Abstract
This work explores both the chromatin loss and the differential genome methylation in the sea lamprey (Petromyzon marinus) from a molecular cytogenetic point of view. Fluorescent in situ hybridization experiments on meiotic bivalents and mitotic chromosomes corroborate the chromatin loss previously observed during the development of the sea lamprey and demonstrate that the elimination affects not only to Germ1 sequences but also to the rpt200 satellite DNA and most part of the major ribosomal DNA present on the germinal line. 5-Methylcytosine immunolocation revealed that the GC-rich heterochromatin is highly methylated in the germ line but significantly less in somatic chromosomes. These findings not only support previous observations about genome rearrangements but also give new information about epigenetic changes in P. marinus. The key position of lampreys in the vertebrate phylogenetic tree makes them an interesting taxon to provide relevant information about genome evolution in vertebrates.
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References
Almeida-Toledo LF, Viegas-Péquignot E, Coutinho-Barbosa AC, Foresti F, Niveleau A, de Almeida Toledo-Filho S (1998) Localization of 5-methylcytosine in metaphase chromosomes of diploid and triploid pacu fish, Piaractus mesopotamicus (Pisces, Characiformes). Cytogenet Cell Genet 83:21–24. doi:10.1159/000015158
Bella JL, García de la Vega C, López-Fernández C, Gosálvez J (1986) Changes in acridine orange binding and its use in the characterisation of heterochromatic regions. Heredity 57:79–83. doi:10.1038/hdy.1986.90
Boán F, Viñas A, Rodríguez JM, Sánchez L, Gómez-Márquez J (1996) A new EcoRI family of satellite DNA in lampreys. FEBS Lett 394:187–190. doi:10.1016/0014-5793(96)00947-7
Bracht JR (2014) Beyond transcriptional silencing: is methylcytosine a widely conserved eukaryotic DNA elimination mechanism? BioEssays 36:346–352. doi:10.1002/bies.201300123
Bracht JR, Perlman DH, Landweber LF (2012) Cytosine methylation and hydroxymethylation mark DNA for elimination in Oxytricha trifallax. Genome Biol 13:R99. doi:10.1186/gb-2012-13-10-r99
Caputo V, Giovannotti M, Cerioni PN, Splendiani A, Tagliavini J, Olmo E (2011) Chromosomal study of a lamprey (Lampetra zanandreai Vladykov, 1955) (Petromyzonida: Petromyzontiformes): conventional and FISH analysis. Chromosome Res 19:481–491. doi:10.1007/s10577-011-9197-4
Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406. doi:10.1146/annurev.arplant.58.032806.103835
Dricu E (2012) Methylation: from DNA, RNA and histones to diseases and treatment. InTech, Rijeka. doi:10.5772/2932
Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627. doi:10.1126/science.1190614
Fujiwara A, Nishida-Umehara C, Sakamoto T, Okamoto N, Nakayama I, Abe S (2001) Improved fish lymphocyte culture for chromosome preparation. Genetica 111:77–89. doi:10.1023/A:1013788626712
Grishanin A (2014) Chromatin diminution in Copepoda (Crustacea): pattern, biological role and evolutionary aspects. Comp Cytogenet 8:1–10. doi:10.3897/CompCytogen.v8i1.5913
Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254. doi:10.1038/ng1089
Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492. doi:10.1038/nrg3230
Kirtiklis L, Boron A, Porycka K (2005) Chromosome banding patterns of the gudgeon, Gobio gobio (Actinopterygii, Cyprinidae). Acta Ichthyol Piscat 35:119–123
Kloc M, Zagrodzinska B (2001) Chromatin elimination—an oddity or a common mechanism in differentiation and development? Differentiation 68:84–91. doi:10.1046/j.1432-0436.2001.680202.x
Laurent L, Wong E, Li G et al (2010) Dynamic changes in the human methylome during differentiation. Genome Res 20:320–331. doi:10.1101/gr.101907.109
Matzke MA, Mette MF, Matzke AJM (2000) Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates. Plant Mol Biol 43:401–415. doi:10.1023/A:1006484806925
Müller F, Tobler H (2000) Chromatin diminution in the parasitic nematodes Ascaris suum and Parascaris univalens. Int J Parasitol 30:391–399. doi:10.1016/S0020-7519(99)00199-X
Nakai Y, Kubota S, Kohno S (1991) Chromatin diminution and chromosome elimination in four Japanese hagfish species. Cytogenet Cell Genet 56:196–198. doi:10.1159/000133087
Pérez-García C, Guerra-Varela J, Morán P, Pasantes JJ (2010) Chromosomal mapping of rRNA genes, core histone genes and telomeric sequences in Brachidontes puniceus and Brachidontes rodriguezi (Bivalvia, Mytilidae). BMC Genet 11:109. doi:10.1186/1471-2156-11-109
Potter IC, Robinson ES (1981) New developments in vertebrate cytotaxonomy V. Cytotaxonomy of lampreys. Genetica 56:149–151. doi:10.1007/BF00055414
Potter IC, Rothwell B (1970) The mitotic chromosomes of the lamprey, Petromyzon marinus L. Experientia 26:429–430. doi:10.1007/BF01896930
Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093. doi:10.1126/science.1063443
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386. doi:10.1385/1-59259-192-2:365
Smith JJ, Antonacci F, Eichler EE, Amemiya CT (2009) Programmed loss of millions of base pairs from a vertebrate genome. PNAS 106:11212–11217. doi:10.1073/pnas.0902358106
Smith JJ, Stuart AB, Sauka-Spengler T, Clifton SW, Amemiya CT (2010) Development and analysis of a germline BAC resource for the sea lamprey, a vertebrate that undergoes substantial chromatin diminution. Chromosoma 119:381–389. doi:10.1007/s00412-010-0263-z
Smith JJ, Kuraku S, Holt C et al (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Gent 45:415–421. doi:10.1038/ng.2568
Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306. doi:10.1016/0014-4827(72)90558-7
Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465–476. doi:10.1038/nrg2341
Suzuki A, Ikeda Y, Nakayama K, Matsui F (1999) Chromosomes and Ag-NORs of three species of Lampetra (Petromyzontiformes). Chromosome Res 3:150
Takezaki N, Figueroa F, Zaleska-Rutczynska Z, Klein J (2003) Molecular phylogeny of early vertebrates: monophyly of the agnathans as revealed by sequences of 35 genes. Mol Biol Evol 20:287–292. doi:10.1093/molbev/msg040
Vilgalys R (2005) Conserved primer sequences for PCR amplification and sequencing from nuclear ribosomal RNA. Duke University, USA. http://biology.duke.edu/fungi/mycolab/primers.htm. Accessed 10 July 2014
Völker M, Ráb P, Kullmann H (2005) Karyotype differentiation in Chromaphyosemion killifishes (Cyprinodontiformes, Nothobranchiidae). I: chromosome banding patterns of C. alpha, C. kouamense and C. lugens. Genetica 125:33–41. doi:10.1007/s10709-005-4267-1
Acknowledgments
We wish to thank Pilar Alvariño for her technical assistance and Manuel Ángel Pombal Diego and Manuel Megías Pacheco for kindly providing the lampreys. This work was partly funded by grants from Xunta de Galicia and Fondos FEDER: “Unha maneira de facer Europa” (PGIDIT03PXIC30102PN; 08MMA023310PR; Grupos de Referencia Competitiva, 2010/80; Grupos con Potencial Crecimiento, GPC2013-011). The author Lara Covelo-Soto has a predoctoral fellowship from the Xunta de Galicia (Plan I2C).
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Covelo-Soto, L., Morán, P., Pasantes, J.J. et al. Cytogenetic evidences of genome rearrangement and differential epigenetic chromatin modification in the sea lamprey (Petromyzon marinus). Genetica 142, 545–554 (2014). https://doi.org/10.1007/s10709-014-9802-5
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DOI: https://doi.org/10.1007/s10709-014-9802-5