Review Special Issues

Comparative epigenomics: an emerging field with breakthrough potential to understand evolution of epigenetic regulation

  • Received: 02 November 2014 Accepted: 15 December 2014 Published: 17 December 2014
  • Epigenetic mechanisms regulate gene expression, thereby mediating the interaction between environment, genotype and phenotype. Changes to epigenetic regulation of genes may be heritable, permitting rapid adaptation of a species to environmental cues. However, most of the current understanding of epigenetic gene regulation has been gained from studies of mice and humans, with only a limited understanding of the conservation of epigenetic mechanisms across divergent taxa. The relative ease at which genome sequence data is now obtained and the advancements made in epigenomics techniques for non-model species provides a basis for carrying out comparative epigenomic studies across a wider range of species, making it possible to start unraveling the evolution of epigenetic mechanisms. We review the current knowledge of epigenetic mechanisms obtained from studying model organisms, give an example of how comparative epigenomics using non-model species is helping to trace the evolutionary history of X chromosome inactivation in mammals and explore the opportunities to study comparative epigenomics in biological systems displaying adaptation between species, such as the immune system and sex determination.

    Citation: Janine E. Deakin, Renae Domaschenz, Pek Siew Lim, Tariq Ezaz, Sudha Rao. Comparative epigenomics: an emerging field with breakthrough potential to understand evolution of epigenetic regulation[J]. AIMS Genetics, 2014, 1(1): 34-54. doi: 10.3934/genet.2014.1.34

    Related Papers:

  • Epigenetic mechanisms regulate gene expression, thereby mediating the interaction between environment, genotype and phenotype. Changes to epigenetic regulation of genes may be heritable, permitting rapid adaptation of a species to environmental cues. However, most of the current understanding of epigenetic gene regulation has been gained from studies of mice and humans, with only a limited understanding of the conservation of epigenetic mechanisms across divergent taxa. The relative ease at which genome sequence data is now obtained and the advancements made in epigenomics techniques for non-model species provides a basis for carrying out comparative epigenomic studies across a wider range of species, making it possible to start unraveling the evolution of epigenetic mechanisms. We review the current knowledge of epigenetic mechanisms obtained from studying model organisms, give an example of how comparative epigenomics using non-model species is helping to trace the evolutionary history of X chromosome inactivation in mammals and explore the opportunities to study comparative epigenomics in biological systems displaying adaptation between species, such as the immune system and sex determination.


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    [1] Consortium EP, Bernstein BE, Birney E, et al. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74. doi: 10.1038/nature11247
    [2] Waddington CH (1942) The epigenotype. Endeavour 1: 18-20.
    [3] Lee JT (2011) Gracefully ageing at 50, X-chromosome inactivation becomes a paradigm for RNA and chromatin control. Nat Rev Mol Cell Biol 12: 815-826. doi: 10.1038/nrm3231
    [4] Koerner MV, Barlow DP (2010) Genomic imprinting-an epigenetic gene-regulatory model. Curr Opin Genet Dev 20: 164-170. doi: 10.1016/j.gde.2010.01.009
    [5] Feinberg AP, Tycko B (2004) The history of cancer epigenetics. Nat Rev Cancer 4: 143-153. doi: 10.1038/nrc1279
    [6] Lim PS, Li J, Holloway AF, et al. (2013) Epigenetic regulation of inducible gene expression in the immune system. Immunology 139: 285-293. doi: 10.1111/imm.12100
    [7] Gomes MV, Pelosi GG (2013) Epigenetic vulnerability and the environmental influence on health. Exp Biol Med (Maywood) 238: 859-865. doi: 10.1177/1535370213490630
    [8] Richards EJ (2008) Population epigenetics. Curr Opin Genet Dev 18: 221-226. doi: 10.1016/j.gde.2008.01.014
    [9] Gupta S (2013) Epigenetics posited as important for evolutionary success. Nature News.
    [10] Liebl AL, Schrey AW, Richards CL, et al. (2013) Patterns of DNA methylation throughout a range expansion of an introduced songbird. Integr Comp Biol 53: 351-358. doi: 10.1093/icb/ict007
    [11] Richards CL, Schrey AW, Pigliucci M (2012) Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol Lett 15: 1016-1025. doi: 10.1111/j.1461-0248.2012.01824.x
    [12] Luger K, Mader AW, Richmond RK, et al. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
    [13] Hager GL, McNally JG, Misteli T (2009) Transcription dynamics. Mol Cell 35: 741-753. doi: 10.1016/j.molcel.2009.09.005
    [14] Reid G, Gallais R, Metivier R (2009) Marking time: the dynamic role of chromatin and covalent modification in transcription. Int J Biochem Cell Biol 41: 155-163. doi: 10.1016/j.biocel.2008.08.028
    [15] Wolffe AP (2001) Histone genes. In: Breener S, Miller JH, editors. Encyclopedia of Genetics. San Diego & London: Academic Press. 948-952.
    [16] Munshi A, Shafi G, Aliya N, et al. (2009) Histone modifications dictate specific biological readouts. J Genet Genomics 36: 75-88. doi: 10.1016/S1673-8527(08)60094-6
    [17] Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14: R546-551. doi: 10.1016/j.cub.2004.07.007
    [18] Tan M, Luo H, Lee S, et al. (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146: 1016-1028. doi: 10.1016/j.cell.2011.08.008
    [19] Ho JW, Jung YL, Liu T, et al. (2014) Comparative analysis of metazoan chromatin organization. Nature 512: 449-452. doi: 10.1038/nature13415
    [20] Fuchs J, Demidov D, Houben A, et al. (2006) Chromosomal histone modification patterns--from conservation to diversity. Trends Plant Sci 11: 199-208. doi: 10.1016/j.tplants.2006.02.008
    [21] de Ruijter AJ, van Gennip AH, Caron HN, et al. (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370: 737-749. doi: 10.1042/BJ20021321
    [22] Marmorstein R, Roth SY (2001) Histone acetyltransferases: function, structure, and catalysis. Curr Opin Genet Dev 11: 155-161. doi: 10.1016/S0959-437X(00)00173-8
    [23] Marzluff WF, Gongidi P, Woods KR, et al. (2002) The human and mouse replication-dependent histone genes. Genomics 80: 487-498. doi: 10.1006/geno.2002.6850
    [24] Boulard M, Bouvet P, Kundu TK, et al. (2007) Histone variant nucleosomes: structure, function and implication in disease. Subcell Biochem 41: 71-89.
    [25] Talbert PB, Henikoff S (2010) Histone variants--ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275.
    [26] Yelagandula R, Stroud H, Holec S, et al. (2014) The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158: 98-109.
    [27] Marino-Ramirez L, Kann MG, Shoemaker BA, et al. (2005) Histone structure and nucleosome stability. Expert Rev Proteomics 2: 719-729. doi: 10.1586/14789450.2.5.719
    [28] Talbert PB, Ahmad K, Almouzni G, et al. (2012) A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 5: 7. doi: 10.1186/1756-8935-5-7
    [29] Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304. doi: 10.1146/annurev.biochem.77.062706.153223
    [30] Smith CL, Peterson CL (2005) A conserved Swi2/Snf2 ATPase motif couples ATP hydrolysis to chromatin remodeling. Mol Cell Biol 25: 5880-5892. doi: 10.1128/MCB.25.14.5880-5892.2005
    [31] Saha A, Wittmeyer J, Cairns BR (2006) Chromatin remodelling: the industrial revolution of DNA around histones. Nat Rev Mol Cell Biol 7: 437-447.
    [32] Shen W, Xu C, Huang W, et al. (2007) Solution structure of human Brg1 bromodomain and its specific binding to acetylated histone tails. Biochemistry 46: 2100-2110. doi: 10.1021/bi0611208
    [33] Mohrmann L, Verrijzer CP (2005) Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim Biophys Acta 1681: 59-73. doi: 10.1016/j.bbaexp.2004.10.005
    [34] Bultman S, Gebuhr T, Yee D, et al. (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6: 1287-1295. doi: 10.1016/S1097-2765(00)00127-1
    [35] Bestor TH, Verdine GL (1994) DNA methyltransferases. Curr Opin Cell Biol 6: 380-389. doi: 10.1016/0955-0674(94)90030-2
    [36] Ooi SK, O'Donnell AH, Bestor TH (2009) Mammalian cytosine methylation at a glance. J Cell Sci 122: 2787-2791. doi: 10.1242/jcs.015123
    [37] Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514. doi: 10.1146/annurev.biochem.74.010904.153721
    [38] Jeltsch A (2010) Phylogeny of methylomes. Science 328: 837-838. doi: 10.1126/science.1190738
    [39] Lyko F, Foret S, Kucharski R, et al. (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8: e1000506. doi: 10.1371/journal.pbio.1000506
    [40] Feng S, Cokus SJ, Zhang X, et al. (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 107: 8689-8694. doi: 10.1073/pnas.1002720107
    [41] Zemach A, McDaniel IE, Silva P, et al. (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-919. doi: 10.1126/science.1186366
    [42] Zilberman D, Gehring M, Tran RK, et al. (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39: 61-69. doi: 10.1038/ng1929
    [43] Falckenhayn C, Boerjan B, Raddatz G, et al. (2013) Characterization of genome methylation patterns in the desert locust Schistocerca gregaria. J Exp Biol 216: 1423-1429. doi: 10.1242/jeb.080754
    [44] Fneich S, Dheilly N, Adema C, et al. (2013) 5-methyl-cytosine and 5-hydroxy-methyl-cytosine in the genome of Biomphalaria glabrata, a snail intermediate host of Schistosoma mansoni. Parasit Vectors 6: 167. doi: 10.1186/1756-3305-6-167
    [45] Tahiliani M, Koh KP, Shen Y, et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935. doi: 10.1126/science.1170116
    [46] Spruijt CG, Gnerlich F, Smits AH, et al. (2013) Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152: 1146-1159. doi: 10.1016/j.cell.2013.02.004
    [47] Almeida RD, Sottile V, Loose M, et al. (2012) Semi-quantitative immunohistochemical detection of 5-hydroxymethyl-cytosine reveals conservation of its tissue distribution between amphibians and mammals. Epigenetics 7: 137-140. doi: 10.4161/epi.7.2.18949
    [48] Almeida RD, Loose M, Sottile V, et al. (2012) 5-hydroxymethyl-cytosine enrichment of non-committed cells is not a universal feature of vertebrate development. Epigenetics 7: 383-389. doi: 10.4161/epi.19375
    [49] Wojciechowski M, Rafalski D, Kucharski R, et al. (2014) Insights into DNA hydroxymethylation in the honeybee from in-depth analyses of TET dioxygenase. Open Biol 4.
    [50] Khalil AM, Guttman M, Huarte M, et al. (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106: 11667-11672. doi: 10.1073/pnas.0904715106
    [51] Koziol MJ, Rinn JL (2010) RNA traffic control of chromatin complexes. Curr Opin Genet Dev 20: 142-148. doi: 10.1016/j.gde.2010.03.003
    [52] Mercer TR, Mattick JS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20: 300-307. doi: 10.1038/nsmb.2480
    [53] Bernstein E, Allis CD (2005) RNA meets chromatin. Genes Dev 19: 1635-1655. doi: 10.1101/gad.1324305
    [54] Gendrel AV, Colot V (2005) Arabidopsis epigenetics: when RNA meets chromatin. Curr Opin Plant Biol 8: 142-147. doi: 10.1016/j.pbi.2005.01.007
    [55] Hall IM, Noma K, Grewal SI (2003) RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc Natl Acad Sci U S A 100: 193-198. doi: 10.1073/pnas.232688099
    [56] Volpe TA, Kidner C, Hall IM, et al. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833-1837. doi: 10.1126/science.1074973
    [57] Grewal SI, Moazed D (2003) Heterochromatin and epigenetic control of gene expression. Science 301: 798-802. doi: 10.1126/science.1086887
    [58] Hannon GJ (2002) RNA interference. Nature 418: 244-251. doi: 10.1038/418244a
    [59] Meister G, Tuschl T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343-349. doi: 10.1038/nature02873
    [60] Tomari Y, Zamore PD (2005) Perspective: machines for RNAi. Genes Dev 19: 517-529. doi: 10.1101/gad.1284105
    [61] Quach H, Barreiro LB, Laval G, et al. (2009) Signatures of purifying and local positive selection in human miRNAs. Am J Hum Genet 84: 316-327. doi: 10.1016/j.ajhg.2009.01.022
    [62] Clark AM, Goldstein LD, Tevlin M, et al. (2010) The microRNA miR-124 controls gene expression in the sensory nervous system of Caenorhabditis elegans. Nucleic Acids Res 38: 3780-3793. doi: 10.1093/nar/gkq083
    [63] Aboobaker AA, Tomancak P, Patel N, et al. (2005) Drosophila microRNAs exhibit diverse spatial expression patterns during embryonic development. Proc Natl Acad Sci U S A 102: 18017-18022. doi: 10.1073/pnas.0508823102
    [64] Deo M, Yu JY, Chung KH, et al. (2006) Detection of mammalian microRNA expression by in situ hybridization with RNA oligonucleotides. Dev Dyn 235: 2538-2548. doi: 10.1002/dvdy.20847
    [65] Wienholds E, Kloosterman WP, Miska E, et al. (2005) MicroRNA expression in zebrafish embryonic development. Science 309: 310-311. doi: 10.1126/science.1114519
    [66] Mor E, Shomron N (2013) Species-specific microRNA regulation influences phenotypic variability: perspectives on species-specific microRNA regulation. Bioessays 35: 881-888.
    [67] Xi QY, Xiong YY, Wang YM, et al. (2014) Genome-wide discovery of novel and conserved microRNAs in white shrimp (Litopenaeus vannamei). Mol Biol Rep [Epub ahead of print].
    [68] Jain M, Chevala VN, Garg R (2014) Genome-wide discovery and differential regulation of conserved and novel microRNAs in chickpea via deep sequencing. J Exp Bot 65: 5945-5958. doi: 10.1093/jxb/eru333
    [69] Cowled C, Stewart CR, Likic VA, et al. (2014) Characterisation of novel microRNAs in the Black flying fox (Pteropus alecto) by deep sequencing. BMC Genomics 15: 682. doi: 10.1186/1471-2164-15-682
    [70] Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42: D68-73. doi: 10.1093/nar/gkt1181
    [71] Disteche CM (2012) Dosage compensation of the sex chromosomes. Annu Rev Genet 46: 537-560. doi: 10.1146/annurev-genet-110711-155454
    [72] Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190: 372-373. doi: 10.1038/190372a0
    [73] Deakin JE (2013) Marsupial X chromosome inactivation: past, present and future. Aust J Zool 61: 13-23. doi: 10.1071/ZO12113
    [74] Glas R, Marshall Graves JA, Toder R, et al. (1999) Cross-species chromosome painting between human and marsupial directly demonstrates the ancient region of the mammalian X. Mamm Genome 10: 1115-1116. doi: 10.1007/s003359901174
    [75] Graves JA (1995) The evolution of mammalian sex chromosomes and the origin of sex determining genes. Philos Trans R Soc Lond B Biol Sci 350: 305-311; discussion 311-302. doi: 10.1098/rstb.1995.0166
    [76] Grant J, Mahadevaiah SK, Khil P, et al. (2012) Rsx is a metatherian RNA with Xist-like properties in X-chromosome inactivation. Nature 487: 254-258. doi: 10.1038/nature11171
    [77] Borsani G, Tonlorenzi R, Simmler MC, et al. (1991) Characterization of a murine gene expressed from the inactive X chromosome. Nature 351: 325-329. doi: 10.1038/351325a0
    [78] Heard E (2005) Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr Opin Genet Dev 15: 482-489. doi: 10.1016/j.gde.2005.08.009
    [79] Koina E, Chaumeil J, Greaves IK, et al. (2009) Specific patterns of histone marks accompany X chromosome inactivation in a marsupial. Chromosome Res 17: 115-126. doi: 10.1007/s10577-009-9020-7
    [80] Rens W, Wallduck MS, Lovell FL, et al. (2010) Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc Natl Acad Sci U S A 107: 17657-17662. doi: 10.1073/pnas.0910322107
    [81] Zakharova IS, Shevchenko AI, Shilov AG, et al. (2011) Histone H3 trimethylation at lysine 9 marks the inactive metaphase X chromosome in the marsupial Monodelphis domestica. Chromosoma 120: 177-183. doi: 10.1007/s00412-010-0300-y
    [82] Chaumeil J, Waters PD, Koina E, et al. (2011) Evolution from XIST-independent to XIST-controlled X-chromosome inactivation: epigenetic modifications in distantly related mammals. PLoS One 6: e19040. doi: 10.1371/journal.pone.0019040
    [83] Mahadevaiah SK, Royo H, VandeBerg JL, et al. (2009) Key features of the X inactivation process are conserved between marsupials and eutherians. Curr Biol 19: 1478-1484. doi: 10.1016/j.cub.2009.07.041
    [84] Plath K, Fang J, Mlynarczyk-Evans SK, et al. (2003) Role of histone H3 lysine 27 methylation in X inactivation. Science 300: 131-135. doi: 10.1126/science.1084274
    [85] Zhao J, Sun BK, Erwin JA, et al. (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756. doi: 10.1126/science.1163045
    [86] Costanzi C, Pehrson JR (1998) Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393: 599-601. doi: 10.1038/31275
    [87] Hornecker JL, Samollow PB, Robinson ES, et al. (2007) Meiotic sex chromosome inactivation in the marsupial Monodelphis domestica. Genesis 45: 696-708. doi: 10.1002/dvg.20345
    [88] Kaslow DC, Migeon BR, Persico MG, et al. (1987) Molecular studies of marsupial X chromosomes reveal limited sequence homology of mammalian X-linked genes. Genomics 1: 19-28. doi: 10.1016/0888-7543(87)90100-5
    [89] Loebel DA, Johnston PG (1996) Methylation analysis of a marsupial X-linked CpG island by bisulfite genomic sequencing. Genome Res 6: 114-123. doi: 10.1101/gr.6.2.114
    [90] Wang X, Douglas KC, Vandeberg JL, et al. (2013) Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica. Genome Res 24: 70-83.
    [91] Loebel DA, Johnston PG (1993) Analysis of DNase 1 sensitivity and methylation of active and inactive X chromosomes of kangaroos (Macropus robustus) by in situ nick translation. Chromosoma 102: 81-87. doi: 10.1007/BF00356024
    [92] Hellman A, Chess A (2007) Gene body-specific methylation on the active X chromosome. Science 315: 1141-1143. doi: 10.1126/science.1136352
    [93] Deakin JE, Hore TA, Koina E, et al. (2008) The status of dosage compensation in the multiple X chromosomes of the platypus. PLoS Genet 4: e1000140. doi: 10.1371/journal.pgen.1000140
    [94] Livernois AM, Waters SA, Deakin JE, et al. (2013) Independent evolution of transcriptional inactivation on sex chromosomes in birds and mammals. PLoS Genet 9: e1003635. doi: 10.1371/journal.pgen.1003635
    [95] Livernois AM (2013) Evolution of transcriptional inactivation on sex chromosomes in birds and mammals: The Australian National University. 145.
    [96] Kondilis-Mangum HD, Wade PA (2013) Epigenetics and the adaptive immune response. Mol Aspects Med 34: 813-825. doi: 10.1016/j.mam.2012.06.008
    [97] Seita J, Weissman IL (2010) Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip Rev Syst Biol Med 2: 640-653. doi: 10.1002/wsbm.86
    [98] Zediak VP, Wherry EJ, Berger SL (2011) The contribution of epigenetic memory to immunologic memory. Curr Opin Genet Dev 21: 154-159. doi: 10.1016/j.gde.2011.01.016
    [99] Araki Y, Wang Z, Zang C, et al. (2009) Genome-wide Analysis of Histone Methylation Reveals Chromatin State-Based Regulation of Gene Transcription and Function of Memory CD8(+) T Cells. Immunity 30: 912-925. doi: 10.1016/j.immuni.2009.05.006
    [100] Barski A, Cuddapah S, Cui K, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837. doi: 10.1016/j.cell.2007.05.009
    [101] Roh TY, Cuddapah S, Cui K, et al. (2006) The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci U S A 103: 15782-15787. doi: 10.1073/pnas.0607617103
    [102] Roh TY, Cuddapah S, Zhao K (2005) Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19: 542-552. doi: 10.1101/gad.1272505
    [103] Roh TY, Ngau WC, Cui K, et al. (2004) High-resolution genome-wide mapping of histone modifications. Nat Biotechnol 22: 1013-1016. doi: 10.1038/nbt990
    [104] Schones DE, Cui K, Cuddapah S, et al. (2008) Dynamic regulation of nucleosome positioning in the human genome. Cell 132: 887-898. doi: 10.1016/j.cell.2008.02.022
    [105] Wang Z, Zang C, Rosenfeld JA, et al. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903. doi: 10.1038/ng.154
    [106] Lim PS, Shannon MF, Hardy K (2010) Epigenetic control of inducible gene expression in the immune system. Epigenomics 2: 775-795. doi: 10.2217/epi.10.55
    [107] Wei G, Wei L, Zhu J, et al. (2009) Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30: 155-167. doi: 10.1016/j.immuni.2008.12.009
    [108] Lim PS, Hardy K, Bunting KL, et al. (2009) Defining the chromatin signature of inducible genes in T cells. Genome Biol 10: R107. doi: 10.1186/gb-2009-10-10-r107
    [109] Smith AE, Chronis C, Christodoulakis M, et al. (2009) Epigenetics of human T cells during the G0-->G1 transition. Genome Res 19: 1325-1337. doi: 10.1101/gr.085530.108
    [110] Barski A, Jothi R, Cuddapah S, et al. (2009) Chromatin poises miRNA- and protein-coding genes for expression. Genome Res 19: 1742-1751. doi: 10.1101/gr.090951.109
    [111] Belov K, Sanderson CE, Deakin JE, et al. (2007) Characterization of the opossum immune genome provides insights into the evolution of the mammalian immune system. Genome Res 17: 982-991. doi: 10.1101/gr.6121807
    [112] Deakin JE, Belov K, Curach NC, et al. (2005) High levels of variability in immune response using antigens from two reproductive proteins in brushtail possums. Wildlife Res 32: 1-6. doi: 10.1071/WR03107
    [113] Yadav M (1971) The transmissions of antibodies across the gut of pouch-young marsupials. Immunology 21: 839-851.
    [114] Duncan LG, Nair SV, Deane EM (2009) The marsupial CD8 gene locus: molecular cloning and expression analysis of the alpha and beta sequences in the gray short-tailed opossum (Monodelphis domestica) and the tammar wallaby (Macropus eugenii). Vet Immunol Immunopathol 129: 14-27. doi: 10.1016/j.vetimm.2008.12.003
    [115] Wong ES, Papenfuss AT, Belov K (2011) Immunome database for marsupials and monotremes. BMC Immunol 12: 48. doi: 10.1186/1471-2172-12-48
    [116] Duncan L, Webster K, Gupta V, et al. (2010) Molecular characterisation of the CD79a and CD79b subunits of the B cell receptor complex in the gray short-tailed opossum (Monodelphis domestica) and tammar wallaby (Macropus eugenii): Delayed B cell immunocompetence in marsupial neonates. Vet Immunol Immunopathol 136: 235-247. doi: 10.1016/j.vetimm.2010.03.013
    [117] Duncan LG, Nair SV, Deane EM (2012) Immunohistochemical localization of T-lymphocyte subsets in the developing lymphoid tissues of the tammar wallaby (Macropus eugenii). Dev Comp Immunol 38: 475-486. doi: 10.1016/j.dci.2012.06.015
    [118] Hussein MF, Badir N, Elridi R, et al. (1978) Effect of Seasonal-Variation on Lymphoid-Tissues of Lizards, Mabuya-Quinquetaeniata Licht and Uromastyx-Aegyptia Forsk. Dev Comp Immunol 2: 469-478. doi: 10.1016/S0145-305X(78)80008-1
    [119] Hussein MF, Badir N, Elridi R, et al. (1979) Lymphoid-Tissues of the Snake, Spalerosophis-Diadema, in the Different Seasons. Dev Comp Immunol 3: 77-88. doi: 10.1016/S0145-305X(79)80008-7
    [120] Hussein MF, Badir N, Ridi RE, et al. (1978) Differential Effect of Seasonal-Variation on Lymphoid-Tissue of Lizard, Chalcides-Ocellatus. Dev Comp Immunol 2: 297-309. doi: 10.1016/S0145-305X(78)80072-X
    [121] Elridi R, Badir N, Elrouby S (1981) Effect of Seasonal-Variations on the Immune-System of the Snake, Psammophis-Schokari. J Exp Zool 216: 357-365. doi: 10.1002/jez.1402160303
    [122] Hussein MF, Badir N, Elridi R, et al. (1979) Effect of Seasonal-Variation on Immune System of the Lizard, Scincus-Scincus. J Exp Zool 209: 91-96. doi: 10.1002/jez.1402090111
    [123] Alfoldi J, Di Palma F, Grabherr M, et al. (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477: 587-591. doi: 10.1038/nature10390
    [124] Castoe TA, de Koning AP, Hall KT, et al. (2013) The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc Natl Acad Sci U S A 110: 20645-20650. doi: 10.1073/pnas.1314475110
    [125] Shaffer HB, Minx P, Warren DE, et al. (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14: R28. doi: 10.1186/gb-2013-14-3-r28
    [126] Vonk FJ, Casewell NR, Henkel CV, et al. (2013) The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci U S A 110: 20651-20656. doi: 10.1073/pnas.1314702110
    [127] Wang Z, Pascual-Anaya J, Zadissa A, et al. (2013) The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat Genet 45: 701-706. doi: 10.1038/ng.2615
    [128] McPherson FJ, Chenoweth PJ (2012) Mammalian sexual dimorphism. Anim Reprod Sci 131: 109-122. doi: 10.1016/j.anireprosci.2012.02.007
    [129] Kuroki S, Matoba S, Akiyoshi M, et al. (2013) Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a. Science 341: 1106-1109. doi: 10.1126/science.1239864
    [130] Charnier M (1966) [Action of temperature on the sex ratio in the Agama agama (Agamidae, Lacertilia) embryo]. C R Seances Soc Biol Fil 160: 620-622.
    [131] Piferrer F (2013) Epigenetics of sex determination and gonadogenesis. Dev Dyn 242: 360-370. doi: 10.1002/dvdy.23924
    [132] Gorelick R (2003) Evolution of dioecy and sex chromosomes via methylation driving Muller's ratchet. Biol J Linn Soc 80: 353-368. doi: 10.1046/j.1095-8312.2003.00244.x
    [133] Eggert C (2004) Sex determination: the amphibian models. Reprod Nutr Dev 44: 539-549. doi: 10.1051/rnd:2004062
    [134] Martinez-Arguelles DB, Papadopoulos V (2010) Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action. Steroids 75: 467-476. doi: 10.1016/j.steroids.2010.02.004
    [135] Zhang X, Ho SM (2011) Epigenetics meets endocrinology. J Mol Endocrinol 46: R11-32. doi: 10.1677/JME-10-0053
    [136] Navarro-Martin L, Vinas J, Ribas L, et al. (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet 7: e1002447. doi: 10.1371/journal.pgen.1002447
    [137] Ramsey M, Shoemaker C, Crews D (2007) Gonadal expression of Sf1 and aromatase during sex determination in the red-eared slider turtle (Trachemys scripta), a reptile with temperature-dependent sex determination. Differentiation 75: 978-991.
    [138] Matsumoto Y, Buemio A, Chu R, et al. (2013) Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles. PLoS One 8: e63599. doi: 10.1371/journal.pone.0063599
    [139] Shao C, Li Q, Chen S, et al. (2014) Epigenetic modification and inheritance in sexual reversal of fish. Genome Res 24: 604-615. doi: 10.1101/gr.162172.113
    [140] Chen S, Zhang G, Shao C, et al. (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46: 253-260. doi: 10.1038/ng.2890
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