Skip to main content
SpringerLink
Log in

Phylogeny of Pyroleae (Ericaceae): implications for character evolution

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Pyroleae (Ericaceae) consist of four genera, all of which are distributed widely in temperate coniferous or sometimes deciduous forests of the Northern Hemisphere. To investigate the phylogenetic relationships among these genera and to explore the evolution of the characteristics of the subfamily, we conducted maximum parsimony and Bayesian analyses with nrDNA ITS and three cpDNA intergenic spacers (atpB-rbcL, trnS-trnG and trnL-trnF). The results from cpDNA and combined cpDNA + ITS data sets strongly support the monophyly of Pyroleae as well as a sister relationship between Pyrola and Moneses–Chimaphila, with Orthilia as the basal lineage. The sister-group relationship between Moneses and Chimaphila is supported by a set of synapomorphies, e.g., single flower, colpate pollen, five bundles in the style, straight fruiting pedicel orientation, complete capsule dehiscence, and the basic chromosome number, x = 13. The Moneses–Chimaphila–Pyrola clade is supported by at least one homologous character of pollen in tetrads. Conflicts associated with the phylogenetic position of Orthilia may imply a hybrid origin for it, and therefore further study is needed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderberg AA (1993) Cladistic interrelationships and major clades of the Ericales. Plant Syst Evol 184:207–231

    Article  Google Scholar 

  • Anderberg AA (1994) Cladistic analysis of Enkianthus with notes on the early diversification of the Ericaceae. Nord J Bot 14:385–401

    Article  Google Scholar 

  • Andres H (1914) Piroleen-Studien. Beiträge zur Kenntnis der Morphologie, Phytogeographie und allgemeinen Systematik der Pirolaceae. Verh Bot Vereins Prov Brandenburg 56:1–76

    Google Scholar 

  • Björkman E (1960) Monotropa hypopithys L.—an epiparasite on tree roots. Physiol Plant 13:399–401

    Google Scholar 

  • Böcher TW (1961) Studies in Pyrolaceae-two interesting wintergreen from West Greenland. Bot Tidsskr 57:28–37

    Google Scholar 

  • Bull JJ, Huelsenbeck JP, Cunningham CW, Swofford DL, Waddell PJ (1993) Partitioning and combining data in phylogenetic analysis. Syst Biol 42:384

    Google Scholar 

  • Chippindale PT, Wiens JJ (1994) Weighting, partitioning, and combining characters in phylogenetic analysis. Syst Biol 43:278

    Google Scholar 

  • Copeland HF (1941) Further studies on Monotropoideae. Madroño 6:97–119

    Google Scholar 

  • Copeland HF (1947) Observations on the structure and classification of the Pyroleae. Madroño 9:65–102

    Google Scholar 

  • Cronquist A (1981) An integrated system of classification of flowering plants. Columbia University Press, New York

    Google Scholar 

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

    Google Scholar 

  • Drude O (1889) Pirolaceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, vol 4. Engelmann, Leipzig, pp 3–11

    Google Scholar 

  • Erdtman G (1952) Pollen morphology and plant taxonomy. Angiosperms. Almqvist & Wiksell, Stockholm

    Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1995) Constructing a significance test for incongruence. Syst Biol 44:570

    Google Scholar 

  • Freudenstein JV (1990) A phylogenetic study of the Pyroloideae (Ericaceae). Am J Bot 77:132

    Google Scholar 

  • Freudenstein JV (1999) Relationships and character transformation in Pyroloideae (Ericaceae) based on ITS sequences, morphology, and development. Syst Bot 24:398–408

    Article  Google Scholar 

  • Haber E, Cruise JE (1974) Generic limits in the Pyroloideae (Ericaceae). Can J Bot 52:877–883

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523

    PubMed  CAS  Google Scholar 

  • Henderson MW (1919) A comparative study of the structure and saprophytism of the Pyrolaceae and Monotropaceae with reference to their derivation from the Ericaceae. Contr Bot Lab Univ Pennsylvania 5:42–109

    Google Scholar 

  • House HD (1921) Nomenclatorial notes on certain American plants. I. Am Midl Nat 7:126–135

    Article  Google Scholar 

  • Huelsenbeck J, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny, version 3.1. 2. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Jensen LCW (1961) Pollination studies with native Minnesota Pyrola and Moneses species. Proc Minn Acad Sci 29:210–218

    Google Scholar 

  • Judd WS, Kron KA (1993) Circumscription of Ericaceae (Ericales) as determined by preliminary cladistic analyses based on morphological, anatomical, and embryological features. Brittonia 45:99–114

    Article  Google Scholar 

  • Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 87:482–498

    Article  Google Scholar 

  • Knaben G, Engelskjøn T (1968) Studies in Pyrolaceae, especially in the Pyrola rotundifolia complex. Arb Univ Bergen Mat Naturvitensk Ser 1967:1–71

    Google Scholar 

  • Knudsen JT, Olesen JM (1993) Buzz-pollination and patterns in sexual traits in North European Pyrolaceae. Am J Bot 80:900–913

    Article  Google Scholar 

  • Křísa B (1971) Bertrag zur taxonomie und chorologie der gattung Pyrola L. Bot Jahrb Syst 90:476–508

    Google Scholar 

  • Kron KA (1996) Phylogenetic relationships of Empetraceae, Epacridaceae, Ericaceae, Monotropaceae, and Pyrolaceae: evidence from nuclear ribosomal 18 s sequence data. Ann Bot 77:293–303

    Article  Google Scholar 

  • Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of Ericaceae: molecular and morphological evidence. Bot Rev 68:335–423

    Article  Google Scholar 

  • Landhäusser SM, Stadt KJ, Lieffers VJ (1997) Photosynthetic strategies of summergreen and evergreen understory herbs of the boreal mixedwood forest. Oecologia 112:173–178

    Article  Google Scholar 

  • Maddison WP, Maddison DR (2005) Mesquite: a modular system for evolutionary analysis. Version 1.06. http://mesquiteproject.org. Accessed 22 Sept 2006

  • Manen JF, Natali A, Ehrendorfer F (1994) Phylogeny of Rubiaceae-Rubieae inferred from the sequence of a cpDNA intergene region. Plant Syst Evol 190:195–211

    Article  CAS  Google Scholar 

  • Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524

    Article  Google Scholar 

  • Müller KF (2005) SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics 4:65–69

    Article  PubMed  Google Scholar 

  • Nowicke JW (1966) Pollen morphology and classification of the Pyrolaceae and Monotropaceae. Ann Mo Bot Gard 53:213–219

    Article  Google Scholar 

  • Nylander JAA (2004) MrModeltest (version 2.2). http://www.abc.se/~nylander/

  • Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Qin HN, Stevens PF (2005) Ericaceae. In: Fang MY, Fang RZ, He MY, Hu LZ, Yang HB, Qin HN, Min TL, Chamberlain DF, Stevens PF, Wallace GD, Anderberg AA (eds) Flora of China, vol 14. Missouri Botanical Garden, St. Louis, pp 245–255

    Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  PubMed  CAS  Google Scholar 

  • Singh P, Carew GC (1990) Inland spruce cone rust of black spruce: Effect on cone and seed yield, and seed quality. Eur J Forest Pathol 20:397–404

    Article  Google Scholar 

  • Stevens PF (1971) A classification of the Ericaceae: subfamilies and tribes. Bot J Linn Soc 64:1–53

    Article  Google Scholar 

  • Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony (* and other methods), vers. 4.0b10. Sinauer, Sunderland

    Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H (1988) Pollen morphology and systematics in two subfamilies of the Ericaceae: Pyroloideae and Monotropoideae. J Korean Plant Taxon 18:9–17

    Google Scholar 

  • Takhtajan AL (1980) Outline of the classification of flowering plants (Magnoliophyta). Bot Rev 46:225–359

    Article  Google Scholar 

  • Tedersoo L, Pellet P, Kõljalg U, Selosse MA (2007) Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151:206–217

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Thorne RF (1983) Proposed new realignments in the angiosperms. Nord J Bot 3:85–117

    Article  Google Scholar 

  • Thorne RF (1992) Classification and geography of the flowering plants. Bot Rev 58:225–327

    Article  Google Scholar 

  • Wallace GD (1975) Interrelationships of the subfamilies of the Ericaceae and derivation of the Monotropoideae. Bot Not 128:286–298

    Google Scholar 

  • Warner BG, Chinnappa CC (1986) Taxonomic implications and evolutionary trends in pollen of Canadian Ericales. Can J Bot 64:3113–3126

    Article  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications, vol 18. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wood CE Jr (1961) The genera of Ericaceae in the southeastern United States. J Arnold Arbor 42:10–80

    Google Scholar 

Download references

Acknowledgments

This study was part of a PhD project by Zhen-wen Liu and was supported by the National Natural Science Foundation of China (Grant 30900075). The authors are grateful to John V. Freudenstein, Hidie Takahashima and Shu-dong Zhang for allowing us to use DNA samples and leaf material. We thank Xun Gong for support during the laboratory work. We appreciate Sylvia Phillips, Julian Harber and David Boufford for polishing our English language. We are greatly indebted to two anonymous reviewers, whose comments were of great help in improving the quality of this paper.

Author information

Authors and Affiliations

  1. Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650204, China

    Zhen-wen Liu, Ze-huan Wang, Jing Zhou & Hua Peng

  2. Graduate School of Chinese Academy of Sciences, Beijing, 100049, China

    Zhen-wen Liu & Ze-huan Wang

  3. School of Pharmaceutical Science, Kunming Medical University, No. 191 West Renmin Rd., Kunming, 650031, China

    Jing Zhou

Authors
  1. Zhen-wen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ze-huan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hua Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hua Peng.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 24 kb)

Supplementary material 2 (XLS 30 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Zw., Wang, Zh., Zhou, J. et al. Phylogeny of Pyroleae (Ericaceae): implications for character evolution. J Plant Res 124, 325–337 (2011). https://doi.org/10.1007/s10265-010-0376-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-010-0376-8

Keywords

Search

Navigation