Skip to main content
SpringerLink
Log in

Marked Intragenomic Heterogeneity and Geographical Differentiation of nrDNA ITS in Larix potaninii (Pinaceae)

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Nuclear ribosomal DNA (nrDNA) of gymnosperms, especially Pinaceae, is characterized by slow concerted evolution and exhibits substantial ITS-region length variation (975–3663 bp), in sharp contrast to the narrow range (565–700 bp) in angiosperms. Here we examined intra- and intergenomic heterogeneity of the nrDNA internal transcribed spacer (ITS) region in four varieties of Larix potaninii, a species from the mountainous areas of western China. Two clones with more than a 100-bp deletion in ITS1 were detected in L. potaninii var. chinensis and L. potaninii var. australis, respectively. The deletion resulted in the loss of most part, including the motif sequence, of subrepeat 1 (SR1). Sequence divergence and phylogenetic analyses showed that some clones would be pseudogenes given their low GC content, high substitution rates, unique positions in the phylogenetic trees, or significant length variation. These clones might represent orphons or paralogues at minor loci resulting from large-scale gene or chromosome reorganization. Some recombinants characterized by chimeric structure and discordant phylogenetic positions in partitioned sequence analyses indicate that unequal crossing-over plays an important role in the process of nrDNA concerted evolution. In addition, some varieties of L. potaninii might have experienced an nrDNA founder effect parallel to their geographical isolation.

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.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. RG Allaby TA Brown (2001) ArticleTitleNetwork analysis provides insights into evolution of 5S rDNA arrays in Triticum and Aegilops. Genetics 157 1331–1341 Occurrence Handle1:CAS:528:DC%2BD3MXisFyktbg%3D Occurrence Handle11238418

    CAS  PubMed  Google Scholar 

  2. N Arnhein (1983) Concerted evolution of multigene families. M Nei RK Koehn (Eds) Evolution of genes and proteins. Sinauer Sunderland MA 38–61

    Google Scholar 

  3. BG Baldwin MJ Sanderson JM Porter MF Wojciechowski CS Campbell MJ Donoghue (1995) ArticleTitleThe ITS region of nuclear ribosomal DNA: A valuable source of evidence on angiosperm phylogeny. Ann Mo Bot Gard 82 247–277

    Google Scholar 

  4. MS Bobola DE Smith AS Klein (1992) ArticleTitleFive major nuclear ribosomal repeats represent a large and variable fraction of the genomic DNA of Picea rubens and P. mariana. Mol Biol Evol 9 125–137 Occurrence Handle1:CAS:528:DyaK38XnslKluw%3D%3D Occurrence Handle1552835

    CAS  PubMed  Google Scholar 

  5. RD Bradley DM Hillis (1997) ArticleTitleRecombinant DNA sequences generated by PCR amplification. Mol Biol Evol 14 592–593 Occurrence Handle1:CAS:528:DyaK2sXjtVGntr4%3D Occurrence Handle9159937

    CAS  PubMed  Google Scholar 

  6. GR Brown JE Carlson (1997) ArticleTitleMolecular cytogenetics of the genes encoding 18S-5.8S-26S rRNA and 5S rRNA in two species of spruce (Picea). Theor Appl Genet 95 1–9 Occurrence Handle1:CAS:528:DyaK2sXlvVakt7g%3D

    CAS  Google Scholar 

  7. ES Buckler IV TP Holtsford (1996a) ArticleTitle Zea ribosomal repeat evolution and mutation patterns. Mol Biol Evol 13 623–632

    Google Scholar 

  8. ES Buckler IV TP Holtsfo (1996b) ArticleTitle Zea systematics: ribosomal ITS evidence. Mol Biol Evol 13 612–622

    Google Scholar 

  9. ES Buckler A Ippolito TP Holtsford (1997) ArticleTitleThe evolution of ribosomal DNA: Divergent paralogues and phylogenetic implications. Genetics 145 821–832 Occurrence Handle1:CAS:528:DyaK2sXmsVaktLc%3D Occurrence Handle9055091

    CAS  PubMed  Google Scholar 

  10. CE Carlson LE Theroux (1993) ArticleTitleCone and seed morphology of western larch (Larix occidentalis), alpine larch (Larix lyallii), and their hybrids. Can J For Res 21 1264–1269

    Google Scholar 

  11. G Childs R Maxson RH Cohn L Kedes (1981) ArticleTitleOrphons: Dispersed genetic elements derived from tandem repetitive genes of Eucaryotes. Cell 23 651–663 Occurrence Handle1:CAS:528:DyaL3MXhs12ltLY%3D Occurrence Handle6784929

    CAS  PubMed  Google Scholar 

  12. GP Copenhaver JH Doelling JS Gens CS Pikaard (1995) ArticleTitleUse of RFLPs larger than 100-kb to map the position and internal organization of the nucleolus organizer region on chromosome-2 in Arabidopsis thaliana. Plant J 7 273–286 Occurrence Handle10.1046/j.1365-313X.1995.7020273.x Occurrence Handle1:CAS:528:DyaK2MXkslGntLw%3D

    Article  CAS  Google Scholar 

  13. RL Doudrick JS Heslop-Harrison CD Nelson T Schmidt WL Nance T Schwarzacher (1995) ArticleTitleKaryotype of slash pine (Pinus elliottii var. elliottii) using patterns of fluorescence in situ hybridization and fluorochrome banding. J Hered 86 289–296

    Google Scholar 

  14. A Farjon (1990) Pinaceae. Koeltz Scientific Books Konigstein, Germany

    Google Scholar 

  15. A Farjon (2001) World checklist and bibliography of conifers, 2nd ed. Royal Botanic Gardens Kew, UK

    Google Scholar 

  16. J Felsenstein (1985) ArticleTitleConfidence limits on phylogenies: An approach using the bootstrap. Evolution 39 783–791

    Google Scholar 

  17. R Florin (1963) ArticleTitleThe distribution of conifers and taxad genera in time and space. Acta Hort Berg 20 121–312

    Google Scholar 

  18. L-K Fu N Li RR Mill (1999) Larix. Z-Y Wu PH Raven (Eds) Flora of China (4). Science Press, Beijing, and Missouri Botanical Garden Press St. Louis 33–37

    Google Scholar 

  19. J Germane AS Klein (1999) ArticleTitleSpecies-specific nuclear and chloroplast single nucleotide polymorphisms to distinguish Picea glauca, P. mariana and P. rubens. Theor Appl Genet 99 37–49 Occurrence Handle10.1007/s001220051206 Occurrence Handle1:CAS:528:DyaK1MXlvFGlt7o%3D

    Article  CAS  Google Scholar 

  20. DS Gernandt A Liston (1999) ArticleTitleInternal transcribed spacer region evolution in Larix and Pseudotsuga (Pinaceae). Am J Bot 86 711–723 Occurrence Handle1:CAS:528:DyaK1MXjslersr0%3D Occurrence Handle10330075

    CAS  PubMed  Google Scholar 

  21. DS Gernandt A Liston D Piñero (2001) ArticleTitleVariation in the nrDNA ITS of Pinus subsection Cembroides: Implications for molecular systematic studies of pine species complexes. Mol Phylogenet Evol 21 449–467 Occurrence Handle10.1006/mpev.2001.1026 Occurrence Handle1:CAS:528:DC%2BD3MXptVWhsbs%3D Occurrence Handle11741386

    Article  CAS  PubMed  Google Scholar 

  22. DM Hillis C Moritz CA Porter RJ Baker (1991) ArticleTitleEvidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251 308–310 Occurrence Handle1:CAS:528:DyaK3MXps1WjsQ%3D%3D Occurrence Handle1987647

    CAS  PubMed  Google Scholar 

  23. KW Hughes RH Petersen (2001) ArticleTitleApparent recombination or gene conversion in the ribosomal ITS region of a flammulina (Fungi, Agaricales) hybrid. Mol Biol Evol 18 94–96 Occurrence Handle1:CAS:528:DC%2BD3MXhtVSmsL8%3D Occurrence Handle11141197

    CAS  PubMed  Google Scholar 

  24. P Karvonen M Karjalainen O Savolainen (1993) ArticleTitleRibosomal RNA genes in Scots pine (Pinus sylvestris L.): Chromosomal organization and structure. Genetica 88 59–68 Occurrence Handle1:CAS:528:DyaK2cXpslKrsQ%3D%3D

    CAS  Google Scholar 

  25. P Karvonen O Savolainen (1993) ArticleTitleVariation and inheritance of ribosomal DNA in Pinus sylvestris L. (Scots pine). Heredity 71 614–622 Occurrence Handle1:CAS:528:DyaK2cXitFaksbw%3D

    CAS  Google Scholar 

  26. M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16 111–120 Occurrence Handle7463489

    PubMed  Google Scholar 

  27. Y Kita M Ito (2000) ArticleTitleNuclear ribosomal ITS sequences and phylogeny in East Asian Aconitum subgenus Aconitum (Ranunculaceae), with special reference to extensive polymorphism in individual plants. Plant Syst Evol 225 1–13 Occurrence Handle1:CAS:528:DC%2BD3MXhsFGjsrk%3D

    CAS  Google Scholar 

  28. S Kumar K Tamura IB Jakobsen M Nei (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Arizona State University Tempe

    Google Scholar 

  29. BA LePage JF Basinger (1991) ArticleTitleA new species of Larix (Pinaceae) from the early Tertiary of Axel Heiberg Island, Arctic Canada. Rev Palaeobot Palyno 70 89–111 Occurrence Handle10.1016/0034-6667(91)90080-M

    Article  Google Scholar 

  30. BA LePage JF Basinger (1995) ArticleTitleThe evolutionary history of the genus Larix (Pinaceae). USDA For Serv Int Res Sta GTR-INT 319 19–29

    Google Scholar 

  31. A Liston WA Robinson JM Oliphant (1996) ArticleTitleLength variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants. Syst Bot 21 109–120

    Google Scholar 

  32. Z-L Liu D Zhang X-R Wang (2003) ArticleTitleChromosomal localization of 5S and 18S-5.8S-25S ribosomal DNA sites in five Asian pines using fluorescence in situ hybridization. Theor Appl Genet 106 198–204 Occurrence Handle1:CAS:528:DC%2BD3sXltlehtQ%3D%3D Occurrence Handle12582844

    CAS  PubMed  Google Scholar 

  33. EO Long IB Dawid (1980) ArticleTitleRepeated genes in eukaryotes. Annu Rev Biochem 49 727–764 Occurrence Handle1:CAS:528:DyaL3cXltV2jt7s%3D Occurrence Handle6996571

    CAS  PubMed  Google Scholar 

  34. O Lubaretz J Fuchs R Ahne A Meister I Schubert (1996) ArticleTitleKaryotyping of three Pinaceae species via fluorescent in situ hybridization and computer-aided chromosome analysis. Theor Appl Genet 92 411–416 Occurrence Handle10.1007/s001220050143

    Article  Google Scholar 

  35. F Maggini R Marrocco MT Gelati RI De Dominicis (1998) ArticleTitleLengths and nucleotide sequences of the internal spacers of nuclear ribosomal DNA in gymnosperms and pteridophytes. Plant Syst Evol 213 199–205

    Google Scholar 

  36. F Maggini M Frediani MT Gelati (2000) ArticleTitleNucleotide sequence of the internal transcribed spacers of ribosomal DNA in Picea abies Karst. DNA Seq 11 87–89 Occurrence Handle1:CAS:528:DC%2BD3MXhtVGru7s%3D Occurrence Handle10902913

    CAS  PubMed  Google Scholar 

  37. R Marrocco MT Gelati F Maggini (1996) ArticleTitleNucleotide sequence of the internal transcribed spacers and 5.8S region of ribosomal DNA in Pinus pinea L. DNA Seq 6 175–177 Occurrence Handle1:CAS:528:DyaK2sXotFOrsg%3D%3D Occurrence Handle8722573

    CAS  PubMed  Google Scholar 

  38. CI Millar (1993) ArticleTitleImpact of the Eocene on the evolution of Pinus L. Ann Mo Bot Gard 80 471–498

    Google Scholar 

  39. G Muir CC Fleming C Schlotterer (2001) ArticleTitleThree divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Mol Biol Evol 18 112–119 Occurrence Handle1:CAS:528:DC%2BD3MXotVOmsg%3D%3D Occurrence Handle11158370

    CAS  PubMed  Google Scholar 

  40. BG Murray (1998) ArticleTitleNuclear DNA amounts in gymnosperms. Ann Bot 82 IssueIDSuppl A 3–15 Occurrence Handle1:CAS:528:DyaK1MXkt1Wksg%3D%3D

    CAS  Google Scholar 

  41. T Nagylaki (1984) ArticleTitleEvolution of multigene families under interchromosomal gene conversion. Proc Natl Acad Sci USA 81 3769–3800

    Google Scholar 

  42. T Nagylaki TD Petes (1982) ArticleTitleIntrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. Genetics 100 315–337 Occurrence Handle1:CAS:528:DyaL38Xlt1Wgt70%3D Occurrence Handle7106560

    CAS  PubMed  Google Scholar 

  43. W Niu D Zhang (2002) ArticleTitleEvolution of 5S rRNA genes in Ophiopogon xylorrhizus Wang et Dai and O. sylvicola Wang et Tang (Convallariaceae). Acta Bot Sin 44 329–336 Occurrence Handle1:CAS:528:DC%2BD38XktVaksbo%3D

    CAS  Google Scholar 

  44. CH Ostenfeld CS Larsen (1930) ArticleTitleThe species of the genus Larix and their geographic distribution. Biol Meddel Kongel Danske Vidensk Selsk 9 1–107

    Google Scholar 

  45. JN Owens T Takaso CJ Runions (1998) ArticleTitlePollination in conifers. Trends Plant Sci 3 479–485 Occurrence Handle10.1016/S1360-1385(98)01337-5

    Article  Google Scholar 

  46. W Patschke (1913) ArticleTitleÜber die extratropischen ostasiatischen Coniferen und ihre Bedeutung für die pflanzengeographische Gliederung Ostasiens. Bot Jahrb Syst 48 626–776

    Google Scholar 

  47. LD Potter J Rowley (1960) ArticleTitlePollen rain and vegetation, San Augustin Plains, New Mexico. Bot Gaz 122 1–25 Occurrence Handle10.1086/336081

    Article  Google Scholar 

  48. A Quijada A Liston P Delgado A Vazquez-Lobo ER Alvarez-Buylla (1998) ArticleTitleVariation in the nuclear ribosomal DNA internal transcribed spacer (ITS) region of Pinus rzedowskii revealed by PCR-RFLP. Theor Appl Genet 96 539–544 Occurrence Handle10.1007/s001220050771 Occurrence Handle1:CAS:528:DyaK1cXivVWlsLo%3D

    Article  CAS  Google Scholar 

  49. SO Rogers AJ Bendich (1987) ArticleTitleRibosomal RNA genes in plants: Variability in copy number and in the intergenic spacer. Plant Mol Biol 9 509–520 Occurrence Handle1:CAS:528:DyaL2sXmtFartbw%3D

    CAS  Google Scholar 

  50. SO Rogers AJ Bendich (1988) ArticleTitleExtraction of DNA from plant tissues. Plant Mol Biol Manual A6 1–10

    Google Scholar 

  51. C Schlötterer D Tautz (1994) ArticleTitleChromosomal homogeneity and Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol 47 777–783

    Google Scholar 

  52. HE Schorn (1994) ArticleTitleA preliminary discussion of fossil larches (Larix, Pinaceae) from the Arctic. Quat Internal 22/23 173–183 Occurrence Handle10.1016/1040-6182(94)90011-6

    Article  Google Scholar 

  53. VL Semerikov M Lascoux (1999) ArticleTitleGenetic relationship among Eurasian and American Larix species based on allozymes. Heredity 83 62–70 Occurrence Handle10.1038/sj.hdy.6885310 Occurrence Handle1:CAS:528:DyaK1MXlsFygu7Y%3D Occurrence Handle10447704

    Article  CAS  PubMed  Google Scholar 

  54. GP Smith (1976) ArticleTitleEvolution of repeated DNA sequences by unequal crossover. Science 191 528–535 Occurrence Handle1:CAS:528:DyaE28Xhs1Srurg%3D Occurrence Handle1251186

    CAS  PubMed  Google Scholar 

  55. DL Swofford (1998) PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Sunderland, MA

    Google Scholar 

  56. KJ Sytsma BA Schaal (1990) ArticleTitleRibosomal DNA variation within and among individuals of Lisianthius (Gentianaceae) populations. Plant Syst Evol 170 97–106 Occurrence Handle1:CAS:528:DyaK3MXjs1ygsQ%3D%3D

    CAS  Google Scholar 

  57. N Tagashira K Kondo (2001) ArticleTitleChromosome phylogeny of Zamia and Ceratozamia by means of Robertsonian changes detected by fluorescence in situ hybridization (FISH) technique of rDNA. Plant Syst Evol 227 145–155 Occurrence Handle1:CAS:528:DC%2BD3MXms1ehs78%3D

    CAS  Google Scholar 

  58. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleCLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25 4876–4882 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    CAS  PubMed  Google Scholar 

  59. Vining TF (1999) Molecular phylogenetics of Pinaceae. PhD dissertation. University of Maine, Orono

  60. TF Vining CS Campbell (1997) ArticleTitlePhylogenetic signal in sequence repeats within nuclear ribosomal DNA internal transcribed spacer 1 in Tsuga. Am J Bot 84 IssueIDSuppl 702

    Google Scholar 

  61. X-Q Wang DC Tank T Sang (2000) ArticleTitlePhylogeny and divergence times in Pinaceae: evidence from three genomes. Mol Biol Evol 17 773–781 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Gjtb8%3D Occurrence Handle10779538

    CAS  PubMed  Google Scholar 

  62. X-X Wei X-Q Wang (2003) ArticleTitlePhylogenetic split of Larix: Evidence from paternally inherited cpDNA trnT-trnF region. Plant Syst Evol 239:67–77 239 67–77 Occurrence Handle10.1007/s00606-002-0264-3

    Article  Google Scholar 

  63. JF Wendel A Schnabel T Seelanan (1995) ArticleTitleBidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92 280–284 Occurrence Handle1:CAS:528:DyaK2MXjtVens7o%3D Occurrence Handle7816833

    CAS  PubMed  Google Scholar 

  64. TJT White SL Bruns J Taylor (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. M Innis D Gelfand J Sninsky T White (Eds) PCR protocols: A guide to methods and applications. Academic Press San Diego 315–322

    Google Scholar 

  65. EO Wilson (1992) The diversity of life. Belknap Press of Harvard University Press Cambridge, MA

    Google Scholar 

  66. Q-P Xiang Q-Y Xiang A Listen L-K Fu D-Z Fu (2000) ArticleTitleLength variation of the nuclear ribosomal DNA internal transcribed spacer in the genus Abies, with reference to its systematic utility in Pinaceae. Acta Bot Sin 42 946–951 Occurrence Handle1:CAS:528:DC%2BD3cXotVamurg%3D

    CAS  Google Scholar 

  67. D Zhang T Sang (1999) ArticleTitlePhysical mapping of ribosomal RNA genes in peonies (Paeonia, Paeoniaceae) by fluorescent in situ hybridization: Implications for phylogeny and concerted evolution. Am J Bot 86 735–740 Occurrence Handle1:CAS:528:DyaK1MXjslersrs%3D Occurrence Handle10330077

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Drs. Zhou Shi-Liang and Ding Kai-Yu for help in field collection and Miss Sun Ying-Xue for help in sequencing. This work was supported by grants from the State Key Basic Research and Development Plan (Grant G2000046804) and Chinese Academy of Sciences (Grant kscxz-sw-101A and the special fund to Wang Xiao-Quan).

Author information

Authors and Affiliations

  1. Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 20 Nanxincun, Xiangshan, Beijing 100093, China

    Xiao-Xin Wei, Xiao-Quan Wang & De-Yuan Hong

Authors
  1. Xiao-Xin Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao-Quan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. De-Yuan Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiao-Quan Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wei, XX., Wang, XQ. & Hong, DY. Marked Intragenomic Heterogeneity and Geographical Differentiation of nrDNA ITS in Larix potaninii (Pinaceae) . J Mol Evol 57, 623–635 (2003). https://doi.org/10.1007/s00239-003-2512-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2512-8

Keywords

Search

Navigation