Transgenerational propagation and quantitative maintenance of paternal centromeres depends on Cid/Cenp-A presence in Drosophila sperm

PLoS Biol. 2012;10(12):e1001434. doi: 10.1371/journal.pbio.1001434. Epub 2012 Dec 27.

Abstract

In Drosophila melanogaster, as in many animal and plant species, centromere identity is specified epigenetically. In proliferating cells, a centromere-specific histone H3 variant (CenH3), named Cid in Drosophila and Cenp-A in humans, is a crucial component of the epigenetic centromere mark. Hence, maintenance of the amount and chromosomal location of CenH3 during mitotic proliferation is important. Interestingly, CenH3 may have different roles during meiosis and the onset of embryogenesis. In gametes of Caenorhabditis elegans, and possibly in plants, centromere marking is independent of CenH3. Moreover, male gamete differentiation in animals often includes global nucleosome for protamine exchange that potentially could remove CenH3 nucleosomes. Here we demonstrate that the control of Cid loading during male meiosis is distinct from the regulation observed during the mitotic cycles of early embryogenesis. But Cid is present in mature sperm. After strong Cid depletion in sperm, paternal centromeres fail to integrate into the gonomeric spindle of the first mitosis, resulting in gynogenetic haploid embryos. Furthermore, after moderate depletion, paternal centromeres are unable to re-acquire normal Cid levels in the next generation. We conclude that Cid in sperm is an essential component of the epigenetic centromere mark on paternal chromosomes and it exerts quantitative control over centromeric Cid levels throughout development. Hence, the amount of Cid that is loaded during each cell cycle appears to be determined primarily by the preexisting centromeric Cid, with little flexibility for compensation of accidental losses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Centromere / metabolism*
  • Centromere Protein A
  • Chromosomal Proteins, Non-Histone / metabolism
  • Chromosomes / metabolism
  • DNA-Binding Proteins / metabolism*
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics*
  • Embryonic Development / genetics
  • Fertilization
  • G2 Phase / genetics
  • Green Fluorescent Proteins / metabolism
  • Histones / metabolism*
  • Inheritance Patterns / genetics*
  • Kinetochores / metabolism
  • Male
  • Recombinant Fusion Proteins / metabolism
  • Spermatogenesis / genetics
  • Spermatozoa / metabolism*

Substances

  • Centromere Protein A
  • Chromosomal Proteins, Non-Histone
  • Cid protein, Drosophila
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Histones
  • Recombinant Fusion Proteins
  • centromere protein C
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins

Grant support

This work was supported by grants from the Deutsche Forschungsgemeinschaft (DFG Le987/6-1), the Swiss National Science Foundation (310003A-120276), and the French National Research Agency (ANR-08-BLAN-0139-01). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.