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Siniperca Chuatsi) Growth Hormone Gene Polymorphisms and Growth Traits Journal of Genetics (2019) 98:58 © Indian Academy of Sciences https://doi.org/10.1007/s12041-019-1100-7 RESEARCH ARTICLE Correlation analysis of mandarin fish (Siniperca chuatsi) growth hormone gene polymorphisms and growth traits CHENG-FEI SUN1,2, HAI-LIN SUN1,2, JUN-JIAN DONG1, YUAN-YUAN TIAN1,JIEHU1 and XING YE1,2∗ 1Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou 510380, People’s Republic of China 2College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, People’s Republic of China *For correspondence. E-mail: [email protected]. Received 1 July 2018; revised 4 December 2018; accepted 30 January 2019; published online 3 June 2019 Abstract. Screening of trait-associated molecular markers can be used to enhance the efficiency of selective breeding. Previously, we produced the first high-density genetic linkage map for the mandarin fish (Siniperca chuatsi) and identified 11 quantitative-trait loci significantly associated with growth, of which one is located within the growth hormone (GH) gene. To investigate the GH gene polymorphisms and their correlation with growth, the complete sequence was cloned and 32 single-nucleotide polymorphisms (SNPs) and one simple-sequence repeat (SSR) were identified. Of which, eight SNPs (G1–G8) and the SSR (GH-AG) were selected for genotyping and correlation analysis with growth traits in a random population. The results showed that the four novel polymorphic loci (G1, G2, G3 and GH-AG) were significantly correlated with growth traits of mandarin fish (P < 0.05). Of these, G1, G3 and GH-AG showed highly significant correlations with multiple growth traits (P < 0.01) and the combined SNP analysis showed that G1–G3 formed four effective diplotypes (D1–D4), among which D1 was highly significantly greater than D4 (P < 0.01) for some important growth traits. In conclusion, our results show that the four polymorphic loci G1–G3 and GH-AG within the mandarin fish GH gene are significantly correlated with growth traits and could be used as candidate molecular markers for selective breeding of superior varieties of mandarin fish. Keywords. growth hormone; polymorphism; growth trait; Siniperca chuatsi. Introduction relevant molecular markers for use in the process of trait improvement in mandarin fish. The mandarin fish (Siniperca chuatsi) belongs to the fam- Growth hormone (GH) is a single-chain polypeptide ily Serranidae and order Perciformes. It grows rapidly, that is synthesized and secreted by the anterior pituitary is delicious and has a high market value, it is now gland. GHs have a wide range of physiological regulatory an important superior freshwater aquaculture fish in functions, as they can regulate the metabolism of three China, with an annual production of 300,000 t (Sun major substances (sugars, lipids and proteins), and their et al. 2015a, b). However, for a long period of time, dur- primary effect on animals is to significantly increase the ing the artificial breeding of this fish there was lack of growth rate, promote the growth of muscles and bones, scientific selective breeding and management. This has and decrease the fat content, thereby affecting the growth resulted in decreased growth rates and disease resistance, and development (Sweeney 2002; Reinecke et al. 2005). which severely affect breeding benefits, quality and safety. Mutations in the GH gene can result in deficiency of GHs, Therefore, there is a need to carry out screening of which is manifested as dwarfism in humans (Kamijo et al. 1999; Fofanova et al. 2003). In animals, GH gene poly- morphism is often associated with growth or production Cheng-Fei Sun and Hai-Lin Sun contributed equally to this work. performance (Hua et al. 2009; Wu et al. 2012; Cheng et al. Electronic supplementary material: The online version of this article (https://doi.org/10.1007/s12041-019-1100-7) contains supplemen- tary material, which is available to authorized users. 1 58 Page 2 of 10 Cheng-Fei Sun et al. 2016). GHs have significant growth-promoting effects in G > fish, as they can promote protein synthesis, decrease fat content and accelerate the longitudinal growth of bones GH-AG (Chatakondi et al. 1995; Forsyth and Wallis 2002). In g.2558C addition, they can also promote food conversion effi- ciency and sexual maturity (Cavari et al. 1993; Tsai et al. 1994). GH gene transfer in fishes such as Carassius auratus C C G G > > (Zhu et al. 1985), Oreochromis niloticus (Brem et al. 1988), > > Cyprinus carpio (Zhang et al. 1990) and Salmo salar (Fletcher et al. 2005) has exhibited significant growth- promoting effects. Of these fishes, GH transgenic salmon has already been approved for human consumption in the US and Canada, and was first sold openly in Canada in August 2017 (Waltz 2017). The importance of the GH A g.2521A T g.3412G T g.4642A C g.1169A > > > gene means that it has become an important target gene > for the selective breeding of growth traits. GH gene poly- morphism studies have been carried out in many types of fishes, which has resulted in the identification of molecu- g.3307C lar markers that are significantly associated with growth traits in fishes such as Cynoglossus semilaevis(Zhaoet al. A C g.2519G 2014), Pelteobagrus fulvidraco (Li et al. 2016), Oreochromis G g.4582C C g.980A > > > niloticus (Jaser et al. 2017) and Cyprinus carpio (Liu et al. > 2017). In recent years, there have been two studies on the g.3262G correlation between the GH gene and growth in man- darin fish. In the first study, Tian et al. (2014) employed direct sequencing of the 4th and 5th introns and 5th T g.4564A A T g.2294T G g.742T exon of the GH gene in mandarin fish; they identi- G > > > > fied four single-nucleotide polymorphisms (SNPs) and > found three were significantly associated with growth. In the other study, Wang et al. (2016) performed high- g.340T resolution melting curve analysis of the 5th exon and intron of the mandarin fish GH and found that two SNPs showed significant correlation with growth traits. In a T T g.2228C A g.3004G G g.4200A A G g.738C > previous study, members of our laboratory used ddRAD- > > > > > sequencing technology to establish the first genetic linkage Siniperca chuatsi. map for mandarin fish and detected 11 quantitative trait g.197C g.4948A g.2846C loci (QTLs) that were significantly associated with growth g.3834A traits. Among these markers, r_23000 was associated with gene of the increase in the total body length. It was located at GH 56.141 cM of LG16, and correspondingly contributed C C G G G A g.2170C G g.724A A > > > > > > > to 14.1% of the phenotypic variation (Sun et al. 2017) > (table 1 in electronic supplementary material at http:// www.ias.ac.in/jgenet/). Further analysis revealed that it lies g.5045T g.4940A g.5234T g.2146T g.2643C in the second intron of the GH gene, and we hypoth- g.3665A esize that there may be more loci in the GH gene of mandarin fish that are intimately associated with growth traits. Therefore, there is a need for further mining of GH gene polymorphisms. In this study, we employed direct sequencing to screen for polymorphic loci in the complete GH gene sequence of mandarin fish. We then randomly selected 200 individuals in a selective breed- ing population for growth correlation analysis to obtain The locations of polymorphic loci in the additional molecular markers that are associated with growth for application in the selective breeding of man- Table 1. LocationIntron 1 Number 3The bold loci are selected for correlation analysis g.107T of growth traits. SNPs and SSR Exon 5 1 Intron 2 20 g.719A Intron 4Intron 5 2 1 darin fish. Intron 3 6 Correlation analysis of S. chuatsi growth hormone gene polymorphisms and growth traits Page 3 of 10 58 Materials and methods H2O, 14 μL; upstream and downstream primers (10 μM), 2 μL each and template DNA (500 ng/μL), 2 μL. PCR Experimental animals and genomic DNA extraction amplification conditions were as follows: predenaturation at 94◦C for 3 min, followed by 35 cycles of denatu- Fishes for this study were obtained from Yushun Animal ration at 95◦C for 30 s, annealing at 55◦Cfor30s, Husbandry and Fishery Science and Technology Service extension at 72◦C for 60 s, and a final extension step at (Qingyuan, Guangdong, China) by artificial breeding and 72◦C for 10 min, before being stored at 4◦C. Agarose gel culturing. The broodstock of experimental fishes were (1%) electrophoresis was used to examine the PCR prod- imported from Guangdong, Anhui and Hunan province ucts. to establish the F0 generation. After breeding and incu- Single PCR amplification products were sent for bating, the fingerings of F1 were cultivated to 10 cm sequencing by Ige Biotechnology, Ltd (Guangzhou, in total length, then were labelled with electronic tags China). PCR products with nonspecific bands were gel in abdomen and released into the same pond for cul- extracted and purified before sequencing. Referring to turing. Having cultured for five months, the fishes were Ozteti’s means of sequences analysis (Oztetik et al. 2015), harvested in December of the same year and scanned the BioEdit software was used for alignment and analy- to record their individual number and their correspond- sis of the sequencing results to select for SNP and simple ing growth traits (body weight, total length, body length, sequence repeat (SSR) loci in the various fragments of the head length, body height, caudal peduncle height and GH gene. eye diameter).
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