Daphnids are fresh water microcrustaceans, many of which follow a cyclically parthenogenetic life cycle. Daphnia species have been well studied in the context of ecology, toxicology, and evolution, but their epigenetics remain largely unexamined even though sex determination, the production of sexual females and males, and distinct adult morphological phenotypes, are determined epigenetically. Here, we report on the characterization of histone modifications in Daphnia. We show that a number of histone H3 and H4 modifications are present in Daphnia embryos and histone H3 dimethylated at lysine 4 (H3K4me2) is present nonuniformly in the nucleus in a cell cycle-dependent manner. In addition, this histone modification, while present in blastula and gastrula cells as well as the somatic cells of adults, is absent or reduced in oocytes and nurse cells. Thus, the epigenetic repertoire of Daphnia includes modified histones and as these epigenetic forces act on a genetically homogeneous clonal population Daphnia offers an exceptional tool to investigate the mechanism and role of epigenetics in the life cycle and development of an ecologically important species. 1. Introduction Daphnids are freshwater crustaceans that hold the distinction of being among the relatively few genera that reproduce parthenogenetically. Under most circumstances conventional oogenesis is modified. The first meiotic division is abortive so only the mitosis-like equational division occurs producing clonal diploid eggs [1, 2]. While homologs do pair in the abortive first meiotic division [2] and many of the same meiotic genes are expressed in parthenogenetic and sexual reproduction [3], there is no cytological [2] or genetic [3, 4] evidence for recombination. As a result, other than rare mitotic recombination, conversion, or mutational events [5], the progeny produced are genetically identical [1, 2, 4]. However, while the offspring are genetically identical to each other and their mother, they are not necessarily epigenetically identical. Under stressful conditions some of these clonal diploid eggs develop as males rather than females [1, 6–8]. Additionally, in many species stressful conditions similarly trigger the restoration of conventional meiosis allowing production of haploid eggs and sperm [1–3, 6, 8]. Importantly, parthenogenetically reproducing females and sexually reproducing females are genetically identical, and both are identical to their mothers [1, 4, 5]. Moreover, parthenogenetically produced males are genetically identical to parthenogenetically produced females [1, 4,
References
[1]
F. Zaffagnini, “Reproduction in Daphnia,” Memorie dell'Istituto Italiano di Idrobiologia, vol. 45, pp. 245–284, 1987.
[2]
C. Hiruta, C. Nishida, and S. Tochinai, “Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex,” Chromosome Research, vol. 18, no. 7, pp. 833–840, 2010.
[3]
A. M. Schurko, J. M. Logsdon, and B. D. Eads, “Meiosis genes in Daphnia pulex and the role of parthenogenesis in genome evolution,” BMC Evolutionary Biology, vol. 9, no. 1, article 78, 2009.
[4]
P. D. Hebert and R. D. Ward, “Inheritance during parthenogenesis in Daphnia magna,” Genetics, vol. 71, no. 4, pp. 639–642, 1972.
[5]
A. R. Omilian, M. E. A. Cristescu, J. L. Dudycha, and M. Lynch, “Ameiotic recombination in asexual lineages of Daphnia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 49, pp. 18638–18643, 2006.
[6]
O. T. Kleiven, P. Larsson, and A. Hobaek, “Sexual reproduction in Daphnia magna requires three stimuli,” Oikos, vol. 65, no. 2, pp. 197–206, 1992.
[7]
A. W. Olmstead and G. A. LeBlanc, “The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean,” International Journal of Biological Sciences, vol. 3, no. 2, pp. 77–84, 2007.
[8]
Y. Kato, K. Kobayashi, H. Watanabe, and T. Iguchi, “Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway,” PLoS Genetics, vol. 7, no. 3, Article ID e1001345, 2011.
[9]
C. Laforsch and R. Tollrian, “Embryological aspects of inducible morphological defenses in Daphnia,” Journal of Morphology, vol. 262, no. 3, pp. 701–707, 2004.
[10]
A. A. Agrawal, C. Laforsch, and R. Tollrian, “Transgenerational induction of defences in animals and plants,” Nature, vol. 401, no. 6748, pp. 60–63, 1999.
[11]
H. Miyakawa, M. Imai, N. Sugimoto et al., “Gene up-regulation in response to predator kairomones in the water flea, Daphnia pulex,” BMC Developmental Biology, vol. 10, article 45, 2010.
[12]
J. K. Colbourne, V. R. Singan, and D. G. Gilbert, “wFleaBase: the Daphnia genome database,” BMC Bioinformatics, vol. 6, article 45, 2005.
[13]
J. K. Colbourne, M. E. Pfrender, D. Gilbert et al., “The ecoresponsive genome of Daphnia pulex,” Science, vol. 331, no. 6017, pp. 555–561, 2011.
[14]
H. Watanabe, N. Tatarazako, S. Oda et al., “Analysis of expressed sequence tags of the water flea Daphnia magna,” Genome, vol. 48, no. 4, pp. 606–609, 2005.
[15]
C. E. W. Steinberg, S. R. Stürzenbaum, and R. Menzel, “Genes and environment—Striking the fine balance between sophisticated biomonitoring and true functional environmental genomics,” Science of the Total Environment, vol. 400, no. 1–3, pp. 142–161, 2008.
[16]
S. Keeney, “Methods for meiotic chromosome preparation, immunofluorescence, and fluorescence in situ hybridization in Daphnia pulex,” in Meiosis: Volume 2, Cytological Methods, D. Tsuchiya, B. D. Eads, and M. E. Zolan, Eds., vol. 558 of Methods in Molecular Biology, pp. 235–249, 2009.
[17]
C. D. Robinson, S. Lourido, S. P. Whelan, J. L. Dudycha, M. Lynch, and S. Isern, “Viral transgenesis of embryonic cell cultures from the freshwater microcrustacean Daphnia,” Journal of Experimental Zoology Part A: Comparative Experimental Biology, vol. 305, no. 1, pp. 62–67, 2006.
[18]
Y. Kato, K. Kobayashi, H. Watanabe, and T. Iguchi, “Introduction of foreign DNA into the water flea, Daphnia magna, by electroporation,” Ecotoxicology, vol. 19, no. 3, pp. 589–592, 2010.
[19]
Y. Kato, Y. Shiga, K. Kobayashi et al., “Development of an RNA interference method in the cladoceran crustacean Daphnia magna,” Development Genes and Evolution, vol. 220, no. 11-12, pp. 337–345, 2011.
[20]
M. B. Vandegehuchte, T. Kyndt, B. Vanholme, A. Haegeman, G. Gheysen, and C. R. Janssen, “Occurrence of DNA methylation in Daphnia magna and influence of multigeneration Cd exposure,” Environment International, vol. 35, no. 4, pp. 700–706, 2009.
[21]
M. B. Vandegehuchte, F. Lemière, and C. R. Janssen, “Quantitative DNA-methylation in Daphnia magna and effects of multigeneration Zn exposure,” Comparative Biochemistry and Physiology, vol. 150, no. 3, pp. 343–348, 2009.
[22]
K. Sagawa, H. Yamagata, and Y. Shiga, “Exploring embryonic germ line development in the water flea, Daphnia magna, by zinc-finger-containing VASA as a marker,” Gene Expression Patterns, vol. 5, no. 5, pp. 669–678, 2005.
[23]
J. Gulbrandsen and G. H. Johnsen, “Temperature-dependent development of parthenogenetic embryos in Daphnia pulex de Geer,” Journal of Plankton Research, vol. 12, no. 3, pp. 443–453, 1990.
[24]
T. Jenuwein and C. D. Allis, “Translating the histone code,” Science, vol. 293, no. 5532, pp. 1074–1080, 2001.
[25]
J. S. Lee, E. Smith, and A. Shilatifard, “The language of histone crosstalk,” Cell, vol. 142, no. 5, pp. 682–685, 2010.
[26]
A. J. Bannister and T. Kouzarides, “Regulation of chromatin by histone modifications,” Cell Research, vol. 21, no. 3, pp. 381–395, 2011.
[27]
P. V. Kharchenko, A. A. Alekseyenko, Y. B. Schwartz et al., “Comprehensive analysis of the chromatin landscape in Drosophila melanogaster,” Nature, vol. 471, pp. 480–485, 2011.
[28]
J. Fuchs, D. Demidov, A. Houben, and I. Schubert, “Chromosomal histone modification patterns—from conservation to diversity,” Trends in Plant Science, vol. 11, no. 4, pp. 199–208, 2006.
[29]
E. J. Richards and S. C. R. Elgin, “Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects,” Cell, vol. 108, no. 4, pp. 489–500, 2002.
[30]
R. J. Sims, K. Nishioka, and D. Reinberg, “Histone lysine methylation: a signature for chromatin function,” Trends in Genetics, vol. 19, no. 11, pp. 629–639, 2003.
[31]
F. Fuks, “DNA methylation and histone modifications: teaming up to silence genes,” Current Opinion in Genetics and Development, vol. 15, no. 5, pp. 490–495, 2005.
[32]
W. MacDonald, “Epigenetic mechanisms of genomic imprinting: common themes in the regulation of imprinted regions in mammals, plants, and insects,” Genetics Research International, vol. 2012, Article ID 585024, 17 pages, 2012.
[33]
V. Lloyd, “Parental imprinting in Drosophila,” Genetica, vol. 109, no. 1-2, pp. 35–44, 2001.
[34]
T. Cremer and C. Cremer, “Chromosome territories, nuclear architecture and gene regulation in mammalian cells,” Nature Reviews Genetics, vol. 2, no. 4, pp. 292–301, 2001.
[35]
T. Ragoczy and M. Groudine, “The nucleus inside out-through a rod darkly,” Cell, vol. 137, no. 2, pp. 205–207, 2009.
[36]
I. Solovei, M. Kreysing, C. Lanct?t et al., “Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution,” Cell, vol. 137, no. 2, pp. 356–368, 2009.