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Transcript length mediates developmental timing of gene expression across Drosophila.

Artieri CG, Fraser HB - Mol. Biol. Evol. (2014)

Bottom Line: We find that long zygotically expressed genes show substantial delay in expression relative to their shorter counterparts, which is not observed for maternally deposited transcripts.We further show that highly expressed zygotic genes maintain compact transcribed regions across the Drosophila phylogeny, allowing conservation of embryonic expression patterns.We propose that the physical constraints of intron delay affect patterns of expression and the evolution of gene structure of a substantial portion of the Drosophila transcriptome.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Stanford University.

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Highly expressed zygotic genes show conservation of short intronic length. (A) Highly expressed zygotic genes during the 0–2 h time point of the species timecourse have significantly shorter introns than all other categories. The distributions of mean orthologous intron length are significantly different among all categories (Kruskal–Wallis rank sum test, P < 0.001) with the exception of the comparison between low-expression zygotic and high-expression maternal gene categories (P = 0.40). (B) Highly expressed zygotic genes have significantly lower variability in length than other categories as measured by the corrected CV* in orthologous intron length among the four species (P < 0.01).
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msu226-F5: Highly expressed zygotic genes show conservation of short intronic length. (A) Highly expressed zygotic genes during the 0–2 h time point of the species timecourse have significantly shorter introns than all other categories. The distributions of mean orthologous intron length are significantly different among all categories (Kruskal–Wallis rank sum test, P < 0.001) with the exception of the comparison between low-expression zygotic and high-expression maternal gene categories (P = 0.40). (B) Highly expressed zygotic genes have significantly lower variability in length than other categories as measured by the corrected CV* in orthologous intron length among the four species (P < 0.01).

Mentions: Our observation that longer transcripts have delayed embryonic expression led us to predict that zygotic genes that are highly expressed during early embryogenesis across species should be subject to selection against intron expansion. Consequently, highly expressed zygotic genes should be more conserved for short transcript lengths than other gene categories. We tested this prediction by dividing genes based on their expression levels in the first time point (0–2 h) of the species timecourse: Zygotic genes in the highest- and lowest-expressed quartiles in D. melanogaster (“high-” and “low-expression zygotic”; 100 and 73 genes, respectively), as well as maternal genes in these same quartiles (“high-” and “low-expression maternal”; 142 and 189 genes, respectively). As expected, both zygotic and maternal high-expression genes have shorter mean intron lengths than their corresponding low-expression genes (Kruskal–Wallis rank sum test, P < 10−15) (fig. 5A). Furthermore, the highly expressed zygotic genes have the shortest mean intron lengths overall (P < 10−15). We then measured the variability of orthologous intron lengths in each category across the Drosophila phylogeny by calculating the corrected coefficient of variation (CV*) of intron lengths for the four species (fig. 5B) (see Materials and Methods). The CV* values, as well as intron lengths, of highly expressed zygotic genes are significantly lower than all other categories (P < 0.01), suggesting that there exists significant constraint on the expansion of intron lengths among highly expressed zygotic genes during early fly development.Fig. 5.


Transcript length mediates developmental timing of gene expression across Drosophila.

Artieri CG, Fraser HB - Mol. Biol. Evol. (2014)

Highly expressed zygotic genes show conservation of short intronic length. (A) Highly expressed zygotic genes during the 0–2 h time point of the species timecourse have significantly shorter introns than all other categories. The distributions of mean orthologous intron length are significantly different among all categories (Kruskal–Wallis rank sum test, P < 0.001) with the exception of the comparison between low-expression zygotic and high-expression maternal gene categories (P = 0.40). (B) Highly expressed zygotic genes have significantly lower variability in length than other categories as measured by the corrected CV* in orthologous intron length among the four species (P < 0.01).
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msu226-F5: Highly expressed zygotic genes show conservation of short intronic length. (A) Highly expressed zygotic genes during the 0–2 h time point of the species timecourse have significantly shorter introns than all other categories. The distributions of mean orthologous intron length are significantly different among all categories (Kruskal–Wallis rank sum test, P < 0.001) with the exception of the comparison between low-expression zygotic and high-expression maternal gene categories (P = 0.40). (B) Highly expressed zygotic genes have significantly lower variability in length than other categories as measured by the corrected CV* in orthologous intron length among the four species (P < 0.01).
Mentions: Our observation that longer transcripts have delayed embryonic expression led us to predict that zygotic genes that are highly expressed during early embryogenesis across species should be subject to selection against intron expansion. Consequently, highly expressed zygotic genes should be more conserved for short transcript lengths than other gene categories. We tested this prediction by dividing genes based on their expression levels in the first time point (0–2 h) of the species timecourse: Zygotic genes in the highest- and lowest-expressed quartiles in D. melanogaster (“high-” and “low-expression zygotic”; 100 and 73 genes, respectively), as well as maternal genes in these same quartiles (“high-” and “low-expression maternal”; 142 and 189 genes, respectively). As expected, both zygotic and maternal high-expression genes have shorter mean intron lengths than their corresponding low-expression genes (Kruskal–Wallis rank sum test, P < 10−15) (fig. 5A). Furthermore, the highly expressed zygotic genes have the shortest mean intron lengths overall (P < 10−15). We then measured the variability of orthologous intron lengths in each category across the Drosophila phylogeny by calculating the corrected coefficient of variation (CV*) of intron lengths for the four species (fig. 5B) (see Materials and Methods). The CV* values, as well as intron lengths, of highly expressed zygotic genes are significantly lower than all other categories (P < 0.01), suggesting that there exists significant constraint on the expansion of intron lengths among highly expressed zygotic genes during early fly development.Fig. 5.

Bottom Line: We find that long zygotically expressed genes show substantial delay in expression relative to their shorter counterparts, which is not observed for maternally deposited transcripts.We further show that highly expressed zygotic genes maintain compact transcribed regions across the Drosophila phylogeny, allowing conservation of embryonic expression patterns.We propose that the physical constraints of intron delay affect patterns of expression and the evolution of gene structure of a substantial portion of the Drosophila transcriptome.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Stanford University.

Show MeSH