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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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GO-term enrichment analysis for gene sets.GO-terms associated with ubiquitous, subcellular, cellular, nuclear, oocyte enriched, anterior and posterior gene sets. Shown is also analysis of all ‘localization competent’ mRNAs. Bar plots show the p-values for each GO-term calculated by the modified Fisher Exact test, which results in the EASE score p-value.DOI:http://dx.doi.org/10.7554/eLife.05003.005
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fig1s2: GO-term enrichment analysis for gene sets.GO-terms associated with ubiquitous, subcellular, cellular, nuclear, oocyte enriched, anterior and posterior gene sets. Shown is also analysis of all ‘localization competent’ mRNAs. Bar plots show the p-values for each GO-term calculated by the modified Fisher Exact test, which results in the EASE score p-value.DOI:http://dx.doi.org/10.7554/eLife.05003.005

Mentions: The division of RNAs into gene sets enabled us to address whether genes within each class are functionally related (Figure 1D, Figure 1—figure supplement 2). Gene Ontology (GO) analysis showed that the subcellular gene set is distinct from the cellular and the nuclear gene sets. Consistent with their respective expression, cellular genes are enriched for epithelial development, lipid trafficking and cuticle formation, nuclear genes for RNA regulatory processes and the subcellular gene set for reproductive processes, cytoskeleton organization, and cell cycle regulation. Anterior and posterior gene sets differed: anterior genes were enriched for microtubule terms and, being localized in proximity to the meiotic oocyte nucleus, are additionally associated with chromosome and cell cycle regulation terms. The posterior mRNAs associated strongly with signalling, cell fate commitment, and membrane organization terms. The GO analysis suggests that mRNAs that co-localize in the cytoplasm are functionally related.


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)

GO-term enrichment analysis for gene sets.GO-terms associated with ubiquitous, subcellular, cellular, nuclear, oocyte enriched, anterior and posterior gene sets. Shown is also analysis of all ‘localization competent’ mRNAs. Bar plots show the p-values for each GO-term calculated by the modified Fisher Exact test, which results in the EASE score p-value.DOI:http://dx.doi.org/10.7554/eLife.05003.005
© Copyright Policy
Related In: Results  -  Collection

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

fig1s2: GO-term enrichment analysis for gene sets.GO-terms associated with ubiquitous, subcellular, cellular, nuclear, oocyte enriched, anterior and posterior gene sets. Shown is also analysis of all ‘localization competent’ mRNAs. Bar plots show the p-values for each GO-term calculated by the modified Fisher Exact test, which results in the EASE score p-value.DOI:http://dx.doi.org/10.7554/eLife.05003.005
Mentions: The division of RNAs into gene sets enabled us to address whether genes within each class are functionally related (Figure 1D, Figure 1—figure supplement 2). Gene Ontology (GO) analysis showed that the subcellular gene set is distinct from the cellular and the nuclear gene sets. Consistent with their respective expression, cellular genes are enriched for epithelial development, lipid trafficking and cuticle formation, nuclear genes for RNA regulatory processes and the subcellular gene set for reproductive processes, cytoskeleton organization, and cell cycle regulation. Anterior and posterior gene sets differed: anterior genes were enriched for microtubule terms and, being localized in proximity to the meiotic oocyte nucleus, are additionally associated with chromosome and cell cycle regulation terms. The posterior mRNAs associated strongly with signalling, cell fate commitment, and membrane organization terms. The GO analysis suggests that mRNAs that co-localize in the cytoplasm are functionally related.

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