De novo transcriptome assembly reveals sex-specific selection acting on evolving neo-sex chromosomes in Drosophila miranda

BMC Genomics

Doris Bachtrog¹  Vera B Kaiser² 

[1] Department of Integrative Biology, Center for Theoretical Evolutionary Genomics, University of California, Berkeley, Berkeley, CA 94720, USA;Current Address: MRC Human Genetics Unit, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Western General Hospital, Edinburgh EH4 2XU, UK

关键词: Nonsense mediated decay;    Gene loss;    Transcriptome;    Drosophila;    Sex chromosomes;   

Others  :  1217601
DOI  :  10.1186/1471-2164-15-241

 received in 2013-12-11, accepted in 2014-03-11,  发布年份 2014

【 摘 要 】

Background

The Drosophila miranda neo-sex chromosome system is a useful resource for studying recently evolved sex chromosomes. However, the neo-Y genomic assembly is fragmented due to the accumulation of repetitive sequence. Furthermore, the separate assembly of the neo-X and neo-Y chromosomes into genomic scaffolds has proven to be difficult, due to their low level of sequence divergence, which in coding regions is about 1.5%. Here, we de novo assemble the transcriptome of D. miranda using RNA-seq data from several male and female tissues, and develop a bioinformatic pipeline to separately reconstruct neo-X and neo-Y transcripts.

Results

We obtain 2,141 transcripts from the neo-X and 1,863 from the neo-Y. Neo-Y transcripts are generally shorter than their homologous neo-X transcripts (N50 of 2,048-bp vs. 2,775-bp) and expressed at lower levels. We find that 24% of expressed neo-Y transcripts harbor nonsense mutation within their open reading frames, yet most non-functional neo-Y genes are expressed throughout all of their length. We find evidence of gene loss of male-specific genes on the neo-X chromosome, and transcriptional silencing of testis-specific genes from the neo-X.

Conclusions

Nonsense mediated decay (NMD) has been implicated to degrade transcripts containing pre-mature termination codons (PTC) in Drosophila, but rampant description of neo-Y genes with pre-mature stop codons suggests that it does not play a major role in down-regulating transcripts from the neo-Y. Loss or transcriptional down-regulation of genes from the neo-X with male-biased function provides evidence for beginning demasculinization of the neo-X. Thus, evolving sex chromosomes can rapidly shift their gene content or patterns of gene expression in response to their sex-biased transmission, supporting the idea that sex-specific or sexually antagonistic selection plays a major role in the evolution of heteromorphic sex chromosomes.

【 授权许可】

   
2014 Kaiser and Bachtrog; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Bachtrog D: Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 2013, 14(2):113-124.
• [2]Kaiser VB, Zhou Q, Bachtrog D: Nonrandom gene loss from the Drosophila miranda neo-Y chromosome. Genome Biol Evol 2011, 3:1329-1337.
• [3]Charlesworth B, Charlesworth D: The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 2000, 355(1403):1563-1572.
• [4]Zhou Q, Ellison CE, Kaiser VB, Alekseyenko AA, Gorchakov AA, Bachtrog D: The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation. PLoS Biol 2013, 11(11):e1001711.
• [5]Charlesworth B: The evolution of chromosomal sex determination and dosage compensation. Curr Biol 1996, 6(2):149-162.
• [6]Vicoso B, Charlesworth B: The deficit of male-biased genes on the D. melanogaster X chromosome is expression-dependent: a consequence of dosage compensation? J Mol Evol 2009, 68(5):576-583.
• [7]Bachtrog D, Charlesworth B: Reduced adaptation of a non-recombining neo-Y chromosome. Nature 2002, 416(6878):323-326.
• [8]Steinemann M, Steinemann S: Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica 1998, 102–103(1–6):409-420.
• [9]Zhou Q, Bachtrog D: Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 2012, 337(6092):341-345.
• [10]Carvalho AB, Clark AG: Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 2005, 307(5706):108-110.
• [11]Vicoso B, Bachtrog D: Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 2013, 499(7458):332-335.
• [12]Kervestin S, Jacobson A: NMD: a multifaceted response to premature translational termination. Nat Rev Mol Cell Biol 2012, 13(11):700-712.
• [13]Isken O, Maquat LE: Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev 2007, 21(15):1833-1856.
• [14]Rebbapragada I, Lykke-Andersen J: Execution of nonsense-mediated mRNA decay: what defines a substrate? Curr Opin Cell Biol 2009, 21(3):394-402.
• [15]Chang YF, Imam JS, Wilkinson MF: The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 2007, 76:51-74.
• [16]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-652.
• [17]Bachtrog D, Hom E, Wong KM, Maside X, de Jong P: Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol 2008, 9(2):R30. BioMed Central Full Text
• [18]Huang X, Madan A: CAP3: A DNA sequence assembly program. Genome Res 1999, 9(9):868-877.
• [19]Surget-Groba Y, Montoya-Burgos JI: Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res 2010, 20(10):1432-1440.
• [20]Roberts A, Pachter L: Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 2013, 10(1):71-73.
• [21]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797.
• [22]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17(4):540-552.
• [23]Birney E, Clamp M, Durbin R: GeneWise and Genomewise. Genome Res 2004, 14(5):988-995.
• [24]Palmieri N, Nolte V, Suvorov A, Kosiol C, Schlotterer C: Evaluation of different reference based annotation strategies using RNA-Seq - a case study in Drososphila pseudoobscura. PLoS One 2012, 7(10):e46415.
• [25]Jungreis I, Lin MF, Spokony R, Chan CS, Negre N, Victorsen A, White KP, Kellis M: Evidence of abundant stop codon readthrough in Drosophila and other metazoa. Genome Res 2011, 21(12):2096-2113.
• [26]Ellison CE, Bachtrog D: Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 2013, 342(6160):846-850.
• [27]Sturgill D, Zhang Y, Parisi M, Oliver B: Demasculinization of X chromosomes in the Drosophila genus. Nature 2007, 450(7167):238-241.
• [28]Vicoso B, Charlesworth B: Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 2006, 7(8):645-653.