Abstract
The differentiation of post-meiotic spermatids in animals is characterized by a unique reorganization of their nuclear architecture and chromatin composition. In many species, the formation of sperm nuclei involves the massive replacement of nucleosomes with protamines, followed by a phase of extreme nuclear compaction. At fertilization, the reconstitution of a nucleosome-based paternal chromatin after the removal of protamines requires the deposition of maternally provided histones before the first round of DNA replication. This process exclusively uses the histone H3 variant H3.3 and constitutes a unique case of genome-wide replication-independent (RI) de novo chromatin assembly. We had previously shown that the histone H3.3 chaperone HIRA plays a central role for paternal chromatin assembly in Drosophila. Although several conserved HIRA-interacting proteins have been identified from yeast to human, their conservation in Drosophila, as well as their actual implication in this highly peculiar RI nucleosome assembly process, is an open question. Here, we show that Yemanuclein (YEM), the Drosophila member of the Hpc2/Ubinuclein family, is essential for histone deposition in the male pronucleus. yem loss of function alleles affect male pronucleus formation in a way remarkably similar to Hira mutants and abolish RI paternal chromatin assembly. In addition, we demonstrate that HIRA and YEM proteins interact and are mutually dependent for their targeting to the decondensing male pronucleus. Finally, we show that the alternative ATRX/XNP-dependent H3.3 deposition pathway is not involved in paternal chromatin assembly, thus underlining the specific implication of the HIRA/YEM complex for this essential step of zygote formation.
Publication types
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Research Support, Non-U.S. Gov't
MeSH terms
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Animals
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Cell Cycle Proteins* / genetics
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Cell Cycle Proteins* / metabolism
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Cell Nucleus / genetics
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Cell Nucleus / metabolism
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Chromatin / metabolism
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Chromatin / ultrastructure
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Chromatin Assembly and Disassembly
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DNA Replication / genetics
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DNA-Binding Proteins* / genetics
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DNA-Binding Proteins* / metabolism
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Drosophila Proteins* / genetics
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Drosophila Proteins* / metabolism
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Drosophila melanogaster / genetics
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Drosophila melanogaster / metabolism
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Fertilization / genetics
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Histone Chaperones* / genetics
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Histone Chaperones* / metabolism
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Histones / genetics
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Histones / metabolism
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Male
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Nuclear Proteins* / genetics
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Nuclear Proteins* / metabolism
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Nucleosomes* / genetics
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Nucleosomes* / metabolism
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Spermatozoa / cytology
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Spermatozoa / metabolism
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Transcription Factors* / genetics
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Transcription Factors* / metabolism
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Zygote* / growth & development
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Zygote* / metabolism
Substances
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Cell Cycle Proteins
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Chromatin
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DNA-Binding Proteins
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Drosophila Proteins
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Hira protein, Drosophila
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Histone Chaperones
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Histones
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Nuclear Proteins
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Nucleosomes
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Transcription Factors
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yem protein, Drosophila
Grants and funding
Work in the laboratory of BL was supported by the CNRS, the French Ministry of Research, and the ANR (
http://www.agence-nationale-recherche.fr/) (ANR-08-BLAN-0139-01). GAO was supported by the French Ministry of Research and the Association pour la Recherche sur le Cancer (Fondation ARC,
http://www.arc-cancer.net/)(DOC20100601010). Work in the laboratory of OA-A was supported by the CNRS and the Fondation ARC (ARC 9932). REM was a recipient of a 3-year fellowship from the French Ministry of Research and a 1-year ARC fellowship. AA has been supported by a 4-year fellowship from the Egyptian Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.