Histone modifications are widely recognized for their fundamental importance in regulating gene expression in embryonic development in a wide range of eukaryotes, but they have received relatively little attention in the development of marine invertebrates. We surveyed histone modifications throughout the development of a marine annelid, Polydora cornuta, to determine if modifications could be detected immunohistochemically and if there were characteristic changes in modifications throughout ontogeny (surveyed at representative stages from oocyte to adult). We found a common time of onset for three histone modifications in early cleavage (H3K14ac, H3K9me, and H3K4me2), some differences in the distribution of modifications among germ layers, differences in epifluorescence intensity in specific cell lineages suggesting that hyperacetylation (H3K14ac) and hypermethylation (H3K9me) occur during differentiation, and an overall decrease in the distribution of modifications from larvae to adults. Although preliminary, these results suggest that histone modifications are involved in activating early development and differentiation in a marine invertebrate. 1. Introduction One of the central questions in biology is how differences in gene expression during development lead to the generation of form. Epigenetic mechanisms such as histone modifications activate or silence gene expression and thereby provide rapid, reversible mechanisms that regulate gene expression in embryonic development. The importance of histone modifications in development has been extensively studied in model systems. As this approach is gradually extended to nonmodel species, histone modifications are being discovered as mechanisms that are highly conserved in a wide variety of eukaryotes and critically important in regulating fundamental developmental processes, including meiosis [1], cell differentiation [2], organ development in plants [3], sexual and asexual reproduction in fungi [4], genomic imprinting in plants and insects [5], and X-inactivation in mammals [6]. Despite the clearly established importance of histone modifications in the development of many eukaryotes, they have received almost no attention in the development of benthic marine invertebrates. Benthic marine invertebrates represent an exciting group for epigenetic research as they not only are morphologically diverse as adults, but their larvae are morphologically and behaviorally distinct from adults and form the basis for an impressive diversity of life-history patterns. Our objectives are to determine if histone
References
[1]
T. Endo, K. Naito, F. Aoki, S. Kume, and H. Tojo, “Changes in histone modifications during in vitro maturation of porcine oocytes,” Molecular Reproduction and Development, vol. 71, no. 1, pp. 123–128, 2005.
[2]
C. Kovach, P. Mattar, and C. Schuurmans, “The role of epigenetics in nervous system development,” in Epigenetics: Linking Genotype and Phenotype in Development and Evolution, B. Hallgrimsson and B. Hall, Eds., pp. 137–163, Berkeley, Calif, USA, The University of California Press, 2011.
[3]
L. Tian, M. P. Fong, J. J. Wang et al., “Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development,” Genetics, vol. 169, no. 1, pp. 337–345, 2005.
[4]
K. K. Adhvaryu, S. A. Morris, B. D. Strahl, and E. U. Selker, “Methylation of histone H3 lysine 36 is required for normal development in Neurospora crassa,” Eukaryotic Cell, vol. 4, no. 8, pp. 1455–1464, 2005.
[5]
L. A. McEachern and V. Lloyd, “The epigenetics of genomic imprinting: core epigenetic processes are conserved in mammals, insects and plants,” in Epigenetics: Linking Genotype and Phenotype in Development and Evolution, B. Hallgrimsson and B. Hall, Eds., pp. 43–69, University of California Press, Berkeley, Calif, USA, 2011.
[6]
I. Okamoto, A. P. Otte, C. D. Allis, D. Reinberg, and E. Heard, “Epigenetic dynamics of imprinted X inactivation during early mouse development,” Science, vol. 303, no. 5658, pp. 644–649, 2004.
[7]
G. Bellan, “Polydora cornuta bosc, 1802,” in World Polychaeta Database. Accessed Through: World Register of Marine Species, G. Read and K. Fauchald, Eds., 2011, http://www.marinespecies.org/aphia.php?p=taxdetails&id=131143.
[8]
V. I. Radashevsky, “On adult and larval morphology of Polydora cornuta Bosc, 1802 (Annelida: Spionidae),” Zootaxa, no. 1064, pp. 1–24, 2005.
[9]
J. A. Blake, “Reproduction and larval development of Polydora from northern New England (Polychaeta: Spionidae),” Ophelia, vol. 7, pp. 1–63, 1969.
[10]
R. N. Zajac, “The effects of sublethal predation on reproduction in the spionid polychaete Polydora ligni Webster,” Journal of Experimental Marine Biology and Ecology, vol. 88, no. 1, pp. 1–19, 1985.
[11]
J. MacKay and G. Gibson, “The influence of nurse eggs on variable larval development in Polydora cornuta (Polychaeta: Spionidae),” Invertebrate Reproduction and Development, vol. 35, no. 3, pp. 167–176, 1999.
[12]
S. A. Rice and K. A. Rice, “Variable modes of larval development in the Polydora cornuta complex (Polychaeta: Spionidae) are directly related to stored sperm availability,” Zoosymposia, vol. 2, pp. 397–414, 2009.
[13]
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.
[14]
T. Jenuwein and C. D. Allis, “Translating the histone code,” Science, vol. 293, no. 5532, pp. 1074–1080, 2001.
[15]
J. S. Lee, E. Smith, and A. Shilatifard, “The language of histone crosstalk,” Cell, vol. 142, no. 5, pp. 682–685, 2010.
[16]
A. J. Bannister and T. Kouzarides, “Regulation of chromatin by histone modifications,” Cell Research, vol. 21, pp. 381–395, 2011.
[17]
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.
[18]
B. M. Turner, “Cellular memory and the histone code,” Cell, vol. 111, no. 3, pp. 285–291, 2002.
[19]
P. Lefevre, C. Lacroix, H. Tagoh et al., “Differentiation-dependent alterations in histone methylation and chromatin architecture at the inducible chicken lysozyme gene,” Journal of Biological Chemistry, vol. 280, no. 30, pp. 27552–27560, 2005.
[20]
H. Santos-Rosa, R. Schneider, A. J. Bannister et al., “Active genes are tri-methylated at K4 of histone H3,” Nature, vol. 419, no. 6905, pp. 407–411, 2002.
[21]
B. M. Turner, “Defining an epigenetic code,” Nature Cell Biology, vol. 9, no. 1, pp. 2–6, 2007.
[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]
R. Sugioka-Sugiyama and T. Sugiyama, “A novel nuclear protein essential for telomeric silencing and genomic stability in Schizosaccharomyces pombe,” Biochemical and Biophysical Research Communications, vol. 406, pp. 444–448, 2011.
[24]
S. Fritah, E. Col, C. Boyault et al., “Heat-shock factor 1 controls genome-wide acetylation in heat-shocked cells,” Molecular Biology of the Cell, vol. 20, no. 23, pp. 4976–4984, 2009.
[25]
H. Wen, J. Li, T. Song et al., “Recognition of histone H3K4 trimethylation by the plant homeodomain of PHF2 modulates histone demethylation,” Journal of Biological Chemistry, vol. 285, no. 13, pp. 9322–9326, 2010.
[26]
A. Eberharter and P. B. Becker, “Histone acetylation: a switch between repressive and permissive chromatin. Second in review on chromatin dynamics,” EMBO Reports, vol. 3, no. 3, pp. 224–229, 2002.
[27]
J. M. Kim, H. Liu, M. Tazaki, M. Nagata, and F. Aoki, “Changes in histone acetylation during mouse oocyte meiosis,” Journal of Cell Biology, vol. 162, no. 1, pp. 37–46, 2003.
[28]
I. Ivanovska, T. Khandan, T. Ito, and T. L. Orr-Weaver, “A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes,” Genes and Development, vol. 19, no. 21, pp. 2571–2582, 2005.
[29]
E. C. Seaver, “Segmentation: mono- or polyphyletic?” International Journal of Developmental Biology, vol. 47, no. 7-8, pp. 583–595, 2003.
[30]
F. Chen, H. Kan, V. Castranova, et al., “Methylation of lysine 9 of histone 3: role of heterochromatin modulation and tumorigenesis,” in Handbook of Epigenetics: The New Molecular and Medical Genetics, T. Tollefsbol, Ed., pp. 149–157, Academic Press, Amsterdam, The Netherlands, 2011.
[31]
M. D. Stewart, J. Li, and J. Wong, “Relationship between histone H3 lysine 9 methylation, transcription repression, and heterochromatin protein 1 recruitment,” Molecular and Cellular Biology, vol. 25, no. 7, pp. 2525–2538, 2005.
[32]
B. E. Bernstein, T. S. Mikkelsen, X. Xie et al., “A bivalent chromatin structure marks key developmental genes in embryonic stem cells,” Cell, vol. 125, no. 2, pp. 315–326, 2006.
[33]
K. L. Arney and A. G. Fisher, “Epigenetic aspects of differentiation,” Journal of Cell Science, vol. 117, no. 19, pp. 4355–4363, 2004.
[34]
C. Arenas-Mena, K. S. Y. Wong, and N. R. Arandi-Foroshani, “Histone H2A.Z expression in two indirectly developing marine invertebrates correlates with undifferentiated and multipotent cells,” Evolution and Development, vol. 9, no. 3, pp. 231–243, 2007.
