scholarly journals Gametic specialization of centromeric histone paralogs in Drosophila virilis

2021 ◽  
Vol 4 (7) ◽  
pp. e202000992
Author(s):  
Lisa E Kursel ◽  
Hannah McConnell ◽  
Aida Flor A de la Cruz ◽  
Harmit S Malik
Keyword(s):  
Animal Species ◽  
Epigenetic Inheritance ◽  
Early Embryo ◽  
Male Meiosis ◽  
Drosophila Virilis ◽  
Gene Duplications ◽  
Functional Requirements ◽  
Cytological Localization ◽  
Intralocus Conflict ◽  
Mitosis And Meiosis

In most eukaryotes, centromeric histone (CenH3) proteins mediate mitosis and meiosis and ensure epigenetic inheritance of centromere identity. We hypothesized that disparate chromatin environments in soma versus germline might impose divergent functional requirements on single CenH3 genes, which could be ameliorated by gene duplications and subsequent specialization. Here, we analyzed the cytological localization of two recently identified CenH3 paralogs, Cid1 and Cid5, in Drosophila virilis using specific antibodies and epitope-tagged transgenic strains. We find that only ancestral Cid1 is present in somatic cells, whereas both Cid1 and Cid5 are expressed in testes and ovaries. However, Cid1 is lost in male meiosis but retained throughout oogenesis, whereas Cid5 is lost during female meiosis but retained in mature sperm. Following fertilization, only Cid1 is detectable in the early embryo, suggesting that maternally deposited Cid1 is rapidly loaded onto paternal centromeres during the protamine-to-histone transition. Our studies reveal mutually exclusive gametic specialization of divergent CenH3 paralogs. Duplication and divergence might allow essential centromeric genes to resolve an intralocus conflict between maternal and paternal centromeric requirements in many animal species.

scholarly journals Gametic specialization of centromeric histone paralogs in Drosophila virilis

2019 ◽  
Author(s):  
Lisa E. Kursel ◽  
Harmit S. Malik
Keyword(s):  
Chromosome Segregation ◽  
Epigenetic Inheritance ◽  
Male Meiosis ◽  
Drosophila Virilis ◽  
Sperm Chromatin ◽  
Kinetochore Assembly ◽  
Assembly Factor ◽  
Cytological Localization ◽  
Multicellular Organisms ◽  
Intralocus Conflict

AbstractIn most eukaryotes, centromeric histone (CenH3) proteins mediate the highly conserved process of chromosome segregation as the foundational kinetochore assembly factor. However, in multicellular organisms, CenH3 proteins have to perform their essential functions in different chromatin environments. CenH3 proteins not only mediate mitosis and meiosis but also ensure epigenetic inheritance of centromere identity on sperm chromatin, which is highly compact and almost completely stripped of histones during spermiogenesis. We hypothesized that such disparate chromatin environments might impose different functional constraints on CenH3. If so, gene duplications could ameliorate the difficulty of encoding divergent and even potentially incompatible centromeric functions in the same gene. Here, we analyzed the cytological localization of two recently identified CenH3 paralogs, Cid1 and Cid5, in D. virilis using specific antibodies and epitope-tagged transgenic strains. We find that only ancestral Cid1 is present in somatic cells, whereas both Cid1 and Cid5 are expressed in testes and ovaries. However, Cid1 and Cid5 are alternately retained in male and female gametes; Cid1 is lost in male meiosis but retained throughout oogenesis, whereas Cid5 is lost during female meiosis but retained in mature sperm. Following fertilization, maternally deposited Cid1 rapidly replaces paternal Cid5 during the protamine-to-histone transition. Our studies reveal mutually exclusive gametic specialization of two divergent CenH3 paralogs. We suggest that centromeric histone duplication and divergence may allow essential genes involved in chromosome segregation to specialize and thereby resolve an intralocus conflict between maternal and paternal centromeric histone requirements in many animal species.

The nucleosome: a little variation goes a long wayThis paper is one of a selection of papers published in this Special Issue, entitled 27th International West Coast Chromatin and Chromosome Conference, and has undergone the Journal's usual peer review process.

2006 ◽  
Vol 84 (4) ◽  
pp. 505-507 ◽  
Author(s):  
Emily Bernstein ◽  
Sandra B. Hake
Keyword(s):  
Peer Review Process ◽  
Gene Activation ◽  
Epigenetic Inheritance ◽  
Histone Variants ◽  
Post Translational Modifications ◽  
Chromatin Compaction ◽  
Cellular Processes ◽  
Chromatin Template ◽  
Mitosis And Meiosis ◽  
Selection Of

Changes in the overall structure of chromatin are essential for the proper regulation of cellular processes, including gene activation and silencing, DNA repair, chromosome segregation during mitosis and meiosis, X chromosome inactivation in female mammals, and chromatin compaction during apoptosis. Such alterations of the chromatin template occur through at least 3 interrelated mechanisms: post-translational modifications of histones, ATP-dependent chromatin remodeling, and the incorporation (or replacement) of specialized histone variants into chromatin. Of these mechanisms, the exchange of variants into and out of chromatin is the least well understood. However, the exchange of conventional histones for variant histones has distinct and profound consequences within the cell. This review focuses on the growing number of mammalian histone variants, their particular biological functions and unique features, and how they may affect the structure of the nucleosome. We propose that a given nucleosome might not consist of heterotypic variants, but rather, that only specific histone variants come together to form a homotypic nucleosome, a hypothesis that we refer to as the nucleosome code. Such nucleosomes might in turn participate in marking specific chromatin domains that may contribute to epigenetic inheritance.

scholarly journals Xist imprinting is promoted by the hemizygous (unpaired) state in the male germ line

2015 ◽  
Vol 112 (47) ◽  
pp. 14415-14422 ◽  
Author(s):  
Sha Sun ◽  
Bernhard Payer ◽  
Satoshi Namekawa ◽  
Jee Young An ◽  
William Press ◽  
...  
Keyword(s):  
X Chromosome ◽  
Germ Line ◽  
Transgenic Animals ◽  
Early Embryo ◽  
Male Meiosis ◽  
Meiotic Pairing ◽  
Male Germ Line ◽  
Specific Expression ◽  
X Chromosomes ◽  
High Level

The long noncoding X-inactivation–specific transcript (Xist gene) is responsible for mammalian X-chromosome dosage compensation between the sexes, the process by which one of the two X chromosomes is inactivated in the female soma. Xist is essential for both the random and imprinted forms of X-chromosome inactivation. In the imprinted form, Xist is paternally marked to be expressed in female embryos. To investigate the mechanism of Xist imprinting, we introduce Xist transgenes (Tg) into the male germ line. Although ectopic high-level Xist expression on autosomes can be compatible with viability, transgenic animals demonstrate reduced fitness, subfertility, defective meiotic pairing, and other germ-cell abnormalities. In the progeny, paternal-specific expression is recapitulated by the 200-kb Xist Tg. However, Xist imprinting occurs efficiently only when it is in an unpaired or unpartnered state during male meiosis. When transmitted from a hemizygous father (+/Tg), the Xist Tg demonstrates paternal-specific expression in the early embryo. When transmitted by a homozygous father (Tg/Tg), the Tg fails to show imprinted expression. Thus, Xist imprinting is directed by sequences within a 200-kb X-linked region, and the hemizygous (unpaired) state of the Xist region promotes its imprinting in the male germ line.

scholarly journals Sperm and seminal plasma RNAs: what roles do they play beyond fertilization?

Reproduction ◽  
2019 ◽  
Vol 158 (4) ◽  
pp. R113-R123 ◽  
Author(s):  
Meritxell Jodar
Keyword(s):  
Gene Expression ◽  
Embryo Development ◽  
Seminal Plasma ◽  
Preimplantation Embryo ◽  
Epigenetic Inheritance ◽  
Early Embryo ◽  
Female Reproductive Tract ◽  
Transcriptional Level ◽  
Preimplantation Embryo Development ◽  
The Impact

The paternal contribution to the new individual is not just limited to half the diploid genome. Recent findings have shown that sperm delivers to the oocyte several components, including a complex population of RNAs, which may influence early embryo development and the long-term phenotype of the offspring. Although the majority of sperm RNAs may only represent spermatogenic leftovers with no further function, the male gamete provides a specific set of RNAs to the oocyte that is able to modulate gene expression in the preimplantation embryo. Those sperm transcripts include coding and non-coding RNAs that might either be translated by the oocyte machinery or directly regulate embryo gene expression at the transcriptional or post-transcriptional level. Interestingly, some sperm RNAs seem to be acquired during post-testicular maturation through active communication between sperm and epididymal and seminal exosomes released by the epididymis and the male accessory sex glands, respectively. Exosomes contained in the seminal plasma seem to not only interact with the spermatozoa but also with cells from the female reproductive tract, modulating their gene expression and influencing female immune response triggered by the semen. This review also considers the findings that indicate the role of semen RNAs in preimplantation embryo development and offspring phenotypes. In this regard, different studies supporting the hypothesis of paternal epigenetic inheritance of altered metabolic phenotypes associated with environmental exposures are discussed. Lastly, potential mechanisms that could explain the impact of semen RNAs to both early embryogenesis and paternal epigenetic inheritance are suggested.

scholarly journals A Burst of Genetic Innovation in Drosophila Actin-Related Proteins for Testis-Specific Function

2019 ◽  
Vol 37 (3) ◽  
pp. 757-772
Author(s):  
Courtney M Schroeder ◽  
John R Valenzuela ◽  
Isabel Mejia Natividad ◽  
Glen M Hocky ◽  
Harmit S Malik
Keyword(s):  
Positive Selection ◽  
Male Meiosis ◽  
Cytoskeletal Proteins ◽  
Gene Duplications ◽  
Actin Networks ◽  
Male Germline ◽  
Phylogenomic Analyses ◽  
Sperm Heteromorphism ◽  
Related Proteins ◽  
Obscura Group

Abstract Many cytoskeletal proteins perform fundamental biological processes and are evolutionarily ancient. For example, the superfamily of actin-related proteins (Arps) specialized early in eukaryotic evolution for diverse cellular roles in the cytoplasm and the nucleus. Despite its strict conservation across eukaryotes, we find that the Arp superfamily has undergone dramatic lineage-specific diversification in Drosophila. Our phylogenomic analyses reveal four independent Arp gene duplications that occurred in the common ancestor of the obscura group of Drosophila and have been mostly preserved in this lineage. All four obscura-specific Arp paralogs are predominantly expressed in the male germline and have evolved under positive selection. We focus our analyses on the divergent Arp2D paralog, which arose via a retroduplication event from Arp2, a component of the Arp2/3 complex that polymerizes branched actin networks. Computational modeling analyses suggest that Arp2D can replace Arp2 in the Arp2/3 complex and bind actin monomers. Together with the signature of positive selection, our findings suggest that Arp2D may augment Arp2’s functions in the male germline. Indeed, we find that Arp2D is expressed during and following male meiosis, where it localizes to distinct locations such as actin cones—specialized cytoskeletal structures that separate bundled spermatids into individual mature sperm. We hypothesize that this unprecedented burst of genetic innovation in cytoskeletal proteins may have been driven by the evolution of sperm heteromorphism in the obscura group of Drosophila.

DNA methylation in the vertebrate germline: balancing memory and erasure

2019 ◽  
Vol 63 (6) ◽  
pp. 649-661 ◽  
Author(s):  
Oscar Ortega-Recalde ◽  
Timothy Alexander Hore
Keyword(s):  
Dna Methylation ◽  
Cytosine Methylation ◽  
Epigenetic Modification ◽  
Epigenetic Inheritance ◽  
Direct Consequence ◽  
Early Embryo ◽  
Germline Development ◽  
Evolutionary Mechanisms ◽  
Information Module ◽  
Methylation Patterns

Abstract Cytosine methylation is a DNA modification that is critical for vertebrate development and provides a plastic yet stable information module in addition to the DNA code. DNA methylation memory establishment, maintenance and erasure is carefully balanced by molecular machinery highly conserved among vertebrates. In mammals, extensive erasure of epigenetic marks, including 5-methylcytosine (5mC), is a hallmark of early embryo and germline development. Conversely, global cytosine methylation patterns are preserved in at least some non-mammalian vertebrates over comparable developmental windows. The evolutionary mechanisms which drove this divergence are unknown, nevertheless a direct consequence of retaining epigenetic memory in the form of 5mC is the enhanced potential for transgenerational epigenetic inheritance (TEI). Given that DNA methylation dynamics remains underexplored in most vertebrate lineages, the extent of information transferred to offspring by epigenetic modification might be underestimated.

scholarly journals Drosophila Centrosomin Protein is Required for Male Meiosis and Assembly of the Flagellar Axoneme

1998 ◽  
Vol 141 (2) ◽  
pp. 455-467 ◽  
Author(s):  
Kaijun Li ◽  
Eugene Yujun Xu ◽  
Jeffrey K. Cecil ◽  
F. Rudolf Turner ◽  
Timothy L. Megraw ◽  
...  
Keyword(s):  
Drosophila Melanogaster ◽  
Cell Division ◽  
Basal Body ◽  
Mutational Analysis ◽  
Male Meiosis ◽  
Mitosis And Meiosis ◽  
Flagellar Axoneme

Centrosomes and microtubules play crucial roles during cell division and differentiation. Spermatogenesis is a useful system for studying centrosomal function since it involves both mitosis and meiosis, and also transformation of the centriole into the sperm basal body. Centrosomin is a protein localized to the mitotic centrosomes in Drosophila melanogaster. We have found a novel isoform of centrosomin expressed during spermatogenesis. Additionally, an anticentrosomin antibody labels both the mitotic and meiotic centrosomes as well as the basal body. Mutational analysis shows that centrosomin is required for spindle organization during meiosis and for organization of the sperm axoneme. These results suggest that centrosomin is a necessary component of the meiotic centrosomes and the spermatid basal body.

scholarly journals Mutations in New Cell Cycle Genes That Fail to Complement a Multiply Mutant Third Chromosome of Drosophila

Genetics ◽  
1996 ◽  
Vol 144 (3) ◽  
pp. 1097-1111 ◽  
Author(s):  
Helen White-Cooper ◽  
Mar Cannena ◽  
Cayetano Gonzalez ◽  
David M Glover
Keyword(s):  
Cell Cycle ◽  
Male Meiosis ◽  
Mitotic Abnormalities ◽  
New Gene ◽  
Complementation Groups ◽  
In Trans ◽  
Lethal Allele ◽  
Mitosis And Meiosis ◽  
Pharate Adult ◽  
New Alleles

Abstract We have simultaneously screened for new alleles and second site mutations that fail to complement five cell cycle mutations of Drosophila carried on a single third chromosome (gnu, polo, mgr, asp, stg). Females that are either transheterozygous for scott of the antartic (scant) and polo, or homozygous for scant produce embryos that show mitotic defects. A maternal effect upon embryonic mitoses is also seen in embryos derived from females transheterozygous with helter skelter (hsk) and either mgr or asp. deopatra (cleo), fails to complement asp but is not uncovered by a deficiency for asp. The mitotic phenotype of larvae heterozygous for cleo and the multiple mutant chromosome is similar to weak alleles of asp, but there are no defects in male meiosis. Mutations that failed to complement stgfell into two complementation groups corresponding to stg and a new gene noose. Three of the new stg alleles are early zygotic lethals, whereas the fourth is a pharate adult lethal allele that affects both mitosis and meiosis. Mutations in noose fully complement a small deficiency that removes stg, but when placed in trans to certain stg alleles, result in late lethality and mitotic abnormalities in larval brains.

scholarly journals Haspin participates in Aurora phosphorylation at centromeres and contributes to chromosome congression in male mouse meiosis

2021 ◽  
Author(s):  
Ines Berenguer ◽  
Pablo Lopez Jimenez ◽  
Irene Mena ◽  
Alberto Viera ◽  
Jesus Page ◽  
...  
Keyword(s):  
Relevant Information ◽  
Male Meiosis ◽  
Histone Mark ◽  
Aurora B ◽  
Genetic Mouse Model ◽  
Chromosome Congression ◽  
Chromosomal Passenger ◽  
Mitosis And Meiosis

Chromosome segregation requires that centromeres properly attach to spindle microtubules. This is an essential step towards the accuracy of cell division and therefore must be precisely regulated in both mitosis and meiosis. One of the main centromeric regulatory signaling pathways is the Haspin-H3T3ph-chromosomal passenger complex (CPC) cascade, which is responsible for the recruitment of the CPC to the centromeres. In mitosis, Haspin kinase phosphorylates H3 at threonine 3 (H3T3ph), the essential histone mark that recruits the CPC whose catalytic component is Aurora B kinase. To date, no data has yet been presented about the action of the centromeric Haspin-H3T3ph-CPC pathway in mammalian male meiosis. We have analyzed the consequences of Haspin chemical inhibition in cultured spermatocytes using LDN-192960. Our in vitro studies suggest that Haspin kinase activity is required for proper chromosome congression during both meiotic divisions and for the recruitment of phosphorylated Aurora B at meiotic centromeres. These results have been confirmed by the characterization of the meiotic phenotype of the genetic mouse model Haspin-/-, which displays similar defects. In addition, our work demonstrates that the absence of H3T3ph histone mark does not alter SGO2 localization to meiotic centromeres. These results add new and relevant information regarding the regulation of centromere function during meiosis.

Drosophila virilis oskar transgenes direct body patterning but not pole cell formation or maintenance of mRNA localization in D. melanogaster

Development ◽  
1994 ◽  
Vol 120 (7) ◽  
pp. 2027-2037 ◽  
Author(s):  
P.J. Webster ◽  
J. Suen ◽  
P.M. Macdonald
Keyword(s):  
Drosophila Melanogaster ◽  
Germ Cell ◽  
Cell Formation ◽  
Mrna Localization ◽  
Early Embryo ◽  
Posterior Pole ◽  
Early Embryogenesis ◽  
Drosophila Virilis ◽  
Pole Cell ◽  
Body Patterning

The Drosophila melanogaster gene oskar is required for both posterior body patterning and germline formation in the early embryo; precisely how oskar functions is unknown. The oskar transcript is localized to the posterior pole of the developing oocyte, and oskar mRNA and protein are maintained at the pole through early embryogenesis. The posterior maintenance of oskar mRNA is dependent upon the presence of oskar protein. We have cloned and characterized the Drosophila virilis oskar homologue, virosk, and examined its activity as a transgene in Drosophila melanogaster flies. We find that the cis-acting mRNA localization signals are conserved, although the virosk transcript also transiently accumulates at novel intermediate sites. The virosk protein, however, shows substantial differences from oskar: while virosk is able to rescue body patterning in a D. melanogaster oskar- background, it is impaired in both mRNA maintenance and pole cell formation. Furthermore, virosk induces a dominant maternal-effect lethality when introduced into a wild-type background, and interferes with the posterior maintenance of the endogenous oskar transcript in early embryogenesis. Our data suggest that virosk protein is unable to anchor at the posterior pole of the early embryo; this defect could account for all of the characteristics of virosk mentioned above. Our observations support a model in which oskar protein functions both by nucleating the factors necessary for the activation of the posterior body patterning determinant and the germ cell determinant, and by anchoring these factors to the posterior pole of the embryo. While the posterior body patterning determinant need not be correctly localized to provide body patterning activity, the germ cell determinant may need to be highly concentrated adjacent to the cortex in order to direct pole cell formation.

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