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Systematic imaging reveals features and changing localization of mRNAs in Drosophila development.

Jambor H, Surendranath V, Kalinka AT, Mejstrik P, Saalfeld S, Tomancak P - Elife (2015)

Bottom Line: We combined transcriptomics and systematic imaging to determine the tissue-specific expression and subcellular distribution of 5862 mRNAs during Drosophila oogenesis. mRNA localization is widespread in the ovary and detectable in all of its cell types-the somatic epithelial, the nurse cells, and the oocyte.Genes defined by a common RNA localization share distinct gene features and differ in expression level, 3'UTR length and sequence conservation from unlocalized mRNAs.Comparison of mRNA localizations in different contexts revealed that localization of individual mRNAs changes over time in the oocyte and between ovarian and embryonic cell types.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

ABSTRACT
mRNA localization is critical for eukaryotic cells and affects numerous transcripts, yet how cells regulate distribution of many mRNAs to their subcellular destinations is still unknown. We combined transcriptomics and systematic imaging to determine the tissue-specific expression and subcellular distribution of 5862 mRNAs during Drosophila oogenesis. mRNA localization is widespread in the ovary and detectable in all of its cell types-the somatic epithelial, the nurse cells, and the oocyte. Genes defined by a common RNA localization share distinct gene features and differ in expression level, 3'UTR length and sequence conservation from unlocalized mRNAs. Comparison of mRNA localizations in different contexts revealed that localization of individual mRNAs changes over time in the oocyte and between ovarian and embryonic cell types. This genome scale image-based resource (Dresden Ovary Table, DOT, http://tomancak-srv1.mpi-cbg.de/DOT/main.html) enables the transition from mechanistic dissection of singular mRNA localization events towards global understanding of how mRNAs transcribed in the nucleus distribute in cells.

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Ovary gene sets have specific expression patterns during embryogenesis.Linear hierarchy (Tomancak et al., 2007) plot showing at which embryonic stage and in which tissue the oogenesis gene sets are re-expressed during embryogenesis. Each colour-coded bar represents organ systems of the embryo from its stage-specific anlagen to primordia to final differentiated structures. The width of the bar is proportional to the frequency with which this annotation term was used in the embryo data set; the height corresponds to a z-score of over- (above axis) or under-representation (below axis) of the term in the set of genes defined by ovary annotation. The following oogenesis gene sets are shown: ubiquitous, nuclear, cellular, subcellular, no signal, nurse cells perinuclear, oocyte-enriched, oocyte anterior and oocyte posterior and apical in epithelial cells. Genes expressed ubiquitously in the ovary mostly remained ubiquitous in the embryo and were additionally enriched in meso- and endoderm; genes of the cellular gene set are enriched in ectoderm/epidermis cells of the late embryo; subcellular genes were highly expressed in the ectoderm and nervous system of the embryo. Most ‘no signal’ genes are also underrepresented in almost all stages and tissues of embryogenesis, apart from the PNS and ectodermal derivatives in the late stages of embryogenesis. Perinuclear enriched genes are highly expressed in meso- and endoderm tissues. Oocyte enriched, oocyte anterior, and oocyte posterior genes are overall very similarly expressed during embryogenesis, being high in the polarized CNS and ectoderm tissues.DOI:http://dx.doi.org/10.7554/eLife.05003.009
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fig3s1: Ovary gene sets have specific expression patterns during embryogenesis.Linear hierarchy (Tomancak et al., 2007) plot showing at which embryonic stage and in which tissue the oogenesis gene sets are re-expressed during embryogenesis. Each colour-coded bar represents organ systems of the embryo from its stage-specific anlagen to primordia to final differentiated structures. The width of the bar is proportional to the frequency with which this annotation term was used in the embryo data set; the height corresponds to a z-score of over- (above axis) or under-representation (below axis) of the term in the set of genes defined by ovary annotation. The following oogenesis gene sets are shown: ubiquitous, nuclear, cellular, subcellular, no signal, nurse cells perinuclear, oocyte-enriched, oocyte anterior and oocyte posterior and apical in epithelial cells. Genes expressed ubiquitously in the ovary mostly remained ubiquitous in the embryo and were additionally enriched in meso- and endoderm; genes of the cellular gene set are enriched in ectoderm/epidermis cells of the late embryo; subcellular genes were highly expressed in the ectoderm and nervous system of the embryo. Most ‘no signal’ genes are also underrepresented in almost all stages and tissues of embryogenesis, apart from the PNS and ectodermal derivatives in the late stages of embryogenesis. Perinuclear enriched genes are highly expressed in meso- and endoderm tissues. Oocyte enriched, oocyte anterior, and oocyte posterior genes are overall very similarly expressed during embryogenesis, being high in the polarized CNS and ectoderm tissues.DOI:http://dx.doi.org/10.7554/eLife.05003.009

Mentions: We next asked whether the proteins encoded by the mRNAs show physical interactions. To this end, we analysed the protein interaction data (mentha interactome database [Calderone et al., 2013]), which revealed that proteins of the posterior gene set participate in significantly more protein–protein interactions than of the anterior gene set (Figure 3B). This suggests that the close proximity of their transcripts in the cell could be of functional importance. The gene sets defined by our ovary screen also maintained distinct expression patterns during embryogenesis. Genes of the subcellular sets are enriched among genes expressed in the central nervous system and epithelia, suggesting an interesting relatedness of these polarized tissues (Figure 3A, Figure 3—figure supplement 1). Thus, gene sets defined by ovary expression are co-regulated also beyond oogenesis.10.7554/eLife.05003.008Figure 3.Localized mRNAs show gene set specific features.


Systematic imaging reveals features and changing localization of mRNAs in Drosophila development.

Jambor H, Surendranath V, Kalinka AT, Mejstrik P, Saalfeld S, Tomancak P - Elife (2015)

Ovary gene sets have specific expression patterns during embryogenesis.Linear hierarchy (Tomancak et al., 2007) plot showing at which embryonic stage and in which tissue the oogenesis gene sets are re-expressed during embryogenesis. Each colour-coded bar represents organ systems of the embryo from its stage-specific anlagen to primordia to final differentiated structures. The width of the bar is proportional to the frequency with which this annotation term was used in the embryo data set; the height corresponds to a z-score of over- (above axis) or under-representation (below axis) of the term in the set of genes defined by ovary annotation. The following oogenesis gene sets are shown: ubiquitous, nuclear, cellular, subcellular, no signal, nurse cells perinuclear, oocyte-enriched, oocyte anterior and oocyte posterior and apical in epithelial cells. Genes expressed ubiquitously in the ovary mostly remained ubiquitous in the embryo and were additionally enriched in meso- and endoderm; genes of the cellular gene set are enriched in ectoderm/epidermis cells of the late embryo; subcellular genes were highly expressed in the ectoderm and nervous system of the embryo. Most ‘no signal’ genes are also underrepresented in almost all stages and tissues of embryogenesis, apart from the PNS and ectodermal derivatives in the late stages of embryogenesis. Perinuclear enriched genes are highly expressed in meso- and endoderm tissues. Oocyte enriched, oocyte anterior, and oocyte posterior genes are overall very similarly expressed during embryogenesis, being high in the polarized CNS and ectoderm tissues.DOI:http://dx.doi.org/10.7554/eLife.05003.009
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Related In: Results  -  Collection

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fig3s1: Ovary gene sets have specific expression patterns during embryogenesis.Linear hierarchy (Tomancak et al., 2007) plot showing at which embryonic stage and in which tissue the oogenesis gene sets are re-expressed during embryogenesis. Each colour-coded bar represents organ systems of the embryo from its stage-specific anlagen to primordia to final differentiated structures. The width of the bar is proportional to the frequency with which this annotation term was used in the embryo data set; the height corresponds to a z-score of over- (above axis) or under-representation (below axis) of the term in the set of genes defined by ovary annotation. The following oogenesis gene sets are shown: ubiquitous, nuclear, cellular, subcellular, no signal, nurse cells perinuclear, oocyte-enriched, oocyte anterior and oocyte posterior and apical in epithelial cells. Genes expressed ubiquitously in the ovary mostly remained ubiquitous in the embryo and were additionally enriched in meso- and endoderm; genes of the cellular gene set are enriched in ectoderm/epidermis cells of the late embryo; subcellular genes were highly expressed in the ectoderm and nervous system of the embryo. Most ‘no signal’ genes are also underrepresented in almost all stages and tissues of embryogenesis, apart from the PNS and ectodermal derivatives in the late stages of embryogenesis. Perinuclear enriched genes are highly expressed in meso- and endoderm tissues. Oocyte enriched, oocyte anterior, and oocyte posterior genes are overall very similarly expressed during embryogenesis, being high in the polarized CNS and ectoderm tissues.DOI:http://dx.doi.org/10.7554/eLife.05003.009
Mentions: We next asked whether the proteins encoded by the mRNAs show physical interactions. To this end, we analysed the protein interaction data (mentha interactome database [Calderone et al., 2013]), which revealed that proteins of the posterior gene set participate in significantly more protein–protein interactions than of the anterior gene set (Figure 3B). This suggests that the close proximity of their transcripts in the cell could be of functional importance. The gene sets defined by our ovary screen also maintained distinct expression patterns during embryogenesis. Genes of the subcellular sets are enriched among genes expressed in the central nervous system and epithelia, suggesting an interesting relatedness of these polarized tissues (Figure 3A, Figure 3—figure supplement 1). Thus, gene sets defined by ovary expression are co-regulated also beyond oogenesis.10.7554/eLife.05003.008Figure 3.Localized mRNAs show gene set specific features.

Bottom Line: We combined transcriptomics and systematic imaging to determine the tissue-specific expression and subcellular distribution of 5862 mRNAs during Drosophila oogenesis. mRNA localization is widespread in the ovary and detectable in all of its cell types-the somatic epithelial, the nurse cells, and the oocyte.Genes defined by a common RNA localization share distinct gene features and differ in expression level, 3'UTR length and sequence conservation from unlocalized mRNAs.Comparison of mRNA localizations in different contexts revealed that localization of individual mRNAs changes over time in the oocyte and between ovarian and embryonic cell types.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

ABSTRACT
mRNA localization is critical for eukaryotic cells and affects numerous transcripts, yet how cells regulate distribution of many mRNAs to their subcellular destinations is still unknown. We combined transcriptomics and systematic imaging to determine the tissue-specific expression and subcellular distribution of 5862 mRNAs during Drosophila oogenesis. mRNA localization is widespread in the ovary and detectable in all of its cell types-the somatic epithelial, the nurse cells, and the oocyte. Genes defined by a common RNA localization share distinct gene features and differ in expression level, 3'UTR length and sequence conservation from unlocalized mRNAs. Comparison of mRNA localizations in different contexts revealed that localization of individual mRNAs changes over time in the oocyte and between ovarian and embryonic cell types. This genome scale image-based resource (Dresden Ovary Table, DOT, http://tomancak-srv1.mpi-cbg.de/DOT/main.html) enables the transition from mechanistic dissection of singular mRNA localization events towards global understanding of how mRNAs transcribed in the nucleus distribute in cells.

Show MeSH