In silico characterization of bHLH transcription factor genes in the genome of rainbow trout (Oncorhynchus mykiss)

The significance of seafood in nutrition has started to be better understood after the change in the understanding of nutrition in the world. One of the most common species cultivated in the world is rainbow trout (Oncorhynchus mykiss) from the origin of North America. Transcription factors are a group of proteins containing different functional components for the accomplishment of various activities. The basic helix (bHLH) domain is a highly preserved amino acid motif that characterizes a family of transcription factors. The bHLH gene family in the rainbow trout (Oncorhynchus mykiss) genome has been identified in the current study for the first-time using bioinformatics tools. According to the results, 441 bHLH genes (OmybHLH) were identified in the rainbow trout genome and the physicochemical properties of those proteins were determined. The highest number of the genes was in 7th chromosome of rainbow trout with 29 OmybHLH genes. 38 of OmybHLH genes had no intronic regions. OmybHLH proteins were divided into 4 main groups in the phylogenetic tree consistent with their motif content. The common biological function of OmybHLH proteins was the regulation of biological processes. The mode of action of OmybHLH proteins was binding activity. The OmybHLH gene family in the rainbow trout and the bHLH gene family in the Atlantic salmon (SsabHLH) had 95 orthologous gene relationships and average separation times of those orthologous genes were found to be 298 million years ago (MYA). Almost all the OmybHLH protein family members have dominated by the α-helix motif which is a stable conformation. Identification of the bHLH proteins and evaluation of their properties in rainbow trout can open new perspectives for aquaculture applications and fish culture to get better yield using genetic data.


Atchley, W. R., Terhalle, W. & Dress, A. (1999). Positional dependence, cliques and predictive motifs in the bHLH protein domain. Journal of Molecular Evolution, 48(5): 501–516.

Aydın, F. (2009). Alabalık biyolojisi ve yetiştirme teknikleri. Ankara Üniversitesi Ziraat Fakültesi Su Ürünleri Bölümü, Ankara, Turkey. 30p.

Bailey, T. L., Johnson, J., Grant, C. E. & Noble, W. S. (2015). The MEME suite. Nucleic Acids Research, 43(1): 39-49.

Ben Arie, N. (1996). Evolutionary conservation of sequence and expression of the bHLH protein atonal suggests a conserved role in neurogenesis. Human Molecular Genetics, 5(9): 1207–1216.

Benezra, R., Davis, R. L., Lockshon, D., Turner, D. L. & Weintraub, H. (1990). The protein id: A negative regulator of helix-loop-helix DNA binding proteins. Trends in Genetics, 61(1): 49-59.

Berkes, C. A. & Tapscott, S. J. (2005). MyoD and the transcriptional control of myogenesis. Seminars in Cell, Developmental Biology, 16(4-5): 585–595.

Borges, M., Linnoila, R. I., van de Velde, H. J. K., Chen, H., Nelkin, B. D., Mabry, M. & Ball, D. W. (1997). An Achaete-Scute homologue essential for neuroendocrine differentiation in the lung. Nature, 386(6627): 852–855.

Buck, M. J. & Atchley, W. R. (2003). Phylogenetic analysis of plant basic helix-loop helix proteins. Journal of Molecular Evolution, 56(6): 742–750.

Buckingham, M., Bajard, L., Chang, T., Daubas, P., Hadchouel, J., Meilhac, S. & Relaix, F. (2003). The Formation of Skeletal Muscle: From Somite to Limb. Journal of Anatomy, 202(1): 59–68.

Campuzano, S. (1985). Molecular genetics of the Achaete-Scute gene complex of D. melanogaster. Cell, 40(2): 327–338.

Conesa, A., Gotz, S., Garcia-Gomez, J. M., Terol, J., Talon, M. & Robles, M. (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18): 3674–3676.

Dang, C., Wang, Y., Zhang, D., Yao, Q. & Chen, K. (2011). A genome-wide survey on basic helix-loop-helix transcription factors in giant panda. PLoS One, 6(11): e26878.

Doğan, K., & Güven, E. (2005). Ülkemizde (Türkiye) Su ürünleri yetiştiriciliği yapan işletmeler, üretim kapasiteleri, illere göre dağılımları ve ekonomik analizleri. Su Ürünleri Mühendisleri Derneği Dergisi, 1(4): 28-33. 0.22392/egirdir.414488

Drake, C. J., Brandt, S. J., Trusk, T. C., Little, C. D. (1997). TAL1/SCL Is Expressed in Endothelial Progenitor Cells/Angioblasts and Defines a Dorsal-toVentral Gradient of Vasculogenesis. Developmental Biology, 192(1): 17–30.

Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., Bairoch, A. (2005). Protein Identification and Analysis Tools on the ExPASy Server. The Proteomics Protocols Handbook, 571– 607.

Gering, M., Rodaway, A. R. F., & Göttgens, B., & Patient, R. K. & Green, A. R. (1998). The SCL gene specifies haemangioblast development from early mesoderm. The EMBO Journal, 17(14): 4029–4045.

Guillemot, F. (1995). Analysis of the role of basic-helix-loophelix transcription factors in the development of neural lineages in the mouse. Biology of the Cell, 84(1-2): 3–6.

Guillemot, F. (2007). Spatial and temporal specification of neural fates by transcription factor codes. Development, 134(21): 3771–3780. dev.006379

Guillemot, F., Lo, L. C., Johnson, J. E., Auerbach, A., Anderson, D. J. & Joyner, A. L. (1993). Mammalian Achaete-Scute Momolog 1 is required for the early development of olfactory and autonomic neurons. Cell, 75(3): 463–476.

Hodgkinson, C. A., Moore, K. J., Nakayama, A., Steingrimsson, E., Copeland, N. G., Jenkins, N. A. & Arnheiter, H. (1993). Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic- helix- loop- helix- zipper protein. Cell, 74(2): 395- 404.

Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J. & Gao, G. (2014). GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31(8): 1296–1297.

Ishido, M., Kami, K. & Masuhara, M. (2004). In Vivo expression patterns of MyoD, p21, and Rb proteins in myonuclei and satellite cells of denervated rat skeletal muscle. American Journal of Physiology, Cell Physiology, 287(2): 484-C493. 00080.2004

İzci, L., Günlü, A. & Bilgin, Ş. (2009). Ülkemizde gökkuşağı alabalığı (Oncorhynchus mykiss Walbaum, 1792)’nın değerlendirilme şekilleri. Eğirdir Su Ürünleri Fakültesi Dergisi, 5(1-2): 73-79.

Jahan, I., Kersigo, J., Pan, N. & Fritzsch, B. (2010). Neurod1 regulates survival and formation of connections in mouse ear and brain. Cell and Tissue Research, 341(1): 95–110.

Jones, S. (2004). An overview of the basic helix-loop-helix proteins. Genome Biology, 5(6): 226.

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. E. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10: 845–858.

Kocaman, E. & Sayili, M. (2014). Gümüşhane ilinde gökkuşaği alabalik işletmelerinin ekonomik analizi. Anadolu Tarım Bilimleri Dergisi, 29(1): 36-45.

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35(6): 1547-1549. molbev/msy096

Ledent, V., Paquet, O. & Vervoort, M. (2002). Phylogenetic analysis of the human basic helix-loop-helix proteins. Genome Biology, 3(6): research0030.1-0030.18.

Ledent, V. & Vervoort, M. (2001). The basic helix-loop-helix protein family: Comparative genomics and phylogenetic analysis. Genome Research, 11(5): 754–770.

Legerlotz, K. & Smith, H. K. (2008). Role of MyoD in denervated, disused, and exercised muscle. Muscle, Nerve, 38(3): 1087–1100.

Letunic, I. & Bork, P. (2019). Interactive tree of life (iTOL) v4: Recent updates and new developments. Nucleic Acids Research, 47(W1): W256-W259.

Levy, C., Khaled, M. & Fisher, D. E. (2006). MITF: Master regulator of melanocyte development and melanoma oncogene. Trends in Molecular Medicine, 12(9): 406– 414.

Li, F. & Liu, W. (2017). Genome-wide identification, classification, and functional analysis of the basic helix– loop–helix transcription factors in the cattle, Bos taurus. Mammalian Genome, 28(5-6): 176-197.

Li, K. B. (2003). ClustalW-MPI: ClustalW analysis using distributed and parallel computing. Bioinformatics, 19(12): 1585–1586. bioinformatics/btg192

Liu, A., Wang, Y., Dang, C., Zhang, D., Song, H., Yao, Q. & Chen, K. (2012). A genome-wide identification and analysis of the basic helix-loop-helix transcription factors in the ponerine ant, Harpegnathos saltator. BMC evolutionary biology, 12(1): 165.

Liu, W. (2015). Genome-wide identification, classification and functional analyses of the bHLH transcription factor family in the pig, Sus scrofa. Molecular genetics and genomics, 290(4): 1415-1433. s00438-015-1007-9

Liu, W. & Zhao, C. (2011). Molecular phylogenetic analysis of zebra finch basic helix-loop-helix transcription factors. Biochemical Genetics, 49(3-4): 226-241.

Liu, X. T., Wang, Y., Wang, X. H., Tao, X. F., Yao, Q. & Chen, K. P. (2014). A genome-wide identification and classification of basic helix-loop-helix genes in the jewel wasp, Nasonia vitripennis (Hymenoptera: Pteromalidae). Genome, 57(10): 525-536.

Malecki, M. T., Jhala, U. S., Antonellis, A., Fields, L., Doria, A., Orban, T. & Krolewski, A. S. (1999). Mutations in NEUROD1 are associated with the development of type 2 diabetes mellitus. Nature Genetics, 23(3): 323–328.

Miyata, T., Maeda, T. & Lee, J. E. (1999). NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Development, 13(13): 1647– 1652.

Molkentin, J. D. & Olson, E. N. (1996). Defining the regulatory networks for muscle development. Current Opinion in Genetics, Development, 6(4): 445–453.

Muralidhar, M. G., Callahan, C. A. & Thomas, J. B. (1993). Single-minded regulation of genes in the embryonic midline of the drosophila central nervous system. Mechanisms of Development, 41(2-3): 129–138.

Murre, C. (2019). Helix-loop-helix proteins and the advent of cellular diversity: 30 years of discovery. Genes Development, 33: 6-25.

Murre, C., McCaw, P. S. & Baltimore, D. (1989). A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and Myc proteins. Cell, 56(5): 777–783.

Nambu, J. R., Lewis, J. O., Wharton, K. A. & Crews, S. T. (1991). The drosophila single- minded gene encodes a helixloop- helix protein that acts as a master regulator of cns midline development. Cell, 67(6): 1157-1167.

Norton, J. D. (2000). Id helix loop helix proteins in cell growth, differentiation and tumorigenesis. Journal of Cell Science, 113(22): 3897-3905.

Olson, J. M., Asakura, A., Snider, L., Hawkes, R., Strand, A., Stoeck, J. & Tapscott, S. J. (2001). NeuroD2 is necessary for development and survival of central nervous system neurons. Developmental Biology, 234(1): 174–187.

Perk, J., Iavarone, A. & Benezra, R. (2005). Id family of helixloop-helix proteins in cancer. Nature Reviews Cancer, 5(8): 603–614.

Perry, R. L., Parker, M. H. & Rudnicki, M. A. (2001). Activated MEK1 binds the nuclear MyoD transcriptional complex to repress transactivation. Molecular Cell, 8(2): 291–301.

Pires, N. & Dolan, L. (2010). Origin and diversification of basichelix-loop-helix proteins in plants. Molecular Biology and Evolution, 27(4): 862-874.

Pownall, M. E., Gustafsson, M. K. & Emerson, C. P. (2002). Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annual Review of Cell and Developmental Biology, 18(1): 747– 783. 18.012502.1

Puri, P. L. & Sartorelli, V. (2000). Regulation of muscle regulatory factors by DNA-binding, interacting proteins, and post-transcriptional modifications. Journal of Cellular Physiology, 185(2): 155–173. 4652(200011)185:2<155::aid-jcp1>;2-z

Robinson, K. A. & Lopes, J. M. (2000). Survey and summary: Saccharomyces cerevisiae basic helix–loop–helix proteins regulate diverse biological processes. Nucleic Acids Research, 28(7): 1499-1505.

Sailsbery, J. K., Atchley, W. R. & Dean, R. A. (2012). Phylogenetic analysis and classification of the fungal bHLH domain. Molecular Biology and Evolution, 29(5): 1301–1318.

Sayılı, M., Karataş, M., Yücer, A. & Akça, H. (1999). Tokat ilinde alabalık yetiştiriciliği yapan işletmelerin yapısal ve ekonomik analizi. Ekin Dergisi, 7: 66-72.

Steingrimsson, E., Copeland, N. G. & Jenkins, N. A. (2004). Melanocytes and the microphthalmia transcription factor network. Annual Review of Genetics, 38(1): 365– 411.

Suyama, M., Torrents, D. & Bork, P. (2006). PAL2NAL: Robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research, 34(Web Server): W609-W612.

Tapscott, S. J. (2005). The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development, 132(12): 2685–2695.

Voorrips, R. E. (2002). MapChart: Software for the graphical presentation of linkage maps and QTLs. Journal of Heredity, 93(1): 77–78.

Voytik, S. L., Przyborski, M., Badylak, S. F. & Konieczny, S. F. (1993). Differential expression of muscle regulatory factor genes in normal and denervated adult rat hindlimb muscles. Developmental Dynamics, 198(3): 214-224.

Walters, E. H., Stickland, N. C. & Loughna, P. T. (2000). The expression of the myogenic regulatory factors in denervated and normal muscles of different phenotypes. Journal of Muscle Research, Cell Motility, 21(7): 647-653.

Wang, X. H., Wang, Y., Liu, A. K., Liu, X. T., Zhou, Y., Yao, Q. & Chen, K. P. (2015). Genome-wide identification and analysis of basic helix-loop-helix domains in dog, Canis lupus familiaris. Molecular Genetics and Genomics, 290(2): 633-648. 0950-1

Wang, Y., Chen, K., Yao, Q., Wang, W. & Zhu, Z. (2007). The basic helix-loop-helix transcription factor family in Bombyx mori. Development Genes and Evolution, 217(10): 715-723. 0184-x

Wang, Y., Chen, K., Yao, Q., Zheng, X. & Yang, Z. (2009). Phylogenetic analysis of zebrafish basic helix-loop-helix transcription factors. Journal of Molecular Evolution, 68(6): 629-640. 9232-7

Wei, K. & Chen, H. (2018). Comparative functional genomics analysis of bHLH gene family in rice, maize and wheat. BMC Plant Biology, 18(1): 309.

Yasunami, M., Suzuki, K., Maruyama, H., Kawakami, H., Nagai, Y., Hagiwara, M. & Ohkubo, H. (1996). Molecular Cloning and Characterization of a cDNA Encoding a Novel Basic Helix- Loop- Helix Protein Structurally Related to Neuro-D/BHF1. Biochemical and Biophysical Research Communications, 220(3): 754-758.

Yiğit, M. & Aral, O. (1999). Gökkuşağı alabalığı’nın (Oncorhynchus mykiss W., 1792) tatlısu ve denizsuyundaki büyüme farklılıklarının karşılaştırılması. Turkish Journal of Veterinary and Animal Sciences, 23: 53-59.

Kaynak Göster

  • ISSN: 2147-9666
  • Yayın Aralığı: Yılda 4 Sayı
  • Başlangıç: 2012
  • Yayıncı: Adem Yavuz Sönmez

787 147