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Evolutionary dynamics of abundant stop codon readthrough in Anopheles and Drosophila

Irwin Jungreis, Clara S Chan, Robert M Waterhouse, Gabriel Fields, Michael F Lin, Manolis Kellis
doi: https://doi.org/10.1101/051557
Irwin Jungreis
1MIT Computer Science and Artificial Intelligence Laboratory, 32 Vassar Street, Cambridge, Massachusetts 02139, USA;
2Broad Institute of MIT and Harvard, 415 Main Street, Cambridge, Massachusetts 02142, USA;
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Clara S Chan
1MIT Computer Science and Artificial Intelligence Laboratory, 32 Vassar Street, Cambridge, Massachusetts 02139, USA;
2Broad Institute of MIT and Harvard, 415 Main Street, Cambridge, Massachusetts 02142, USA;
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Robert M Waterhouse
1MIT Computer Science and Artificial Intelligence Laboratory, 32 Vassar Street, Cambridge, Massachusetts 02139, USA;
2Broad Institute of MIT and Harvard, 415 Main Street, Cambridge, Massachusetts 02142, USA;
3Department of Genetic Medicine and Development, University of Geneva Medical School, rue Michel-Servet 1, 1211, Geneva, Switzerland;
4Swiss Institute of Bioinformatics, rue Michel-Servet 1, 1211 Geneva, Switzerland;
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Gabriel Fields
5MIT, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139;
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Michael F Lin
6DNAnexus, Mountain View, CA 94040, USA.
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Manolis Kellis
1MIT Computer Science and Artificial Intelligence Laboratory, 32 Vassar Street, Cambridge, Massachusetts 02139, USA;
2Broad Institute of MIT and Harvard, 415 Main Street, Cambridge, Massachusetts 02142, USA;
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  • For correspondence: manoli@mit.edu
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Abstract

Translational stop codon readthrough was virtually unknown in eukaryotic genomes until recent developments in comparative genomics and new experimental techniques revealed evidence of readthrough in hundreds of fly genes and several human, worm, and yeast genes. Here, we use the genomes of 21 species of Anopheles mosquitoes and improved comparative techniques to identify evolutionary signatures of conserved, functional readthrough of 353 stop codons in the malaria vector, Anopheles gambiae, and 51 additional Drosophila melanogaster stop codons, with several cases of double and triple readthrough including readthrough of two adjacent stop codons, supporting our earlier prediction of abundant readthrough in pancrustacea genomes. Comparisons between Anopheles and Drosophila allow us to transcend the static picture provided by single-clade analysis to explore the evolutionary dynamics of abundant readthrough. We find that most differences between the readthrough repertoires of the two species are due to readthrough gain or loss in existing genes, rather than to birth of new genes or to gene death; that RNA structures are sometimes gained or lost while readthrough persists; and that readthrough is more likely to be lost at TAA and TAG stop codons. We also determine which characteristic properties of readthrough predate readthrough and which are clade-specific. We estimate that there are more than 600 functional readthrough stop codons in A. gambiae and 900 in D. melanogaster. We find evidence that readthrough is used to regulate peroxisomal targeting in two genes. Finally, we use the sequenced centipede genome to refine the phylogenetic extent of abundant readthrough.

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Posted May 03, 2016.
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Evolutionary dynamics of abundant stop codon readthrough in Anopheles and Drosophila
Irwin Jungreis, Clara S Chan, Robert M Waterhouse, Gabriel Fields, Michael F Lin, Manolis Kellis
bioRxiv 051557; doi: https://doi.org/10.1101/051557
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Evolutionary dynamics of abundant stop codon readthrough in Anopheles and Drosophila
Irwin Jungreis, Clara S Chan, Robert M Waterhouse, Gabriel Fields, Michael F Lin, Manolis Kellis
bioRxiv 051557; doi: https://doi.org/10.1101/051557

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