Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis
Autoři:
Alfredo Rago aff001; John H. Werren aff002; John K. Colbourne aff001
Působiště autorů:
School of Biosciences, The University of Birmingham, Birmingham, United Kingdom
aff001; Department of Biology, University of Rochester, Rochester, NY, United States of America
aff002
Vyšlo v časopise:
Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis. PLoS Genet 16(1): e32767. doi:10.1371/journal.pgen.1008518
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008518
Souhrn
Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.
Klíčová slova:
DNA transcription – Embryos – Gene expression – Gene regulation – Genetic networks – Gonads – Invertebrate genomics – Sexual differentiation
Zdroje
1. Capel B. Vertebrate sex determination: Evolutionary plasticity of a fundamental switch. Nat Rev Genet. 2017;18: 675–689. doi: 10.1038/nrg.2017.60 28804140
2. Parma P, Veyrunes F, Pailhoux E. Sex Reversal in Non-Human Placental Mammals. Sex Dev. 2016;10: 326–344. doi: 10.1159/000448361 27529721
3. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature. 1991;351: 117–121. doi: 10.1038/351117a0 2030730
4. Colvin JS, Green RP, Schmahl J, Capel B, Ornitz DM. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell. 2001;104: 875–889. Available: http://www.ncbi.nlm.nih.gov/pubmed/11290325 doi: 10.1016/s0092-8674(01)00284-7 11290325
5. Ventura T, Manor R, Aflalo ED, Weil S, Rosen O, Sagi A. Timing Sexual Differentiation: Full Functional Sex Reversal Achieved Through Silencing of a Single Insulin-Like Gene in the Prawn, Macrobrachium rosenbergii1. Biol Reprod. 2012;86: 1–6. doi: 10.1095/biolreprod.111.097261 22133694
6. Verhulst EC, Beukeboom LW, van de Zande L. Maternal Control of Haplodiploid Sex Determination in the Wasp Nasonia. Science (80-). 2010;328: 620–623. doi: 10.1126/science.1185805 20431014
7. Chew KY, Renfree MB. Inducing Sex Reversal in Marsupial Mammals. Sex Dev. 2016;10: 301–312. doi: 10.1159/000450927 27794571
8. Flament S. Sex Reversal in Amphibians. Sex Dev. 2016;10: 267–278. doi: 10.1159/000448797 27648840
9. Olmstead AW, LeBlanc GA. The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean. Int J Biol Sci. 2007;3: 77–84. doi: 10.7150/ijbs.3.77 17205107
10. Ge C, Ye J, Weber C, Sun W, Zhang H, Zhou Y, et al. The histone demethylase KDM6B regulates temperature-dependent sex determination in a turtle species. Science (80-). 2018;360: 645–648. doi: 10.1126/science.aap8328 29748283
11. Holleley CE, Sarre SD, O’Meally D, Georges A. Sex Reversal in Reptiles: Reproductive Oddity or Powerful Driver of Evolutionary Change? Sex Dev. 2016;10: 279–287. doi: 10.1159/000450972 27794577
12. Ashman T-L, Bachtrog D, Blackmon H, Goldberg EE, Hahn MW, Kirkpatrick M, et al. Tree of Sex: A database of sexual systems. Sci Data. 2014;1: 1–8. doi: 10.1038/sdata.2014.15 25977773
13. Verhulst EC, van de Zande L, Beukeboom LW. Insect sex determination: it all evolves around transformer. Curr Opin Genet Dev. 2010;20: 376–83. doi: 10.1016/j.gde.2010.05.001 20570131
14. Duncan EJ, Leask MP, Dearden PK. The pea aphid (Acyrthosiphon pisum) genome encodes two divergent early developmental programs. Dev Biol. 2013;377: 262–74. doi: 10.1016/j.ydbio.2013.01.036 23416037
15. Van Doorn GS. Intralocus sexual conflict. Ann N Y Acad Sci. 2009;1168: 52–71. doi: 10.1111/j.1749-6632.2009.04573.x 19566703
16. Van Doorn GS, Bonduriansky R, Chenoweth SF. Intralocus sexual conflict. Trends Ecol Evol. 2009;24: 280–8. doi: 10.1016/j.tree.2008.12.005 19307043
17. Chippindale a K, Gibson JR, Rice WR. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci. 2001;98: 1671–5. doi: 10.1073/pnas.041378098 11172009
18. Kulmuni J, Pamilo P. Introgression in hybrid ants is favored in females but selected against in males. Proc Natl Acad Sci. 2014;111: 12805–12810. doi: 10.1073/pnas.1323045111 25136088
19. Innocenti P, Morrow EH. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol. 2010;8: e1000335. doi: 10.1371/journal.pbio.1000335 20305719
20. Chang PL, Dunham JP, Nuzhdin SV, Arbeitman MN. Somatic sex-specific transcriptome differences in Drosophila revealed by whole transcriptome sequencing. BMC Genomics. 2011;12: 364. doi: 10.1186/1471-2164-12-364 21756339
21. Wang X, Werren JH, Clark AG. Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti. Proc Natl Acad Sci. 2015;112: E3545–E3554. doi: 10.1073/pnas.1510338112 26100871
22. Perry JC, Harrison PW, Mank JE. The ontogeny and evolution of sex-biased gene expression in drosophila melanogaster. Mol Biol Evol. 2014;31: 1206–1219. doi: 10.1093/molbev/msu072 24526011
23. Mank JE, Nam K, Brunstrom B, Ellegren H. Ontogenetic Complexity of Sexual Dimorphism and Sex-Specific Selection. Mol Biol Evol. 2010;27: 1570–1578. doi: 10.1093/molbev/msq042 20142440
24. Zhao M, Zha X-F, Liu J, Zhang W-J, He N-J, Cheng D-J, et al. Global expression profile of silkworm genes from larval to pupal stages: Toward a comprehensive understanding of sexual differences. Insect Sci. 2011;18: 607–618. doi: 10.1111/j.1744-7917.2010.01392.x
25. Telonis-Scott M, Kopp A, Wayne ML, Nuzhdin SV., McIntyre LM. Sex-Specific Splicing in Drosophila: Widespread Occurrence, Tissue Specificity and Evolutionary Conservation. Genetics. 2008;181: 421–434. doi: 10.1534/genetics.108.096743 19015538
26. Hartmann B, Castelo R, Minana B, Peden E, Blanchette M, Rio DC, et al. Distinct regulatory programs establish widespread sex-specific alternative splicing in Drosophila melanogaster. RNA. 2011;17: 453–468. doi: 10.1261/rna.2460411 21233220
27. Brown JB, Boley N, Eisman R, May GE, Stoiber MH, Duff MO, et al. Diversity and dynamics of the Drosophila transcriptome. Nature. 2014;512: 393–399. doi: 10.1038/nature12962 24670639
28. Verhulst EC, Lynch JA, Bopp D, Beukeboom LW, van de Zande L. A new component of the nasonia sex determining cascade is maternally silenced and regulates transformer expression. PLoS One. 2013;8: e63618. doi: 10.1371/journal.pone.0063618 23717455
29. Ament Sa, Blatti Ca, Alaux C, Wheeler MM, Toth AL, Le Conte Y, et al. New meta-analysis tools reveal common transcriptional regulatory basis for multiple determinants of behavior. Proc Natl Acad Sci. 2012;109: E1801–E1810. doi: 10.1073/pnas.1205283109 22691501
30. Spitz F, Furlong EEM. Transcription factors: from enhancer binding to developmental control. Nat Rev Genet. 2012;13: 613–626. doi: 10.1038/nrg3207 22868264
31. Boyle AP, Araya CL, Brdlik C, Cayting P, Cheng C, Cheng Y, et al. Comparative analysis of regulatory information and circuits across distant species. Nature. 2014;512: 453–456. doi: 10.1038/nature13668 25164757
32. Arnold AP, van Nas A, Lusis AJ. Systems biology asks new questions about sex differences. Trends Endocrinol Metab. 2009;20: 471–476. doi: 10.1016/j.tem.2009.06.007 19783453
33. Van Nas A, Guhathakurta D, Wang SS, Yehya N, Horvath S, Zhang B, et al. Elucidating the role of gonadal hormones in sexually dimorphic gene coexpression networks. Endocrinology. 2009;150: 1235–1249. doi: 10.1210/en.2008-0563 18974276
34. Tesson BM, Breitling R, Jansen RC. DiffCoEx: a simple and sensitive method to find differentially coexpressed gene modules. BMC Bioinformatics. 2010;11: 497. doi: 10.1186/1471-2105-11-497 20925918
35. Yang J, Yu H, Liu BH, Zhao Z, Liu L, Ma LX, et al. DCGL v2.0: An R package for unveiling differential regulation from differential co-expression. PLoS One. 2013;8: 4–11. doi: 10.1371/journal.pone.0079729 24278165
36. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9: 559. doi: 10.1186/1471-2105-9-559 19114008
37. Zampieri M, Soranzo N, Altafini C. Discerning static and causal interactions in genome-wide reverse engineering problems. Bioinformatics. 2008;24: 1510–5. doi: 10.1093/bioinformatics/btn220 18467346
38. de la Fuente A. From differential expression to differential networking: identification of dysfunctional regulatory networks in diseases. Trends Genet. 2010;26: 326–333. doi: 10.1016/j.tig.2010.05.001 20570387
39. Mozhui K, Lu L, Armstrong WE, Williams RW. Sex-specific modulation of gene expression networks in murine hypothalamus. Front Neurosci. 2012;6: 1–18. doi: 10.3389/fnins.2012.00001
40. Whiting PW. The chromosomes of Mormoniella. J Hered. 1968;59: 19–22. Available: http://www.ncbi.nlm.nih.gov/pubmed/5656911 doi: 10.1093/oxfordjournals.jhered.a107631 5656911
41. Heimpel GE, de Boer JG. Sex determination in the hymenoptera. Annu Rev Entomol. 2008;53: 209–30. doi: 10.1146/annurev.ento.53.103106.093441 17803453
42. Godfray HCJ. Nasonia: a jewel among wasps. Heredity (Edinb). 2010;104: 235–6. doi: 10.1038/hdy.2010.3 20160755
43. Pultz MA, Leaf DS. The jewel wasp Nasonia: querying the genome with haplo-diploid genetics. Genesis. 2003;35: 185–91. doi: 10.1002/gene.10189 12640624
44. Heraty J. Parasitoid biodiversity and insect pest management. Insect Biodivers Sci Soc. 2009; 445–462.
45. Heraty JM, Burks RA, Cruaud A, Gibson GAP, Liljeblad J, Munro J, et al. A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). Cladistics. 2013;29: 466–542. doi: 10.1111/cla.12006
46. Werren JH, Richards S, Desjardins Ca, Niehuis O, Gadau J, Colbourne JK, et al. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science (80-). 2010;327: 343–8. doi: 10.1126/science.1178028 20075255
47. The Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006;443: 931–949. doi: 10.1038/nature05260 17073008
48. Branstetter MG, Childers AK, Cox-Foster D, Hopper KR, Kapheim KM, Toth AL, et al. Genomes of the Hymenoptera. Curr Opin Insect Sci. 2018;25: 65–75. doi: 10.1016/j.cois.2017.11.008 29602364
49. Clark ME, O’Hara FP, Chawla A, Werren JH. Behavioral and spermatogenic hybrid male breakdown in Nasonia. Heredity (Edinb). 2010;104: 289–301. doi: 10.1038/hdy.2009.152 20087395
50. Desjardins CA, Gadau J, Lopez JA, Niehuis O, Avery AR, Loehlin DW, et al. Fine-Scale Mapping of the Nasonia Genome to Chromosomes Using a High-Density Genotyping Microarray. G3 Genes Genomes Genet. 2013;3: 205–215. doi: 10.1534/g3.112.004739 23390597
51. Thompson MJ, Jiggins CD. Supergenes and their role in evolution. Heredity (Edinb). 2014;113: 1–8. doi: 10.1038/hdy.2014.20 24642887
52. Kovalick GE, Griffin DL. Characterization of the SCP/TAPS gene family in Drosophila melanogaster. Insect Biochem Mol Biol. 2005;35: 825–835. doi: 10.1016/j.ibmb.2005.03.003 15944079
53. Ellegren H, Parsch J. The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet. 2007;8: 689–98. doi: 10.1038/nrg2167 17680007
54. Yeaman S. Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proc Natl Acad Sci. 2013 [cited 23 Apr 2013]. doi: 10.1073/pnas.1219381110 23610436
55. Hirano T. Condensins and the evolution of torsion-mediated genome organization. Trends Cell Biol. 2014;24: 727–733. doi: 10.1016/j.tcb.2014.06.007 25092191
56. Davies NJ, Tauber E. WaspAtlas: a Nasonia vitripennis gene database and analysis platform. Database. 2015;2015: bav103. doi: 10.1093/database/bav103 26452372
57. Akbari OS, Antoshechkin I, Hay Ba, Ferree PM. Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio. G3 (Bethesda). 2013;3: 1597–605. doi: 10.1534/g3.113.007583 23893741
58. Rago A, Gilbert DG, Choi J-H, Sackton TB, Wang X, Kelkar YD, et al. OGS2: genome re-annotation of the jewel wasp Nasonia vitripennis. BMC Genomics. 2016;17: 5303. doi: 10.1186/s12864-016-2886-9 27561358
59. Hoedjes KM, Smid HM, Schijlen EG, Vet LE, van Vugt JJ. Learning-induced gene expression in the heads of two Nasonia species that differ in long-term memory formation. BMC Genomics. 2015;16: 1–13. doi: 10.1186/1471-2164-16-1
60. Baker RH, Narechania A, Johns PM, Wilkinson GS. Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae). Philos Trans R Soc Lond B Biol Sci. 2012;367: 2357–75. doi: 10.1098/rstb.2011.0287 22777023
61. Gallach M, Betrán E. Intralocus sexual conflict resolved through gene duplication. Trends Ecol Evol. 2011;26: 222–8. doi: 10.1016/j.tree.2011.02.004 21397976
62. Parsch J, Ellegren H. The evolutionary causes and consequences of sex-biased gene expression. Nat Rev Genet. 2013;14: 83–7. doi: 10.1038/nrg3376 23329110
63. Wyman MJ, Cutter AD, Rowe L. Gene duplication in the evolution of sexual dimorphism. Evolution (N Y). 2012;66: 1556–1566. doi: 10.1111/j.1558-5646.2011.01525.x 22519790
64. Sackton TB, Werren JH, Clark AG. Characterizing the infection-induced transcriptome of Nasonia vitripennis reveals a preponderance of taxonomically-restricted immune genes. PLoS One. 2013;8: e83984. doi: 10.1371/journal.pone.0083984 24386321
65. Lindsey ARI, Kelkar YD, Wu X, Sun D, Martinson EO, Yan Z, et al. Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum. BMC Biol. 2018;16: 54. doi: 10.1186/s12915-018-0520-9 29776407
66. Peters RS, Niehuis O, Gunkel S, Bläser M, Mayer C, Podsiadlowski L, et al. Transcriptome sequence-based phylogeny of chalcidoid wasps (Hymenoptera: Chalcidoidea) reveals a history of rapid radiations, convergence, and evolutionary success. Mol Phylogenet Evol. 2018;120: 286–296. doi: 10.1016/j.ympev.2017.12.005 29247847
67. Martinson EOEO, Mrinalini Kelkar YDYD, Chang C-HCH, Werren JHJH. The evolution of venom by co-option of single copy genes. Curr Biol. 2017;In this is: 2007—2013.e8. doi: 10.1016/j.cub.2017.05.032 28648823
68. Ometto L, Shoemaker D, Ross KG, Keller L. Evolution of Gene Expression in Fire Ants: The Effects of Developmental Stage, Caste, and Species. Mol Biol Evol. 2011;28: 1381–1392. doi: 10.1093/molbev/msq322 21172833
69. Connallon T, Clark AG. Sex linkage, sex-specific selection, and the role of recombination in the evolution of sexually dimorphic gene expression. Evolution (N Y). 2010;64: 3417–3442. doi: 10.1111/j.1558-5646.2010.01136.x 20874735
70. Tennessen JM, Bertagnolli NM, Evans J, Sieber MH, Cox J, Thummel CS. Coordinated metabolic transitions during Drosophila embryogenesis and the onset of aerobic glycolysis. G3 (Bethesda). 2014;4: 839–50. doi: 10.1534/g3.114.010652 24622332
71. Verhulst EC, Beukeboom LW, van de Zande L. Maternal Control of Haplodiploid Sex Determination in the Wasp Nasonia. Science (80-). 2010;328: 620–623. doi: 10.1126/science.1185805 20431014
72. Park J, Peng Z, Zeng J, Elango N, Park T, Wheeler D, et al. Comparative analyses of DNA methylation and sequence evolution using Nasonia genomes. Mol Biol Evol. 2011;28: 3345–54. doi: 10.1093/molbev/msr168 21693438
73. Wang X, Wheeler D, Avery A, Rago A, Choi J-H, Colbourne JK, et al. Function and evolution of DNA methylation in Nasonia vitripennis. PLoS Genet. 2013;9: e1003872. doi: 10.1371/journal.pgen.1003872 24130511
74. Marbach D, Costello JC, Küffner R, Vega NM, Prill RJ, Camacho DM, et al. Wisdom of crowds for robust gene network inference. Nat Methods. 2012;9: 796–804. doi: 10.1038/nmeth.2016 22796662
75. Wang Y, Cho DY, Lee H, Fear J, Oliver B, Przytycka TM. Reprogramming of regulatory network using expression uncovers sex-specific gene regulation in Drosophila. Nat Commun. 2018;9. doi: 10.1038/s41467-018-06382-z 30283019
76. Moyers Ba., Zhang J. Phylostratigraphic Bias Creates Spurious Patterns of Genome Evolution. Mol Biol Evol. 2014;32: 258–267. doi: 10.1093/molbev/msu286 25312911
77. Ding Y, Zhao L, Yang S, Jiang Y, Chen Y, Zhao R, et al. A young drosophila duplicate gene plays essential roles in spermatogenesis by regulating several Y-linked male fertility genes. PLoS Genet. 2010;6: 1–12. doi: 10.1371/journal.pgen.1001255 21203494
78. Dai H, Chen Y, Chen S, Mao Q, Kennedy D, Landback P, et al. The evolution of courtship behaviours through the origination of a new gene in Drosophila. Proc Natl Acad Sci. 2008;105: 7478–7483. doi: 10.1073/pnas.0800693105 18508971
79. Ferreira PG, Patalano S, Chauhan R, Ffrench-Constant R, Gabaldón T, Guigó R, et al. Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes. Genome Biol. 2013;14: R20. doi: 10.1186/gb-2013-14-2-r20 23442883
80. Dessimoz C, Škunca N, editors. The Gene Ontology Handbook. New York, NY: Springer New York; 2017. doi: 10.1007/978-1-4939-3743-1
81. Werren JH. The Evolution of Inbreeding in Haplodiploid Organisms. Nat Hist Inbreeding Outbreeding Theor Empir Perspect. 1993; 42.
82. Bull AL. Stages of living embryos in the jewel wasp Mormoniella (nasonia) vitripennis (walker) (hymenoptera: pteromalidae). Int J Insect Morphol Embryol. 1982;11: 1–23. doi: 10.1016/0020-7322(82)90034-4
83. Lopez J, Colbourne J. Dual Labeled Expression-Tiling Microarray Protocol for Empirical Annotation of Genome Sequences. CGB Tech Rep. 2011;2011. doi: 10.2506/cgbtr-201101
84. Rago A, Colbourne JK. FESTA: Flexible Exon-based Splicing and Transcription Annotation. bioRxiv. 2018; 300947. doi: 10.1101/300947
85. Hsu C, Juan H-F, Huang H-C. Functional Analysis and Characterization of Differential Coexpression Networks. Sci Rep. 2015;5: 13295. doi: 10.1038/srep13295 26282208
86. Zhang B, Horvath S. A General Framework for Weighted Gene Co-Expression Network Analysis. Stat Appl Genet Mol Biol. 2005;4. doi: 10.2202/1544-6115.1128 16646834
87. Jeong H, Mason SP, Barabási A-L, Oltvai ZN. Lethality and centrality in protein networks. Nature. 2001;411: 41–42. Available: http://www.nature.com/nature/journal/v411/n6833/abs/411041a0.html doi: 10.1038/35075138 11333967
88. Wagner A, Fell DA. The small world inside large metabolic networks. Proc R Soc B Biol Sci. 2001;268: 1803–1810. doi: 10.1098/rspb.2001.1711 11522199
89. Barabási A-LL, Oltvai ZN. Network biology: understanding the cell’s functional organization. Nat Rev Genet. 2004;5: 101–13. doi: 10.1038/nrg1272 14735121
90. Opsahl T. Structure and Evolution of Weighted Networks. University of London (Queen Mary College), London, UK; 2009. Available: http://toreopsahl.com/publications/thesis/
91. Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions Using {R} and Bioconductor. New York: Springer; 2005. pp. 397–420.
92. Strimmer K. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics. 2008;24: 1461–2. doi: 10.1093/bioinformatics/btn209 18441000
93. Ma H, Schadt EE, Kaplan LM, Zhao H. COSINE: COndition-SpecIfic sub-NEtwork identification using a global optimization method. Bioinformatics. 2011;27: 1290–1298. doi: 10.1093/bioinformatics/btr136 21414987
94. Liu X, Wang Y, Ji H, Aihara K, Chen L. Personalized characterization of diseases using sample-specific networks. Nucleic Acids Res. 2016;44: gkw772. doi: 10.1093/nar/gkw772 27596597
95. Cao M, Pietras CM, Feng X, Doroschak KJ, Schaffner T, Park J, et al. New directions for diffusion-based network prediction of protein function: Incorporating pathways with confidence. Bioinformatics. 2014;30: 219–227. doi: 10.1093/bioinformatics/btu263 24931987
96. Yu H, Liu B-H, Ye Z-Q, Li C, Li Y-X, Li Y-Y. Link-based quantitative methods to identify differentially coexpressed genes and gene pairs. BMC Bioinformatics. 2011;12: 315. doi: 10.1186/1471-2105-12-315 21806838
97. Walley A, Jacobson P, Falchi M, Bottolo L, Andersson J, Petretto E, et al. Differential coexpression analysis of obesity-associated networks in human subcutaneous adipose tissue. Int J Obes. 2012;36: 1–11. doi: 10.1038/ijo.2011.22 21427694
98. Horvath S, Dong J. Geometric interpretation of gene coexpression network analysis. PLoS Comput Biol. 2008;4: e1000117. doi: 10.1371/journal.pcbi.1000117 18704157
99. Dong J, Horvath S. Understanding network concepts in modules. BMC Syst Biol. 2007;1: 24. doi: 10.1186/1752-0509-1-24 17547772
100. Barton K. MuMIn: Multi-model inference. 2011. Available: http://cran.r-project.org/package=MuMIn
101. Domazet-Lošo T, Tautz D. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature. 2010;468: 815–8. doi: 10.1038/nature09632 21150997
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