© 2001 by The Society for Integrative and Comparative Biology
Yolk Synthesis in the Marine Shrimp, Penaeus vannamei1
1 Department of Biological Sciences, University of North Carolina at Wilmington, Wilmington, North Carolina 28403
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Eyestalk neuroendocrine factors control specific yolk protein synthesis in the ovaries of the shrimp, Penaeus vannamei. A bioassay was developed to measure specific yolk protein synthesis in vitro. The eyestalk neuroendocrine complex may also produce a peptide capable of stimulation of yolk synthesis.
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Crustacean reproduction is characterized by the production of eggs laden with yolk protein. Vitellogenesis is the process of the biosynthesis of these proteins, and their transport and storage in the ovary (Charniaux-Cotton, 1985
). The yolk proteins occur as large molecular weight proteins (300–500 kDa) that also have carotenoid, sugar and lipid moieties attached during biosynthesis. It is these characters which distinguish yolk proteins from the other proteins circulating in the hemolymph (for example: hemocyanin). The primary role of the yolk proteins is to provide nutrition to the developing crustacean embryos. In many cases, crustaceans rely on the yolk proteins for several days after release from the females for their nutrition. Crustaceans may have as much as 60 to 90% of the total egg proteins as yolk protein.
The sites of yolk biosynthesis vary according to the species examined. Some crustaceans rely solely on the ovary to complete vitellogenesis (Penaeus japonicas, Yano and Chinzei, 1987). Other may use the fat body as a primary source of yolk (Amphipods, Isopods) as is the case with most insects (Bowner, 1986; Charniaux-Cotton, 1978; Gohar et al., 1984; Souty and Picaud, 1984). The hepatopancreas and ovary are common sites for yolk biosynthesis several penaeid shrimp (Penaeus vannamei, Penaeus semisulcatus, Penaeus monodon, Parapenaeus longirostris, Browdy et al., 1990; Chen and Chen, 1993, 1994; Quackenbush, 1989a, b; Quintio et al., 1990; Tom et al., 1992).
Coordination of reproduction and yolk biosynthesis is achieved via the endocrine system. The eyestalk neuroendocrine system is the critical component (Fingerman, 1987; Quackenbush, 1986). Reproduction must be timed to allow for maternal yolk investment and optimal larval survival. For many years, it has been known that eyestalk removal and the consequent loss of the eyestalk neuroendocrine system results in rapid loss of inhibitory control of both molting and yolk biosynthesis.
In this paper, I will provide an overview of one of the best-studied models of crustacean yolk biosynthesis, using examples from research on the common penaeid shrimp used in aquaculture, Penaeus vannamei. The objective is to review the present state of our knowledge in this general area, and provide a framework for future studies.
Penaeus vannamei example
As a result of the common use of Penaeus vannamei, in aquaculture in both North American and South American shrimp farms, we now know a considerable amount regarding their basic biology and reproductive patterns (Chamberlain, 1985; Quackenbush, 1991). This wide spread genus has many species under cultivation worldwide. There are some very significant differences among the species with regards to the details of reproduction, but the overall and basic pattern remains quite similar (Browdy et al., 1990; Chen and Chen, 1993; Quintio et al., 1990; Tom et al., 1992).
Penaeid shrimp are broadcast spawnners; they release fertilized eggs directly into the ocean, with little or no parental care. Fertilization by the males quickly follows ovulation, and generally occurs at night. A mature female (30–60 g weight) will produce about 60,000 to 200,000 eggs per spawning event. At release, the eggs are about 300 um in size, and they are covered with a cortical granule protein (Bradfield et al., 1989; Rankin, 1989). During a normal reproductive season, the females are capable of producing ripe collections of eggs (4–6% total body weight) in about four weeks. As the female grow, there are capable of producing larger broods. After egg release, the developing shrimp larvae are entirely dependent on their yolk reserves for nutrition. Penaeid larvae are not hatched with functional mouthparts. They require up to four post hatch molts before they are capable of independent prey capture and feeding. This emphasizes the importance of yolk biosynthesis for the success of the developing nauplii. This pattern of early independent young also favored this species for systematic aquaculture operations (Chamberlain, 1985).
Ovarian maturation in penaeid shrimp is divided into primary and secondary vitellogenesis. Primary vitellogenesis is described by little change in overall size or diameter. Secondary vitellogenesis is where the eggs actually grow in size from around 50 um to 300 um. In most crustaceans, the production of primary oocytes derived from oogonia continues throughout adult life. These small eggs undergo several cytological changes during their transition to secondary vitellogenesis. Ribosomes appear and an extensive endoplasmic reticulum develops. The primary oocytes also increase in size. Follicle cells, surrounding the primary oocyte, also hypertrophy. During secondary vitellogenesis, yolk proteins are stored in the oocyte. This yolk protein storage results in the significant enlargement of the cell. Yolk proteins may be produced in follicle cells (Penaeus japonicas, Yano and Chinzei, 1987) or the ovary or even the hepatopancreas and fat body (Quackenbush, 1991). In Penaeus vannamei, both ovary and hepatopancreas contribute to the yolk investment (see below).
In order to more fully understand this process, a series of experiments and observations were conducted and reported. The results are summarized herein.
Yolk biosynthesis in Penaeus vannamei
Anatomical observations of the mature ovary and hepatopancreas led me to believe that in this species the hepatopancreas may play a role in yolk biosynthesis. The ovary is a paired tubular structure, located just ventral to their cardiac chamber, and extending forward along and attached to the hepatopancreas. When fully developed the ovary will extend posterior through several abdominal segments located on either side of the midline, adjacent to the gut tube. The compact hepatopancreas is covered in a membranous tunic, within which are the usual crustacean tubules that connect to form a network that eventually connects to the gut. Two distinct tubules emerge from the posterior face of the hepatopancreas and connect directly to the sac like covering of the ovary tubules. The terminations of these hepatopancreas ducts are in either the left or right ovary sac. Thus, it appears that it is not necessary for hepatopancreas products to circulate through the hemolymph to get to the ovary, products could pass back and forth between the tissues via these ducts. In many crustaceans, the yolk made in the ovaries or hepatopancreas or other tissues is transported through the hemolymph before being sequestered back in the developing oocytes (Charniaux-Cotton, 1985; Quackenbush, 1991, 1994 for reviews).
A preliminary analysis of the crude homogenates of both ovary and hepatopancreas tissues revealed that both tissues contained peptides, which were lipid positive, sugar positive, and contained carotenoid pigments (Quackenbush, 1989a). These proteins all fulfill the minimum criteria to be called yolk proteins, and they were not found in male tissues. One subunit of the several proteins observed (158,000; 103,000; 97,000; 95,000 and 76,000) was common to the ovary and hepatopancreas, the 97-kDa protein. Work subsequently focussed on this peptide fragment, because it was shared between both tissues, and met all the criteria for a yolk protein. This protein was also one of the most abundant peptides found in the fully developed ovary or egg (Quackenbush, 1989a, Fig. 2).
In order to measure yolk protein biosynthesis in both tissues, and to measure the effect of potential endocrine regulators an in vitro bioassay was developed (Quackenbush, 1989a, b; Quackenbush, 1992). The antibody produced in rabbits to the 97-kDa yolk protein was a critically important tool used in further investigations. The in vitro assay measured 14C-Leucine incorporation into newly produced proteins, and using the antibody we could compare the biosynthesis of all ovarian proteins or hepatopancreas proteins to the particular biosynthesis of the 97-kDa protein. The effect of eyestalk ablation on the biosynthetic capacity of both tissues was first documented. Seven days after eyestalk ablation both tissues responded with increased production of all proteins, and especially the yolk proteins. The ovary incorporated more label than the hepatopancreas initially. However, over time, after eyestalk ablation, both tissues declined in their capacity to incorporate label, the hepatopancreas especially declined below initial levels. Using the specific antibody to the 97-kDa yolk protein it was also possible to partition the amount of yolk protein relative to the total protein in these tissues. Prior to eyestalk ablation, both tissues had about 1–2% 97-kDa yolk protein. Fourteen days after ablation, ovarian synthesis of this protein increased to 4% of the total protein, and reached a maximum of 8% three weeks after ablation. During this period the hepatopancreas maintained a stable 1–2% yolk protein to total protein ratio. Thus, over time, the ovary was accumulating newly made 97 kDa proteins, but the hepatopancreas was not storing or increasing its store of any yolk protein (Quackenbush, 1989b). These observations are consistent with the role of the ovary as a storage depot for yolk protein, and the hepatopancreas as a producer of yolk. As much as 8% of all ovarian protein was the 97 kDa yolk protein. This level of protein was confirmed in a later analysis of fertile eggs produced in a shrimp hatchery. Eggs were obtained from five different females, and a portion of each spawning was analyzed using the antibody for 97-kDa yolk protein. There was wide variation among each spawn as to the total protein (560 ng ± 276 ng) and as to yolk protein (53 ng ± 8.0 ng). The average amount of specific yolk protein in the fertile eggs was 10% of total egg protein, near the figure measured from ovarian fragments in vitro (8% see above) from shrimp after eyestalk ablation.
An enzyme-linked immunoassay was developed for the analysis of yolk proteins using the antibody produced against the 97-kDa yolk protein. This allowed the measurement of yolk protein from small hemolymph (10 ul) samples obtained from shrimp undergoing normal and induced (eyestalk ablation) gonadal maturation. Prior to ablation a control serum profile showed little if any detectable yolk protein in hemolymph of the shrimp. One week after eyestalk removal, traces (0.10 mg/ml) of the 97 kDa proteins were measured in shrimp hemolymph. External observations of the gonads also showed significant changes at this time as well. By the second week post ablation, serum levels reached a maximum of nearly 1 mg/ml 97 kDa yolk protein. Likewise gonadal development also continued to a nearly fully mature, stage 4 (Quackenbush, 1989b). The rise in serum yolk protein, and the consequent fall in serum yolk protein in the eyestalk ablated shrimp was paralleled by the serum profile pattern in intact shrimp undergoing normal gonadal maturation. That is, the timing and pattern of yolk appearance in the serum was similar whether the shrimp were eyestalk ablated or intact. Eyestalk ablation induced vitellogenesis in the shrimp, the pattern and timing of this process was similar to a control group undergoing natural (not-induced) maturation. The data from the in vitro studies of tissue from shrimp after ablation also supports the timing and pattern of vitellogenesis observed in this serum profile study. As the gonads developed to a fully ripe condition (stage 5), the observed hemolymph level of yolk protein fell, as did the ratio of 97 kDa yolk protein to total protein in the tissue itself. This suggests several processes are at work at the same time. One process is the coordination of the ovary and hepatopancreas in their capacity for yolk protein production. Another process is the development of a new protein just at the end of vitellogenesis, now identified as a cortical granule protein (Rankin et al., 1989; Bradfield et al., 1989).
Endocrine regulation of yolk biosynthesis
The eyestalk neuroendocrine system has long been known to play a critical role in gonadal maturation (Panouse, 1943; Fingerman, 1987; Quackenbush, 1986, 1991, 1994). Upon the removal of the adult eyestalks, either gonadal maturation or molting ensues. The eyestalks are a source of general inhibiting hormones with targets on the gonads and epidermal tissues. The in vitro bioassay of yolk biosynthesis in ovary and hepatopancreas tissues made an ideal bioassay for the characterization of these hormone factors. Crude homogenates of eyestalk inhibited shrimp ovarian yolk synthesis, extracts from either brain or thoracic ganglions were ineffective on yolk synthesis (but see Eastman Reks and Fingerman, 1985 for effects in crabs). The eyestalk homogenates affected the synthesis of 97-kDa yolk protein; the eyestalk material had no effect on the general protein synthesis of other ovarian proteins. That is, this eyestalk material was specific and did not produce a general toxic response or inhibition of overall protein synthesis. Using the in vitro bioassay of protein synthesis a partial purification of the eyestalk material was obtained. A fraction (#30) was obtained that inhibited 50% of in vitro yolk synthesis at a level of treatment of 66 ng/ml. This fraction produced no effect at 0.66 ng/ml, inhibition was maximal at 66 ng/ml (Quackenbush, 1989a, b). Using eyestalk material from a local crayfish, Procambarus bouvierii, Huberman's lab was able to obtain a pure peptide that inhibited ovarian yolk synthesis in vitro. This Vitellogenesis—Inhibiting—Hormone or VIH was fully characterized and partial sequences were obtained (Aguilar et al., 1992; Huberman et al., 1995). Since that time, VIH from several different crustaceans was sequenced; all these peptides are members of the Crustacean Hyperglycemic Hormone (CHH) family of peptide hormones (Khayat et al., 1998; Greve et al., 1999; Soyez et al., 1991). To date we have no serum profiles of these eyestalk peptides, nor do we know the mechanisms regulating their synthesis and release.
In addition to the VIH factor which inhibits yolk synthesis in vitro, Huberman's group also isolated a peptide which stimulated yolk biosynthesis by as much as 300% (Huberman et al., 1995). This Gonad Stimulating Factor had been postulated before based on several assays of crude homogenates from many different neural tissues in various bioassays (Fingerman, 1987; Quackenbush, 1986). The use of the same bioassay for both VIH and the gonad stimulating factor, suggests that both hormones regulate the same process. This pattern is similar to the antagonistic chromatophore regulating peptides, which are fully characterized (Rao and Rhiem, 2001).
The role of steroid hormones in controlling the process of crustacean reproduction has been suggested from several preliminary studies (Yano, 1987 and Fingerman, 1987; Quackenbush, 1989 for reviews). However, to date little substantial information has outlined which of a long list of endocrine candidates may actually have a normal role in crustacean reproduction. I tested several potential hormone candidates for their effects on the yolk biosynthesis in vitro of the ovarian fragments from shrimp. As expected, several steroid hormones had little measurable effect on yolk synthesis (testosterone, estrogen, ecdysterone) in vitro (Quackenbush, 1992). However, progesterone did have a dramatic and significant effect on crude protein biosynthesis in vitro, and minor but likewise significant effect on yolk protein biosynthesis in vitro. Estradiol had a specific effect of stimulating yolk biosynthesis in vitro, while having no effect on the other proteins being made in the ovarian tissue fragments. This singular report needs to be confirmed and extended to expand on the potential role of these steroids in yolk protein biosynthesis. It remains to be determined if there is a physiological role for estradiol in the crustacean yolk biosynthesis process, in many vertebrates estradiol plays a key role in yolk biosynthesis (Hadley, 1996).
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The control of reproduction is critical for those animals that produce huge numbers of small eggs like the penaeid shrimp (Quackenbush, 1992
). The shrimp have a significant investment of both time and energy resources into the developing eggs, and since there is little parental care, the quality of the yolk investment is even more critical. For many years, shrimp hatcheries have devised extraordinary diets for their broodstock providing essential vitamins, minerals and especially lipids (Chamberlain et al., 1985). Lipid components of maturation diets are critical for subsequent larval survival and molting. The yolk proteins produced in both the ovary and hepatopancreas carry the vital lipids to the developing eggs. The crustacean hepatopancreas is the primary site for lipid digestion and metabolism (Chang and O'Connor, 1983; Gibson and Barker, 1979). Since the lipid is carried in the hemolymph on carrier proteins, the role of yolk proteins as a lipid shuttle to the developing eggs should be further characterized (Shenker et al., 1993; Quackenbush, 1989).
The pattern of yolk protein biosynthesis after eyestalk ablation is now well described. However, without normal endocrine control mechanisms in place in the eyestalk, yolk protein biosynthesis does not continue indefinitely without decrement. For years, shrimp hatcheries have noticed a distinct decline in egg quality and naupliar survival from spawns of females that have undergone eyestalk ablation (Chamberlain et al., 1985). This egg quality decline was attributed to the exhaustion of lipid and protein reserves required to produce viable eggs. This decline in egg quality suggests an important role for the eyestalk peptide hormones controlling gonadal maturation. VIH's function is to restrain yolk synthesis until suitable organic reserves are in place in either the hepatopancreas and or the ovary.
The availability of pure hormones from several different sources should now open up the study of the endocrine control of crustacean reproduction (Greve et al., 1999). Despite the full sequence for the VIH from Homarus americanus (Soyez et al., 1991) and the isopod, Armadillium vulgare (Greve et al., 1999), the direct mechanism for action of this peptide at the ovary is still not described. The further characterization of the Gonad Stimulating Hormone should provide its sequence; it is likely a part of the CHH family (Huberman et al., 1995). In addition to the need for identifying the actual roles of these peptide hormones, the physiological roles, if any, of the steroid hormones in the process of vitellogenesis has to be resolved. We have only fragmentary information about these well-characterized hormones, and this area should provide a fertile area for future research. The crustacean juvenile hormone, methyl farnesoate, may also have a significant contribution in the regulation of reproduction (Homola and Chang, 1997; Sagi et al., 1997; Wainwright et al., 1996). This terpenoid hormone may have a critical role in the juvenile to adult transition so prominent in many crustaceans; it may also have a role in yolk protein biosynthesis (See Borst, 2001; Laufer, 2001).
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ACKNOWLEDGMENTS |
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I acknowledge the hidden and not so hidden contributions of Milton Fingerman. A young scientist could have had no better mentor as a researcher, a teacher, and a human being than Milton Fingerman. I also thank all the agencies that have supported this work; NOAA and the Sea Grant programs of Texas and Florida; the Florida Department of Environmental Protection; and the U.S. Mexico Foundation. I thank all the students and staff of my lab for the past ten years that contributed so much to this work.
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1 From the Symposium Recent Advances in Crustacean Endocrinology: A Symposium in Honour of Milton Fingerman presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: quackenbushs{at}uncwil.edu
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