Article thumbnail
Location of Repository

Positive Selection Drives the Evolution of rhino, a Member of the Heterochromatin Protein 1 Family in Drosophila

By Danielle Vermaak, Steven Henikoff and Harmit S Malik

Abstract

Heterochromatin comprises a significant component of many eukaryotic genomes. In comparison to euchromatin, heterochromatin is gene poor, transposon rich, and late replicating. It serves many important biological roles, from gene silencing to accurate chromosome segregation, yet little is known about the evolutionary constraints that shape heterochromatin. A complementary approach to the traditional one of directly studying heterochromatic DNA sequence is to study the evolution of proteins that bind and define heterochromatin. One of the best markers for heterochromatin is the heterochromatin protein 1 (HP1), which is an essential, nonhistone chromosomal protein. Here we investigate the molecular evolution of five HP1 paralogs present in Drosophila melanogaster. Three of these paralogs have ubiquitous expression patterns in adult Drosophila tissues, whereas HP1D/rhino and HP1E are expressed predominantly in ovaries and testes respectively. The HP1 paralogs also have distinct localization preferences in Drosophila cells. Thus, Rhino localizes to the heterochromatic compartment in Drosophila tissue culture cells, but in a pattern distinct from HP1A and lysine-9 dimethylated H3. Using molecular evolution and population genetic analyses, we find that rhino has been subject to positive selection in all three domains of the protein: the N-terminal chromo domain, the C-terminal chromo-shadow domain, and the hinge region that connects these two modules. Maximum likelihood analysis of rhino sequences from 20 species of Drosophila reveals that a small number of residues of the chromo and shadow domains have been subject to repeated positive selection. The rapid and positive selection of rhino is highly unusual for a gene encoding a chromosomal protein and suggests that rhino is involved in a genetic conflict that affects the germline, belying the notion that heterochromatin is simply a passive recipient of “junk DNA” in eukaryotic genomes

Topics: Research Article
Publisher: Public Library of Science
Year: 2005
DOI identifier: 10.1371/journal.pgen.0010009
OAI identifier: oai:pubmedcentral.nih.gov:1183528
Provided by: PubMed Central

Suggested articles

Citations

  1. (1990). A kinesin-like protein required for distributive chromosome segregation in Drosophila.
  2. (1999). A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation.
  3. (1973). A new evolutionary law.
  4. (1997). A screen for fast evolving genes from Drosophila.
  5. (1991). A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants.
  6. (1994). A study of the interaction of DAPI with DNA containing AT and non-AT sequences—molecular specificity of minor groove binding drugs.
  7. (1987). A test of neutral molecular evolution based on nucleotide data.
  8. (2002). Accuracy and power of Bayes prediction of amino acid sites under positive selection.
  9. (2004). Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites.
  10. (2004). Adaptive evolution of centromere proteins in plants and animals.
  11. (2001). Adaptive evolution of Cid, a centromerespecific histone in Drosophila.
  12. (1991). Adaptive protein evolution at the Adh locus in Drosophila.
  13. (2004). Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS
  14. (2003). bind to sets of developmentally coexpressed genes depending on chromosomal location.
  15. (2003). Cell cycle behavior of human HP1 subtypes: Distinct molecular domains of HP1 are required for their centromeric localization during interphase and metaphase.
  16. (2002). Centromere round-up at the heterochromatin corral.
  17. (2002). Centromere targeting element within the histone fold domain of Cid.
  18. (1990). Chovnick A
  19. (2004). cis-Acting determinants of heterochromatin formation on Drosophila melanogaster chromosome four.
  20. (2000). Cn3D: Sequence and structure views for Entrez.
  21. (2002). Conflict begets complexity: The evolution of centromeres.
  22. (2000). Dimerisation of a chromo shadow domain and distinctions from the chromodomain as revealed by structural analysis.
  23. (1994). DNA Strider. A Macintosh program for handling protein and nucleic acid sequences.
  24. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods.
  25. (2002). Does heterochromatin protein 1 always follow code?
  26. (2001). Domain organization at the centromere and neocentromere.
  27. (2000). Down-regulation of HP1Hsalpha expression is associated with the metastatic phenotype in breast cancer.
  28. (2001). Drosophila rhino encodes a female-specific chromo-domain protein that affects chromosome structure and egg polarity.
  29. (2003). Effects of tethering HP1 to euchromatic regions of the Drosophila genome.
  30. (2003). Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice.
  31. (2002). Epigenetic codes for heterochromatin formation and silencing: Rounding up the usual suspects.
  32. (2004). Eukaryotic gene regulation by targeted chromatin remodeling at dispersed, middle-repetitive sequence elements.
  33. (1996). Excess amino acid polymorphism in mitochondrial DNA: Contrasts among genes from Drosophila, mice, and humans.
  34. (2001). Expression and functional analysis of three isoforms of human heterochromatin-associated protein HP1 in Drosophila.
  35. (1995). Functional analysis of the chromo domain of HP1.
  36. (1999). Genetic variation in rates of PLoS Genetics | www.plosgenetics.org
  37. (2000). Heterochromatic deposition of centromeric histone H3-like proteins.
  38. (2002). Heterochromatic sequences in a Drosophila whole-genome shotgun assembly.
  39. (2004). Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery.
  40. (2003). Heterochromatin and epigenetic control of gene expression.
  41. (1995). Heterochromatin and gene expression in Drosophila.
  42. (2004). Heterochromatin structure and function.
  43. (2002). Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals.
  44. (2003). HP1 binding to native chromatin in vitro is determined by the hinge region and not by the chromodomain.
  45. (2003). HP1/ORC complex and heterochromatin assembly.
  46. (2000). HP1gamma associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes.
  47. (1986). Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene.
  48. (2000). Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase.
  49. (1995). Identification of the chromosome localization domain of the Drosophila nod kinesin-like protein.
  50. (2001). Immunolocalization of HP1 proteins in metaphasic mammalian chromosomes.
  51. (1999). K-Estimator: Calculation of the number of nucleotide substitutions per site and the confidence intervals.
  52. (1999). Large number of replacement polymorphisms in rapidly evolving genes of Drosophila. Implications for genome-wide surveys of DNA polymorphism.
  53. (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins.
  54. (2002). Microdissection and sequence analysis of pericentric heterochromatin from the Drosophila melanogaster mutant Suppressor of Underreplication.
  55. (2003). Mobile elements and mammalian genome evolution.
  56. (2004). Mobile elements: Drivers of genome evolution.
  57. (2001). Molecular biology of the chromo domain: an ancient chromatin module comes of age.
  58. (2005). Mutations in the heterochromatin protein 1 (HP1) hinge domain affect HP1 protein interactions and chromosomal distribution.
  59. (1997). PAML: A program package for phylogenetic analysis by maximum likelihood.
  60. (2001). PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4: Sunderland (Massachusetts): Sinauer Associates.
  61. (2004). Planting the seeds of a new paradigm.
  62. (2003). Protein-DNA interaction mapping using genomic tiling path microarrays in Drosophila.
  63. (2002). Recurrent evolution of DNAbinding motifs in the Drosophila centromeric histone.
  64. (2001). Requirement of heterochromatin for cohesion at centromeres.
  65. (2001). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain.
  66. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
  67. (1993). Statistical tests of neutrality of mutations.
  68. (2004). Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin.
  69. (2002). Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail.
  70. (2004). Subcellular distribution of HP1 proteins is altered in ICF syndrome.
  71. (2001). The centromere paradox: Stable inheritance with rapidly evolving DNA.
  72. (1995). The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1.
  73. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
  74. (2003). The Drosophila HOAP protein is required for telomere capping.
  75. (1990). The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster.
  76. (2000). The genome sequence of Drosophila melanogaster.
  77. (1992). The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation.
  78. (2001). The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins.
  79. (2000). The HP1 chromo shadow domain binds a consensus peptide pentamer.
  80. (2000). The HP1 protein family: getting a grip on chromatin.
  81. (1991). The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila.
  82. (2000). The structure of mouse HP1 suggests a unique mode of single peptide recognition by the shadow chromo domain dimer.
  83. (2002). The transposable elements of the Drosophila melanogaster euchromatin: A genomics perspective.
  84. (1990). Transcripts of individual Drosophila actin genes are differentially distributed during embryogenesis.

To submit an update or takedown request for this paper, please submit an Update/Correction/Removal Request.