Advertisement

Journal of Plant Research

, Volume 122, Issue 5, pp 509–521 | Cite as

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

  • Kiyomi Tsutsui
  • Atsushi Suwa
  • Kei’ichi Sawada
  • Toshihide Kato
  • Takeshi A. Ohsawa
  • Yasuyuki WatanoEmail author
Regular Paper

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.

Keywords

Introgression Lineage sorting Mitochondrial DNA Phylogeny incongruence Pinus subgenus Strobus 

Notes

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.

Supplementary material

10265_2009_246_MOESM1_ESM.pdf (92 kb)
Table S1. List of species sampled and INSD accessions of the sequences (PDF 92 kb)
10265_2009_246_MOESM2_ESM.pdf (159 kb)
Table S2. Fasta format file of the combined dataset of mtDNA nad1 intron 2 and nad5 intron 1 (PDF 159 kb)

References

  1. Abbott RJ, Brochmann C (2003) History and evolution of the arctic flora: in the footsteps of Eric Hultén. Mol Ecol 12:99–313Google Scholar
  2. 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 103:12447–12450CrossRefPubMedGoogle Scholar
  3. Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201CrossRefPubMedGoogle Scholar
  4. 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 103:513–527PubMedGoogle Scholar
  5. 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 92:63–73CrossRefGoogle Scholar
  6. 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 32:833–848CrossRefGoogle Scholar
  7. Burban C, Petit RJ (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Mol Ecol 12:1487–1495CrossRefPubMedGoogle Scholar
  8. 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 34:2508–2516CrossRefGoogle Scholar
  9. Critchfield WB (1986) Hybridization and classification of the white pines (Pinus section Strobus). Taxon 35:647–656CrossRefGoogle Scholar
  10. Cronn R, Wendel JF (2004) Cryptic trysts, genomic mergers, and plant speciation. New Phytol 161:133–142CrossRefGoogle Scholar
  11. 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 4:129–131CrossRefPubMedGoogle Scholar
  12. Dong J, Wagner DB (1993) Taxonomic and population differentiation of mitochondrial diversity in Pinus banksiana and Pinus contorta. Theor Appl Genet 86:573–578CrossRefGoogle Scholar
  13. Eckert AJ, Hall BD (2006) Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): phylogenetic tests of fossil-based hypotheses. Mol Phylogenet Evol 40:166–182CrossRefPubMedGoogle Scholar
  14. Engelmann G (1880) Revision of the genus Pinus, and description of Pinus elliottii. Trans Acad Sci St Louis 4:161–190Google Scholar
  15. Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  16. Garrett PW (1979) Species hybridization in the genus Pinus. USDA Forest Service Research Paper NE-436Google Scholar
  17. 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 21:449–467CrossRefPubMedGoogle Scholar
  18. Gernandt DS, Lopez GG, Garcia SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–45CrossRefGoogle Scholar
  19. 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 10:1489–1497CrossRefPubMedGoogle Scholar
  20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  21. Hultén E (1937) Outline of the history of Arctic and Boreal biota during the Quaternary period. Cramer, New YorkGoogle Scholar
  22. Jaramillo-Correa JP, Bousquet J (2005) Mitochondrial genome recombination in the zone of contact between two hybridizing conifers. Genetics 171:1951–1962CrossRefPubMedGoogle Scholar
  23. Knoop V (2004) The mitochondrial DNA of land plants: peculiarities in phylogenetic perspective. Curr Genet 46:123–139CrossRefPubMedGoogle Scholar
  24. 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 11:95–109CrossRefPubMedGoogle Scholar
  25. 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 16:3926–3937CrossRefPubMedGoogle Scholar
  26. Little EL, Critchfield WB (1969) Subdivision of the genus Pinus (pines), USDA Forest Service, Washington, DC, Miscellaneous Publication Number 1144Google Scholar
  27. Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30CrossRefPubMedGoogle Scholar
  28. Matos JA, Schaal BA (2000) Chloroplast evolution in the Pinus montezumae complex: a coalescent approach to hybridization. Evolution 54:1218–1233PubMedGoogle Scholar
  29. Matthews JV, Ovenden LE (1990) Late Tertiary plant macrofossils from localities in arctic/subarctic North America: a review of the data. Arctic 43:364–392Google Scholar
  30. Michel F, Umesono K, Ozeki H (1989) Comparative and functional anatomy of group II catalytic introns—a review. Gene 82:5–30CrossRefPubMedGoogle Scholar
  31. Mirov NT (1967) The genus Pinus. Ronald, New YorkGoogle Scholar
  32. Müller K (2005) SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Appl Bioinformatics 4:65–69CrossRefPubMedGoogle Scholar
  33. Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77:212–216CrossRefGoogle Scholar
  34. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  35. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  36. 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 49–68Google Scholar
  37. 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 11:215–227CrossRefPubMedGoogle Scholar
  38. Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trend Plant 5:65–84Google Scholar
  39. Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798–804CrossRefPubMedGoogle Scholar
  40. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  41. 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 112:97–105CrossRefGoogle Scholar
  42. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence based phylogenetic analyses. Syst Biol 49:369–381CrossRefPubMedGoogle Scholar
  43. Suyama Y, Yoshimaru H, Tsumura Y (2000) Molecular phylogenetic position of Japanese Abies (Pinaceae) based on chloroplast DNA sequences. Mol Phylogenet Evol 16:271–277CrossRefPubMedGoogle Scholar
  44. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). version 4. Sinauer Associates, SunderlandGoogle Scholar
  45. 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 92:2086–2100CrossRefGoogle Scholar
  46. Syring J, Farrell K, Businsky R, Cronn R, Liston A (2007) Widespread genealogical nonmonophyly in species of Pinus Subgenus Strobus. Syst Biol 56:163–181CrossRefPubMedGoogle Scholar
  47. 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 91:510–518CrossRefPubMedGoogle Scholar
  48. 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 102:664–675CrossRefGoogle Scholar
  49. Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244CrossRefGoogle Scholar
  50. 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 25:4876–4882CrossRefPubMedGoogle Scholar
  51. 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 84:2097–2100CrossRefPubMedGoogle Scholar
  52. Wagner DB, Dong J, Carlson MR, Yanchuk AD (1991) Paternal leakage of mitochondrial DNA in Pinus. Theor Appl Genet 82:510–514CrossRefGoogle Scholar
  53. 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 86:1742–1753CrossRefPubMedGoogle Scholar
  54. Wang XQ, Tank DC, Sang T (2000) Phylogeny and divergence times in Pinaceae: evidence from three genomes. Mol Biol Evol 17:773–781PubMedGoogle Scholar
  55. 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 108:493–499CrossRefGoogle Scholar
  56. 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 109:403–408CrossRefGoogle Scholar
  57. 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 91:65–72CrossRefGoogle Scholar
  58. 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 265–296Google Scholar
  59. 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 24:90–101CrossRefPubMedGoogle Scholar
  60. Won H, Renner SS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100:10824–10829CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2009

Authors and Affiliations

  • Kiyomi Tsutsui
    • 1
  • Atsushi Suwa
    • 1
  • Kei’ichi Sawada
    • 1
  • Toshihide Kato
    • 1
  • Takeshi A. Ohsawa
    • 2
  • Yasuyuki Watano
    • 2
    Email author
  1. 1.Department of Biology, Faculty of ScienceChiba UniversityChibaJapan
  2. 2.Department of Biology, Graduate School of ScienceChiba UniversityChibaJapan

Personalised recommendations