Histone removal in sperm protects paternal chromosomes from premature division at fertilization
The global replacement of histones with protamines in sperm chromatin is widespread in animals, including insects, but its actual function remains enigmatic. We show that in the Drosophila paternal effect mutant paternal loss ( pal ), sperm chromatin retains germline histones H3 and H4 genome wide w...
Saved in:
Published in | Science (American Association for the Advancement of Science) Vol. 382; no. 6671; pp. 725 - 731 |
---|---|
Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
Washington
The American Association for the Advancement of Science
10.11.2023
|
Subjects | |
Online Access | Get full text |
Cover
Loading…
Summary: | The global replacement of histones with protamines in sperm chromatin is widespread in animals, including insects, but its actual function remains enigmatic. We show that in the
Drosophila
paternal effect mutant
paternal loss
(
pal
), sperm chromatin retains germline histones H3 and H4 genome wide without impairing sperm viability. However, after fertilization,
pal
sperm chromosomes are targeted by the egg chromosomal passenger complex and engage into a catastrophic premature division in synchrony with female meiosis II. We show that
pal
encodes a rapidly evolving transition protein specifically required for the eviction of (H3-H4)
2
tetramers from spermatid DNA after the removal of H2A-H2B dimers. Our study thus reveals an unsuspected role of histone eviction from insect sperm chromatin: safeguarding the integrity of the male pronucleus during female meiosis.
Editor’s summary
Ultracompaction of sperm DNA in many species is often associated with genome-wide replacement of histones with protamines, but the actual role of this radical change in chromatin organization remains largely enigmatic. Looking at a multidecade-old
Drosophila
mutant, Dubruille
et al
. found that histones were massively retained in sperm without affecting its ability to fertilize (see the Perspective by Levine). However, at fertilization, male chromosomes were aberrantly recognized by maternal factors that control female meiotic progression, leading to a deleterious premature division and early loss of male chromosomes. This work highlights the role of sperm chromatin in protecting male chromosomes in the egg. —Di Jiang
Histone retention in
Drosophila
sperm chromatin jeopardizes paternal chromosome integrity during female meiosis. |
---|---|
Bibliography: | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors contributed equally to this work. Present address: Department of Genetics, University of Geneva, Geneva, Switzerland. Present address: Institute of Ecology and Evolution, University of Edinburgh, Edinburgh, UK. Author contributions: Conceptualization: R.D., C.-H.C., and B.L.; Methodology: R.D., M.H., C.-H.C., B.H., and B.L.; Investigation: R.D., M.H., M.R., B.H., C.-H.C., and B.L.; Visualization: R.D., M.H., C.-H.C., B.H., and B.L.; Funding acquisition: R.D., C.-H.C., and B.L.; Supervision: R.D. and B.L.; Writing – original draft: B.L.; Writing – review and editing: R.D., M.H., B.H., C.-H.C., and B.L. |
ISSN: | 0036-8075 1095-9203 |
DOI: | 10.1126/science.adh0037 |