Transcriptome profiling of natural dichromatism in the annual fishes Nothobranchius furzeri and Nothobranchius kadleci

BMC Genomics

Alessandro Cellerino²  Matthias Platzer¹  Roberto Ripa²  Marco Groth¹  Enoch Ng’oma¹ 

[1] Leibniz Institute for Age Research – Fritz Lipmann Institute, Beutenbergstraße 11, 07745 Jena, Germany;Neurobiology Laboratory, Scuola Normale Superiore, Pisa, Italy

关键词: Muscle genes;    Erythrophore;    Xanthophore;    Melanin biosynthesis pathway;    Functional Annotation Clustering;    Tail pigmentation;   

Others  :  1140924
DOI  :  10.1186/1471-2164-15-754

 received in 2014-03-02, accepted in 2014-08-26,  发布年份 2014

【 摘 要 】

Background

The annual fish Nothobranchius furzeri is characterized by a natural dichromatism with yellow-tailed and red-tailed male individuals. These differences are due to different distributions of xanthophores and erythrophores in the two morphs. Previous crossing studies have showed that dichromatism in N. furzeri is inherited as a simple Mendelian trait with the yellow morph dominant over the red morph. The causative genetic variation was mapped by linkage analysis in a chromosome region containing the Mc1r locus. However, subsequent mapping showed that Mc1r is most likely not responsible for the color difference in N. furzeri. To gain further insight into the molecular basis of this phenotype, we performed RNA-seq on F2 progeny of a cross between N. furzeri male and N. kadleci female.

Results

We identified 210 differentially-expressed genes between yellow and red fin samples. Functional annotation analysis revealed that genes with higher transcript levels in the yellow morph are enriched for the melanin synthesis pathway indicating that xanthophores are more similar to melanophores than are the erythrophores. Genes with higher expression levels in red-tails included xanthine dehydrogenase (Xdh), coding for a biosynthetic enzyme in the pteridine synthesis pathway, and genes related to muscle contraction. Comparison of DEGs obtained in this study with genes associated with pigmentation in the Midas cichlid (A. citrinellus) reveal similarities like involvement of the melanin biosynthesis pathway, the genes Ptgir, Rasef (RAS and EF-hand domain containing), as well as genes primarily expressed in muscle such as Ttn and Ttnb (titin, titin b).

Conclusions

Regulation of genes in the melanin synthetic pathway is an expected finding and shows that N. furzeri is a genetically-tractable species for studying the genetic basis of natural phenotypic variations. The current list of differentially-expressed genes can be compared with the results of fine-mapping, to reveal the genetic architecture of this natural phenotype. However, an evolutionarily-conserved role of muscle-related genes in tail fin pigmentation is novel finding and interesting perspective for the future.

【 授权许可】

   
2014 Ng’oma et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Elmer KR, Lehtonen TK, Meyer A: Color assortative mating contributes to sympatric divergence of neotropical cichlid fish. Evolution 2009, 63(10):2750-2757.
• [2]Henning F, Jones J, Franchini P, Meyer A: Transcriptomics of morphological color change in polychromatic Midas cichlids. BMC Genomics 2013, 14(1):171. BioMed Central Full Text
• [3]Hollocher H, Hatcher JL, Dyreson EG: Evolution of abdominal pigmentation differences across species in the Drosophila dunni subgroup. Evolution 2000, 54(6):2046-2056.
• [4]Roberts RB, Ser JR, Kocher TD: Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science (New York, NY) 2009, 326(5955):998-1001.
• [5]Greenwood AK, Cech JN, Peichel CL: Molecular and developmental contributions to divergent pigment patterns in marine and freshwater sticklebacks. Evol Dev 2012, 14(4):351-362.
• [6]Gross JB, Borowsky R, Tabin CJ: A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 2009, 5(1):e1000326.
• [7]Hoekstra HE: Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 2006, 97:222-234.
• [8]Hubbard JK, Uy JA, Hauber ME, Hoekstra HE, Safran RJ: Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet 2010, 26(5):231-239.
• [9]O'Quin CT, Drilea AC, Roberts RB, Kocher TD: A Small Number of Genes Underlie Male Pigmentation Traits in Lake Malawi Cichlid Fishes. J Exp Zool B Mol Dev Evol 2012, 318(3):199-208.
• [10]Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ: Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet 2006, 38(1):107-111.
• [11]Braasch I, Schartl M, Volff JN: Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 2007, 7:74. BioMed Central Full Text
• [12]Cheng KC: Skin color in fish and humans: impacts on science and society. Zebrafish 2008, 5(4):237-242.
• [13]Fujii R: The regulation of motile activity in fish chromatophores. Pigment Cell Res 2000, 13(5):300-319.
• [14]Baube CL: Manipulations of signalling environment affect male competitive success in three-spined sticklebacks. Anim Behav 1997, 53(4):819-833.
• [15]Grether GF, Hudon J, Endler JA: Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proc R Soc B 2001, 268(1473):1245-1253.
• [16]Theis A, Salzburger W, Egger B: The Function of Anal Fin Egg-Spots in the Cichlid Fish Astatotilapia burtoni. PLoS One 2012, 7(1):e29878.
• [17]Petzold A, Reichwald K, Groth M, Taudien S, Hartmann N, Priebe S, Shagin D, Englert C, Platzer M: The transcript catalogue of the short-lived fish Nothobranchius furzeri provides insights into age-dependent changes of mRNA levels. BMC Genomics 2013, 14(1):185. BioMed Central Full Text
• [18]Reichard M, Polacik M, Sedlacek O: Distribution, colour polymorphism and habitat use of the African killifish Nothobranchius furzeri, the vertebrate with the shortest life span. J Fish Biol 2009, 74(1):198-212.
• [19]Bartakova V, Reichard M, Janko K, Pola Ik M, Bla Ek R, Reichwald K, Cellerino A, Bryja J: Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evol Biol 2013, 13(1):196. BioMed Central Full Text
• [20]Dorn A, Ng'oma E, Janko K, Reichwald K, Polacik M, Platzer M, Cellerino A, Reichard M: Phylogeny, genetic variability and colour polymorphism of an emerging animal model: the short-lived annual Nothobranchius fishes from southern Mozambique. Mol Phylogen Evol 2011, 61(3):739-749.
• [21]Valenzano DR, Kirschner J, Kamber RA, Zhang E, Weber D, Cellerino A, Englert C, Platzer M, Reichwald K, Brunet A: Mapping loci associated with tail color and sex determination in the short-lived fish Nothobranchius furzeri. Genetics 2009, 183(4):1385-1395.
• [22]Terzibasi E, Valenzano DR, Benedetti M, Roncaglia P, Cattaneo A, Domenici L, Cellerino A: Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS One 2008, 3(12):e3866.
• [23]Murisier F, Beermann F: Genetics of pigment cells: lessons from the tyrosinase gene family. Histol Histopathol 2006, 21(5):567-578.
• [24]Baumgart M, Groth M, Priebe S, Savino A, Testa G, Dix A, Ripa R, Spallotta F, Gaetano C, Ori M, Eva Terzibasi T, Reinhard G, Matthias P, Alessandro C: RNA-seq of the aging brain in the short-lived fish N. furzeri - conserved pathways and novel genes associated with neurogenesis. Aging Cell 2014. doi:10.1111/acel.12257. [Epub ahead of print]
• [25]Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protocols 2008, 4(1):44-57.
• [26]del Marmol V, Beermann F: Tyrosinase and related proteins in mammalian pigmentation. FEBS Lett 1996, 381(3):165-168.
• [27]Cook AL, Smith AG, Smit DJ, Leonard JH, Sturm RA: Co-expression of SOX9 and SOX10 during melanocytic differentiation in vitro. Exp Cell Res 2005, 308(1):222-235.
• [28]Murisier F, Guichard S, Beermann F: The tyrosinase enhancer is activated by Sox10 and Mitf in mouse melanocytes. Pigment Cell Res 2007, 20(3):173-184.
• [29]Lamason RL: SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science (New York, NY) 2005, 310:1782-1786.
• [30]Hammond CL, Hinits Y, Osborn DPS, Minchin JEN, Tettamanti G, Hughes SM: Signals and myogenic regulatory factors restrict Pax3 and Pax7 expression to dermomyotome-like tissue in zebrafish. Dev Biol 2007, 302(2):504-521.
• [31]Minchin JE, Hughes SM: Sequential actions of Pax3 and Pax7 drive xanthophore development in zebrafish neural crest. Dev Biol 2008, 317(2):508-522.
• [32]Medic S, Rizos H, Ziman M: Differential PAX3 functions in normal skin melanocytes and melanoma cells. Biochem Biophys Res Commun 2011, 411(4):832-837.
• [33]Wu X, Bowers B, Rao K, Wei Q, Hammer JA 3rd: Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function In vivo. J Cell Biol 1998, 143(7):1899-1918.
• [34]Wu XS, Masedunskas A, Weigert R, Copeland NG, Jenkins NA, Hammer JA: Melanoregulin regulates a shedding mechanism that drives melanosome transfer from melanocytes to keratinocytes. Proc Natl Acad Sci U S A 2012, 109(31):E2101-E2109.
• [35]Baumgart M, Groth M, Priebe S, Appelt J, Guthke R, Platzer M, Cellerino A: Age-dependent regulation of tumor-related microRNAs in the brain of the annual fish Nothobranchius furzeri. Mech Ageing Dev 2012, 133(5):226-233.
• [36]Robinson MD, Oshlack A: A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11(3):R25. BioMed Central Full Text
• [37]Anders S, Huber W: Differential expression analysis for sequence count data. Genome Biol 2010, 11(10):R106. BioMed Central Full Text
• [38]Benjamini Y, Hochberg Y: Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stati Soc B 1995, 57(1):289-300.
• [39]MGFLI. count_genes_per_transcript.pl. https://github.com/MGFLI/RNAseq/tree/master webcite
• [40]Huang DW, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, Huang Da HC, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R: DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 2007, 35(suppl 2):W169-W175.
• [41]Koia JH, Moyle RL, Botella JR: Microarray analysis of gene expression profiles in ripening pineapple fruits. BMC Plant Biol 2012, 12:240. BioMed Central Full Text
• [42]Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30(9):1-10.