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The influence of saibo donor and host on the nacre deposits of pearls produced from Pinctada fucata martensii.

ABSTRACT The pearl oyster Pinctada fucata martensii is the dominant species for production of marine pearls in China. To explore the relative contributions of donor and host oysters to nacre deposition in cultured pearls, donors of 3 size groups--large, medium, and small--and hosts of different sizes were used for pearl production. Resulting pearls were numbered to allow tracing of donor and host. Results showed that pearls developed from the 3 different groups of donors showed no significant difference in diameter, weight, and nacre thickness; however pearls cultured in different-size hosts differed significantly with regard to these parameters. Specifically, pearl size, weight, and nacre thickness correlated positively with the size and weight of host oysters, with coefficients ranging from 0.22-0.34. It is suggested that in selection of host oysters used for pearl production, if other conditions are equal, those of larger size and weight are more preferable, for they will presumably produce pearls of larger size and nacre thickness.

KEY WORDS: Pinctada fucata martensii, pearl nacre, donor oyster, host oyster

INTRODUCTION

The pearl oyster Pinctada fucata martensii, also called Pinctadafucata or Pinctada martensii, is the main species used for production of marine pearls, especially in China and Japan (Shi et al. 2009, Wang et al. 2011). Today, China is the leading country in pearl production from P. fucata martensii (Zhang 2002), and is one of the most important marine culture industries in several southern provinces of China (Shi et al. 2009). However, pearl farming using P. fucata martensii has many problems to overcome,

The culture of marine pearls involves 4 steps: preoperative conditioning, nucleus (spherical shell bead) and saibo (mantle graft) implantation, postoperative care, and culturing and harvest (Taylor & Strack 2008, Inoue et al. 2011). Of the 4 steps, the selection of saibo during the second step plays a key role in pearl production, for it may determine directly the growth and quality of the resulting pearl, especially the color and luster (Gervis & Sims 1992, Wada & Komaru 1996). The saibo is a piece of mantle tissue that is excised from a donor and transplanted with a nucleus into the gonad of a recipient oyster (host oyster). After implantation, the saibo develops into a pearl sac around the nucleus via proliferation of the outer mantle epithelial cells (Kawakami 1953, Arnaud-Haond et al. 2007, Fang et al. 2008, Taylor & Strack 2008). Pearl sac epithelia secrete various shell matrix proteins, which are responsible for secreting nacre and the nacreous layers (Fougerouse et al. 2008, Taylor & Strack 2008, Inoue et al. 2010, McGinty et al. 2010, Wang et al. 2010, Kinoshita et al. 2011, McGinty et al. 2011). The development of saibo tissue in the host oyster explains why the general quality of nacre deposition in the shells of donor pearl oysters will be reflected in the resulting pearls. Nacre layer thickness is a significant criterion of pearl quality, for thick nacre means good durability. Nacre is secreted directly by the pearl sac, but development of the pearl sac and the resulting pearl occur entirely within the host oyster. Therefore, it may be possible that both donor and host oysters contribute to the nacre layer thickness of the resulting pearls. So far, however, there has been no convincing evidence of the respective influences of donor and host on the size of cultured pearls. We sought to determine the exact contribution of donor and host oysters to nacre thickness. A total of 170 individuals of 3 size groups were used as donor oysters for pearl production.

MATERIALS AND METHODS

Materials and Study Site

Both donor and host oysters, bred during October 2009, were 2 y old when nucleus implantation was carried out. The breeding and culture of both donor and host oysters, and nucleus implantation were undertaken in Li'an Lagoon, Hainan Island, using the procedures described in Gu et al. (2011).

Implantation

A total of 170 oysters were collected randomly as donors during October 2011. Their shell height, total weight, and shell weight were measured with vernier calipers and an electronic balance after cleaning the oysters. The donor oysters were then divided into 3 size groups: large (n = 58), medium (n = 57), and small (n = 55) according to shell height (Table 1). Every donor produced 10 pieces of mantle graft on average. In other words, the mantle pieces of 1 donor oyster were implanted into 10 hosts.

Host oysters were used randomly during implantation. They all underwent preoperative conditioning, implantation, postoperative care, and culturing in accordance with the procedures described by Wang et al. (2010). Nucleus implantation was carried out by a skilled technician by inserting a nucleus (diameter, 6.7 mm) with a piece of mantle graft into the gonad of host oysters. Host oysters were marked to allow tracing of saibo origin.

Measurement of Host Oyster and Pearl

Eight months later, pearls were harvested and the shell height, total weight, and shell weight of the host oysters were measured with vernier calipers and an electronic balance after cleaning the oysters. Pearls covered with nacre were collected and labeled to allow tracing of both donor and host oysters.

Pearl weight and diameter were measured with an electronic balance and vernier calipers. Thickness of the nacreous layer of all pearls was measured using a coherence tomographic scanner (OSLF-1500; Shenzhen Certainn Technology Co., Ltd.).

Statistical Analysis

Software SPSS version 18.0 was used for statistical analyses. Mean and SDs were analyzed for the donor oysters, host oysters, and pearls. A general linear model and Tukey's test were used for analysis of variance and multiple comparisons, respectively. Differences among groups were considered significant at P < 0.05. Correlations among the parameters of pearls and those of donor or host shells were conducted using a Pearson's correlation matrix.

RESULTS

Characteristics of Donor Oysters

There were significant differences among the 3 donor groups in all 3 growth parameters: shell height, total weight, and shell weight. The 3 groups had at least a 10% difference in shell height and an approximately 20% difference in total weight and shell weight among each another (Table 1).

Characteristics of Host Oysters

Host oysters were used randomly for pearl production. The corresponding hosts implanted with saibo from the 3 size groups demonstrated no significant difference in shell height, total weight, and shell weight (Table 2).

Characteristics of Pearls Produced by Three Groups of Donor Oysters

Eight months after implantation, 754 pearls covered with nacre were harvested. Donors of the large, medium, and small groups produced 269, 255, and 230 pearls, respectively. Pearls produced from different donor groups showed no difference in diameter, weight, and nacre thickness (Table 3).

Correlation Analysis Among Pearls and Donors or Hosts

The 754 harvested pearls were taken as an entirety to analyze the relative contributions of donor and host oysters to the diameter, weight, and nacre thickness of the pearls. Correlation analysis revealed that there was not any significant relationship between the pearl size parameters and the donor size parameters. However, there were significant positive correlations between pearl size parameters (diameter, weight, and nacre thickness) and morphometric parameters of host oysters (shell height, total weight, and shell weight). The coefficients ranged from 0.22-0.34, and all 3 parameters of pearl size correlated most closely with shell weight of the host oyster (Table 4).

DISCUSSION

With regard to pearl development within hosts, Shi et al. (1985) set forth a hypothesis based on studies of pearl sac development in the freshwater bivalve Hyriopsis cumjngii. According to this hypothesis, after transplantation, the mantle graft in the host degenerates gradually to develop the primary pearl sac, which is composed of a single epithelial cell layer around the nucleus. Then, the mantle graft is excluded by the host oyster because of an immunoreaction, resulting in the death and disorganization of the primary pearl sac. Then, because of the activation of the mantle graft or primary pearl sac, connective tissue in the host oyster develops into the secondary pearl sac, which is the organ responsible for secreting nacre to form a pearl. Therefore, Shiet al. (1985) deemed that mantle graft cells of the donor oyster were completely dead at harvest and that it was the host oyster that controlled the formation of the pearl sac and the resulting pearl. However, other studies on both freshwater and marine pearl development suggest that mantle graft cells are not entirely dead. The pearl sac originates from donor oyster tissue rather than host oyster tissue (Zhang & Zhang 1962, Zhang 1975, Meng & Li 1983, Wada 1989, Panha & Kosavititkul 1997). Studies on the ultrastructure of pearl sacs from Pinctada fucata martensii show that it develops from epithelial cells of mantle graft tissue (Duet al. 2010). Microsatellite analysis suggests that DNA originating from the donor oyster can still be detected in the pearl sac of pearl oysters (Arnaud-Haond et al. 2007). Moreover, studies of the expression of 2 species-specific biomineralization genes (N66 and N44) in 2 pearl oyster species (Pinctada maxima and Pinctada margaritifera) revealed that donor oyster biomineralization genes are transcriptionally active in the pearl sac at the time of pearl harvest (McGinty et al. 2011). Therefore, both host oyster and donor oyster are indispensible for pearl production.

Studies of xenografts and pearl production in Pinctada maxima and Pinctada margaritifera suggest that mantle xenografts affect pearl color, complexion, and shape (McGinty et al. 2010). Results from a study of Pintada fucata martensii showed that the frequency of yellow pearls was significantly lower in a group produced by grafting mantle tissue from the inbred white line than from brown lines (Wada & Komaru 1996). In addition, a study of the digital color of P. fucata martensii showed that the nacre color of the donor oysters contributed to the resulting pearl color (Gu et al. 2012). The findings presently available suggest that donor oyster tissue presumably influences pearl color.

In this study, the pearls developed from the 3 donor size groups were similar in diameter, weight, and nacre thickness. In addition, no significant relationship was detected between pearl diameter, weight, and nacre thickness, and donor shell height, total weight, and shell weight. These results indicate that donor oyster or mantle graft may not affect the rate of nacre secretion or the nacre thickness of pearls. Wada and Komaru (1996) also reported that pearl weight did not differ between 2 groups produced by grafting mantle tissue from donors with either white or brown nacre. In another study, xenografts and pearl production from Pinctada maxima and Pinctada margaritifera showed that mantle grafts did influence the rate of pearl nacre deposition and nacre weight (McGinty et al. 2010). These divergent findings may result from differences in species and/o) nacre deposition criteria used in these studies. Further studies on these pearl oysters are needed to determine the true role of donor oyster tissue in nacre deposition and nacre weight.

A study of Pinctada fucata martensii showed that there was positive correlation between pearl weight and shell weight of host oysters (Wada & Komaru 1996). Our results reveal that there are several positive correlations between pearl and host oyster. Pearl diameter, weight, and nacre thickness showed a significant positive correlation with host oyster shell height, total weight, and shell weight. Therefore, it is reasonable to assume that host oysters of P. fucata martensii contribute to the nacre secretion rate and the nacre thickness of pearls. The nucleus had no direct contact with the host oyster but was enveloped within the pearl sac. How, then, does a host oyster affect the rate of nacre secretion onto the developing pearl? Because the pearl sac and pearl are embedded entirely in the visceral mass of the host oyster, the host presumably affects pearl development in 3 ways. First, the host oyster regulates metabolism activation of the pearl sac. The pearl sac depends on the host oyster to supply nutrition throughout the period of pearl formation. A strong host oyster can afford sufficient nutrition and potentially a more suitable environment for the pearl sac, resulting in greater vigor of the pearl sac, promoting nacre secretion rates. Second, biomineralization proteins produced by host oysters may contribute directly to pearl development. There is a consecutive circulatory system that connects the pearl sac and the host oyster. Through this circulatory system, biomineralization proteins produced by host oysters can be transported to the pearl sac to induce nacre assembling and deposition on the surface of the nucleus. Last, genes of host oysters may upregulate the expression of biomineralization genes in the pearl sac. In this way, expression levels of biomineralization genes in the pearl sac are controlled by the host oyster, and are involved indirectly in nacre deposition on the nucleus.

Our study shows that, among the 3 morphometric parameters of the hosts, shell weight had the largest coefficients with the pearl characteristics. The comparatively higher correlation between shell weight and the size parameters of the resulting pearls suggests that shell weight is a reliable indicator of pearl size, thus should be given primary consideration while oysters are selected as hosts in pearl production. However, the measurement of shell weight requires the killing of pearl oysters, so the use of shell weight as an indicator for host oyster selection is impractical in pearl production. By comparison, the correlation coefficients between the total weights of host oysters and pearl characteristics were merely a little lower than those between shell weight of host oysters and pearl characteristics, and total weight can be determined nondestructively, hence is a pragmatically suitable selection criterion of host oysters in pearl production.

In summary, although both donor and host oysters may be involved in pearl formation in Pinctada fucata martensii, they probably play different roles. Donor oyster tissue influences pearl color to a great extent, whereas the host oyster may play a key role in regulating the rate of nacre secretion during pearl development. There are still some questions about the role of donor oyster tissue in regulating the rate of nacre secretion and nacre thickness. Further studies are required to clarify the exact role of donor oyster tissue during pearl formation.

ACKNOWLEDGMENTS

This study was funded by the National Program on Key Basic Research Program of China (973 Program, 2010CB 126405), the National High Technology Research and Development Program of China (863 Program, 2012AA100814), the National Science Foundation of China (30960295), the National Science & Technology Pillar Program (2012BAC18B04), the International S&T Cooperation Program of China (2013 DFA31780), and the Key Project of Chinese Ministry of Education (no. 211143).

LITERATURE CITED

Arnaud-Haond, S., E. Goyard, V. Vonau, C. Herbaut, J. Prou & D. Saulnier. 2007. Pearl formation: persistence of the graft during the entire process of biomineralization. Mar. Biotechnol. (NY) 9: 113-116.

Du, X. D., Y. Jiao, Y. W. Deng, Q. H. Wang & R. L. Huang. 2010. Ultrastructure of the pearl sac cells of pearl oyster Pinctada martensii. Acta Oceanol. Sin. 32:160-164. (In Chinese, with English abstract).

Fang, Z., Q. Feng, Y. Chi, L. Xie & R. Zhang. 2008. Investigation of cell proliferation and differentiation in the mantle of Pinctada fucata (Bivalvia, Mollusca). Mar. Biotechnol. (NY) 153:745-754.

Fougerouse, A., M. Rousseau & J. S. Lucas. 2008. Soft tissue anatomy, shell structure and biomineralisation. In: P. C. Southgate & J. S. Lucas, editors. The pearl oyster. Oxford: Elsevier. pp. 77-102.

Gervis, M. H. & N. A. Sims. 1992. The biology and culture of pearl oysters (Bivalvia: Pteriidae), ICLARM Stud. Rev., Manila, Philippines. 49 pp.

Gu, Z. F., F. S. Huang, H. Wang, K. Gan, X. Zhan, Y. H. Shi & A. M. Wang. 2012. Contribution of donor and host oysters to the cultured pearl colour in Pinctada martensii. Aquacult. Res. (online)

Gu, Z. F., Y. H. Shi, Y. Wang & A. M. Wang. 2011. Heritable characteristics in the pearl oyster Pinctada martensii: comparisons of growth and shell morphology of Chinese and Indian populations, and reciprocal crosses. J. Shellfish Res. 30(241-246.

Inoue, N., R. Ishibashi, T. Ishikawa, T. Atsumi, H. Aoki & A. Komaru. 2010. Gene expression patterns and pearl formation in the Japanese pearl oyster (Pinctada fucata): a comparison of gene expression patterns between the pearl sac and mantle tissues. Aquaculture 308: S68-S74.

Inoue, N., R. Ishibashi, T. Ishikawa, T. Atsumi, H. Aoki & A. Komaru. 2011. Can the quality of pearls from the Japanese pearl oyster (Pinctada fucata) be explained by the gene expression patterns of the major shell matrix proteins in the pearl sac? Mar. Biotechnol. (NY) 13:48-55.

Kawakami, K. I. 1953. Studies on pearl-sac formation II: the effect of water temperature and freshness of transplant on pearl-sac formation. Annot. Zool. Jpn. 26:217-223.

Kinoshita, S., N. Wang, H. Inoue, K. Maeyama, K. Okamoto, K. Nagai, H. Kondo, I. Hirono, S. Asakawa & S. Watabe. 2011. Deep sequencing of ESTs from nacreous and prismatic layer producing tissues and a screen for novel shell formation-related genes in the pearl oyster. PLoS One 6:e21238.

McGinty, E. L., B. S. Evans, J. U. U. Taylor & D. R. Jerry. 2010. Xenografts and pearl production in two pearl oyster species, P. maxima and P. margaritifera: effect on pearl quality and a key to understanding genetic contribution. Aquaculture 302:175-181.

McGinty, E. L., K. R. Zenger, J. Taylor, B. S. Evans & D. R. Jerry. 2011. Diagnostic genetic markers unravel the interplay between host and donor oyster contribution in cultured pearl formation. Aquaculture 316:20-24.

Meng, Z. M. & X. Z. Li. 1983. Studies on mantle graft transplantation and pearl formation of Pinctada maxima. Vol. 1: paper collections of mollusk. Beijing: Science Press. pp. 97-101. (In Chinese).

Panha, S. & P. Kosavititkul. 1997. Mantle transplantations in freshwater pearl mussels in Thailand. Aquacult. Int. 5:267-276.

Shi, Y. H., K. Hong, X. M. Guo, Z. F. Gu, Y. Wang & A. M. Wang. 2009. Genetic linkage map of the pearl oyster, Pinctada martensii (Dunker). Aquacult. Res. 41:35-44.

Shi, A. J., M. Zhang, Z. W. Wu & X. F. Peng. 1985. On the formation of pearl sac in freshwater mussel. J. Fish. China 9:247-253. (In Chinese, with English abstract).

Taylor, J. & E. Strack. 2008. Pearl production. In: P. C. Southgate & J. S. Lucas, editors. The pearl oyster. Oxford: Elsevier. pp. 273-302.

Wada, K. T. 1989. Allograft and xenograft mantle transplantation in freshwater mussels. Jap. J. Malacol. 48:174-190.

Wada, K. T. & A. Komaru. 1996. Color and weight of pearls produced by grafting the mantle tissue from a selected population for white shell color of the Japanese pearl oyster Pinctada fucata martensii (Dunker). Aquaculture 142:25-32.

Wang, A. M., Y. H. Shi, Y. Wang & Z. F. Gu. 2010. Biology and culture techniques of P. fucata martensii. Beijing: Agriculture Science and Technique Press of China. pp. 88-90. (In Chinese).

Wang, A. M., Y. H. Wang, Z. F. Gu, S. F. Li, Y. H. Shi & X. M. Guo. 2011. Development of expressed sequence tags from the pearl oyster, Pinctada martensii Dunker. Mar. Biotechnol. (N Y) 13:275-283.

Zhang, Y. P. 1975. Culture techniques for freshwater pearl. Changsha. Hunan People's Press 33-34:76-77. (In Chinese).

Zhang, L. 2002. The development of international pearl industry and the countermeasures taken by China to speed up Chinese pearl industry. Mark. Sci. 26:10-13. (In Chinese, with English abstract).

Zhang, X. & F. S. Zhang. 1962. Pearl oyster and formation of pearl. Bull. Biol. 1:1-4. (In Chinese, with English abstract).

SHI YAOHUA WANG, HAI ZHAN XIN, GU ZHIFENG * AND WANG AIMIN

Key Laboratory of Tropic Biological Resources, Ministry of Education, Hainan Key Laboratory of Tropical Hydrobiological Technology, The Ocean College, Hainan University, Haikou 570228

* Corresponding author. E-mail: hnugu@163.com

DOI: 10.2983/035.032.0204
TABLE 1.
Shell height, total weight, and shell weight of different size
groups of Pinctada fucata martensu used as saibo donors.

Donor oyster Shell height Total weight
 groups n (mm) (g)

Large 58 8.13 [+ or -] 0.44 (a) 43.40 [+ or -] 6.55 (a)
Medium 57 7.38 [+ or -] 0.34 (b) 36.46 [+ or -] 4.86 (b)
Small 55 6.66 [+ or -] 0.33 (c) 28.69 [+ or -] 3.70 (c)

Donor oyster Shell weight
 groups (g)

Large 23.55 [+ or -] 3.96 (a)
Medium 19.54 [+ or -] 2.50 (b)
Small 15.64 [+ or -] 1.95 (c)

All values represent mean [+ or -] SD. Mean values with different
superscripts are significantly different (Tukey's test, P < 0.05).

TABLE 2.
Shell height, total weight, and shell weight of hosts
corresponding to different donor groups of Pinctada fucata
martensii.

Donor oyster Shell height Total weight
 groups n (mm) (g)

Large 269 76.28 [+ or -] 6.87 37.35 [+ or -] 8.35
Medium 255 77.57 [+ or -] 6.62 35.78 [+ or -] 7.09
Small 230 76.34 [+ or -] 6.66 36.46 [+ or -] 7.56

Donor oyster Shell weight
 groups (g)

Large 20.03 [+ or -] 3.66
Medium 19.89 [+ or -] 3.52
Small 19.78 [+ or -] 3.59

TABLE 3.
Size, weight, and nacre thickness of pearls produced from
different donor groups of Pinctada fiicata martensii.

Donor oyster Pearl diameter Pearl weight
 groups n (mm) (g)

Large 269 7.39 [+ or -] 0.26 0.61 [+ or -] 0.06
Medium 255 7.36 [+ or -] 0.26 0.61 [+ or -] 0.06
Small 230 7.35 [+ or -] 0.29 0.60 [+ or -] 0.06

Donor oyster Nacre layers
 groups thickness (mm)

Large 0.33 [+ or -] 0.11
Medium 0.34 [+ or -] 0.11
Small 0.33 [+ or -] 0.11

TABLE 4.
Correlations between pearl characteristics and host or donor
oyster morphometrics of Pinctada fucata martensii.

 Host oysters Donor oysters

 Shell Total Shell Shell Total Shell
Pearl characters height weight weight height weight weight

Pearl diameter R 0.22 0.25 0.27 0.06 0.04 0.06
 P 0.00 0.00 0.00 0.08 0.33 0.08
Pearl weight R 0.24 0.25 0.27 0.04 0.05 0.06
 P 0.00 0.00 0.00 0.26 0.20 0.08
Nacreous layer R 0.29 0.30 0.34 -0.01 -0.02 0.02
 thickness P 0.00 0.00 0.00 0.83 0.56 0.60

R, correlation coefficient; P, significance level.
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Author:Wang, Shi Yaohua; Xin, Hai Zhan; Zhifeng, Gu; Aimin, Wang
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:9CHIN
Date:Aug 1, 2013
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