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Ribosomal DNA variation among populations of a Pinus rigida Mill. (pitch pine) ecosystem: I. Distribution of copy numbers
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  • Original Article
  • Published: 01 August 1992

Ribosomal DNA variation among populations of a Pinus rigida Mill. (pitch pine) ecosystem: I. Distribution of copy numbers

  • Diddahally R Govindaraju1 &
  • Christopher A Cullis1 

Heredity volume 69, pages 133–140 (1992)Cite this article

  • 928 Accesses

  • 19 Citations

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Abstract

We determined the number and distribution of rRNA genes among individuals of eight pitch pine populations representing a small ecosystem. While these populations show little or no variation for allozymes and also experience high gene flow, they exhibit large amounts of morphological diversity, apparently caused by environmental stress. Nine to ten contigously distributed individuals, located approximately at the centre of the plots in seven out of eight populations, were used toward determining copy numbers. These ranged from 355 to 7356. Approximately, a 12-fold variation among individuals within populations, and 21-fold variation between the lowest and the highest values, among populations was recorded. Numbers of rDNA copies were found to be lower among populations subjected to environmental stress. We conclude that strong diversifying selection may influence the abundance of rRNA genes among pitch pine populations.

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References

  • Anonymous. 1973. Pinelands National Reserve: Soils, nos. 8, 17, 24, 25, 26. NJ Agricultural and Experimental Station, New Brunsuick, NJ.

  • Buescher, P J, Phillips, R L, and Brambl, R. 1984. Ribosomal RNA contents of maize genotypes with different ribosomal RNA gene number. Biochem Genet, 22, 923–930.

    Article  CAS  PubMed  Google Scholar 

  • Cullis, C A. 1987. The generation of somatic and heritable variation in response to stress. Am Nat, 130, S62–73.

    Article  Google Scholar 

  • Cullis, C A, Criessen, G P, Gorman, S W, and Teasdale, R T. 1988. The 25S, 18S and 5S ribosomal RNA genes from Pinus radiata D. Don. In: Cheliak, W. M. & Yapa, Y. C. (eds) Molecular Genetics of Trees. Petawawa National Forestry Institute, Chalk River, Ontario, pp. 34–40.

    Google Scholar 

  • Cluster, P D, Marincovic, D, Allard, R W, and Ayala, F J. 1987. Correlation between developmental rates, enzyme activities, ribosomal DNA spacer-length phenotypes, and adaptation in Drosophila melanogaster. Proc Natl Acad Sci USA, 84, 610–614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhillon, S S, Berlyn, G P, and Miksche, P. 1978. Nuclear DNA content in populations of Pinus rigida. Am J Bot, 65, 192–196.

    Article  CAS  Google Scholar 

  • Dobzhansky, Th. 1970. Genetics of the Evolutionary Process. Columbia University Press, New York, NY.

    Google Scholar 

  • Dover, G A. 1982. Molecular drive: a cohesive mode of species evolution. Nature, 299, 111–117.

    Article  CAS  PubMed  Google Scholar 

  • Dover, G A. 1986. Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet, 2, 159–165.

    Article  CAS  Google Scholar 

  • Dover, G A. 1989. Linkage disequilibrium and molecular drive in the rDNA gene family. Genetics, 122, 249–252.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dutton, F L, and Krieder, H M. 1985. Expression and amplification of the genes for ribosomal RNA in bobbed mutants of Drosophila melanogaster. Genet Res, 45, 155–165.

    Article  CAS  PubMed  Google Scholar 

  • Endler, J A. 1977. Geographic Variation, Speciation and Clines. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Endler, J A. 1986. Natural Selection in the Wild. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Feinberg, A P, and Vogelstein, B. 1983. A technique for radio-labelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem, 132, 6–13.

    Article  CAS  PubMed  Google Scholar 

  • Flavell, R B. 1983. Repeated sequences and genome architecture. In: Cifferi, O. & Dure, L. (eds) Structure and Function of Plant Genomes. Plenum Press, New York, NY, pp. 1–14.

    Google Scholar 

  • Flavell, R B, O'Dell, M, Sharp, P, Nevo, E, and Beiles, A. 1986. Variation in the intergenic spacer of ribosomal DNA of wild wheat, Triticum dicoccoides in Israel. Mol Biol Evol, 3, 547–558.

    CAS  Google Scholar 

  • Forman, R T T. 1979. The Pine Barrens of New Jersey: An ecological mosaic. In: Forman R. T. T. (ed.) Pine Barrens Ecosystem and Landscape. Academic Press, New York, NY, pp. 569–585.

    Google Scholar 

  • Frankham, R, Brisco, D A, and Nuthen, R K. 1980. Unequal crossing over at the rDNA tandem as a source of quantitative genetic variation. Genetics, 95, 727–745.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Givnish, T. 1981. Serotiny, geography and fire in the Pine Barrens of New Jersey. Evolution, 35, 101–123.

    Article  PubMed  Google Scholar 

  • Good, R, and Good, N. 1975. Growth characteristics of populations of Pinus rigida Mill, from the Pine Barrens of New Jersey. Ecology, 56, 1215–1220.

    Article  Google Scholar 

  • Govindaraju, D R. 1988. Dispersal ability and levels of gene flow in plants. Oikos, 52, 31–35.

    Article  Google Scholar 

  • Govindaraju, D R. 1989a. Estimates of gene flow in forest trees. Biol J Linn Soc, 37, 345–357.

    Article  Google Scholar 

  • Govindaraju, D R. 1989b. Viability selection and self-thinning in conifers. Evol Trends Plants, 3, 121–126.

    Google Scholar 

  • Govindaraju, D R, and Dancik, B P. 1987a. Allozyme heterozygosity and homeostasis in germinating seeds of jack pine. Heredity, 59, 279–284.

    Article  Google Scholar 

  • Govindaraju, D R, and Dancik, B P. 1987b. Environmental stresses and the relationship among allozyme heterozygosity, biomass and biomass components in jack pine (Pinus bandana Lamb.). Genetica, 73, 173–179.

    Article  Google Scholar 

  • Guries, R P, and Ledig, F T. 1978. Analysis of population structure in from allozyme frequencies. Proc Fourteenth So For Tree Improv Conf, University of Florida, Gainsville, FL. pp. 246–253.

    Google Scholar 

  • Haldane, J B S. 1948. The interaction of nature and nurture. Ann Eugen 13, 197–205.

    Article  Google Scholar 

  • Kohne, D E. 1970. Evolution of higher organism DNA. Quart Rev Biophys 33, 327–375.

    Article  Google Scholar 

  • Labarca, C, and Paigen, K. 1980. A simple, rapid and sensitive DNA assay procedure. Anal Biochem, 102, 344–352.

    Article  CAS  PubMed  Google Scholar 

  • Ledig, F T, and Fryer, J H. 1972. A pocket of variability in Pinus rigida. Evolution, 26, 259–266.

    Article  PubMed  Google Scholar 

  • Li, W-H, and Graur, D. 1991. Fundamentals of Molecular Evolution, Sinauer Associates, Inc., Sunderland, MA.

    Google Scholar 

  • Long, O, and Dawid, I B. 1980. Repeated genes in eukaryotes. Ann Rev Biochem, 49, 727–764.

    Article  CAS  PubMed  Google Scholar 

  • McCormick, C F, and Buell, M F. 1968. The Plains: Pigmy forest of New Jersey Pine Barrens, a review and annotated bibliography. Bull NJ Acad Sci, 13, 20–34.

    Google Scholar 

  • MacIntyre, R J. 1976. Evolution and ecological value of duplicate genes. Ann Rev Ecol Syst, 7, 421–468.

    Article  CAS  Google Scholar 

  • Maniatis, T, Fritsch, E F, and Sambrook, J. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, NY.

    Google Scholar 

  • Markley, M L. 1979. Soil series of the Pine Barrens. In: Forman R. T. T. (ed.) Pine Barrens Ecosystem And Landscape. Academic Press, New York, NY, pp. 81–93.

    Google Scholar 

  • Murphy, T M, and Thompson, W F. 1988. Molecular Plant Development. Prentice Hall, Englewood Cliffs, NJ.

    Google Scholar 

  • Nevo, E. 1988. Genetic diversity in nature: Patterns and theory. Evol Biol, 23, 217–245.

    Article  Google Scholar 

  • Ohta, T. 1988. Multigene and supergene families. Oxf Surv Evol Biol, 5, 41–65.

    Google Scholar 

  • Ohta, T. 1990. How gene families evolve. Theor Pop Biol, 37, 213–219.

    Article  CAS  Google Scholar 

  • Ohta, T, and Dover, G A. 1983. Population genetics of multigene families that are dispersed in two or more chromosomes. Proc Natl Acad Sci, USA, 80, 4079–4083.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riley, J, Jenner, D, Smith, J C, and Markham, A E. 1989. Rapid determination of DNA in multiple samples. Nuc Acids Res, 17, 8383.

    Article  CAS  Google Scholar 

  • Ritossa, F M, Atwood, K C, and Spiegelman, S. 1966. A molecular explanation of the bobbed mutants of Drosophila as partial deficiencies of ‘ribosomal’ DNA. Genetics, 54, 819–834.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rivin, C, Cullis, C A, and Walbot, V. 1986. Evaluating quantitative variation in the genome of Zea mays. Genetics, 113, 1009–1019.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers, S, and Bendich, A J. 1987. Variation in the ribosomal RNA genes among individuals of Vicia faba. Plant Molec Biol, 9, 509–520.

    Article  CAS  Google Scholar 

  • Russell, P J, and Rodland, K D. 1986. Magnification of rDNA gene number in a Neurospora crassa strain with a partial deletion of the nucleolus organizer. Chromosoma, 93, 337–340.

    Article  CAS  PubMed  Google Scholar 

  • Stephan, W. 1989. Tandem repetitive non-coding DNA: forms and forces. Molec Biol Evol, 6, 198–212.

    CAS  PubMed  Google Scholar 

  • Stern, S, Poers, T, Chang-Chien, L-M, and Noller, H F. 1989. RNA-protein interactions in 30S ribosomal subunit; folding and function of 16S rRNA. Science, 244, 783–789.

    Article  CAS  PubMed  Google Scholar 

  • Strauss, S H, and Howe, G T. 1990. An investigation of somatic variability for ribosomal RNA genes number in old-growth Sitka spruce. Can J For Res, 20, 853–856.

    Article  CAS  Google Scholar 

  • Strauss, S H, and Tsai, C-H. 1988. Ribosomal gene number variability in Douglas-fir. J Hered, 79, 453–458.

    Article  Google Scholar 

  • Tajima, F, and Mukai, T. 1990. Some consideration on diversifying selection. Jap J Genet, 65, 193–200.

    Article  CAS  Google Scholar 

  • Tartoff, K D. 1975. Redundant genes. Ann Rev Genet 9, 355–385.

    Article  Google Scholar 

  • Templeton, A R, Hollocher, H, Lawler, S, and Johnston, J S. 1989. Natural selection and ribosomal DNA in Drosophila. Genome, 31, 296–303.

    Article  CAS  PubMed  Google Scholar 

  • Timmis, J N, and Ingle, J. 1973. Environmentally induced changes in rDNA gene redundancy. Nature, 244, 235–236.

    Article  CAS  Google Scholar 

  • Wade, M P, and Kalisz, S. 1990. The causes of natural selection. Evolution, 44, 1947–1955.

    Article  PubMed  Google Scholar 

  • Wagner, D B, Furnier, G R, Saghai-Maroof, M A, Williams, S M, Dancik, B P, and Allard, R W. 1987. Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proc Natl Acad Sci USA, 84, 2097–2100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams, S M. 1990. The opportunity for natural selection in multigene families. Genetics, 124, 439–441.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zar, J H. 1984. Biostatistical Analysis. Prentice-Hall, Inc., Englewood-Cliffs, NJ.

    Google Scholar 

  • Zhang, Q, Saghai-Maroof, M A, and Allard, R W. 1990. Effects of adaptedness on variations in ribosomal DNA copy number in populations of wild barley (Hordeum vulgare ssp. spontaneum). Proc Natl Acad Sci, USA, 87, 8741–8745.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank R. Good, R. Montgomerie, R. Schneeberger and F. Zampella for help in various ways, and an anonymous reviewer for invaluable suggestions. DRG is grateful to Drs S. Rogers, M. Timko, R. Vilgalys and S. Williams for discussions. Financial support was provided by the Ohio Board of Regents (CAC) and the American Philosophical Society (DRG).

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Authors and Affiliations

  1. Department of Biology, Case Western Reserve University, Cleveland, 44106, OH, USA

    Diddahally R Govindaraju & Christopher A Cullis

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  1. Diddahally R Govindaraju
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  2. Christopher A Cullis
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Govindaraju, D., Cullis, C. Ribosomal DNA variation among populations of a Pinus rigida Mill. (pitch pine) ecosystem: I. Distribution of copy numbers. Heredity 69, 133–140 (1992). https://doi.org/10.1038/hdy.1992.106

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  • Received: 04 October 1991

  • Issue date: 01 August 1992

  • DOI: https://doi.org/10.1038/hdy.1992.106

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Keywords

  • diversifying selection
  • molecular drive
  • multigene families
  • pitch pine
  • rDNA copy numbers

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