Dinoflagellates are of great importance to the marine ecosystem, yet scant details of how gene expression is regulated at the transcriptional level are available. Transcription is of interest in the context of the chromatin structure in the dinoflagellates as it shows many differences from more typical eukaryotic cells. Here we canvas recent transcriptome profiles to identify the molecular building blocks available for the construction of the transcriptional machinery and contrast these with those used by other systems. Dinoflagellates display a clear paucity of specific transcription factors, although surprisingly, the rest of the basic transcriptional machinery is not markedly different from what is found in the close relatives to the dinoflagellates.
References
[1]
Field, C.B.; Behrenfeld, M.J.; Randerson, J.T.; Falkowski, P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 1998, 281, 237–240, doi:10.1126/science.281.5374.237.
[2]
Muscatine, L.; McCloskey, L.R.; Marian, R.E. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 1981, 26, 601–611, doi:10.4319/lo.1981.26.4.0601.
Schmitter, R.E.; Njus, D.; Sulzman, F.M.; Gooch, V.D.; Hastings, J.W. Dinoflagellate bioluminescence: A comparative study of in vitro components. J. Cell. Physiol. 1976, 87, 123–134, doi:10.1002/jcp.1040870115.
[5]
Hastings, J.W.; Sweeney, B.M. A persistent diurnal rhythm of luminescence in Gonyaulax polyedra. Biol. Bull. 1958, 115, 444–458.
[6]
Hastings, J.W.; Astrachan, L.; Sweeney, B.M. A persistent daily rhythm in photosynthesis. J. Gen. Physiol. 1961, 45, 69–76, doi:10.1085/jgp.45.1.69.
[7]
Sweeney, B.M. The photosynthetic rhythm in single cells of Gonyaulax polyedra. Cold Spring Harb. Symp. Quant. Biol. 1960, 25, 145–148, doi:10.1101/SQB.1960.025.01.013.
[8]
Roenneberg, T.; Colfax, G.N.; Hastings, J.W. A circadian rhythm of population behavior in Gonyaulax polyedra. J. Biol. Rhythms 1989, 4, 201–216.
[9]
Hastings, J.W. The Gonyaulax clock at 50: Translational control of circadian expression. Cold Spring Harb. Symp. Quant. Biol. 2007, 72, 141–144, doi:10.1101/sqb.2007.72.026.
[10]
Fast, N.M.; Xue, L.; Bingham, S.; Keeling, P.J. Re-examining alveolate evolution using multiple protein molecular phylogenies. J. Eukaryot. Microbiol. 2002, 49, 30–37, doi:10.1111/j.1550-7408.2002.tb00336.x.
[11]
Spector, D.L. Dinoflagellate Nuclei. In Dinoflagellates; Spector, D.L., Ed.; Academic Press: London, UK, 1984; pp. 107–147.
[12]
Lin, S. Genomic understanding of dinoflagellates. Res. Microbiol. 2011, 162, 551–569, doi:10.1016/j.resmic.2011.04.006.
Hackett, J.D.; Anderson, D.M.; Erdner, D.L.; Bhattacharya, D. Dinoflagellates: A remarkable evolutionary experiment. Am. J. Bot. 2004, 91, 1523–1534.
[15]
Livolant, F. Cholesteric organization of DNA in vivo and in vitro. Eur. J. Cell Biol. 1984, 33, 300–311.
[16]
Livolant, F. Positive and negative birefringence in chromosomes. Chromosoma 1978, 68, 45–58, doi:10.1007/BF00330371.
[17]
Herzog, M.; Soyer, M.O. The native structure of dinoflagellate chromosomes and their stabilization by Ca2+ and Mg2+ cations. Eur. J. Cell Biol. 1983, 30, 33–41.
[18]
Sigee, D.C. Structural DNA and genetically active DNA in dinoflagellate chromosomes. Biosystems 1983, 16, 203–210.
[19]
Kornberg, R.D. The molecular basis of eukaryotic transcription. Proc. Natl. Acad. Sci. USA 2007, 104, 12955–12961.
[20]
Smale, S.T.; Kadonaga, J.T. The RNA polymerase II core promoter. Annu. Rev. Biochem. 2003, 72, 449–479, doi:10.1146/annurev.biochem.72.121801.161520.
[21]
Hahn, S. Structure and mechanism of the RNA polymerase II transcription machinery. Nat. Struct. Mol. Biol. 2004, 11, 394–403.
Everett, R.D.; Baty, D.; Chambon, P. The repeated GC-rich motifs upstream from the TATA box are important elements of the SV40 early promoter. Nucleic Acids Res. 1983, 11, 2447–2464.
[24]
Yoshikawa, T.; Takishita, K.; Ishida, Y.; Uchida, A. Molecular cloning and nucleotide sequence analysis of the gene coding for chloroplast-type ferredoxin from the dinoflagellates Peridinium bipes and Alexandrium tamarense. Fish. Sci. 1997, 63, 692–700.
[25]
Wong, J.M.; Liu, F.; Bateman, E. Isolation of genomic DNA encoding transcription factor TFIID from Acanthamoeba castellanii: Characterization of the promoter. Nucleic Acids Res. 1992, 20, 4817–4824, doi:10.1093/nar/20.18.4817.
[26]
Huang, W.; Bateman, E. Cloning, expression, and characterization of the TATA-binding protein (TBP) promoter binding factor, a transcription activator of the Acanthamoeba TBP gene. J. Biol. Chem. 1995, 270, 28839–28847, doi:10.1074/jbc.270.48.28839.
[27]
Cohen, S.M.; Knecht, D.; Lodish, H.F.; Loomis, W.F. DNA sequences required for expression of a Dictyostelium actin gene. EMBO J. 1986, 5, 3361–3366.
[28]
Kimmel, A.R.; Firtel, R.A. Sequence organization in Dictyostelium: Unique structure at the 5′-ends of protein coding genes. Nucleic Acids Res. 1983, 11, 541–552, doi:10.1093/nar/11.2.541.
[29]
Liston, D.R.; Johnson, P.J. Analysis of a ubiquitous promoter element in a primitive eukaryote: Early evolution of the initiator element. Mol. Cell. Biol. 1999, 19, 2380–2388.
[30]
McAndrew, M.B.; Read, M.; Sims, P.F.; Hyde, J.E. Characterisation of the gene encoding an unusually divergent TATA-binding protein (TBP) from the extremely A+T-rich human malaria parasite Plasmodium falciparum. Gene 1993, 124, 165–171.
[31]
Luo, H.; Gilinger, G.; Mukherjee, D.; Bellofatto, V. Transcription initiation at the TATA-less spliced leader RNA gene promoter requires at least two DNA-binding proteins and a tripartite architecture that includes an initiator element. J. Biol. Chem. 1999, 274, 31947–31954.
[32]
Quon, D.V.; Delgadillo, M.G.; Johnson, P.J. Transcription in the early diverging eukaryote Trichomonas vaginalis: An unusual RNA polymerase II and alpha-amanitin-resistant transcription of protein-coding genes. J. Mol. Evol. 1996, 43, 253–262.
[33]
Quon, D.V.; Delgadillo, M.G.; Khachi, A.; Smale, S.T.; Johnson, P.J. Similarity between a ubiquitous promoter element in an ancient eukaryote and mammalian initiator elements. Proc. Natl. Acad. Sci. USA 1994, 91, 4579–4583, doi:10.1073/pnas.91.10.4579.
[34]
Le, Q.H.; Markovic, P.; Hastings, J.W.; Jovine, R.V.; Morse, D. Structure and organization of the peridinin-chlorophyll a-binding protein gene in Gonyaulax polyedra. Mol. Gen. Genet. 1997, 255, 595–604.
[35]
Li, L.; Hastings, J.W. The structure and organization of the luciferase gene in the photosynthetic dinoflagellate Gonyaulax polyedra. Plant Mol. Biol. 1998, 36, 275–284, doi:10.1023/A:1005941421474.
[36]
Machabee, S.; Wall, L.; Morse, D. Expression and genomic organization of a dinoflagellate gene family. Plant Mol. Biol. 1994, 25, 23–31, doi:10.1007/BF00024195.
[37]
Lee, D.H.; Mittag, M.; Sczekan, S.; Morse, D.; Hastings, J.W. Molecular cloning and genomic organization of a gene for luciferin-binding protein from the dinoflagellate Gonyaulax polyedra. J. Biol. Chem. 1993, 268, 8842–8850.
[38]
Okamoto, O.K.; Liu, L.; Robertson, D.L.; Hastings, J.W. Members of a dinoflagellate luciferase gene family differ in synonymous substitution rates. Biochemistry 2001, 40, 15862–15868, doi:10.1021/bi011651q.
[39]
Bachvaroff, T.R.; Place, A.R. From stop to start: Tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 2008, 3, e2929, doi:10.1371/journal.pone.0002929.
[40]
Jackson, A.P. Tandem gene arrays in Trypanosoma brucei: Comparative phylogenomic analysis of duplicate sequence variation. BMC Evol. Biol. 2007, 7, doi:10.1186/1471-2148-7-54.
[41]
Beauchemin, M.; Roy, S.; Daoust, P.; Dagenais-Bellefeuille, S.; Bertomeu, T.; Letourneau, L.; Lang, B.F.; Morse, D. Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic. Proc. Natl. Acad. Sci. USA 2012, 109, 15793–15798, doi:10.1073/pnas.1206683109.
[42]
Rizzo, P.J. RNA synthesis in isolated nuclei of the dinoflagellate Crypthecodinium cohnii. J. Protozool. 1979, 26, 290–294.
[43]
Palenchar, J.B.; Bellofatto, V. Gene transcription in trypanosomes. Mol. Biochem. Parasitol. 2006, 146, 135–141, doi:10.1016/j.molbiopara.2005.12.008.
[44]
Orphanides, G.; Lagrange, T.; Reinberg, D. The general transcription factors of RNA polymerase II. Genes Dev. 1996, 10, 2657–2683, doi:10.1101/gad.10.21.2657.
[45]
Conaway, J.W.; Bond, M.W.; Conaway, R.C. An RNA polymerase II transcription system from rat liver. Purification of an essential component. J. Biol. Chem. 1987, 262, 8293–8297.
[46]
Conaway, R.C.; Conaway, J.W. An RNA polymerase II transcription factor has an associated DNA-dependent ATPase (dATPase) activity strongly stimulated by the TATA region of promoters. Proc. Natl. Acad. Sci. USA 1989, 86, 7356–7360, doi:10.1073/pnas.86.19.7356.
[47]
Conaway, J.W.; Conaway, R.C. A multisubunit transcription factor essential for accurate initiation by RNA polymerase II. J. Biol. Chem. 1989, 264, 2357–2362.
[48]
Conaway, J.W.; Reines, D.; Conaway, R.C. Transcription initiated by RNA polymerase II and purified transcription factors from liver. Cooperative action of transcription factors τ and ε in initial complex formation. J. Biol. Chem. 1990, 265, 7552–7558.
[49]
Sumimoto, H.; Ohkuma, Y.; Yamamoto, T.; Horikoshi, M.; Roeder, R.G. Factors involved in specific transcription by mammalian RNA polymerase II: Identification of general transcription factor TFIIG. Proc. Natl. Acad. Sci. USA 1990, 87, 9158–9162, doi:10.1073/pnas.87.23.9158.
[50]
Poon, D.; Bai, Y.; Campbell, A.M.; Bjorklund, S.; Kim, Y.J.; Zhou, S.; Kornberg, R.D.; Weil, P.A. Identification and characterization of a TFIID-like multiprotein complex from Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1995, 92, 8224–8228.
[51]
Sanders, S.L.; Weil, P.A. Identification of two novel TAF subunits of the yeast Saccharomyces cerevisiae TFIID complex. J. Biol. Chem. 2000, 275, 13895–13900, doi:10.1074/jbc.275.18.13895.
[52]
Chatterjee, S.; Struhl, K. Connecting a promoter-bound protein to TBP bypasses the need for a transcriptional activation domain. Nature 1995, 374, 820–822, doi:10.1038/374820a0.
[53]
Chong, J.A.; Moran, M.M.; Teichmann, M.; Kaczmarek, J.S.; Roeder, R.; Clapham, D.E. TATA-binding protein (TBP)-like factor (TLF) is a functional regulator of transcription: Reciprocal regulation of the neurofibromatosis type 1 and c-fos genes by TLF/TRF2 and TBP. Mol. Cell. Biol. 2005, 25, 2632–2643.
[54]
Holmes, M.C.; Tjian, R. Promoter-selective properties of the TBP-related factor TRF1. Science 2000, 288, 867–870, doi:10.1126/science.288.5467.867.
[55]
Guillebault, D.; Sasorith, S.; Derelle, E.; Wurtz, J.M.; Lozano, J.C.; Bingham, S.; Tora, L.; Moreau, H. A new class of transcription initiation factors, intermediate between TATA box-binding proteins (TBPs) and TBP-like factors (TLFs), is present in the marine unicellular organism, the dinoflagellate Crypthecodinium cohnii. J. Biol. Chem. 2002, 277, 40881–40886, doi:10.1074/jbc.M205624200.
[56]
Bayer, T.; Aranda, M.; Sunagawa, S.; Yum, L.K.; Desalvo, M.K.; Lindquist, E.; Coffroth, M.A.; Voolstra, C.R.; Medina, M. Symbiodinium transcriptomes: Genome insights into the dinoflagellate symbionts of reef-building corals. PLoS One 2012, 7, e35269.
[57]
Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28, 2731–2739, doi:10.1093/molbev/msr121.
[58]
Toulza, E.; Shin, M.S.; Blanc, G.; Audic, S.; Laabir, M.; Collos, Y.; Claverie, J.M.; Grzebyk, D. Gene expression in proliferating cells of the dinoflagellate Alexandrium catenella (Dinophyceae). Appl. Environ. Microbiol. 2010, 76, 4521–4529, doi:10.1128/AEM.02345-09.
[59]
Qiu, X.B.; Lin, Y.L.; Thome, K.C.; Pian, P.; Schlegel, B.P.; Weremowicz, S.; Parvin, J.D.; Dutta, A. An eukaryotic RuvB-like protein (RUVBL1) essential for growth. J. Biol. Chem. 1998, 273, 27786–27793.
[60]
Luger, K.; Mader, A.W.; Richmond, R.K.; Sargent, D.F.; Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389, 251–260, doi:10.1038/38444.
[61]
Eickbush, T.H.; Moudrianakis, E.N. The histone core complex: An octamer assembled by two sets of protein-protein interactions. Biochemistry 1978, 17, 4955–4964, doi:10.1021/bi00616a016.
[62]
Kasinsky, H.E.; Lewis, J.D.; Dacks, J.B.; Ausio, J. Origin of H1 linker histones. FASEB J. 2001, 15, 34–42, doi:10.1096/fj.00-0237rev.
Rizzo, P.J.; Nooden, L.D. Chromosomal proteins in the dinoflagellate alga Gyrodinium cohnii. Science 1972, 176, 796–797.
[68]
Livolant, F. Cholesteric organization of DNA in the stallion sperm head. Tissue Cell 1984, 16, 535–555, doi:10.1016/0040-8166(84)90029-6.
[69]
Balhorn, R. The protamine family of sperm nuclear proteins. Genome Biol. 2007, 8, doi:10.1186/gb-2007-8-9-227.
[70]
Lin, S.; Zhang, H.; Zhuang, Y.; Tran, B.; Gill, J. Spliced leader-based metatranscriptomic analyses lead to recognition of hidden genomic features in dinoflagellates. Proc. Natl. Acad. Sci. USA 2010, 107, 20033–20038.
[71]
Roy, S.; Morse, D. A full suite of histone and histone modifying genes are transcribed in the dinoflagellate Lingulodinium. PLoS One 2012, 7, e34340.
[72]
Rizzo, P.J.; Jones, M.; Ray, S.M. Isolation and properties of isolated nuclei from the Florida red tide dinoflagellate Gymnodinium breve (Davis). J. Protozool. 1982, 29, 217–222, doi:10.1111/j.1550-7408.1982.tb04014.x.
[73]
Kellenberger, E.; Arnold-Schulz-Gahmen, B. Chromatins of low-protein content: Special features of their compaction and condensation. FEMS Microbiol. Lett. 1992, 79, 361–370.
[74]
Holck, A.; Lossius, I.; Aasland, R.; Haarr, L.; Kleppe, K. DNA- and RNA-binding proteins of chromatin from Escherichia coli. Biochim. Biophys. Acta 1987, 908, 188–199, doi:10.1016/0167-4781(87)90058-3.
[75]
Wong, J.T.; New, D.C.; Wong, J.C.; Hung, V.K. Histone-like proteins of the dinoflagellate Crypthecodinium cohnii have homologies to bacterial DNA-binding proteins. Eukaryot. Cell 2003, 2, 646–650, doi:10.1128/EC.2.3.646-650.2003.
[76]
Sala-Rovira, M.; Geraud, M.L.; Caput, D.; Jacques, F.; Soyer-Gobillard, M.O.; Vernet, G.; Herzog, M. Molecular cloning and immunolocalization of two variants of the major basic nuclear protein (HCc) from the histone-less eukaryote Crypthecodinium cohnii (Pyrrhophyta). Chromosoma 1991, 100, 510–518, doi:10.1007/BF00352201.
[77]
Chudnovsky, Y.; Li, J.F.; Rizzo, P.J.; Hastings, J.W.; Fagan, T. Cloning, expression, and characterization of a histone-like protein from the marine dinoflagellate Lingulodinium polyedrum. J. Phycol. 2002, 38, 543–550.
[78]
Gornik, S.G.; Ford, K.L.; Mulhern, T.D.; Bacic, A.; McFadden, G.I.; Waller, R.F. Loss of nucleosomal DNA condensation coincides with appearance of a novel nuclear protein in dinoflagellates. Curr. Biol. 2012, 22, 2303–2312, doi:10.1016/j.cub.2012.10.036.
[79]
Azevedo, C. Fine structure of Perkinsus atlanticus n. sp. (Apicomplexa, Perkinsea) parasite of the clam Ruditapes decussatus from Portugal. J. Parasitol. 1989, 75, 627–635, doi:10.2307/3282915.
[80]
Jaeckisch, N.; Yang, I.; Wohlrab, S.; Glockner, G.; Kroymann, J.; Vogel, H.; Cembella, A.; John, U. Comparative genomic and transcriptomic characterization of the toxigenic marine dinoflagellate Alexandrium ostenfeldii. PLoS One 2011, 6, e28012.
[81]
Minguez, A.; Franca, S.; Moreno Diaz de la Espina, S. Dinoflagellates have a eukaryotic nuclear matrix with lamin-like proteins and topoisomerase II. J. Cell Sci. 1994, 107, 2861–2873.
[82]
Dechat, T.; Pfleghaar, K.; Sengupta, K.; Shimi, T.; Shumaker, D.K.; Solimando, L.; Goldman, R.D. Nuclear lamins: Major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 2008, 22, 832–853.
Bhaud, Y.; Geraud, M.L.; Ausseil, J.; Soyer-Gobillard, M.O.; Moreau, H. Cyclic expression of a nuclear protein in a dinoflagellate. J. Eukaryot. Microbiol. 1999, 46, 259–267, doi:10.1111/j.1550-7408.1999.tb05123.x.
[86]
Guillebault, D.; Derelle, E.; Bhaud, Y.; Moreau, H. Role of nuclear WW domains and proline-rich proteins in dinoflagellate transcription. Protist 2001, 152, 127–138.
[87]
Boggon, T.J.; Shan, W.S.; Santagata, S.; Myers, S.C.; Shapiro, L. Implication of tubby proteins as transcription factors by structure-based functional analysis. Science 1999, 286, 2119–2125, doi:10.1126/science.286.5447.2119.
[88]
Babu, M.M.; Luscombe, N.M.; Aravind, L.; Gerstein, M.; Teichmann, S.A. Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol. 2004, 14, 283–291, doi:10.1016/j.sbi.2004.05.004.
[89]
Sommerville, J. Activities of cold-shock domain proteins in translation control. Bioessays 1999, 21, 319–325.
[90]
Balaji, S.; Babu, M.M.; Iyer, L.M.; Aravind, L. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res. 2005, 33, 3994–4006, doi:10.1093/nar/gki709.
[91]
Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002, 16, 6–21, doi:10.1101/gad.947102.
[92]
Blank, R.J.; Huss, V.A.R.; Kersten, W. Base composition of DNA from symbiotic dinoflagellates: A tool for phylogenetic classification. Arch. Microbiol. 1988, 149, 515–520, doi:10.1007/BF00446754.
[93]
Steele, R.E.; Rae, P.M. Ordered distribution of modified bases in the DNA of a dinoflagellate. Nucleic Acids Res. 1980, 8, 4709–4725, doi:10.1093/nar/8.20.4709.
[94]
Ten Lohuis, M.R.; Miller, D.J. Light-regulated transcription of genes encoding peridinin chlorophyll a proteins and the major intrinsic light-harvesting complex proteins in the dinoflagellate amphidinium carterae hulburt (Dinophycae). Changes In cytosine methylation accompany photoadaptation. Plant Physiol. 1998, 117, 189–196, doi:10.1104/pp.117.1.189.
[95]
Rae, P.M.; Steele, R.E. Modified bases in the DNAs of unicellular eukaryotes: An examination of distributions and possible roles, with emphasis on hydroxymethyluracil in dinoflagellates. Biosystems 1978, 10, 37–53, doi:10.1016/0303-2647(78)90027-8.
[96]
Teebor, G.W.; Frenkel, K.; Goldstein, M.S. Ionizing radiation and tritium transmutation both cause formation of 5-hydroxymethyl-2′-deoxyuridine in cellular DNA. Proc. Natl. Acad. Sci. USA 1984, 81, 318–321, doi:10.1073/pnas.81.2.318.
[97]
Rae, P.M. Hydroxymethyluracil in eukaryote DNA: A natural feature of the pyrrophyta (dinoflagellates). Science 1976, 194, 1062–1064.
[98]
Thomas, S.; Green, A.; Sturm, N.R.; Campbell, D.A.; Myler, P.J. Histone acetylations mark origins of polycistronic transcription in Leishmania major. BMC Genomics 2009, 10, doi:10.1186/1471-2164-10-152.
[99]
Wong, J.T.; Kwok, A.C. Proliferation of dinoflagellates: Blooming or bleaching. Bioessays 2005, 27, 730–740, doi:10.1002/bies.20250.
[100]
Gyula, P.; Schafer, E.; Nagy, F. Light perception and signalling in higher plants. Curr. Opin. Plant Biol. 2003, 6, 446–452, doi:10.1016/S1369-5266(03)00082-7.
[101]
Van Dolah, F.M.; Lidie, K.B.; More, J.S.; Brunelle, S.A.; Ryan, J.C.; Monroe, E.A.; Haynes, B.L. Microarray analysis of diurnal- and circadian-regulated genes in the Florida red-tide dinoflagellate Karenia brevis (Dinophyceae). J. Phycol. 2007, 43, 741–752, doi:10.1111/j.1529-8817.2007.00354.x.
[102]
Lesser, M.P. Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol. Oceanogr. 1996, 41, 271–283, doi:10.4319/lo.1996.41.2.0271.
[103]
Lesser, M.P. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 1997, 16, 187–192.
[104]
Rosic, N.N.; Pernice, M.; Dove, S.; Dunn, S.; Hoegh-Guldberg, O. Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: Possible implications for coral bleaching. Cell Stress Chaperones 2010, 16, 69–80.
[105]
Walsh, C.T.; Garneau-Tsodikova, S.; Gatto, G.J., Jr. Protein posttranslational modifications: The chemistry of proteome diversifications. Angew. Chem. Int. Ed. Engl. 2005, 44, 7342–7372, doi:10.1002/anie.200501023.
[106]
Okamoto, O.K.; Asano, C.S.; Aidar, E.; Colepicolo, P. Of cadmium on growth and superoxide dismutase activity of this species of dinoflagellate. The marine microalga Tetraselmis gracilis. J. Phycol. 1996, 32, 74–79.
[107]
Okamoto, O.K.; Colepicolo, P. Response of superoxide dismutase to pollutant metal stress in the marine dinoflagellate Gonyaulax polyedra. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1998, 119, 67–73, doi:10.1016/S0742-8413(97)00192-8.
[108]
Okamoto, O.K.; Robertson, D.L.; Fagan, T.F.; Hastings, J.W.; Colepicolo, P. Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase. J. Biol. Chem. 2001, 276, 19989–19993.
[109]
Okamoto, O.K.; Hastings, J.W. Genome-wide analysis of redox-regulated genes in a dinoflagellate. Gene 2003, 321, 73–81, doi:10.1016/j.gene.2003.07.003.
[110]
Guo, R.; Ebenezer, V.; Ki, J.S. Transcriptional responses of heat shock protein 70 (Hsp70) to thermal, bisphenol A, and copper stresses in the dinoflagellate Prorocentrum minimu. Chemosphere 2012, 89, 512–520, doi:10.1016/j.chemosphere.2012.05.014.
[111]
Guo, R.; Ki, J.S. Differential transcription of heat shock protein 90 (HSP90) in the dinoflagellate Prorocentrum minimum by copper and endocrine-disrupting chemicals. Ecotoxicology 2012, 21, 1448–1457, doi:10.1007/s10646-012-0898-z.
[112]
Lowe, C.D.; Mello, L.V.; Samatar, N.; Martin, L.E.; Montagnes, D.J.; Watts, P.C. The transcriptome of the novel dinoflagellate Oxyrrhis marina (Alveolata: Dinophyceae): Response to salinity examined by 454 sequencing. BMC Genomics 2011, 12, doi:10.1186/1471-2164-12-519.
[113]
Kondo, T.; Ishiura, M. The circadian clock of cyanobacteria. Bioessays 2000, 22, 10–15, doi:10.1002/(SICI)1521-1878(200001)22:1<10::AID-BIES4>3.0.CO;2-A.
Loros, J.J.; Dunlap, J.C. Genetic and molecular analysis of circadian rhythms in Neurospora. Annu. Rev. Physiol. 2001, 63, 757–794, doi:10.1146/annurev.physiol.63.1.757.
[116]
Rivkees, S.A. The development of circadian rhythms: From animals to humans. Sleep Med. Clin. 2007, 2, 331–341, doi:10.1016/j.jsmc.2007.05.010.
[117]
Roenneberg, T.; Rehman, J. Nitrate, a nonphotic signal for the circadian system. FASEB J. 1996, 10, 1443–1447.
[118]
Roenneberg, T.; Merrow, M. Entrainment of the human circadian clock. Cold Spring Harb. Symp. Quant. Biol. 2007, 72, 293–299, doi:10.1101/sqb.2007.72.043.
[119]
Merrow, M.; Roenneberg, T. Circadian entrainment of Neurospora crassa. Cold Spring Harb. Symp. Quant. Biol. 2007, 72, 279–285, doi:10.1101/sqb.2007.72.032.
[120]
Roenneberg, T.; Kumar, C.J.; Merrow, M. The human circadian clock entrains to sun time. Curr. Biol. 2007, 17, R44–R45, doi:10.1016/j.cub.2006.12.011.
[121]
Woelfle, M.A.; Johnson, C.H. No promoter left behind: Global circadian gene expression in cyanobacteria. J. Biol. Rhythms 2006, 21, 419–431, doi:10.1177/0748730406294418.
[122]
Ito, H.; Mutsuda, M.; Murayama, Y.; Tomita, J.; Hosokawa, N.; Terauchi, K.; Sugita, C.; Sugita, M.; Kondo, T.; Iwasaki, H. Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc. Natl. Acad. Sci. USA 2009, 106, 14168–14173, doi:10.1073/pnas.0902587106.
[123]
Okamoto, O.K.; Hastings, J.W. Novel dinoflagellate clock-related genes identified through microarray analysis. J. Phycol. 2003, 39, 519–526.
[124]
Walz, B.; Walz, A.; Sweeney, B.M. A circadian rhythm in RNA in the dinoflagellate, Gonyaulax polyedra. J. Comp. Physiol. 1983, 151, 207–213.
[125]
Dagenais-Bellefeuille, S.; Bertomeu, T.; Morse, D. S-phase and M-phase timing are under independent circadian control in the dinoflagellate Lingulodinium. J. Biol. Rhythms 2008, 23, 400–408, doi:10.1177/0748730408321749.
[126]
Bertomeu, T.; Rivoal, J.; Morse, D. A dinoflagellate CDK5-like cyclin-dependent kinase. Biol. Cell 2007, 99, 531–540, doi:10.1042/BC20070018.
[127]
Karakashian, M.W.; Hastings, J.W. The inhibition of a biological clock by actinomycin D. Proc. Natl. Acad. Sci. USA 1962, 48, 2130–2137, doi:10.1073/pnas.48.12.2130.
[128]
Rossini, C.; Taylor, W.; Fagan, T.; Hastings, J.W. Lifetimes of mRNAs for clock-regulated proteins in a dinoflagellate. Chronobiol. Int. 2003, 20, 963–976, doi:10.1081/CBI-120025248.
[129]
Morey, J.S.; Monroe, E.A.; Kinney, A.L.; Beal, M.; Johnson, J.G.; Hitchcock, G.L.; van Dolah, F.M. Transcriptomic response of the red tide dinoflagellate, Karenia brevis, to nitrogen and phosphorus depletion and addition. BMC Genomics 2011, 12, doi:10.1186/1471-2164-12-346.
[130]
Lin, X.; Zhang, H.; Huang, B.; Lin, S. Alkaline phosphatase gene sequence and transcriptional regulation by phosphate limitation in Amphidinium carterae (dinophyceae). J. Phycol. 2011, 47, 1110–1120, doi:10.1111/j.1529-8817.2011.01038.x.
[131]
Lin, X.; Zhang, H.; Huang, B.; Lin, S. Alkaline phosphatase gene sequence characteristics and transcriptional regulation by phosphate limitation in Karenia brevis (Dinophyceae). Harmful Algae 2012, 17, 14–24.
[132]
Lee, T.C.; Kwok, O.T.; Ho, K.C.; Lee, F.W. Effects of different nitrate and phosphate concentrations on the growth and toxin production of an Alexandrium tamarense strain collected from Drake Passage. Mar. Environ. Res. 2012, 81, 62–69, doi:10.1016/j.marenvres.2012.08.009.
[133]
Yang, I.; Beszteri, S.; Tillmann, U.; Cembella, A.; John, U. Growth- and nutrient-dependent gene expression in the toxigenic marine dinoflagellate Alexandrium minutum. Harmful Algae 2011, 12, 55–69, doi:10.1016/j.hal.2011.08.012.
[134]
Moustafa, A.; Evans, A.N.; Kulis, D.M.; Hackett, J.D.; Erdner, D.L.; Anderson, D.M.; Bhattacharya, D. Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PLoS One 2010, 5, e9688, doi:10.1371/journal.pone.0009688.
[135]
Johnson, J.G.; Morey, J.S.; Neely, M.G.; Ryan, J.C.; van Dolah, F.M. Transcriptome remodeling associated with chronological aging in the dinoflagellate, Karenia brevis. Mar. Genomics 2012, 5, 15–25.
[136]
Yang, I.; John, U.; Beszteri, S.; Glockner, G.; Krock, B.; Goesmann, A.; Cembella, A.D. Comparative gene expression in toxic versus non-toxic strains of the marine dinoflagellate Alexandrium minutum. BMC Genomics 2010, 11, doi:10.1186/1471-2164-11-248.
[137]
Salcedo, T.; Upadhyay, R.J.; Nagasaki, K.; Bhattacharya, D. Dozens of toxin-related genes are expressed in a nontoxic strain of the dinoflagellate Heterocapsa circularisquama. Mol. Biol. Evol. 2012, 29, 1503–1506, doi:10.1093/molbev/mss007.
[138]
Nassoury, N.; Cappadocia, M.; Morse, D. Plastid ultrastructure defines the protein import pathway in dinoflagellates. J. Cell Sci. 2003, 116, 2867–2874, doi:10.1242/jcs.00517.
[139]
Shi, X.; Zhang, H.; Lin, S. Tandem repeats, high copy number and remarkable diel expression rhythm of form II RuBisCO in Prorocentrum donghaiense (dinophyceae). PLoS One 2013, 8, e71232.
[140]
Gast, R.J.; Beaudoin, D.J.; Caron, D.A. Isolation of symbiotically expressed genes from the dinoflagellate symbiont of the solitary radiolarian Thalassicolla nucleata. Biol. Bull. 2003, 204, 210–214, doi:10.2307/1543561.
[141]
Bertucci, A.; Tambutte, E.; Tambutte, S.; Allemand, D.; Zoccola, D. Symbiosis-dependent gene expression in coral-dinoflagellate association: Cloning and characterization of a P-type H+-ATPase gene. Proc. Biol. Sci. 2010, 277, 87–95, doi:10.1098/rspb.2009.1266.
[142]
Leggat, W.; Seneca, F.; Wasmund, K.; Ukani, L.; Yellowlees, D.; Ainsworth, T.D. Differential responses of the coral host and their algal symbiont to thermal stress. PLoS One 2011, 6, e26687.
[143]
Wohlrab, S.; Iversen, M.H.; John, U. A molecular and co-evolutionary context for grazer induced toxin production in Alexandrium tamarense. PLoS One 2010, 5, e15039.
[144]
Yang, E.; van Nimwegen, E.; Zavolan, M.; Rajewsky, N.; Schroeder, M.; Magnasco, M.; Darnell, J.E., Jr. Decay rates of human mRNAs: Correlation with functional characteristics and sequence attributes. Genome Res. 2003, 13, 1863–1872.
[145]
Kinniburgh, A.J.; Mertz, J.E.; Ross, J. The precursor of mouse beta-globin messenger RNA contains two intervening RNA sequences. Cell 1978, 14, 681–693, doi:10.1016/0092-8674(78)90251-9.
[146]
Chow, L.T.; Gelinas, R.E.; Broker, T.R.; Roberts, R.J. An amazing sequence arrangement at the 5′ ends of adenovirus 2 messenger RNA. Cell 1977, 12, 1–8, doi:10.1016/0092-8674(77)90180-5.
[147]
Berget, S.M.; Moore, C.; Sharp, P.A. Spliced segments at the 5′ terminus of adenovirus 2 late mRNA. Proc. Natl. Acad. Sci. USA 1977, 74, 3171–3175, doi:10.1073/pnas.74.8.3171.
[148]
Zhang, H.; Lin, S. Complex gene structure of the form II Rubisco in the dinoflagellate Prorocentrum minimum (Dinophyceae). J. Phycol. 2003, 39, 1160–1171, doi:10.1111/j.0022-3646.2003.03-055.x.
[149]
Rowan, R.; Whitney, S.M.; Fowler, A.; Yellowlees, D. Rubisco in marine symbiotic dinoflagellates: Form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 1996, 8, 539–553.
[150]
Orr, R.J.; Stuken, A.; Murray, S.A.; Jakobsen, K.S. Evolutionary acquisition and loss of saxitoxin biosynthesis in dinoflagellates: The second “core” gene, sxtG. Appl. Environ. Microbiol. 2013, 79, 2128–2136, doi:10.1128/AEM.03279-12.
[151]
Kitamura-Abe, S.; Itoh, H.; Washio, T.; Tsutsumi, A.; Tomita, M. Characterization of the splice sites in GT-AG and GC-AG introns in higher eukaryotes using full-length cDNAs. J. Bioinform. Comput. Biol. 2004, 2, 309–331, doi:10.1142/S0219720004000570.
[152]
Nilsen, T.W. The spliceosome: No assembly required? Mol. Cell 2002, 9, 8–9, doi:10.1016/S1097-2765(02)00430-6.
[153]
Reddy, R.; Spector, D.; Henning, D.; Liu, M.H.; Busch, H. Isolation and partial characterization of dinoflagellate U1–U6 small RNAs homologous to rat U small nuclear RNAs. J. Biol. Chem. 1983, 258, 13965–13969.
[154]
Alverca, E.; Franca, S.; Diaz de la Espina, S.M. Topology of splicing and snRNP biogenesis in dinoflagellate nuclei. Biol. Cell 2006, 98, 709–720, doi:10.1042/BC20050083.
[155]
Zhang, H.; Hou, Y.; Miranda, L.; Campbell, D.A.; Sturm, N.R.; Gaasterland, T.; Lin, S. Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. USA 2007, 104, 4618–4623.
[156]
Boothroyd, J.C.; Cross, G.A. Transcripts coding for variant surface glycoproteins of Trypanosoma brucei have a short, identical exon at their 5′ end. Gene 1982, 20, 281–289, doi:10.1016/0378-1119(82)90046-4.
[157]
Agabian, N. Trans splicing of nuclear pre-mRNAs. Cell 1990, 61, 1157–1160, doi:10.1016/0092-8674(90)90674-4.
[158]
Douris, V.; Telford, M.J.; Averof, M. Evidence for multiple independent origins of trans-splicing in Metazoa. Mol. Biol. Evol. 2010, 27, 684–693, doi:10.1093/molbev/msp286.
[159]
Hastings, K.E. SL trans-splicing: Easy come or easy go? Trends Genet. 2005, 21, 240–247, doi:10.1016/j.tig.2005.02.005.
Vandenberghe, A.E.; Meedel, T.H.; Hastings, K.E. mRNA 5′-leader trans-splicing in the chordates. Genes Dev. 2001, 15, 294–303, doi:10.1101/gad.865401.
[162]
Davis, R.E. Surprising diversity and distribution of spliced leader RNAs in flatworms. Mol. Biochem. Parasitol. 1997, 87, 29–48, doi:10.1016/S0166-6851(97)00040-6.
[163]
Jackson, C.J.; Waller, R.F. A widespread and unusual RNA trans-splicing type in dinoflagellate mitochondria. PLoS One 2013, 8, e56777, doi:10.1371/journal.pone.0056777.
[164]
Hearne, J.L.; Pitula, J.S. Identification of two spliced leader RNA transcripts from Perkinsus marinus. J. Eukaryot. Microbiol. 2011, 58, 266–268.
[165]
Slamovits, C.H.; Keeling, P.J. Widespread recycling of processed cDNAs in dinoflagellates. Curr. Biol. 2008, 18, R550–R552, doi:10.1016/j.cub.2008.04.054.
[166]
Zhang, H.; Dungan, C.F.; Lin, S. Introns, alternative splicing, spliced leader trans-splicing and differential expression of pcna and cyclin in Perkinsus marinu. Protist 2011, 162, 154–167, doi:10.1016/j.protis.2010.03.003.
[167]
Suntharalingam, M.; Wente, S.R. Peering through the pore: Nuclear pore complex structure, assembly, and function. Dev. Cell 2003, 4, 775–789, doi:10.1016/S1534-5807(03)00162-X.
Fried, H.; Kutay, U. Nucleocytoplasmic transport: Taking an inventory. Cell. Mol. Life Sci. 2003, 60, 1659–1688, doi:10.1007/s00018-003-3070-3.
[170]
Frankel, M.B.; Knoll, L.J. The ins and outs of nuclear trafficking: Unusual aspects in apicomplexan parasites. DNA Cell Biol. 2009, 28, 277–284, doi:10.1089/dna.2009.0853.
[171]
Kohler, A.; Hurt, E. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 2007, 8, 761–773.
[172]
Zhang, J.; Sun, X.; Qian, Y.; LaDuca, J.P.; Maquat, L.E. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: A possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol. 1998, 18, 5272–5283.
[173]
Zhang, J.; Sun, X.; Qian, Y.; Maquat, L.E. Intron function in the nonsense-mediated decay of beta-globin mRNA: Indications that pre-mRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 1998, 4, 801–815, doi:10.1017/S1355838298971849.
[174]
Isken, O.; Maquat, L.E. Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function. Genes Dev. 2007, 21, 1833–1856, doi:10.1101/gad.1566807.
[175]
Ito-Harashima, S.; Kuroha, K.; Tatematsu, T.; Inada, T. Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev. 2007, 21, 519–524, doi:10.1101/gad.1490207.
[176]
Wu, S.; Wang, W.; Kong, X.; Congdon, L.M.; Yokomori, K.; Kirschner, M.W.; Rice, J.C. Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev. 2010, 24, 2531–2542, doi:10.1101/gad.1984210.
