Faint gray bands in Drosophila melanogaster polytene chromosomes are formed by coding sequences of housekeeping genes

Chromosoma. 2020 Mar;129(1):25-44. doi: 10.1007/s00412-019-00728-2. Epub 2019 Dec 9.

Abstract

In Drosophila melanogaster, the chromatin of interphase polytene chromosomes appears as alternating decondensed interbands and dense black or thin gray bands. Recently, we uncovered four principle chromatin states (4НММ model) in the fruit fly, and these were matched to the structures observed in polytene chromosomes. Ruby/malachite chromatin states form black bands containing developmental genes, whereas aquamarine chromatin corresponds to interbands enriched with 5' regions of ubiquitously expressed genes. Lazurite chromatin supposedly forms faint gray bands and encompasses the bodies of housekeeping genes. In this report, we test this idea using the X chromosome as the model and MSL1 as a protein marker of the lazurite chromatin. Our bioinformatic analysis indicates that in the X chromosome, it is only the lazurite chromatin that is simultaneously enriched for the proteins and histone marks associated with exons, transcription elongation, and dosage compensation. As a result of FISH and EM mapping of a dosage compensation complex subunit, MSL1, we for the first time provide direct evidence that lazurite chromatin forms faint gray bands. Our analysis proves that overall most of housekeeping genes typically span from the interbands (5' region of the gene) to the gray band (gene body). More rarely, active lazurite chromatin and inactive malachite/ruby chromatin may be found within a common band, where both the housekeeping and the developmental genes reside together.

Keywords: 4HMM chromatin model; Chromatin types; Drosophila; Housekeeping genes; MSL1; Polytene chromosome bands and interbands.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis Proteins / metabolism
  • Chromatin / genetics
  • Chromosome Banding*
  • Computational Biology / methods
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Female
  • Gene Rearrangement
  • Genes, Essential*
  • Histones / metabolism
  • In Situ Hybridization, Fluorescence
  • Ion Channels / metabolism
  • Male
  • Mutation
  • Open Reading Frames*
  • Polytene Chromosomes / genetics*
  • Protein Serine-Threonine Kinases / metabolism
  • Sex Chromosomes

Substances

  • AT4G00290 protein, Arabidopsis
  • Arabidopsis Proteins
  • Chromatin
  • Drosophila Proteins
  • Histones
  • Ion Channels
  • JIL-1 protein, Drosophila
  • Protein Serine-Threonine Kinases