Selection breeding program of Nan'ao Golden Scallop Chlamys nobilis with higher nutritional values and less susceptible to stress

Journal Pre-proof Selection breeding program of Nan'ao Golden Scallop Chlamys nobilis with higher nutritional values and less susceptible to stress

Tan Kar Soon, Huankong Zhang, Leongseng Lim, Huaiping Zheng PII:

S0044-8486(19)32585-2

DOI:

https://doi.org/10.1016/j.aquaculture.2019.734769

Reference:

AQUA 734769

To appear in:

aquaculture

Received date:

1 October 2019

Revised date:

22 November 2019

Accepted date:

22 November 2019

Please cite this article as: T.K. Soon, H. Zhang, L. Lim, et al., Selection breeding program of Nan'ao Golden Scallop Chlamys nobilis with higher nutritional values and less susceptible to stress, aquaculture (2019), https://doi.org/10.1016/ j.aquaculture.2019.734769

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© 2019 Published by Elsevier.

Journal Pre-proof Selection breeding program of Nan'ao Golden Scallop Chlamys nobilis with higher nutritional values and less susceptible to stress

Running title: Selection breeding program of Nan'ao Golden Scallop

Tan Kar Soona,b,c, Huankong Zhanga,b,c, Leongseng Limd, Huaiping Zhenga,b,c*

Key Laboratory of Marine Biotechnology of Guangdong Province, Shantou

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a

Mariculture Research Center for Subtropical Shellfish & Algae of Guangdong

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Province, Shantou 515063, China

STU-UMT Joint Shellfish Research Laboratory, Shantou University, Shantou

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515063, China

Borneo Marine Research Institute, University Malaysia Sabah, 88400, Malaysia

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d

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b

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University, Shantou, 515063, China

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* All correspondence should be addressed to Dr. Huaiping Zheng Tel: 0086-754-82903285

Fax: 0086-754-86500416

E-mail address: [email protected]

Journal Pre-proof Abstract The Nan'ao Golden Scallop discussed in this paper is a new breed of noble scallop, Chlamys nobilis, produced by four generations of genetic breeding selections and two generations of culture demonstrations. Performed for the first time at Shantou University, the genetic breeding program was motivated by the need to reduce vulnerability and improve the adaptive capacity of noble scallops to the dynamic

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environment. This paper reviews the scientific evidences on aquaculture advantages

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of Nan'ao Golden Scallop, and identifies gaps in knowledge that require further research. From the analysis of published data, it is obvious that Nan'ao Golden

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Scallop is more nutritious and less susceptible to stress than common brown scallops.

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The high TCC of Nan'ao Golden Scallop up-regulate the expression of various

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immune related genes under stressful conditions. Since molluscs do not possess specific immunity, the information in this paper is very useful for improving the

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aquaculture performance of molluscs by selective breeding techniques.

immunity

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Keywords: Chlamys nobilis; Polymorphism; Nan'ao Golden Scallop; Carotenoids;

Journal Pre-proof 1. Introduction The noble scallop Chlamys nobilis, an important edible marine bivalve, belongs to the Pectinidae family. It is naturally distributed in the coastal waters of Japan, Korea, Indonesia, Vietnam and the Southern Sea of China including the waters of Guangdong, Guangxi and Hainan Provinces (Figure 1) (Wang et al., 1998). Noble scallops exhibit polymorphism in the shell color, including orange, yellow, orange-

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purple, purple and brown (Figure 2). The orange and purple shell noble scallops

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usually occur at a much lower frequency of 8.9% and 4.5%, respectively, while the orange-purple and brown shells have a higher occurrence of 53.9% and 32.7%,

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respectively (Zheng et al., 2012ab). In addition to shell color, orange scallops also

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exhibit polymorphism in muscle color, including white and orange colors (Figure 3)

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(Zheng et al., 2010). The occurrence of orange shell and orange muscle scallops is

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extremely low (0.1 to 0.3%) (Zheng et al., 2012b). Since the 1980s, noble scallop aquaculture has developed into a large-scale

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industry in China due to its obvious advantages of fast growth, short cultivation period, high profit, good taste and nutritive (Guo et al., 1999; Zheng et al., 2012b; Tan et al., 2019a). Unlike fish and shrimp aquaculture, bivalve farming is a self-regulating aquaculture that does not require additional feed (environmental friendly) and requires only minimal maintenance (Tan and Ransangan, 2016ab; Tan et al., 2019b). Therefore, the commercial scale noble scallop farming has been extensively carried out (6000-arces farming areas) along the South coast of China, including the Sanya area of Hainan province, Zhanjiang, Shenzhen, Shanwei, and Nan'ao island in Guangdong province, as well as in Dongshan, Zhangpu, Longhai, and Putian in Fujian province (Lan et al., 2018), with an annual production of about 0.1 million tonnes. To date, mollusc aquaculture accounted for 21.42% (17.14 million tonnes) of total

Journal Pre-proof aquaculture production, with Asia, mainly China, being the largest contributor (92.27%) (FAO, 2018). Mollusc aquaculture, especially bivalves farming provides significant social and economic benefits to coastal communities in Asia by providing affordable sources of animal proteins (Tan and Ransangan, 2016c; Tan et al., 2019cd). Unfortunately, cultured noble scallops have often suffered from large-scale mortalities in the past two decades (Huang, 2000; Zhou et al., 2006; Tan and Zheng,

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2019ab; Tan and Zheng, 2019b). In February 1998, the first mass mortality outbreak

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of noble scallops was documented (Huang, 2000), where almost complete mortality (100%) was recorded at about 1000-arce culture areas in Dongshan with an estimated

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loss of more than 50 million RMB (>7.5 million USD) (Zhou et al., 2006). Since then,

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the mass mortalities of noble scallops have occurred almost annually. In early 2010,

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another terrible mass mortality outbreak occurred in Nan'ao and Dongshan, wiped up the entire noble scallop population with a shell length of more than 4 cm (in-house

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laboratory recorded data).

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Invertebrates do not possess acquired immunity equivalent to that of vertebrates, and their defense mechanisms rely exclusively on innate immunity. Therefore, infectious diseases pose a serious threat to the sustainability of bivalve aquaculture. Treatment of bivalve stocks with antibiotics is not recommended due to concerns about the impact to environment and health of consumers resulting from eating bivalves containing residues of antibiotics or other harmful chemicals. Studying animal immune defense mechanisms is hence important for developing disease control strategies (Gross et al. 2001), as the inbuilt disease resistance can contribute greatly to the full cycle aquaculture of bivalves. Therefore, higher natural disease resistance and stronger natural environmental tolerance are qualities that have

Journal Pre-proof great aquaculture advantages, and considered more practical measures in adapting bivalve aquaculture to unfavourable environment. Nan'ao Golden Scallop has been the subject of intense investigations. There is a great deal of understanding of its unique features, especially those of aquaculture advantages. Notable findings particularly those related to disease resistance and environmental tolerance are elaborated in this paper. For the sake of clarity, we will

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first elaborate on the genetic breeding selection for this species. The Nan'ao Golden

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Scallop and common noble scallops (mainly brown scallops) described in this paper belongs to the same species and are cultivated under the same environment (Nan’ao

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Island, Guangdong Province, China). The only significant difference is that the

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Nan'ao Golden Scallop contains much higher TCC and long-chain polyunsaturated

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fatty acids content than the common noble scallops.

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2. Genetic breeding

In order to investigate the inheritance of shell colors of polymorphic C. nobilis, our laboratory (Key Laboratory of Marine Biotechnology of Guangdong Province, Shantou University, China) has initiated a genetic breeding program for noble scallops in 2008. Cultured polymorphic C. nobilis with different shell colors (golden (G), orange-purple (C), purple (P) and brown (B)) from the Nan’ao Marine Biology Experimental Station of Shantou University, China were crossbreed in the spring 2008, producing twenty two F1 families (Table 1), including eight G♀ × G♂, five C♀ × C♂, six B♀

B♂ and three P♀ × B♂ (Zheng et al., 2012b). Zheng et al. (2012b)

found that the shell color of C. nobilis is inheritable and genetically controlled by the interaction of one pair of non-allelic genes. The phenotypic ratio of 3:1 detected in

Journal Pre-proof G♀ × G♂ 1, 2, 3 and 5 families and all C♀ × C♂ families indicating that golden color is the dominant allele toward orange-purple and purple colors, while orange-purple color may mask the effect of the locus controlling brown color. The phenotypic ratio of 1:1 and 1:0 detected in all P♀× B♂ and B♀ × B♂ families indicating that purple color is dominant toward brown color, and brown color was recessive allele toward all colors. In addition, one-locus-three-allele model was proposed to explain the genotypes of G♀ x G♂ 4, 6, 7 and 8 families, where golden color is dominant allele

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and may mask the effect of the locus controlling orange-purple, purple and brown

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colors. More importantly, the orange color of golden scallop tissues (mantle and

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adductor muscles) is also inheritable (Zheng et al., 2012a).

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Subsequently, F2, F3 and F4 were produced in the spring 2009, 2010 and 2011,

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respectively, by mass-mating (mass selection technique) of about 100 male and 500 female scallops from F1, F2 and F3 strains, respectively. After four generations of

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selection and two generations of aquaculture demonstrations, a new variety named

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“Nan'ao Golden Scallop” (ID: GS-01-009-2014) was bred and authorized in 2015 by the National Aquatic Protospecies and Improved Variety Approval Committee of China. Since then, the Nan'ao Golden Scallop has been widely cultivated in Sanya of Hainan province, Zhanjiang, Shenzhen, Shanwei and Nan'ao of Guangdong province, as well as Dongshan, Zhangpu and Longhai of Fujian province (Lan et al., 2018). It is worth noting that the total long-chain polyunsaturated fatty acids content (Liu et al., 2012) and total carotenoid content (Liu, 2011) in orange scallops can be improved by selective breeding. The TCC and lipid composition of F4 Nan’ao Golden Scallop and common brown scallop were compared. The results demonstrated that Nan'ao Golden Scallop contained much high concentrations of TCC (60 to 120 µg/g) than common brown scallops (38 to 58 µg/g) (Zheng et al., 2012ab). Carotenoids

Journal Pre-proof have received much attention for their potential used in biotechnological, human healthcare, food processing and pharmaceuticals applications (Zhang et al., 2014; Fiedor and Burda, 2014). Moreover, the LC-PUFA content of Nan'ao Golden Scallop was significantly higher than that of common noble scallops (30% and 20% LCPUFA in Nan'ao Golden Scallop and brown scallops, respectively) (Liu et al., 2012). Consumption of foods rich in n-3 LC-PUFA is associated with various beneficial effects on human health, including reducing inflammation (Yates et al., 2014),

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preventing cancer (Sawada et al., 2012), lowering risk of Crohn’s disease (Uchiyama

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et al., 2010), improving glucose homeostasis and insulin sensitivity (Das, 1999), and

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regulating chemotaxis of immune cells (Sperling et al., 1993).

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3. Difference in colors of polymorphic noble scallops

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As emphasized in the introduction, noble scallops not only display polymorphism in shell color, but also exhibit polymorphism in tissues color (Zheng et al., 2012ab). The

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coloration of noble scallops is caused by pigments called carotenoids (Zheng et al., 2012a), which also plays an important role in the pigmentation of a wide variety of aquatic organisms (Maoka, 2011). Zheng et al. (2010) compared the total carotenoid content (TCC) in tissues of male and female, golden and brown C. nobilis from the same farm (Nan’ao Marine Biology Experimental Station of Shantou University, China). The results show that the TCC in C. nobilis ranging from 0.73 to 59.85 µg/g, depending on gender and shell color, with female gonads contain significantly higher TCC than male gonads and golden scallops contain significantly higher TCC than brown scallops in all tissues (Table 2), with decreasing order of TCC concentration in tissues of gonad (15.7 to 59.9 µg/ g versus 3.6 to 26.6 µg/ g; golden scallop versus

Journal Pre-proof brown scallops) > mantle (16.2 to 16.5 µg/ g versus 3.0 to 6.9 µg/ g; golden scallop versus brown scallops) > adductor (10.0 to 15.6 µg/ g versus 0.7 to 3.0 µg/ g; golden scallop versus brown scallops) > gills (7.7 to 10.0 µg/ g versus 2.0 to 2.7 µg/ g; golden scallop versus brown scallops) (Zheng et al., 2010). Zheng (2012a) studied the transportation of TCC in C. nobilis by analyzing the TCC and TLC content in tissues (adductor, mantle and gonads) of male and female C. nobilis with matured and developing (gametocytogenesis) gonads. The findings of Zheng (2012a) revealed that

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accumulate in gonads during gonad maturation.

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the TCC and TLC are transferred from adductor and mantle and selectively

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In aquatic ecosystems, carotenoids are mainly produced by aquatic plants,

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microalgae and some bacteria. Since animals cannot synthesize carotenoids de novo,

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they must therefore be acquired from the diet. It is worth noting that although the golden and brown noble scallops are cultivated at the same farm and share the same

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food source, they still exhibit different shell colors, indicating that the display

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polymorphisms of the shell and tissue color are partly controlled by genes (Zheng et al., 2012ab). In animals, the carotenoid accumulation is controlled by the underlying genetic mechanisms, in which genes encoding appropriate carotenoid-binding and transport proteins or enzymes participating carotenoid metabolism are involved, and therefore certain carotenoid might be preferentially deposited and dietary carotenoids are enzymatically converted into other derived forms (Maoka, 2009). To identify the candidate genes responsible for the different colors of polymorphic noble scallops, Liu et al. (2015) performed transcriptome analysis on F2 golden and brown scallops. A number of 20 golden and 20 brown F2 scallops at 14 months old were randomly collected to extract tissues (gonads, mantle, adductor and gills) for 454 GS-FLX sequencing. A remarkable finding in the transcriptome analysis was a class B

Journal Pre-proof scavenge receptor, designed SRB-like-3 was found to express only in orange scallops but not in brown scallops (Liu et al., 2015). The SRB has been reported to play an important role in the uptake of lutein (Reboul et al., 2005), carotene (van Bennekum et al., 2005), zeaxanthin and xanthophylls (During et al., 2008), and lycopene (Moussa et al., 2008). In golden scallops, down-regulation of SRB-like-3 mRNA has been shown to suppress the levels of blood carotenoid, suggesting that SRB-like-3 gene regulates carotenoid deposition and could responsible for the golden coloration

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in golden scallops (Liu et al., 2015).

4. Performance of Nan’ao Golden Scallop and common brown scallops

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under challenge tests

It is worth emphasizing that in all mass mortality episodes, the survival rate of the

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new variety of noble scallops (Nan’ao Golden Scallop) was significantly higher (86% to 92%) than that of common brown scallops (63% to 69%). It indicates that the

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Nan’ao Golden Scallop is less susceptible to the surrounding environment than the brown scallops (Zheng et al., 2015). These observations were consistent with the challenge tests results of low salinity (Wang et al., 2019), low temperature (Tan et al., 2019e) and high temperature (unpublished data) in the laboratory (Table 3). MDA is an important indicator of membrane system damage and cellular metabolism deterioration (Fan et al., 2012). Wang et al. (2019) revealed that under ambient salinity (30 psu), the MDA content of Nan’ao Golden Scallop and brown scallops was similar. However, under low salinity condition (20 psu), the MDA level of brown scallops (8.1± 0.2 nmol/ ml) was significantly higher than of Nan’ao Golden Scallop (6.0± 0.3 nmol/ ml), indicating that the Nan’ao Golden Scallop is less susceptible to

Journal Pre-proof low salinity. Similar observations were observed at lower temperatures, where the MDA content between Nan’ao Golden Scallops and brown scallops was not statistically significant at 20 ˚C, but the MDA content of brown scallops increased at a much higher rate compare to Nan’ao Golden Scallops at lower temperatures (15 ˚C, 12 ˚C and 10 ˚C) (Tan et al., 2019f). After exposure to high temperature (32 ˚C) for 36 h, the survival rate of

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Nan'ao Golden Scallops was 40 to 90% higher than that of brown scallop, in which

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the Nan'ao Golden Scallops have been demonstrated to up-regulate their mRNA expression levels of Heat shock protein 90 (HSP90) by 1.2 to 2.0 times higher than

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that of brown scallops. Heat shock proteins (HSPs) comprise a group of highly

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conserved proteins that are widely found in prokaryotes and eukaryotes. They have

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biological functions, including improving the tolerance of organisms to stimuli and maintaining cellular cell homeostasis (Wang et al., 2017). HSP90 synthesis induced

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by external stress has previously been reported in various mollusks, such as Chlamys

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farreri (Gao et al., 2007), Argopecten irradians (Gao et al., 2008), Crassostrea gigas (Choi et al., 2008), Haliotis discus hannai (Zhang et al., 2011), Hyriopsis cumingii (Wang et al., 2017).

5. Gene expression related to immune response Intensive studies on immunity of noble scallop were motivated by the high mortality of noble scallops. Under stress conditions, the high TCC of the Nan’ao Golden Scallop has been shown to up-regulate the expression levels of several immunerelated genes, including superoxide dismutase (CuZnSOD) (Han et al., 2016), Toll-

Journal Pre-proof like receptor (TLR-1) (Lu et al., 2016), Vitellogenin (Vg) (Zhang et al., 2016) and thioredoxin-like protein (TRX) gene (Zhang et al., 2018a). 5.1 CuZnSOD A number of 224 sexually matured F4 female Nan’ao Golden Scallop and brown scallops with full gonads were randomly collected and subjected to an acute cold stress experiment (8 ˚C) for 36 h. Han et al. (2016) revealed that acute cold stress

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induced the up-regulation of CuZnSOD gene in gills and mantle of Nan’ao Golden

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Scallop and brown scallops, and the expression of CuZnSOD gene in Nan’ao Golden

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Scallop was significantly higher than that of brown scallops, suggesting that the high TCC in Nan’ao Golden Scallop can further enhance the expression of CuZnSOD gene

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under acute cold stress. 5.2 Toll-like receptors

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Toll-like receptors are important downstream signaling components of pro-

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inflammatory cytokines, including interleukins, interferonS, and TNF, which are responsible for immediate innate responses and trigger adaptive immune cells (Yamamoto and Akirz, 2005). A number of 300 F4 Nan’ao Golden Scallop and brown scallops (150 individuals each) at 12 months age were randomly collected for pathogenic challenges. Under normal conditions, the relative expression of Toll-LikeReceptor 1 (TLR-1) between Nan’ao Golden Scallop and brown scallops was statistically

insignificant,

but

was

up-regulated

under

exposure

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V.

parahaemolyticus, LPS and Poly I:C challenge, indicating the TLR-1 gene involved in anti-bacterial and anti-fungal immune defenses (Lu et al., 2016). The TLR-1 transcripts in tissues of C. nobilis was in the decreasing order of mantle > hemocytes > gills > gonads > kidney > intestines > hepatopancreas > adductor.

Journal Pre-proof 5.3 Vitellogenin (Vg) Vitellogenin (Vg) is a precursor of vitellin (Vn) in egg yolk and expressed in the females of nearly all oviparous species (Robinson, 2008). In many oviparous animals, including bivalves, Vg has been shown to play an important role in host immunity against bacteria and viruses (Wu et al., 2015). To study the effect of TCC on Vg gene expression during pathogenic stress, we challenged 16 months old of F4 Nan’ao

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Golden Scallop and brown scallops with V. anguillarum. The results revealed that the

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relative expression of Vg gene of Nan’ao Golden Scallop was 2 and 2.5 times higher than that of brown scallops at control and V. anguillarum challenge, respectively,

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indicating that carotenoids could up-regulate the expression of Vg gene under

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pathogens stress (Zhang et al., 2016).

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5.4 Thioredoxin-like protein (TRX) gene

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TRXs are the major cellular protein disulphide reductase in the thioredoxin system (Arnér and Holmgren, 2000). A number of 200 F6 golden and brown scallops (100

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individuals each) at 12 months age were randomly collected for V. parahaemolyticus challenge. Under normal conditions, the relative expression of TRX between Nan’ao Golden Scallop and brown scallops was not statistically significant, but it was upregulated under exposure to V. parahaemolyticus (Zhang et al., 2018a). The TLR-1 transcript in tissues of C. nobilis were in the decreasing order of hemocytes > gonads > intestines > hepatopancreas > gills > kidney > mantle > adductor (Zhang et al., 2018a).

6. Conclusions

Journal Pre-proof The high natural antioxidants in the Nan'ao Golden Scallop are indeed beneficial traits for adapting aquaculture to dynamic environment. Important areas for future research on Nan'ao Golden Scallop include improving survival in early larval stages and identifying more beneficial traits to address the complexities of climate change related issues. Since invertebrates do not possess specific immunity, the information in this paper is very useful as a guide for improving the aquaculture performance of molluscs by selective breeding techniques. It is highly recommended to embark more similar

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studies for other aquaculture important mollusc species, especially those species with

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longer generation times, as their ability to acclimate and adapt to changing ocean

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Acknowledgement

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conditions may be reduced.

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Present study was financially supported by the National Natural Science Foundation of China (31872563), National Key R&D Program of China (2018YFD0901400),

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China Modern Agro-industry Technology Research System (CARS-49), Department of Education of Guangdong Province, China (2017KCXTD014), Youth Innovation Talents Project of Colleges and Universities in Guangdong Province (18219443) and Talented Young Scientist Program (MALAYSIA-19-002).

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Figure 1: Natural distribution of noble scallop Chlamys nobilis (Adapted from Lan et al.,

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2018)

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A

B

C

f o

D

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E

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Figure 2: polymorphic noble scallop Chlamys nobilis in shells colours.

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A= Orange / Golden B= Yellow C= orange-purple D= Purple E= Brown

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Adductor

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Figure 3: polymorphic noble scallop Chlamys nobilis in muscle colours. Left= golden

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colour adductor and mantle; Right= white colour adductor and mantle

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Journal Pre-proof Table 1. Phenotypes of F1 shell color from selected polymorphic noble scallops (Adopted from Zheng et al., 2010) Total 410 66 248 308 162 141 494 916 101 348 213 86 31 100 100 20 8400 4000 2200 125 103 59

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B 0 0 0 0 0 29 108 241 25 86 48 22 7 100 100 20 8400 4000 2200 61 52 30

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P 0 0 0 29 39 0 0 0 0 0 0 0 0 0 0 0 0 0 0 64 51 29

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C 0 18 68 52 0 7 18 12 76 262 165 64 24 0 0 0 0 0 0 0 0 0

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G 410 48 180 227 123 105 368 663 0 0 0 0 0 0 0 0 0 0 0 0 0 0

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F1 family G♀ x G♂ (1) G♀ x G♂ (2) G♀ x G♂ (3) G♀ x G♂ (4) G♀ x G♂ (5) G♀ x G♂ (6) G♀ x G♂ (7) G♀ x G♂ (8) C♀ x C♂ (1) C♀ x C♂ (2) C♀ x C♂ (3) C♀ x C♂ (4) C♀ x C♂ (5) B♀ x B♂ (1) B♀ x B♂ (2) B♀ x B♂ (3) B♀ x B♂ (4) B♀ x B♂ (5) B♀ x B♂ (6) P♀ x B♂ (1) P♀ x B♂ (2) P♀ x B♂ (3)

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G= golden; C= Orange-purple; P= purple; B= brown

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Ratio G:O; 1:0 G:O; 2.67:1 G:O; 2.65:1 G:O; 2.8:1 G:O; 3.15:1 G:O; 2.92:1 G:O; 2.92:1 G:O; 2.62:1 C:B; 3.04:1 C:B; 3.054:1 C:B; 3.44:1 C:B; 2.91:1 C:B; 3.43:1 B:O; 1:0 B:O; 1:0 B:O; 1:0 B:O; 1:0 B:O; 1:0 B:O; 1:0 P:B; 1.05:1 P:B; 0.98:1 P:B; 0.97:1

Journal Pre-proof Table 2. Total carotenoids content distribution in tissues of male and female, orange and brown scallops. (Adopted from Zheng et al., 2010, 2012a) Tissue Combination Mantle

Adductor

Gill

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59.9Aa (1.32)

16.2Ba (0.85)

15.6Ba (0.23)

7.77Ca (0.07)

OM

15.7Ab (0.15)

16.5Aa (0.46)

10.0Bb (0.49)

8.99Bb (0.45)

BF

26.6Ac (0.46)

6.93Bb (0.16)

2.98Cc (0.19)

2.65Cc (0.04)

BM

3.58Ad (0.15)

3.04Ac (0.02)

0.73Bd (0.07)

1.96Abd (0.27)

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The value before the parenthesis represents mean value, the number in the parenthesis represents standard deviation (n=6), with uppercase indicating comparison among the same line and lowercase indicating comparison among the same column.

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Table 3. Response of Nan’ao Golden Scallop and brown scallops to stressors Description Nan'ao Golden Scallop has higher survival rates (86% to 92%) than the common noble scallops (63% to 69%)

Location Field observation

Reference Zheng et al., 2015

Low salinity stress (20 psu)

MDA level in brown scallops (8.1± 0.2 nmol/ ml) was significantly higher than of Nan'ao Golden Scallop (6.0± 0.3 nmol/ ml)

Laboratory challenge

Wang et al., 2019

MDA level of brown scallops increased at much higher rate compare to Nan’ao Golden Scallops

Laboratory challenge

Tan et al., 2019e

Nan'ao Golden Scallops exhibited 40 to 90% higher survival rates than brown scallop

Laboratory challenge

Unpublished data

High temperature (32 ˚C)

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Cold stress (15 ˚C, 12 ˚C and 10 ˚C)

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Stressor Mass mortality outbreaks

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Journal Pre-proof Highlight

Nan'ao Golden Scallop is more nutritious and less susceptible to stress than common brown scallops

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The high TCC of Nan'ao Golden Scallop up-regulate the expression of various immune related genes under stressful conditions

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Journal Pre-proof Conflict of interests All authors of this work declare that they have no potential conflict of interest and that there is no financial, consultant, institutional or other relationships that might lead to bias or conflicts of interest in this research. Financial grants, infrastructure and

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fellowships supporting this work are described in the acknowledgements section.

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Figure 1

Figure 2

Figure 3