Skip to main content
SpringerLink
Log in

Incongruence among mitochondrial, chloroplast and nuclear gene trees in Pinus subgenus Strobus (Pinaceae)

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

Abstract

Introgression has been considered to be one of main factors leading to phylogenetic incongruence among different datasets at lower taxonomic levels. In the plants of Pinaceae, the mtDNA, cpDNA, and nuclear DNA (nrDNA) may have different evolutionary histories through introgression because they are inherited maternally, paternally and biparentally, respectively. We compared mtDNA, cpDNA, and two low-copy nrDNA phylogenetic trees in the genus Pinus subgenus Strobus, in order to detect unknown past introgression events in this group. nrDNA trees were mostly congruent with the cpDNA tree, and supported the recent sectional and subsectional classification system. In contrast, mtDNA trees split the members of sect. Quinquefoliae into two groups that were not observed in the other gene trees. The factors constituting incongruence may be divided into the following two categories: the different splits within subsect. Strobus, and the non-monophyly of subsect. Gerardianae. The former was hypothesized to have been caused by the past introgression of cpDNA, mtDNA or both between Eurasian and North American species through Beringia. The latter was likely caused by the chimeric structure of the mtDNA sequence of P. bungeana, which might have originated through past hybridization, or through a horizontal transfer event and subsequent recombination.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbott RJ, Brochmann C (2003) History and evolution of the arctic flora: in the footsteps of Eric Hultén. Mol Ecol 12:99–313

    Google Scholar 

  • Anderson LL, Hu FS, Nelson DM, Petit RJ, Paige KN (2006) Ice-age endurance: DNA evidence of a white spruce refugium in Alaska. Proc Natl Acad Sci USA 103:12447–12450

    Article  CAS  PubMed  Google Scholar 

  • Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201

    Article  CAS  PubMed  Google Scholar 

  • Birky CW, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplast, and some results. Genetics 103:513–527

    PubMed  Google Scholar 

  • Bouillé M, Bousquet J (2005) Trans-species shared polymorphisms at orthologous nuclear gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. Am J Bot 92:63–73

    Article  Google Scholar 

  • Brubaker LB, Anderson PM, Edwards ME, Lozhkin AV (2005) Beringia as a glacial refugium for boreal trees and shrubs: new perspectives from mapped pollen data. J Biogeogr 32:833–848

    Article  Google Scholar 

  • Burban C, Petit RJ (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Mol Ecol 12:1487–1495

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Tauer CG, Bai G, Huang Y, Payton ME, Holley AG (2004) Bidirectional introgression between Pinus taeda and Pinus echinata: evidence from morphological and molecular data. Can J For Res 34:2508–2516

    Article  CAS  Google Scholar 

  • Critchfield WB (1986) Hybridization and classification of the white pines (Pinus section Strobus). Taxon 35:647–656

    Article  Google Scholar 

  • Cronn R, Wendel JF (2004) Cryptic trysts, genomic mergers, and plant speciation. New Phytol 161:133–142

    Article  CAS  Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    Article  CAS  PubMed  Google Scholar 

  • Dong J, Wagner DB (1993) Taxonomic and population differentiation of mitochondrial diversity in Pinus banksiana and Pinus contorta. Theor Appl Genet 86:573–578

    Article  Google Scholar 

  • Eckert AJ, Hall BD (2006) Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): phylogenetic tests of fossil-based hypotheses. Mol Phylogenet Evol 40:166–182

    Article  CAS  PubMed  Google Scholar 

  • Engelmann G (1880) Revision of the genus Pinus, and description of Pinus elliottii. Trans Acad Sci St Louis 4:161–190

    Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Garrett PW (1979) Species hybridization in the genus Pinus. USDA Forest Service Research Paper NE-436

  • Gernandt DS, Liston A, Pinero D (2001) Variation in the nrDNA ITS of Pinus subsection Cembroides: implications for molecular systematic studies of pine species complexes. Mol Phylogenet Evol 21:449–467

    Article  CAS  PubMed  Google Scholar 

  • Gernandt DS, Lopez GG, Garcia SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–45

    Article  Google Scholar 

  • Gugerli F, Senn J, Anzidei M, Madaghiele A, Buchler U, Sperisen C, Vendramin GG (2001) Chloroplast microsatellites and mitochondrial nad1 intron 2 sequences indicate congruent phylogenetic relationships among Swiss stone pine (Pinus cembra), Siberian stone pine (Pinus sibirica), and Siberian dwarf pine (Pinus pumila). Mol Ecol 10:1489–1497

    Article  CAS  PubMed  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 

  • Hultén E (1937) Outline of the history of Arctic and Boreal biota during the Quaternary period. Cramer, New York

    Google Scholar 

  • Jaramillo-Correa JP, Bousquet J (2005) Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics 171:1951–1962

    Article  CAS  PubMed  Google Scholar 

  • Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139

    Article  CAS  PubMed  Google Scholar 

  • Liston A, Robinson WA, Pinero D, Alvarez-Buylla ER (1999) Phylogenetics of Pinus (Pinaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Mol Phylogenet Evol 11:95–109

    Article  CAS  PubMed  Google Scholar 

  • Liston A, Parker-Defeniks M, Syring JV, Willyard A, Cronn R (2007) Interspecific phylogenetic analysis enhances intraspecific phylogeographical inference: a case study in Pinus lambertiana. Mol Ecol 16:3926–3937

    Article  PubMed  Google Scholar 

  • Little EL, Critchfield WB (1969) Subdivision of the genus Pinus (pines), USDA Forest Service, Washington, DC, Miscellaneous Publication Number 1144

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

    Article  PubMed  Google Scholar 

  • Matos JA, Schaal BA (2000) Chloroplast evolution in the Pinus montezumae complex: a coalescent approach to hybridization. Evolution 54:1218–1233

    CAS  PubMed  Google Scholar 

  • Matthews JV, Ovenden LE (1990) Late Tertiary plant macrofossils from localities in arctic/subarctic North America: a review of the data. Arctic 43:364–392

    Google Scholar 

  • Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30

    Article  CAS  PubMed  Google Scholar 

  • Mirov NT (1967) The genus Pinus. Ronald, New York

    Google Scholar 

  • Müller K (2005) SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Appl Bioinformatics 4:65–69

    Article  PubMed  Google Scholar 

  • Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77:212–216

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University

  • Price RA, Liston A, Strauss SH (1998) Phylogeny and systematic of Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 49–68

    Google Scholar 

  • Richardson BA, Brunsfeld SJ, Klopfenstein NB (2002) DNA from bird-dispersed seed and wind-disseminated pollen provides insights into postglacial colonization and population genetic structure of whitebark pine (Pinus albicaulis). Mol Ecol 11:215–227

    Article  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trend Plant 5:65–84

    Google Scholar 

  • Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Senjo M, Kimura K, Watano Y, Ueda K, Shimizu T (1999) Extensive mitochondrial introgression from Pinus pumila to P. parviflora var. pentaphylla (Pinaceae). J Plant Res 112:97–105

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Suyama Y, Yoshimaru H, Tsumura Y (2000) Molecular phylogenetic position of Japanese Abies (Pinaceae) based on chloroplast DNA sequences. Mol Phylogenet Evol 16:271–277

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Syring J, Willyard A, Cronn R, Liston A (2005) Evolutionary relationships among Pinus (Pinaceae) subsections inferred from multiple low-copy nuclear loci. Am J Bot 92:2086–2100

    Article  Google Scholar 

  • Syring J, Farrell K, Businsky R, Cronn R, Liston A (2007) Widespread genealogical nonmonophyly in species of Pinus Subgenus Strobus. Syst Biol 56:163–181

    Article  CAS  PubMed  Google Scholar 

  • Tani N, Maruyama K, Tomaru N, Uchida K, Araki M, Tsumura Y, Yoshimaru H, Ohba K (2003) Genetic diversity of nuclear and mitochondrial genomes in Pinus parviflora Sieb. & Zucc. (Pinaceae) populations. Heredity 91:510–518

    Article  CAS  PubMed  Google Scholar 

  • Temesgen B, Brown GR, Harry DE, Kinlaw CS, Sewell MM, Neale DB (2001) Genetic mapping of expressed sequence tag polymorphism (ESPT) markers in loblolly pine (Pinus taeda L.). Theor Appl Genet 102:664–675

    Article  CAS  Google Scholar 

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wagner DB, Furnier GR, Saghai-Maroof MA, Williams SM, Dancik BP, Allard RW (1987) Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc Natl Acad Sci USA 84:2097–2100

    Article  CAS  PubMed  Google Scholar 

  • Wagner DB, Dong J, Carlson MR, Yanchuk AD (1991) Paternal leakage of mitochondrial DNA in Pinus. Theor Appl Genet 82:510–514

    Article  Google Scholar 

  • Wang XR, Tsumura Y, Yoshimaru H, Nagasaka K, Szmidt AE (1999) Phylogenetic relationships of Eurasian pines (Pinus, Pinaceae) based on chloroplast rbcL, matK, rpl20-rps18 spacer, and trnV intron sequences. Am J Bot 86:1742–1753

    Article  CAS  PubMed  Google Scholar 

  • Wang XQ, Tank DC, Sang T (2000) Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol Biol Evol 17:773–781

    CAS  PubMed  Google Scholar 

  • Watano Y, Imazu M, Shimizu T (1995) Chloroplast DNA typing by PCR-SSCP in the Pinus pumila-P. parviflora var. pentaphylla Complex (Pinaceae). J Plant Res 108:493–499

    Article  CAS  Google Scholar 

  • Watano Y, Imazu M, Shimizu T (1996) Spatial distribution of cpDNA and mtDNA haplotypes in a hybrid zone between Pinus pumila and P. parviflora var. pentaphylla (Pinaceae). J Plant Res 109:403–408

    Article  CAS  Google Scholar 

  • Watano Y, Kanai A, Tani N (2004) Genetic structure of hybrid zones between Pinus pumila and P. parviflora var. pentaphylla (Pinaceae) revealed by molecular hybrid index analysis. Am J Bot 91:65–72

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Willyard A, Syring J, Gernandt DS, Liston A, Cronn R (2007) Fossil calibration of molecular divergence infers a moderate mutation rate and recent radiations for Pinus. Mol Biol Evol 24:90–101

    Article  PubMed  CAS  Google Scholar 

  • Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100:10824–10829

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Yoshihiko Tsumura for providing genomic DNA samples of Pinus sibirica; the Royal Botanic Garden Edinburgh for providing dried leaves of P. albicaulis, P. cembra, P. koraiensis and P. peuce; the Field Science Education and Research Center of Kyoto University for providing leaf samples of many other pine species. This study was partly supported by Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research (B), No. 14340265 and No. 18370033.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Chiba University, Yayoi, Inage, Chiba, 263-8522, Japan

    Kiyomi Tsutsui, Atsushi Suwa, Kei’ichi Sawada & Toshihide Kato

  2. Department of Biology, Graduate School of Science, Chiba University, Yayoi, Inage, Chiba, 263-8522, Japan

    Takeshi A. Ohsawa & Yasuyuki Watano

Authors
  1. Kiyomi Tsutsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Atsushi Suwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kei’ichi Sawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Toshihide Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takeshi A. Ohsawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yasuyuki Watano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasuyuki Watano.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsutsui, K., Suwa, A., Sawada, K. et al. Incongruence among mitochondrial, chloroplast and nuclear gene trees in Pinus subgenus Strobus (Pinaceae). J Plant Res 122, 509–521 (2009). https://doi.org/10.1007/s10265-009-0246-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-009-0246-4

Keywords

Search

Navigation