scholarly journals A Sponge-like Structure Involved in the Association and Transport of Maternal Products during Drosophila Oogenesis

1997 ◽  
Vol 139 (3) ◽  
pp. 817-829 ◽  
Author(s):  
Michaela Wilsch-Bräuninger ◽  
Heinz Schwarz ◽  
Christiane Nüsslein-Volhard

Localization of maternally provided RNAs during oogenesis is required for formation of the antero–posterior axis of the Drosophila embryo. Here we describe a subcellular structure in nurse cells and oocytes which may function as an intracellular compartment for assembly and transport of maternal products involved in RNA localization. This structure, which we have termed “sponge body,” consists of ER-like cisternae, embedded in an amorphous electron-dense mass. It lacks a surrounding membrane and is frequently associated with mitochondria. The sponge bodies are not identical to the Golgi complexes. We suggest that the sponge bodies are homologous to the mitochondrial cloud in Xenopus oocytes, a granulo-fibrillar structure that contains RNAs involved in patterning of the embryo. Exuperantia protein, the earliest factor known to be required for the localization of bicoid mRNA to the anterior pole of the Drosophila oocyte, is highly enriched in the sponge bodies but not an essential structural component of these. RNA staining indicates that sponge bodies contain RNA. However, neither the intensity of this staining nor the accumulation of Exuperantia in the sponge bodies is dependent on the amount of bicoid mRNA present in the ovaries. Sponge bodies surround nuage, a possible polar granule precursor. Microtubules and microfilaments are not present in sponge bodies, although transport of the sponge bodies through the cells is implied by their presence in cytoplasmic bridges. We propose that the sponge bodies are structures that, by assembly and transport of included molecules or associated structures, are involved in localization of mRNAs in Drosophila oocytes.

Development ◽  
1999 ◽  
Vol 126 (22) ◽  
pp. 4943-4953 ◽  
Author(s):  
A.P. Chan ◽  
M. Kloc ◽  
L.D. Etkin

Vegetally localized transcripts have been implicated in a number of important biological functions, including cell fate determination and embryonic patterning. We have isolated a cDNA, fatvg, which encodes a localized maternal transcript that exhibits a localization pattern reminiscent of Vg1 mRNA. fatvg is the homologue of a mammalian gene expressed in adipose tissues. The fatvg transcript, unlike Vg1 which localizes strictly through the Late pathway, also associates with the mitochondrial cloud that is characteristic of the METRO or Early pathway. This suggests that fatvg mRNA may utilize both the METRO and Late pathways to localize to the vegetal cortex during oogenesis. We have dissected the cis-acting localization elements of fatvg mRNA and compared these elements with Vg1 mRNA. Our results indicate that, like most localized RNAs, in a variety of systems, transcripts of fatvg contain localization elements in the 3′UTR. The 3′UTR of fatvg mRNA contains multiple elements that are able to function independently; however, it functions most efficiently when all of the elements are present. We have defined a short 25-nucleotide element that can direct vegetal localization as a single copy. This element differs in sequence from previously described Vg1 localization elements, suggesting that different localization elements are involved in the localization of RNAs through the Late pathway.


2004 ◽  
Vol 121 (1) ◽  
pp. 101-109 ◽  
Author(s):  
Raymond A. Lewis ◽  
Tracy L. Kress ◽  
Colette A. Cote ◽  
Denise Gautreau ◽  
Megan E. Rokop ◽  
...  

Development ◽  
1995 ◽  
Vol 121 (1) ◽  
pp. 201-208 ◽  
Author(s):  
C. Forristall ◽  
M. Pondel ◽  
L. Chen ◽  
M.L. King

In Xenopus, localization of a rare class of mRNAs during oogenesis is believed to initiate pattern formation in the early embryo. We have determined the pattern of RNA localization for one of these RNAs, Xcat-2, which encodes a putative RNA-binding protein related to Drosophila nanos (Mosquera, L., Forristall, C., Zhou, Y. and King, M. L. (1993) Development 117, 377–386). Xcat-2 is exclusively localized to the mitochondrial cloud in stage I oocytes, moves with this body into the vegetal cortex during stage II and, later, partitions into islands consistent with it being a component of the germ plasm. As previously shown, Vg1 is not localized to the vegetal cortex until stage IV and distributes to all vegetal blastomeres during development. We found a direct correlation between the localized condition of these RNAs and their recovery in a detergent-insoluble fraction. We present evidence suggesting that differential RNA binding to a cytoskeletal component(s) in the vegetal cortex determines the pattern of inheritance for that RNA in the embryo.


2007 ◽  
Vol 28 (2) ◽  
pp. 678-686 ◽  
Author(s):  
Raymond A. Lewis ◽  
James A. Gagnon ◽  
Kimberly L. Mowry

ABSTRACT Transport of specific mRNAs to defined regions within the cell cytoplasm is a fundamental mechanism for regulating cell and developmental polarity. In the Xenopus oocyte, Vg1 RNA is transported to the vegetal cytoplasm, where localized expression of the encoded protein is critical for embryonic polarity. The Vg1 localization pathway is directed by interactions between key motifs within Vg1 RNA and protein factors recognizing those RNA sequences. We have investigated how RNA-protein interactions could be modulated to trigger distinct steps in the localization pathway and found that the Vg1 RNP is remodeled during cytoplasmic RNA transport. Our results implicate two RNA-binding proteins with key roles in Vg1 RNA localization, PTB/hnRNP I and Vg1RBP/vera, in this process. We show that PTB/hnRNP I is required for remodeling of the interaction between Vg1 RNA and Vg1RBP/vera. Critically, mutations that block this remodeling event also eliminate vegetal localization of the RNA, suggesting that RNP remodeling is required for localization.


2005 ◽  
Vol 278 (1) ◽  
pp. 103-117 ◽  
Author(s):  
Soheun Choo ◽  
Bianca Heinrich ◽  
J. Nicholas Betley ◽  
Zhao Chen ◽  
James O. Deshler

2019 ◽  
Author(s):  
Kunal Bhutani ◽  
Katherine Stansifer ◽  
Simina Ticau ◽  
Lazar Bojic ◽  
Chloe Villani ◽  
...  

1AbstractMendel’s first law dictates that alleles segregate randomly during meiosis and are distributed to offspring with equal frequency, requiring sperm to be functionally independent of their genetic payload. Developing mammalian spermatids have been thought to accomplish this by freely sharing RNA from virtually all genes through cytoplasmic bridges, equalizing allelic gene expression across different genotypes. Applying single cell RNA sequencing to developing spermatids, we identify a large class of mammalian genes whose allelic expression ratio is informative of the haploid genotype, which we call genoinformative markers (GIMs). 29% of spermatid-expressed genes in mice and 47% in non-human primates are not uniformly shared, and instead show a confident allelic expression bias of at least 2-fold towards the haploid genotype. This property of GIMs was significantly conserved between individuals and between rodents and primates. Consistent with the interpretation of specific RNA localization resulting in incomplete sharing through cytoplasmic bridges, we observe a strong depletion of GIM transcripts from chromatoid bodies, structures involved in shuttling RNA across cytoplasmic bridges, and an enrichment for 3’ UTR motifs involved in RNA localization. If GIMs are translated and functional in the context of fertility, they would be able to violate Mendel’s first law, leading to selective sweeps through a population. Indeed, we show that GIMs are enriched for signatures of positive selection, accounting for dozens of recent mouse, human, and primate selective sweeps. Intense selection at the sperm level risks evolutionary conflict between germline and somatic function, and GIMs show evidence of avoiding this conflict by exhibiting more testis-specific gene expression, paralogs, and isoforms than expression-matched control genes. The widespread existence of GIMs suggests that selective forces acting at the level of individual mammalian sperm are much more frequent than commonly believed.2Author’s summaryMendel’s first law dictates that alleles are distributed to offspring with equal frequency, requiring sperm carrying different genetics to be functionally equivalent. Despite a small number of known exceptions to this, it is widely believed that sharing of gene products through cytoplasmic bridges erases virtually all differences between haploid sperm. Here, we show that a large class of mammalian genes are not completely shared across these bridges, therefore causing sperm phenotype to correspond partly to haploid genotype. We term these genes “genoinformative markers” (GIMs) and show that their identity tends to be conserved from rodents to primates. Because some GIMs can link sperm genotype to function, they can be thought of as selfish genetic elements which lead to natural selection between sperm rather than between organisms, a violation of Mendel’s first law. We find evidence of this biased inheritance, showing that GIMs are strongly enriched for selective sweeps that spread alleles through mouse and human populations. For genes expressed both in sperm and in somatic tissues, this can cause a conflict because optimizing gene function for sperm may be detrimental to its other functions. We show that there is evolutionary pressure to avoid this conflict, as GIMs are strongly enriched for testis-specific gene expression, testis-specific paralogs, and testis-specific isoforms. Therefore, GIMs and sperm-level natural selection may provide an elegant explanation for the peculiarity of testis gene expression patterns, which are an extreme outlier relative to all other tissues.


Author(s):  
James A. Gagnon ◽  
Kimberly L. Mowry

Development ◽  
1997 ◽  
Vol 124 (24) ◽  
pp. 5013-5020 ◽  
Author(s):  
D. Gautreau ◽  
C.A. Cote ◽  
K.L. Mowry

Localization of mRNA has emerged as a fundamental mechanism for generating polarity during development. In vertebrates, one example of this phenomenon is Vg1 RNA, which is localized to the vegetal cortex of Xenopus oocytes. Vegetal localization of Vg1 RNA is directed by a 340-nt sequence element contained within its 3′ untranslated region. To investigate how such cis-acting elements function in the localization process, we have undertaken a detailed analysis of the precise sequence requirements for vegetal localization within the 340-nt localization element. We present evidence for considerable redundancy within the localization element and demonstrate that critical sequences lie at the ends of the element. Importantly, we show that a subelement from the 5′ end of the Vg1 localization element is, when duplicated, sufficient to direct vegetal localization. We suggest that the Vg1 localization element is composed of smaller, redundant sequence motifs and identify one such 6-nt motif as essential for localization. These results allow insight into what constitutes an RNA localization signal and how RNA sequence elements may act in the localization process.


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