Photoperiod is associated to phenotypic plasticity of somatic growth in several teleost species. However, the molecular mechanisms underlying this phenomenon are currently unknown but it is likely that epigenetic regulation by methyltransferases is involved. The MLL (mixed-lineage leukaemia) family comprises histone methyltransferases that play a critical role in regulating gene expression during early development in mammals. So far, these genes have received scant attention in teleost fish. In the present study, the mean weight of Atlantic cod juveniles reared under continuous illumination was found to be 13% greater than those kept under natural photoperiod conditions for 120 days. We newly determined cDNA sequences of five mll (mll1, mll2, mll3a, mll4b and mll5) and two setd1 (setd1a and setd1ba) paralogues from Atlantic cod. Phylogenetic analysis revealed that the cod genes clustered within the appropriate mll clade and comparative mapping of mll paralogues showed that these genes lie within a region of conserved synteny among teleosts. All mll and setd1 genes were highly expressed in gonads and fast muscle of adult cod, albeit at different levels, and they were differentially regulated with photoperiod in muscle of juvenile fish. Following only one day of exposure to constant light, mll1, mll4b and setd1a were up to 57% lower in these fish compared to the natural photoperiod group. In addition, mRNA expression of myogenic regulatory factors (myog and myf-5) and pax7 in fast muscle was also affected by different photoperiod conditions. Notably, myog was significantly elevated in the continuous illumination group throughout the time course of the experiment. The absence of a day/night cycle is associated with a generalised decrease in mll expression concomitant with an increase in myog transcript levels in fast muscle of Atlantic cod, which may be involved in the observed epigenetic regulation of growth by photoperiod in this species.
References
[1]
Kouzarides T (2007) Chromatin modifications and their function. Cell 128: 693–705.
[2]
Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41–45.
[3]
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074–1080.
[4]
Sims RJ , Reinberg D (2006) Histone H3 Lys 4 methylation: caught in a bind? Genes Dev 20: 2779–2786.
[5]
Ansari KI, Mishra BP, Mandal SS (2008) Human CpG binding protein interacts with MLL1, MLL2 and hSet1 and regulates Hox gene expression. Biochimica et Biophysica Acta 1779: 66–73.
[6]
Hess JL (2004) MLL: a histone methyltransferase disrupted in leukemia. Trends in Molecular Medicine 10: 500–507.
[7]
Yu BD, Hanson RD, Hess JL, Horning SE, Korsmeyer SJ (1998) MLL, a mammalian trithorax-group gene, functions as a transcriptional maintenance factor in morphogenesis. Proc Natl Acad Sci U S A 95: 10632–10636.
[8]
Nakanishi S, Sanderson BW, Delventhal KM, Bradford WD, Staehling-Hampton K, et al. (2008) A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nature Structural & Molecular Biology 15: 881–888.
[9]
Schneider J, Wood A, Lee JS, Schuster R, Dueker J, et al. (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19: 849–856.
[10]
Ziemin-van der Poel S, McCabe NR, Gill HJ, Espinosa R , Patel Y, et al. (1991) Identification of a gene, MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Proc Natl Acad Sci U S A 88: 10735–10739.
[11]
FitzGerald KT, Diaz MO (1999) MLL2: A new mammalian member of the trx/MLL family of genes. Genomics 59: 187–192.
[12]
Ruault M, Brun ME, Ventura M, Roizes G, De Sario A (2002) MLL3, a new human member of the TRX/MLL gene family, maps to 7q36, a chromosome region frequently deleted in myeloid leukaemia. Gene 284: 73–81.
[13]
Nightingale KP, Gendreizig S, White DA, Bradbury C, Hollfelder F, et al. (2007) Cross-talk between histone modifications in response to histone deacetylase inhibitors: MLL4 links histone H3 acetylation and histone H3K4 methylation. J Biol Chem 282: 4408–4416.
[14]
Emerling BM, Bonifas J, Kratz CP, Donovan S, Taylor BR, et al. (2002) MLL5, a homolog of Drosophila trithorax located within a segment of chromosome band 7q22 implicated in myeloid leukemia. Oncogene 21: 4849–4854.
[15]
Lee JH, Tate CM, You JS, Skalnik DG (2007) Identification and characterization of the human Set1B histone H3-Lys4 methyltransferase complex. J Biol Chem 282: 13419–13428.
[16]
Yagi H, Deguchi K, Aono A, Tani Y, Kishimoto T, et al. (1998) Growth disturbance in fetal liver hematopoiesis of Mll-mutant mice. Blood 92: 108–117.
[17]
Lappin TR, Grier DG, Thompson A, Halliday HL (2006) HOX genes: seductive science, mysterious mechanisms. Ulster Medical Journal 75: 23–31.
[18]
Guenther MG, Jenner RG, Chevalier B, Nakamura T, Croce CM, et al. (2005) Global and Hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci U S A 102: 8603–8608.
[19]
Yu BD, Hess JL, Horning SE, Brown GA, Korsmeyer SJ (1995) Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378: 505–508.
[20]
McKinnell IW, Ishibashi J, Le Grand F, Punch VG, Addicks GC, et al. (2008) Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat Cell Biol 10: 77–84.
[21]
Sun XJ, Xu PF, Zhou T, Hu M, Fu CT, et al. (2008) Genome-wide survey and developmental expression mapping of zebrafish SET domain-containing genes. PLoS One 3: e1499.
[22]
Sebastian S, Sreenivas P, Sambasivan R, Cheedipudi S, Kandalla P, et al. (2009) MLL5, a trithorax homolog, indirectly regulates H3K4 methylation, represses cyclin A2 expression, and promotes myogenic differentiation. Proc Natl Acad Sci U S A 106: 4719–4724.
[23]
Caldas C, Kim MH, MacGregor A, Cain D, Aparicio S, et al. (1998) Isolation and characterization of a pufferfish MLL (Mixed lineage leukemia)-like gene (fMll) reveals evolutionary conservation in vertebrate genes related to Drosophila trithorax. Oncogene 16: 3233–3241.
[24]
Hansen T, Karlsen O, Taranger GL, Hemre GI, Holm JC, et al. (2001) Growth, gonadal development and spawning time of Atlantic cod (Gadus morhua) reared under different photoperiods. Aquaculture 203: 51–67.
[25]
Endal HP, Taranger GL, Stefansson SO, Hansen T (2000) Effects of continuous additional light on growth and sexual maturity in Atlantic salmon, Salmo salar, reared in sea cages. Aquaculture 191: 337–349.
[26]
Begtashi I, Rodriguez L, Moles G, Zanuy S, Carrillo M (2004) Long-term exposure to continuous light inhibits precocity in juvenile male European sea bass (Dicentrarchus labrax, L.). I. Morphological aspects. Aquaculture 241: 539–559.
[27]
Imsland AK, Foss A, Folkvord A, Stefansson SO, Jonassen TM (2005) Genotypic response to photoperiod treatment in Atlantic cod (Gadus morhua). Aquaculture 250: 525–532.
[28]
Imsland AK, Foss A, Koedijk R, Folkvord A, Stefansson SO, et al. (2007) Persistent growth effects of temperature and photoperiod in Atlantic cod Gadus morhua. Journal of Fish Biology 71: 1371–1382.
[29]
Davie A, Porter MJR, Bromage NR, Migaud H (2007) The role of seasonally altering photoperiod in regulating physiology in Atlantic cod (Gadus morhua). Part II. Somatic growth. Canadian Journal of Fisheries and Aquatic Sciences 64: 98–112.
[30]
Fulberth M, Moran D, Jarlbaek H, Stottrup JG (2009) Growth of juvenile Atlantic cod Gadus morhua in land-based recirculation systems: Effects of feeding regime, photoperiod and diet. Aquaculture 292: 225–231.
[31]
Grant SM, Brown JA (1998) Diel foraging cycles and interactions among juvenile Atlantic cod (Gadus morhua) at a nearshore site in Newfoundland. Canadian Journal of Fisheries and Aquatic Sciences 55: 1307–1316.
[32]
Guasconi V, Puri PL (2009) Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends in Cell Biology 19: 286–294.
[33]
Ansari KI, Mandal SS (2010) Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS Journal 277: 1790–1804.
Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27: 937–945.
[36]
Glaser S, Lubitz S, Loveland KL, Ohbo K, Robb L, et al. (2009) The histone 3 lysine 4 methyltransferase, Mll2, is only required briefly in development and spermatogenesis. Epigenetics Chromatin 2: 5.
[37]
Issaeva I, Zonis Y, Rozovskaia T, Orlovsky K, Croce CM, et al. (2007) Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Molecular and Cellular Biology 27: 1889–1903.
[38]
Molnar J, Fong KS, He QP, Hayashi K, Kim Y, et al. (2003) Structural and functional diversity of lysyl oxidase and the LOX-like proteins. Biochimica et Biophysica Acta 1647: 220–224.
[39]
Fernandes JM, Mackenzie MG, Wright PA, Steele SL, Suzuki Y, et al. (2006) Myogenin in model pufferfish species: Comparative genomic analysis and thermal plasticity of expression during early development. Comp Biochem Physiol Part D Genomics Proteomics 1: 35–45.
[40]
Amali AA, Lin CJF, Chen YH, Wang WL, Gong HY, et al. (2004) Up-regulation of muscle-specific transcription factors during embryonic somitogenesis of zebrafish (Danio rerio) by knock-down of myostatin-1. Developmental Dynamics 229: 847–856.
[41]
Campos C, Valente LM, Borges P, Bizuayehu T, Fernandes JM (2010) Dietary lipid levels have a remarkable impact on the expression of growth-related genes in Senegalese sole (Solea senegalensis Kaup). J Exp Biol 213: 200–209.
[42]
Fernandes JMO, Mommens M, Hagen O, Babiak I, Solberg C (2008) Selection of suitable reference genes for real-time PCR studies of Atlantic halibut development. Comp Biochem Physiol B Biochem Mol Biol 150: 23–32.
[43]
Nagasawa K, Lazado CC, Fernandes JMO (2011) Validation of endogenous reference genes for qPCR quantification of muscle transcripts in Atlantic cod subjected to different photoperiod regimes. In: Muchlisin ZA, editor. Aquaculture / Book 1. Rijeka: InTech.
