Complete dosage compensation and sex-biased gene expression in the moth Manduca sexta

Genome Biology and Evolution

Volumn 6, Issue 3, 2014, Pages 526-537

  Smith, Gilbert ^a   Chen, Yun Ru ^b   Blissard, Gary W ^b   Briscoe, Adriana D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Boyce Thompson Institute for Plant Research   (United States)

Author keywords

Dosage compensation; Lepidoptera; Mushroom body; Olfaction; Phototransduction; Sex biased gene expression

Indexed keywords

TRANSCRIPTOME;

ANIMAL; ARTICLE; CLASSIFICATION; DNA SEQUENCE; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; LEPIDOPTERA; MALE; MANDUCA; MOLECULAR EVOLUTION; MUSHROOM BODY; PHOTOTRANSDUCTION; PHYLOGENY; SEX CHROMOSOME; SEX-BIASED GENE EXPRESSION; SMELLING;

DOSAGE COMPENSATION; LEPIDOPTERA; MUSHROOM BODY; OLFACTION; PHOTOTRANSDUCTION; SEX-BIASED GENE EXPRESSION;

ANIMALS; DOSAGE COMPENSATION, GENETIC; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION; MALE; MANDUCA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEX CHROMOSOMES; TRANSCRIPTOME;

EID: 84902985111     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu035     Document Type: Article

References (72)

1. Adolfsson S, Ellegren H. 2013. Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches. Mol Biol Evol. 30: 806-810.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215: 403-410.
3. Arunkumar KP, Mita K, Nagaraju J. 2009. The silkworm Z chromosome is enriched in testis-specific genes. Genetics 182: 493-501.
4. Ayers KL, et al. 2013. RNA sequencing reveals sexually dimorphic gene expression before gonadal differentiation in chicken and allows comprehensive annotation of the W-chromosome. Genome Biol. 14: 1-17.
5. Belote JM, Lucchesi JC. 1980. Control of X chromosome transcription by the maleless gene in Drosophila. Nature 285: 573-575.
6. Bull JJ. 1983. Evolution of sex determining mechanisms. Menlo Park (CA): The Benjamin/Cummings Publ. Co., Inc.
7. Caron SJC, Ruta V, Abbott LF, Axel R. 2013. Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 497: 113-119.
8. Carrel L, Willard HF. 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
9. Charlesworth B. 1991. The evolution of sex-chromosomes. Science 251: 1030-1033.
10. Charlesworth B, Charlesworth D. 2000. The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci. 355: 1563-1572.
11. Cooper DW, Johnston PG, Watson JM, Graves JAM. 1993. X-inactivation in marsupials and monotremes. Semin Dev Biol. 4: 117-128.
12. Daly KC, Smith BH. 2000. Associative olfactory learning in the moth Manduca sexta. J Exp Biol. 203: 2025-2038.
13. Dasmahapatra KK, et al. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94-98.
14. Deakin JE, Chaumeil J, Hore TA, Graves JA. 2009. Unravelling the evolutionary origins of X chromosome inactivation in mammals: insights from marsupials and monotremes. Chromosome Res. 17: 671-685.
15. Dennis JG, et al. 2003. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4:P3.
16. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. 2009. GOrilla: a tool for discovery and visualization of enriched go terms in ranked gene lists. BMC Bioinformatics 10: 48.
17. Grabherr MG, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29: 644-652.
18. Grosse-Wilde E, et al. 2011. Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci U S A. 108: 7449-7454.
19. Haas BJ, et al. 2013. De novo transcript sequence reconstruction from RNA-Seq using the trinity platform for reference generation and analysis. Nat Protoc. 8: 1494-1512.
20. Harrison PW, Mank JE, Wedell N. 2012. Incomplete sex chromosome dosage compensation in the indian meal moth, Plodia interpunctella, based on de novo transcriptome assembly. Genome Biol Evol. 4: 1118-1126.
21. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 4: 44-57.
22. Itoh Y, et al. 2010. Sex bias and dosage compensation in the zebra finch versus chicken genomes: general and specialized patterns among birds. Genome Res. 20: 512-518.
23. Johnston CM, et al. 2008. Large-scale population study of human cell lines indicates that dosage compensation is virtually complete. PLoS Genet. 4:e9.
24. Jue NK, et al. 2013. Determination of dosage compensation of the mammalian X chromosome by RNA-Seq is dependent on analytical approach. BMC Genomics 14: 150.
25. Julien P, et al. 2012. Mechanisms and evolutionary patterns ofmammalian and avian dosage compensation. PLoS Biol. 10:e1001328.
26. Kaiser VB, Ellegren H. 2006. Nonrandom distribution of genes with sexbiased expression in the chicken genome. Evolution 60: 1945-1951.
27. Kharchenko PV, Xi RB, Park PJ. 2011. Evidence for dosage compensation between the X chromosome and autosomes in mammals. Nat Genet. 43: 1167-1169.
28. Leder EH, et al. 2010. Female-biased expression on the X chromosome as a key step in sex chromosome evolution in threespine sticklebacks. Mol Biol Evol. 27: 1495-1503.
29. Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.
30. Lin F, Xing K, Zhang J, He X. 2012. Expression reduction in mammalian X chromosome evolution refutes Ohno's hypothesis of dosage compensation. Proc Natl Acad Sci U S A. 109: 11752-11757.
31. Lin H, et al. 2007. Dosage compensation in the mouse balances upregulation and silencing of X-linked genes. PLoS Biol. 5:e326.
32. Livernois AM, Graves JA, Waters PD. 2012. The origin and evolution of vertebrate sex chromosomes and dosage compensation. Heredity 108: 50-58.
33. Livernois AM, et al. 2013. Independent evolution of transcriptional inactivation on sex chromosomes in birds and mammals. PLoS Genet. 9: e1003635.
34. Lyon MF. 1961. Gene action in the X-chromosome of the mouse (Mus musculus l.). Nature 190: 372-373.
35. Lyon MF. 1999. X-chromosome inactivation. Curr Biol. 9:R235-R237. (Pubitemid 129749919)
36. Mank JE. 2009. The w, x, y and z of sex-chromosome dosage compensation. Trends Genet. 25: 226-233.
37. Mank JE. 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends Genet. 29: 677-683.
38. Mank JE, Ellegren H. 2009. All dosage compensation is local: gene-bygene regulation of sex-biased expression on the chicken Z chromosome. Heredity 102: 312-320.
39. Mank JE, Hosken DJ,Wedell N. 2011. Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution 65: 2133-2144.
40. Mank JE, Vicoso B, Berlin S, Charlesworth B. 2010. Effective population size and the faster-X effect: empirical results and their interpretation. Evolution 64: 663-674.
41. Matsumoto SG, Hildebrand JG. 1981. Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc Roy Soc Lond B Biol Sci. 213: 249-277.
42. McKay LM, Wrigley JM, Graves JA. 1987. Evolution of mammalian Xchromosome inactivation: sex chromatin in monotremes and marsupials. Aust J Biol Sci. 40: 397-404.
43. Mita K, et al. 2004. The genome sequence of silkworm, Bombyx mori. DNA Res. 11: 27-35.
44. Mukherjee AS, Beermann W. 1965. Synthesis of ribonucleic acid by the Xchromosomes of Drosophilamelanogaster and the problem of dosage compensation. Nature 207: 785-786.
45. Naurin S, Hansson B, Bensch S, Hassequist D. 2010. Why does dosage compensation differ between XY and ZW taxa? Trends Genet. 26: 15-20.
46. Naurin S, Hasselquist D, Bensch S, Hansson B. 2012. Sex-biased gene expression on the avian Z chromosome: highly expressed genes show higher male-biased expression. PLoS One 7:e46854.
47. Nguyen DK, Disteche CM. 2006. Dosage compensation of the active X chromosome in mammals. Nat Genet. 38: 47-53.
48. Ohno S. 1967. Sex chromosomes and sex-linked genes. Berlin (Germany): Springer.
49. Parsch J, Ellegren H. 2013. The evolutionary causes and consequences of sex-biased gene expression. Nat Rev Genet. 14: 83-87.
50. Ploner A. 2012. Heatplus: heatmaps with row and/or column covariates and colored clusters. R package version 2.6.0.
51. Prince EG, Kirkland D, Demuth JP. 2010. Hyperexpression of the X chromosome in both sexes results in extensive female bias of X-linked genes in the flour beetle. Genome Biol Evol. 2: 336-346.
52. Rice WR. 1987. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution 41: 911-914.
53. Robinson MD, McCarthy DJ, Smyth GK. 2010. Edger: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
54. Rospars JP, Hildebrand JG. 2000. Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta. Chem Senses. 25: 119-129.
55. Shields VD, Hildebrand JG. 2001. Recent advances in insect olfaction, specifically regarding the morphology and sensory physiology of antennal sensilla of the female sphinx moth Manduca sexta. Microsc Res Tech. 55: 307-329.
56. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 100: 9440-9445.
57. Straub T, Becker PB. 2007. Dosage compensation: the beginning and end of generalization. Nat Rev Genet. 8: 47-57.
58. Straub T, Gilfillan GD, Maier VK, Becker PB. 2005. The Drosophila MSL complex activates the transcription of target genes. Gene Dev. 19: 2284-2288.
59. Tarazona S, García-Alcalde F, Dopazo J, Ferrer A, Conesa A. 2011. Differential expression in RNA-seq: a matter of depth. Genome Res. 21: 2213-2223.
60. Vicoso B, Bachtrog D. 2009. Progress and prospects toward our understanding of the evolution of dosage compensation. Chromosome Res. 17: 585-602.
61. Vicoso B, Bachtrog D. 2011. Lack of global dosage compensation in Schistosoma mansoni, a female-heterogametic parasite. Genome Biol Evol. 3: 230-235.
62. Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D. 2013. Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. 11:e1001643.
63. Vicoso B, Kaiser VB, Bachtrog D. 2013. Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc Natl Acad Sci U S A. 110: 6453-6458.
64. Walters JR, Hardcastle TJ. 2011. Getting a full dose? Reconsidering sex chromosome dosage compensation in the silkworm, Bombyx mori. Genome Biol Evol. 3: 491-504.
65. Wolf JB, Bryk J. 2011. General lack of global dosage compensation in ZZ/ZW systems? Broadening the perspective with RNA-Seq. BMC Genomics 12: 91.
66. Xia QY, et al. 2004. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937-1940.
67. Xiong YY, et al. 2010. RNA sequencing shows no dosage compensation of the active X-chromosome. Nat Genet. 42: 1043-1047.
68. Zars T. 2000. Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol. 10: 790-795.
69. Zha XF, et al. 2009. Dosage analysis of Z chromosome genes using microarray in silkworm, Bombyx mori. Insect Biochem Mol. 39: 315-321.
70. Zhan S, Merlin C, Boore JL, Reppert SM. 2011. The monarch butterfly genome yields insights into long-distance migration. Cell 147: 1171-1185.
71. Zhang SBO, Mathur S, Hattem G, Tassy O, Pourquie O. 2010. Sex-dimorphic gene expression and ineffective dosage compensation of Z-linked genes in gastrulating chicken embryos. BMC Genomics 11: 1-13.
72. Zhong S, et al. 2011. High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc. 8: 940-949.