, de Vos JM, Keller B, Conti E (2012) Phylogenetic analysis of Primula section Primula reveals rampant non-monophyly among morphologically distinct species. Molec Phylogen Evol 65:23–34

    Article  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molec Biol Evol 16:1114–1116

    Article  CAS  Google Scholar 

  • Smith WW, Fletcher HR (1946) The genus Primula: sections Obconica, Sinenses, Reinii, Pinnatae, Malacoides, Bullatae, Carolinella, Grandis and Denticulata. T Roy Soc Edin 61:415–478

    Article  Google Scholar 

  • Smith WW, Forrest G, Fletcher HR (1941–1949) (facsimile reprint 1977) The genus Primula. Plant Monograph Reprints 11:1–835

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (and other methods). Version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

  • Thomson JD, Gibson TJ, Plewniak F (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  Google Scholar 

  • Trift I, Källersjö M, Anderberg AA (2002) The monophyly of Primula (Primulaceae). Syst Bot 27:396–407

    Google Scholar 

  • Tsutsui K, Suwa A, Sawada K, Kato T, Ohsawa TA, Watano Y (2009) Incongruence among mitochondrial, chloroplast and nuclear gene trees in Pinus subgenus Strobus (Pinaceae). J Pl Res 122:509–521

    Article  CAS  Google Scholar 

  • Wen J, Zimmer EA (1996) Phylogeny and biogeography of Panax L. (the ginseng, Araliaceae): inferences from ITS sequences of nuclear ribosomal DNA. Molec Phylogen Evol 6:166–177

    Article  Google Scholar 

  • Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer Academic Publishers, Dordrecht, pp 265–296

    Chapter  Google Scholar 

  • Wendelbo P (1961) Studies in Primulaceae II. An account of Primula subgenus Sphondylia with a review of the subdivisions of the genus. Arbok for University of Bergen. Mat-Naturv Serie 11:1–49

    Google Scholar 

  • Xu B, Wu N, Gao XF, Zhang LB (2012) Analysis of DNA sequences of six chloroplast and nuclear genes suggests incongruence, introgression, and incomplete lineage sorting in the evolution of Lespedeza (Fabaceae). Molec Phylogen Evol 62:346–358

    Article  Google Scholar 

  • Yan HF, He CH, Peng CI, Hu CM, Hao G (2010) Circumscription of Primula subgenus Auganthus (Primulaceae) based on chloroplast DNA sequences. J Syst Evol 48:123–132

    Article  Google Scholar 

  • Zhang LB, Comes HP, Kadereit JW (2004) The temporal course of quaternary diversification in the European high mountain endemic Primula sect. Auricula (Primulaceae). Int J Pl Sci 165:191–207

    Article  Google Scholar 

  • Zhang YX, Zeng CX, Li DZ (2012) Complex evolution in Arundinarieae (Poaceae: Bambusoideae): incongruence between plastid and nuclear GBSSI gene phylogenies. Molec Phylogen Evol 63:777–797

    Article  Google Scholar 

Download references

Acknowledgments

We thank Xue-Jun Ge and Hai-Fei Yan for technical assistances. We are grateful to the editor and the two anonymous reviewers for their valuable suggestions and comments. This study was financially supported by the National Natural Science Foundation of China (Grants No. 31270260, 31270009).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gang Hao.

Additional information

Handling Editor: Karol Marhold.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, YJ., Liu, J., Hu, CM. et al. Non-monophyly of Primula subgenera Auganthus and Carolinella (Primlaceae) as confirmed by the nuclear DNA sequence variation. Plant Syst Evol 301, 2057–2071 (2015). https://doi.org/10.1007/s00606-015-1207-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-015-1207-0

Keywords

Navigation