The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus.
In sexually reproducing animals, a crucial step in zygote formation is the decondensation of the fertilizing sperm nucleus into a DNA replication-competent male pronucleus. Genome-wide nucleosome assembly on paternal DNA implies the replacement of sperm chromosomal proteins, such as protamines, by maternally provided histones. This fundamental process is specifically impaired in sésame (ssm), a unique Drosophila maternal effect mutant that prevents male pronucleus formation. Here we show that ssm is a point mutation in the Hira gene, thus demonstrating that the histone chaperone protein HIRA is required for nucleosome assembly during sperm nucleus decondensation. In vertebrates, HIRA has recently been shown to be critical for a nucleosome assembly pathway independent of DNA synthesis that specifically involves the H3.3 histone variant. We also show that nucleosomes containing H3.3, and not H3, are specifically assembled in paternal Drosophila chromatin before the first round of DNA replication. The exclusive marking of paternal chromosomes with H3.3 represents a primary epigenetic distinction between parental genomes in the zygote, and underlines an important consequence of the critical and highly specialized function of HIRA at fertilization.
Loppin
Benjamin
B
Centre de Génétique Moléculaire et Cellulaire, U.M.R. 5534, C.N.R.S.-Université Claude Bernard, Lyon-1, 69622 Villeurbanne, France. loppin@cgmc.univ-lyon1.fr
Bonnefoy
Emilie
E
Anselme
Caroline
C
Laurençon
Anne
A
Karr
Timothy L
TL
Couble
Pierre
P
D000595:Amino Acid Sequence; D000818:Animals; D018797:Cell Cycle Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D002467:Cell Nucleus / Q000235:genetics* / Q000378:metabolism*; D002843:Chromatin / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D004261:DNA Replication; D029721:Drosophila Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000166:cytology / Q000235:genetics; D005260:Female; D005306:Fertilization; D056488:Histone Chaperones; D006657:Histones / Q000145:classification / Q000235:genetics / Q000378:metabolism*; D008297:Male; D008745:Methylation; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D010063:Ovum / Q000166:cytology; D013094:Spermatozoa / Q000166:cytology*; D014157:Transcription Factors / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*
D018797:Cell Cycle Proteins; D002843:Chromatin; D029721:Drosophila Proteins; C488124:Hira protein, Drosophila; D056488:Histone Chaperones; D006657:Histones; D014157:Transcription Factors