Transcriptomic Insights into Genetic Diversity of Protein-coding Genes in X. Laevis

Overview

Journal Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2017 Mar 12

PMID 28283406

Citations 5

Authors

Virginia Savova

Esther J Pearl

Elvan Boke

Anwesha Nag

Ivan Adzhubei

Marko E Horb

Leonid Peshkin

Affiliations

Soon will be listed here.

Abstract

We characterize the genetic diversity of Xenopus laevis strains using RNA-seq data and allele-specific analysis. This data provides a catalogue of coding variation, which can be used for improving the genomic sequence, as well as for better sequence alignment, probe design, and proteomic analysis. In addition, we paint a broad picture of the genetic landscape of the species by functionally annotating different classes of mutations with a well-established prediction tool (PolyPhen-2). Further, we specifically compare the variation in the progeny of four crosses: inbred genomic (J)-strain, outbred albino (B)-strain, and two hybrid crosses of J and B strains. We identify a subset of mutations specific to the B strain, which allows us to investigate the selection pressures affecting duplicated genes in this allotetraploid. From these crosses we find the ratio of non-synonymous to synonymous mutations is lower in duplicated genes, which suggests that they are under greater purifying selection. Surprisingly, we also find that function-altering ("damaging") mutations constitute a greater fraction of the non-synonymous variants in this group, which suggests a role for subfunctionalization in coding variation affecting duplicated genes.

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References

Del Viso F, Bhattacharya D, Kong Y, Gilchrist M, Khokha M . Exon capture and bulk segregant analysis: rapid discovery of causative mutations using high-throughput sequencing. BMC Genomics. 2012; 13:649. PMC: 3526394. DOI: 10.1186/1471-2164-13-649. View

Wang J, Raskin L, Samuels D, Shyr Y, Guo Y . Genome measures used for quality control are dependent on gene function and ancestry. Bioinformatics. 2014; 31(3):318-23. PMC: 4308666. DOI: 10.1093/bioinformatics/btu668. View

Hoperskaya O . The development of animals homozygous for a mutation causing periodic albinism (ap) in Xenopus laevis. J Embryol Exp Morphol. 1975; 34(1):253-64. View

Matsuda Y, Uno Y, Kondo M, Gilchrist M, Zorn A, Rokhsar D . A New Nomenclature of Xenopus laevis Chromosomes Based on the Phylogenetic Relationship to Silurana/Xenopus tropicalis. Cytogenet Genome Res. 2015; 145(3-4):187-91. DOI: 10.1159/000381292. View

Jordan I, Wolf Y, Koonin E . Duplicated genes evolve slower than singletons despite the initial rate increase. BMC Evol Biol. 2004; 4:22. PMC: 481058. DOI: 10.1186/1471-2148-4-22. View

Yang Z . PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24(8):1586-91. DOI: 10.1093/molbev/msm088. View

Peshkin L, Wuhr M, Pearl E, Haas W, Freeman Jr R, Gerhart J . On the Relationship of Protein and mRNA Dynamics in Vertebrate Embryonic Development. Dev Cell. 2015; 35(3):383-94. PMC: 4776761. DOI: 10.1016/j.devcel.2015.10.010. View

DePristo M, Banks E, Poplin R, Garimella K, Maguire J, Hartl C . A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011; 43(5):491-8. PMC: 3083463. DOI: 10.1038/ng.806. View

Trapnell C, Pachter L, Salzberg S . TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25(9):1105-11. PMC: 2672628. DOI: 10.1093/bioinformatics/btp120. View

10.

Adzhubei I, Schmidt S, Peshkin L, Ramensky V, Gerasimova A, Bork P . A method and server for predicting damaging missense mutations. Nat Methods. 2010; 7(4):248-9. PMC: 2855889. DOI: 10.1038/nmeth0410-248. View

11.

Hunt T . Nobel Lecture. Protein synthesis, proteolysis, and cell cycle transitions. Biosci Rep. 2003; 22(5-6):465-86. DOI: 10.1023/a:1022077317801. View

12.

Nag A, Savova V, Fung H, Miron A, Yuan G, Zhang K . Chromatin signature of widespread monoallelic expression. Elife. 2014; 2:e01256. PMC: 3873816. DOI: 10.7554/eLife.01256. View

13.

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N . The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25(16):2078-9. PMC: 2723002. DOI: 10.1093/bioinformatics/btp352. View

14.

Pegueroles C, Laurie S, Alba M . Accelerated evolution after gene duplication: a time-dependent process affecting just one copy. Mol Biol Evol. 2013; 30(8):1830-42. DOI: 10.1093/molbev/mst083. View

15.

Izutsu Y, Maeno M . Analyses of immune responses to ontogeny-specific antigens using an inbred strain of Xenopus laevis (J strain). Methods Mol Med. 2004; 105:149-58. DOI: 10.1385/1-59259-826-9:149. View

16.

Cui X, Affourtit J, Shockley K, Woo Y, Churchill G . Inheritance patterns of transcript levels in F1 hybrid mice. Genetics. 2006; 174(2):627-37. PMC: 1602077. DOI: 10.1534/genetics.106.060251. View

17.

Alon S, Garrett S, Levanon E, Olson S, Graveley B, Rosenthal J . The majority of transcripts in the squid nervous system are extensively recoded by A-to-I RNA editing. Elife. 2015; 4. PMC: 4384741. DOI: 10.7554/eLife.05198. View

18.

Gurdon J . The egg and the nucleus: a battle for supremacy. Development. 2013; 140(12):2449-56. DOI: 10.1242/dev.097170. View

19.

Abecasis G, Auton A, Brooks L, DePristo M, Durbin R, Handsaker R . An integrated map of genetic variation from 1,092 human genomes. Nature. 2012; 491(7422):56-65. PMC: 3498066. DOI: 10.1038/nature11632. View

20.

Gantress J, Maniero G, Cohen N, Robert J . Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology. 2003; 311(2):254-62. DOI: 10.1016/s0042-6822(03)00151-x. View