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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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Related in: MedlinePlus

Embryo localized mRNAs also have long, conserved 3′UTRs.Distributions of median 3′UTR length (A) and conservation of the 3′UTR sequence (B, across 24 Drosophila species) for embryo gene sets. Shown are genes that are ubiquitously expressed during embryogenesis, genes whose RNAs were enriched at the apical or basal membrane in blastoderm embryos and RNAs at the posterior pole.DOI:http://dx.doi.org/10.7554/eLife.05003.011
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fig3s3: Embryo localized mRNAs also have long, conserved 3′UTRs.Distributions of median 3′UTR length (A) and conservation of the 3′UTR sequence (B, across 24 Drosophila species) for embryo gene sets. Shown are genes that are ubiquitously expressed during embryogenesis, genes whose RNAs were enriched at the apical or basal membrane in blastoderm embryos and RNAs at the posterior pole.DOI:http://dx.doi.org/10.7554/eLife.05003.011

Mentions: Yet, expression level alone cannot account for subcellular localization. We therefore compared the gene-level variables of each localization class and revealed that subcellular mRNAs had significantly longer 3′UTR sequences and this was more pronounced for the posterior localization class (Figure 3D,D'). The posterior gene set further showed longer gene structures, longer 5′UTRs, longer exons and introns, a higher number of exons and introns, and a higher intron proportion compared to ubiquitous and anterior mRNAs (Figure 3—figure supplement 2B–H). Consistent with the observation that localized mRNAs are enriched in non-coding portions, the exon proportion was the highest in the ubiquitous gene set (Figure 3—figure supplement 2I). The high intron proportion of posterior genes is particularly interesting in light of the recent finding that the stable deposition of the exon junction complex, required for posterior oskar mRNA localization, is correlated with long intron-containing genes (Ashton-Beaucage et al., 2010; Ghosh et al., 2012). Localized genes not only had longer 3′UTRs, but also showed higher 3′UTR sequence conservation than ubiquitous genes, and again this was significantly more pronounced in the posterior gene set (Figure 3E,E'). We also observed longer and more conserved 3′UTRs in the embryo localized mRNAs (apical, posterior) compared to the embryo ubiquitous mRNAs (Figure 3—figure supplement 3A,B based on data from [Lecuyer et al., 2007]), indicating that these features are not specific to oocyte-localized mRNAs.


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)

Embryo localized mRNAs also have long, conserved 3′UTRs.Distributions of median 3′UTR length (A) and conservation of the 3′UTR sequence (B, across 24 Drosophila species) for embryo gene sets. Shown are genes that are ubiquitously expressed during embryogenesis, genes whose RNAs were enriched at the apical or basal membrane in blastoderm embryos and RNAs at the posterior pole.DOI:http://dx.doi.org/10.7554/eLife.05003.011
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4384636&req=5

fig3s3: Embryo localized mRNAs also have long, conserved 3′UTRs.Distributions of median 3′UTR length (A) and conservation of the 3′UTR sequence (B, across 24 Drosophila species) for embryo gene sets. Shown are genes that are ubiquitously expressed during embryogenesis, genes whose RNAs were enriched at the apical or basal membrane in blastoderm embryos and RNAs at the posterior pole.DOI:http://dx.doi.org/10.7554/eLife.05003.011
Mentions: Yet, expression level alone cannot account for subcellular localization. We therefore compared the gene-level variables of each localization class and revealed that subcellular mRNAs had significantly longer 3′UTR sequences and this was more pronounced for the posterior localization class (Figure 3D,D'). The posterior gene set further showed longer gene structures, longer 5′UTRs, longer exons and introns, a higher number of exons and introns, and a higher intron proportion compared to ubiquitous and anterior mRNAs (Figure 3—figure supplement 2B–H). Consistent with the observation that localized mRNAs are enriched in non-coding portions, the exon proportion was the highest in the ubiquitous gene set (Figure 3—figure supplement 2I). The high intron proportion of posterior genes is particularly interesting in light of the recent finding that the stable deposition of the exon junction complex, required for posterior oskar mRNA localization, is correlated with long intron-containing genes (Ashton-Beaucage et al., 2010; Ghosh et al., 2012). Localized genes not only had longer 3′UTRs, but also showed higher 3′UTR sequence conservation than ubiquitous genes, and again this was significantly more pronounced in the posterior gene set (Figure 3E,E'). We also observed longer and more conserved 3′UTRs in the embryo localized mRNAs (apical, posterior) compared to the embryo ubiquitous mRNAs (Figure 3—figure supplement 3A,B based on data from [Lecuyer et al., 2007]), indicating that these features are not specific to oocyte-localized mRNAs.

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
Related in: MedlinePlus