Identification and expression of forkhead box genes in the Chinese giant salamander Andrias davidianus
Qiaomu Hu A , Hanbing Xiao A C , Qilong Wang B , Haifeng Tian A and Yan Meng A
+ Author Affiliations
- Author Affiliations
A Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, Hubei, 430223, China.
B Tengzhou Fisheries Center, Tengzhou, Shandong, 277500, China.
C Corresponding author. Email: xhb@yfi.ac.cn
Reproduction, Fertility and Development 30(4) 634-642 https://doi.org/10.1071/RD17049
Submitted: 8 February 2017 Accepted: 7 September 2017 Published: 26 September 2017
Abstract
In the present study, 21 forkhead box (Fox) genes were identified in Andrias davidianus, including 13 full-length genes and eight partial sequences. Phylogenetic analysis showed that most were conserved in other investigated amphibians, whereas the Foxk1 gene was found exclusively in A. davidianus. Molecular evolution analysis indicated that most Fox genes underwent purifying selection, whereas two sites of the adFoxp4 gene showed positive selection and were located on the adFoxp4 protein surface. Expression profiles of all Fox genes identified were analysed in the hypothalamic–pituitary–gonad axis by reverse transcription–quantitative polymerase chain reaction. Eighteen genes exhibited sexually dimorphic expression (15 ovary-biased and three testis-biased genes), whereas two genes showed no difference between ovary and testis. Further investigation of 12 selected sexually dimorphic Fox genes showed changes in the expression profile of 11 genes in the ovary of larvae reared at high temperatures (28°C). The results of the present study provide information on Fox genes in an amphibian and suggest that they play key roles in sexual development and reproduction in A. davidianus.
Additional keywords: evolution, gene expression.
References
Alam, M. A., Kobayashi, Y., Horiguchi, R., Hirai, T., and Nakamura, M. (2008). Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra. Gen. Comp. Endocrinol. 157, 75–85.| Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtVSnsLo%3D&md5=362b68c4133d3d5a808f96df43ac4d66CAS |
Benayoun, B. A., Caburet, S., and Veitia, R. A. (2011). Forkhead transcription factors: key players in health and disease. Trends Genet. 27, 224–232.
| Forkhead transcription factors: key players in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVaquro%3D&md5=c313e8492f8597af58b280bdf932d7b3CAS |
Boulanger, L., Pannetier, M., Gall, L., Allais-Bonnet, A., Elzaiat, M., Le Bourhis, D., Daniel, N., Richard, C., Cotinot, C., Ghyselinck, N. B., and Pailhoux, E. (2014). FOXL2 is a female sex-determining gene in the goat. Curr. Biol. 24, 404–408.
| FOXL2 is a female sex-determining gene in the goat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1ags74%3D&md5=616eb5d8e2baf132e79a0fdf8a10a5bdCAS |
Carlsson, P., and Mahlapuu, M. (2002). Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250, 1–23.
| Forkhead transcription factors: key players in development and metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVyms70%3D&md5=0325df2185efd7534e9c5c112cf896aaCAS |
Casas-Tinto, S., Gomez-Velazquez, M., Granadino, B., and Fernandez-Funez, P. (2008). FoxK mediates TGF-β signalling during midgut differentiation in flies. J. Cell Biol. 183, 1049–1060.
| FoxK mediates TGF-β signalling during midgut differentiation in flies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCqt7vK&md5=074ef7a8f4f48982cbad280e8eaca82bCAS |
Castrillon, D. H., Miao, L., Kollipara, R., Horner, J. W., and DePinho, R. A. (2003). Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301, 215–218.
| Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsF2ns7g%3D&md5=5276c27908e238d8bddac1e20e2c69d1CAS |
Chi, W., Gao, Y., Hu, Q., Guo, W., and Li, D. P. (2017). Genome-wide analysis of brain and gonad transcripts reveals changes of key sex reversal-related genes expression and signaling pathways in three stages of Monopterus albus. PLoS One 12, e0173974.
| Genome-wide analysis of brain and gonad transcripts reveals changes of key sex reversal-related genes expression and signaling pathways in three stages of Monopterus albus.Crossref | GoogleScholarGoogle Scholar |
DeLano, W. L. (2002). ‘The PyMOL Molecular Graphics System.’ (DeLano Scientific: San Carlos, CA, USA.)
Dong, X. L., Chen, S. L., Ji, X. S., and Shao, C. W. (2011). Molecular cloning, characterization and expression analysis of Sox9a and Foxl2 genes in half-smooth tongue sole (Cynoglossus semilaevis). Acta Oceanol. Sin. 30, 68–77.
| Molecular cloning, characterization and expression analysis of Sox9a and Foxl2 genes in half-smooth tongue sole (Cynoglossus semilaevis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtVCqsbg%3D&md5=d3034fdaf6e8058e19010ad6c927b056CAS |
Dournon, C., and Houillon, C. (1985). Thermosensibilité de la différenciation sexuelle chez l’Amphibien Urodèle, Pleurodeles waltlii Michah. Conditions pour obtenir l’inversion du phénotype sexuel de toutes les femelles génétiques sous l’action de la température d’élevage. Reprod. Nutr. Dev. 25, 671–688.
| Thermosensibilité de la différenciation sexuelle chez l’Amphibien Urodèle, Pleurodeles waltlii Michah. Conditions pour obtenir l’inversion du phénotype sexuel de toutes les femelles génétiques sous l’action de la température d’élevage.Crossref | GoogleScholarGoogle Scholar |
Dournon, C., Guillet, F., Boucher, D., and Lacroix, J. C. (1984). Cytogenetic and genetic evidence of male sexual reversion by heat treatment in the newt Pleurodeles poireti. Chromosoma 90, 261–264.
| Cytogenetic and genetic evidence of male sexual reversion by heat treatment in the newt Pleurodeles poireti.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXitFGktg%3D%3D&md5=b1925ea2d3ec42c9a4eeaa90f83dab1fCAS |
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797.
| 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=d529149e81ff48dec96292a57ffa450cCAS |
Fowler, P. A., Flannigan, S., Mathers, A., Gillanders, K., Lea, R. G., Wood, M. J., Maheshwari, A., Bhattacharya, S., Collie-Duguid, E. S., Baker, P. J., Monteiro, A., and O’Shaughnessy, P. J. (2009). Gene expression analysis of human fetal ovarian primordial follicle formation. J. Clin. Endocrinol. Metab. 94, 1427–1435.
| Gene expression analysis of human fetal ovarian primordial follicle formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksFaiu7s%3D&md5=1c06323846a53900c0bec1d0bf16add0CAS |
Goertz, M. J., Wu, Z., Gallardo, T. D., Hamra, F. K., and Castrillon, D. H. (2011). Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J. Clin. Invest. 121, 3456–3466.
| Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFOhsbnF&md5=a802db7e7cc526ec4feb9804be39284eCAS |
Guo, L. W., Wang, Z. Q., Liu, Q. Q., Zhang, L., and Liang, G. (2013). Morphological study on the postembryonic development of the gonad in the Chinese giant salamander Andrias davidianus. Chinese J. Zool. 48, 457–464.
Hannenhalli, S., and Kaestner, K. H. (2009). The evolution of Fox genes and their role in development and disease. Nat. Rev. Genet. 10, 233–240.
| The evolution of Fox genes and their role in development and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Cku7o%3D&md5=1802352f266bf0cd9bc5b71044c6c78aCAS |
Harris, S. E., Chand, A. L., Winship, I. M., Gersak, K., Aittomäki, K., and Shelling, A. N. (2002). Identification of novel mutations in FOXL2 associated with premature ovarian failure. Mol. Hum. Reprod. 8, 729–733.
| Identification of novel mutations in FOXL2 associated with premature ovarian failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvFOrsbo%3D&md5=6c69b6496fb9531535f1861d392eca8aCAS |
Hosaka, T., Biggs, W. H., Tieu, D., Boyer, A. D., Varki, N. M., Cavenee, W. K., and Arden, K. C. (2004). Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc. Natl Acad. Sci. USA 101, 2975–2980.
| Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitlWhsbk%3D&md5=190971d1b91d8848bd4cbe9ae8ea4b07CAS |
Hu, Q. M., Meng, Y., Tian, H. F., Zhang, Y., and Xiao, H. B. (2016). Sexually dimorphic expression of Foxl2 and Ftz-F1 in Chinese giant salamander Andrias davidianus. J. Exp. Zool. B Mol. Dev. Evol. 326, 363–374.
| Sexually dimorphic expression of Foxl2 and Ftz-F1 in Chinese giant salamander Andrias davidianus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1SjtL%2FI&md5=d0460ae4f6054a09b0bb2302e1c8b5cbCAS |
Hughes, A. L. (1999). Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history. J. Mol. Evol. 48, 565–576.
| Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFGis7o%3D&md5=83bbd8329fcfc2b8241fe661f6202289CAS |
Jackson, B. C., Carpenter, C., Nebert, D. W., and Vasiliou, V. (2010). Update of human and mouse forkhead box (FOX) gene families. Hum. Genomics 4, 345–352.
| 1:CAS:528:DC%2BC3cXhtlGjurnM&md5=991ec34f5b15b38decdb1896c249312aCAS |
Katoh, M., and Katoh, M. (2004). Human FOX gene family. Int. J. Oncol. 25, 1495–1500.
| 1:CAS:528:DC%2BD2cXhtVSktbbK&md5=2de1b4bf6a2b99d618b70e82eac4bc9cCAS |
Katoh, M., Igarashi, M., Fukuda, H., Nakagama, H., and Katoh, M. (2013). Cancer genetics and genomics of human FOX family genes. Cancer Lett. 328, 198–206.
| Cancer genetics and genomics of human FOX family genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1agsLzE&md5=0993eb48d1c05c029fe2b599a02d9be4CAS |
Kunisada, M., Cui, C. Y., Piao, Y., Ko, M. S., and Schlessinger, D. (2009). Requirement for Shh and Fox family genes at different stages in sweat gland development. Hum. Mol. Genet. 18, 1769–1778.
| Requirement for Shh and Fox family genes at different stages in sweat gland development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltV2gsL4%3D&md5=566077a73b6a7acf9e537fadd181f7ffCAS |
Lehmann, O. J., Sowden, J. C., Carlsson, P., Jordan, T., and Bhattacharya, S. S. (2003). Fox’s in development and disease. Trends Genet. 19, 339–344.
| Fox’s in development and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVyqtbg%3D&md5=bfee18a103d291b6317ff21bfa03fc35CAS |
Li, Y., Wang, G. Z., Tian, J., Liu, H. F., Yang, H. P., Yi, Y. Z., Wang, J. H., Shi, X. F., Jiang, F., Yao, B., and Zhang, Z. F. (2012). Transcriptome analysis of the silkworm (Bombyx mori) by high-throughput RNA sequencing. PLoS One 7, e43713.
| Transcriptome analysis of the silkworm (Bombyx mori) by high-throughput RNA sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Khtr3E&md5=c98659136345cf1a875e63a6498f6220CAS |
Li, H. Z., Liu, L. X., Liu, X. L., and Guo, J. S. (2013). Compared study on artificial insemination methods of Andrias davidianus. Guangdong Agric. Sci. 11, 128–129.
Liu, Z., Castrillon, D. H., Zhou, W., and Richards, J. S. (2013). FOXO1/3 depletion in granulosa cells alters follicle growth, death and regulation of pituitary FSH. Mol. Endocrinol. 27, 238–252.
| FOXO1/3 depletion in granulosa cells alters follicle growth, death and regulation of pituitary FSH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOgtbg%3D&md5=82d6d6a31dd6e0c044a2e7aab28fd175CAS |
Pelosi, E., Omari, S., Michel, M., Ding, J., Amano, T., Forabosco, A., Schlessinger, D., and Ottolenghi, C. (2013). Constitutively active Foxo3 in oocytes preserves ovarian reserve in mice. Nat Commun. 4, 1843.
| Constitutively active Foxo3 in oocytes preserves ovarian reserve in mice.Crossref | GoogleScholarGoogle Scholar |
Pohl, B. S., and Knöchel, W. (2004). Isolation and developmental expression of Xenopus FoxJ1 and FoxK1. Dev. Genes Evol. 214, 200–205.
| Isolation and developmental expression of Xenopus FoxJ1 and FoxK1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivFKnu7w%3D&md5=a7966e150dff7840d1ae905691b17ea8CAS |
Pohl, B. S., Rössner, A., and Knöchel, W. (2005). The Fox gene family in Xenopus laevis: FoxI2, FoxM1 and FoxP1 in early development. Int. J. Dev. Biol. 49, 53–58.
| The Fox gene family in Xenopus laevis: FoxI2, FoxM1 and FoxP1 in early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktFans7c%3D&md5=78394cacdeea0670c51483256f6e730cCAS |
Powers, T. R., Virk, S. M., Casilda, T. P., and Serrano, E. E. (2012). Probing the Xenopus laevis inner ear transcriptome for biological function. BMC Genomics 13, 225.
| Probing the Xenopus laevis inner ear transcriptome for biological function.Crossref | GoogleScholarGoogle Scholar |
Qi, Z. C., Zhang, Q. H., Wang, Z. S., Ma, T. Y., Zhou, J. W., Holland, J., and Gao, Q. (2016). Transcriptome analysis of the endangered Chinese giant salamander (Andrias davidianus): immune modulation in response to Aeromonas hydrophila infection. Vet. Immunol. Immunopathol. 169, 85–95.
| Transcriptome analysis of the endangered Chinese giant salamander (Andrias davidianus): immune modulation in response to Aeromonas hydrophila infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFWltLzE&md5=a6132094aaca4e8ba22378d430583714CAS |
Robertson, L. S., and Cornman, R. S. (2014). Transcriptome resources for the frogs Lithobates clamitans and Pseudacris regilla, emphasizing antimicrobial peptides and conserved loci for phylogenetics. Mol. Ecol. Resour. 14, 178–183.
| Transcriptome resources for the frogs Lithobates clamitans and Pseudacris regilla, emphasizing antimicrobial peptides and conserved loci for phylogenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFCjsr3P&md5=d7f36cf5bb32c3257f8ee4d470e364e7CAS |
Roy, A., Kucukural, A., and Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725–738.
| I-TASSER: a unified platform for automated protein structure and function prediction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVahs74%3D&md5=5173cd6c2c8291f87ab57522862becc8CAS |
Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A., and Quackenbush, J. (2006). TM4 microarray software suite. Methods Enzymol. 411, 134–193.
| TM4 microarray software suite.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtV2lt7Y%3D&md5=540f80c6fe190c252b233945be8c8a33CAS |
Shoemaker, C. M., Queen, J., and Crews, D. (2007). Response of candidate sex-determining genes to changes in temperature reveals their involvement in the molecular network underlying temperature-dependent sex determination. Mol. Endocrinol. 21, 2750–2763.
| Response of candidate sex-determining genes to changes in temperature reveals their involvement in the molecular network underlying temperature-dependent sex determination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ynsrfI&md5=d962ca45407f46d6a55ca097efa65aa3CAS |
Song, J., Li, Z., Tong, X., Chen, C., Chen, M., Meng, G., Chen, P., Li, C., Xin, Y., Gai, T., Dai, F., and Lu, C. (2015). Genome-wide identification and characterization of Fox genes in the silkworm, Bombyx mori. Funct. Integr. Genomics 15, 511–522.
| Genome-wide identification and characterization of Fox genes in the silkworm, Bombyx mori.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXms1Kjurg%3D&md5=697966540fbab5d137fca6eaf8aef1c5CAS |
Spring, J. (1997). Vertebrate evolution by interspecific hybridisation – are we polyploid? FEBS Lett. 400, 2–8.
| Vertebrate evolution by interspecific hybridisation – are we polyploid?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFSmsrg%3D&md5=0cfa775dd70cc2a987e2b85792c20596CAS |
Thackray, V. G. (2014). Fox tales: regulation of gonadotropin gene expression by forkhead transcription factors. Mol. Cell. Endocrinol. 385, 62–70.
| Fox tales: regulation of gonadotropin gene expression by forkhead transcription factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Cqt7fP&md5=1260eb679ab97c848bc3ed5ed6671272CAS |
Ting, A. Y., and Zelinski, M. B. (2017). Characterization of FOXO1, 3 and 4 transcription factors in ovaries of fetal, prepubertal and adult rhesus macaques. Biol. Reprod. 96, 1052–1059.
| Characterization of FOXO1, 3 and 4 transcription factors in ovaries of fetal, prepubertal and adult rhesus macaques.Crossref | GoogleScholarGoogle Scholar |
Uchida, T. (1937). Studies on the sexuality of Amphibia. II. Sexual induction in a sexually semi-differentiated salamander. J. Fac. Sci. Hokkaido. Imp. Univ. (Zool) 6, 35–58.
Uhlenhaut, N. H., and Treier, M. (2011). Forkhead transcription factors in ovarian function. Reproduction 142, 489–495.
| Forkhead transcription factors in ovarian function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlyitb%2FN&md5=dd6dfc647073f1982bbb3fb0b733e7caCAS |
Uhlenhaut, N. H., Jakob, S., Anlag, K., Eisenberger, T., Sekido, R., Kress, J., Treier, A. C., Klugmann, C., Klasen, C., Holter, N. I., Riethmacher, D., Schütz, G., Cooney, A. J., Lovell-Badge, R., and Treier, M. (2009). Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139, 1130–1142.
| Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslartrs%3D&md5=a9322460faf62914f624de40267f5b44CAS |
Virant-Klun, I., Knez, K., Tomazevic, T., and Skutella, T. (2013). Gene expression profiling of human oocytes developed and matured in vivo or in vitro. BioMed Res. Int. 2013, 879489.
| Gene expression profiling of human oocytes developed and matured in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar |
Wallace, H. (1987). Abortive development in the crested newt Triturus cristatus. Development 100, 65–72.
Wallace, H., and Wallace, B. M. N. (2000). Sex reversal of the newt Triturus cristatus reared at extreme temperatures. Int. J. Dev. Biol. 44, 807–810.
| 1:STN:280:DC%2BD3M7ivVGgtg%3D%3D&md5=f25d64020f41caabbf326156e2c077f7CAS |
Witschi, E. (1929). Studies on sex differentiation and sex determination in amphibians. III. Rudimentary hermaphroditism and Y chromosome in Rana temporaria. J. Exp. Zool. 54, 157–223.
| Studies on sex differentiation and sex determination in amphibians. III. Rudimentary hermaphroditism and Y chromosome in Rana temporaria.Crossref | GoogleScholarGoogle Scholar |
Xiao, H. B., Liu, J. Y., Yang, Y. Q., and Lin, X. Z. (2006). Artificial propagation of tank-cultured Chinese giant salamander Andrias davidianus. Acta Hydrobiol. Sin. 30, 530–534.
Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591.
| PAML 4: phylogenetic analysis by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrs7c%3D&md5=a10b9c3dd759cfdf5334eef34c0d7150CAS |
Yang, Z., Nielsen, R., Goldman, N., and Pedersen, A. M. (2000). Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431–449.
| 1:CAS:528:DC%2BD3cXjslKhtb4%3D&md5=33be9340a0428fdf2179be1b6fd9244dCAS |
Yang, H., Lan, Q. J., Liu, R. R., Cui, D., Liu, H. X., Xiong, D. M., Li, F. G., Liu, X. L., and Wang, L. X. (2017). Characterization of galectin-1 from Chinese giant salamanders Andrias davidianus and its involvements during immune response. Dev. Comp. Immunol. 70, 59–68.
| Characterization of galectin-1 from Chinese giant salamanders Andrias davidianus and its involvements during immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhtlClsrk%3D&md5=cb2f3a2651f56fae2a06fd84b5bbf62dCAS |
Yuan, J., Tao, W. J., Cheng, Y. Y., Huang, B. F., and Wang, D. S. (2014). Genome-wide identification, phylogeny, and gonadal expression of Fox genes in Nile tilapia, Oreochromis niloticus. Fish Physiol. Biochem. 40, 1239–1252.
| 1:CAS:528:DC%2BC2cXisFWnt78%3D&md5=79b2b520568a423f3046d1375a83ef87CAS |
Zhou, Z. Y., Geng, Y., Liu, X. X., Ren, S. Y., Zhou, Y., Wang, K. Y., Huang, X. L., Chen, D. F., Peng, X., and Lai, W. M. (2013). Characterization of a ranavirus isolated from the Chinese giant salamander (Andrias davidianus, Blanchard, 1871) in China. Aquaculture 384–387, 66–73.
| Characterization of a ranavirus isolated from the Chinese giant salamander (Andrias davidianus, Blanchard, 1871) in China.Crossref | GoogleScholarGoogle Scholar |
