Skip to main content

Evolutionary Aspects of Functional and Pseudogene Members of the Phytochrome Gene Family in Scots Pine

Journal of Molecular Evolution volume 67, pages 222–232 (2008)Cite this article

Abstract

According to the neutral theory of evolution, mutation and genetic drift are the only forces that shape unconstrained, neutral, gene evolution. Thus, pseudogenes (which often evolve neutrally) provide opportunities to obtain direct estimates of mutation rates that are not biased by selection, and gene families comprising functional and pseudogene members provide useful material for both estimating neutral mutation rates and identifying sites that appear to be under positive or negative selection pressures. Conifers could be very useful for such analyses since they have large and complex genomes. There is evidence that pseudogenes make significant contributions to the size and complexity of gene families in pines, although few studies have examined the composition and evolution of gene families in conifers. In this work, I examine the complexity and rates of mutation of the phytochrome gene family in Pinus sylvestris and show that it includes not only functional genes but also pseudogenes. As expected, the functional PHYO does not appear to have evolved neutrally, while phytochrome pseudogenes show signs of unconstrained evolution.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

References

  • Ahuja MR, Neale DB (2005) Evolution of genome size in conifers. Silvae Genetica 54:126–137

    Google Scholar 

  • Akashi H (1997) Distinguishing the effects of mutational biases and natural selection on DNA sequence variation. Genetics 147:1989–1991

    PubMed  CAS  Google Scholar 

  • Akashi H (1999) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:927–935

    Google Scholar 

  • Aukerman MJ, Hirschfeld M, Wester L, Clack T, Amasino RM, Sharrock RA (1997) A deletion in the PHYD gene of the Arabidosis Wassilewskija ecotype defines a role for phytochrome D in far red/red light sensing. Plant Cell 9:1317–1326

    PubMed  Article  CAS  Google Scholar 

  • Balakirev ES, Ayala FJ (2003) Pseudogenes: are they “junk” or functional DNA? Annu Rev Genet 37:123–151

    PubMed  Article  CAS  Google Scholar 

  • Baldauf SL (2003) Phylogeny for the faint of heart: a tutorial. Trends Genet 19:345–351

    PubMed  Article  CAS  Google Scholar 

  • Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303

    PubMed  CAS  Google Scholar 

  • Dvornyk V, Sirviö A, Mikkonen M, Savolainen O (2002) Low nucleotide diversity at the pal1 locus in the widely distributed Pinus sylvestris. Mol Biol Evol 19:179–188

    PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondria DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • García-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12:1195–1206

    PubMed  Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Higgins DG, Sharp PM (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73:237–244

    PubMed  Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    PubMed  Article  CAS  Google Scholar 

  • Hughes AL (2000) Adaptive evolution of genes and genomes. Oxford University Press, New York

    Google Scholar 

  • Kaplan NL, Hudson RR, Langley CH (1989) The hitchhiking effect revisited. Genetics 123:887–899

    PubMed  CAS  Google Scholar 

  • Kinlaw CS, Neale DB (1997) Complex gene families in pine genomes. Trends Plant Sci 2:356–359

    Article  Google Scholar 

  • Kvarnheden A, Albert VA, Engström P (1995) Molecular evolution of cdc2 pseudogenes in spruce (Picea). Plant Mol Biol 36:767–774

    Article  Google Scholar 

  • Li WH (1997) Molecular evolution. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Li WH, Gojobori T, Mei M (1981) Pseudogenes as a paradigm of neutral evolution. Nature 292:237–239

    PubMed  Article  CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    PubMed  Article  CAS  Google Scholar 

  • Mathews S, Donoghue MJ (1999) The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286:947–950

    PubMed  Article  CAS  Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive evolution of the “Adh” locus in “Drosophila”. Nature 351:652–654

    PubMed  Article  CAS  Google Scholar 

  • Mclnerney JO (2006) The causes of protein evolutionary rate variation. Trends Ecol Evol 21:230–232

    Article  Google Scholar 

  • Mighell AJ, Smith NR, Robinson PA, Markham AF (2000) Vertebrate pseudogenes. FEBS Lett 468:109–114

    PubMed  Article  CAS  Google Scholar 

  • Miller CN (1977) Mesozoic conifers. Bot Rev 43:217–280

    Article  Google Scholar 

  • Murray BG (1998) Nuclear DNA amounts in gymnosperms. Ann Bot 82 (Suppl A):3–15

    Article  CAS  Google Scholar 

  • Neff MM, Fankhauser C, Chory J (2000) Light an indicator of time and place. Genes Dev 14:257–271

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Nielsen R (2001) Statistical tests of selective neutrality in the age of genomics. Heredity 86:641–647

    PubMed  Article  CAS  Google Scholar 

  • Petrov DA, Hartl DL (1999) Patterns of nucleotide substitution in Drosophila and mammalian genomes . Proc Natl Acad Sci USA 96:1475–1479

    PubMed  Article  CAS  Google Scholar 

  • Petrov DA, Lozovskaya ER, Hartl DL (1996) High intrinsic rate of DNA loss in Drosophila. Nature 384:346–349

    PubMed  Article  CAS  Google Scholar 

  • Petrov DA, Sangster TA, Johnston S, Hartl DL, Shaw KL (2000) Evidence of DNA loss as a determinant of genome size. Science 287:1060–1062

    PubMed  Article  CAS  Google Scholar 

  • Reed DH, Nicholas AC, Stratton GE (2007) Genetic quality of individuals impacts population dynamics. Anim Conserv 10:275–283

    Article  Google Scholar 

  • Schubert R, Manteuffel R, Eich J, Häger KP (2002) Molecular characterization and evolution of the cytosolic class II 17.0 kDa small heat-shock protein gene family from Picea abies (L.). Plant Sci 163:1–12

    Article  CAS  Google Scholar 

  • Skinner JS, Timko MP (1998). Loblolly pine (Pinus taeda L) contains multiple expressed genes encoding light-dependent NADPH:protochlorophyllide oxidoreductase (POR). Plant Cell Physiol 39:795–806

    PubMed  CAS  Google Scholar 

  • Suzuki Y, Gojobori T (1999) A method for detecting positive selection at single amino acid sites. Mol Biol Evol 16:1315–1328

    PubMed  CAS  Google Scholar 

  • Swanson WJ (2003) Adaptive evolution of genes and gene families. Curr Opin Genet Dev 13:617–622

    PubMed  Article  CAS  Google Scholar 

  • Wakasugi T, Tsudzuki J, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all Ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thumbergii. Proc Natl Acad Sci USA 91:9794–9798

    PubMed  Article  CAS  Google Scholar 

  • Watterson GA (1983) On the time for gene silencing at duplicated loci. Genetics 105:745–766

    PubMed  Google Scholar 

  • Wei XX, Wang XQ (2004) Recolonization and radiation in Larix (Pinaceae): evidence from nuclear ribosomal DNA paralogues. Mol Ecol 13:3115–3123

    PubMed  Article  CAS  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, vol 2. The theory of gene frequencies. University of Chicago Press, Chicago

    Google Scholar 

  • Wright F (1986) The “effective number of codons” used in a gene. Gene 87:23–29

    Article  Google Scholar 

  • Wyckoff GJ, Malcom CM, Vallender EJ, Lahn BT (2005) A highly unexpected strong correlation between fixation probability of nonsynonymous mutations and mutation rate. Trends Genet 21:381–385

    PubMed  Article  CAS  Google Scholar 

  • Xia X (1996) Maximizing transcription efficiency causes codon usage bias. Genetics 144:1309–1320

    PubMed  CAS  Google Scholar 

  • Xia X (2001) Data analysis in molecular biology and evolution. Kluwer Academic, New York

    Google Scholar 

  • Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. TREE 15:496–503

    PubMed  Google Scholar 

Download references

Acknowledgments

I thank Professor Outi Savolainen for useful comments on the manuscript, and I gratefully acknowledge the financial support from the European Science Foundation grant and the Marie Curie fellowship (QLK5-CT-2000-51233) provided under the 5th Framework Programme and Bioscience and Environmental Research Council.

Author information

Authors and Affiliations

  1. Department of Forest Genetics and Plant Physiology, SLU, 90183, Umea, Sweden

    Maria Rosario García-Gil

  2. Department of Biology, University of Oulu, P.O. Box 3000, 90014, Oulu, Finland

    Maria Rosario García-Gil

Authors
  1. Maria Rosario García-Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Rosario García-Gil.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

García-Gil, M.R. Evolutionary Aspects of Functional and Pseudogene Members of the Phytochrome Gene Family in Scots Pine. J Mol Evol 67, 222–232 (2008). https://doi.org/10.1007/s00239-008-9135-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9135-z

Keywords

  • Phytochrome
  • Pseudogenes
  • Gene family evolution
  • Scots pine