© 2005 International Council for the Exploration of the Sea
Using global genome approaches to address problems in cod mariculture1
a Great Lakes WATER Institute, University of Wisconsin Milwaukee 600 E. Greenfield Avenue, Milwaukee, WI 53204, USA
b Woods Hole Oceanographic Institution, Biology Department Woods Hole, MA 02543, USA
c Institute of Marine Research, Austevoll Aquaculture Research Station N-5392 Storebo, Norway
*Correspondence to F. W. Goetz: tel: +1 414 382 1700; fax: +1 414 382 1705. e-mail: rick{at}uwm.edu; lmccauley{at}whoi.edu; birgitta.norberg{at}imr.no.
A number of techniques, including expressed sequence tag (EST) analysis, serial analysis of gene expression, and micro-arrays, are available to study the global expression and regulation of genes. Many of these techniques are being used for intensively reared fish such as trout, salmon, and catfish to study genes involved in growth, reproduction, and health. In contrast, relatively little is known about the composition and regulation of transcriptomes in gadids. However, several bottlenecks in cod mariculture might benefit from the discovery and analysis of genes involved in reproduction, growth, and disease. As a result, we have begun EST analysis of genes in the cod ovary. Complimentary DNA (cDNA) libraries of cod ovaries taken from females at oocyte final maturation and ovulation have been constructed, and 1361 ESTs have been analysed. As expected, several oocyte-related genes were observed, including various zona pellucida egg membrane proteins. However, pivotal cell cycle regulators such as cyclins, genes involved in the regulation of apoptosis such as the Bcl-2-related ovarian killer protein, and hormone receptor components were also observed. Finally, a cDNA for a potential novel cod antifreeze protein was observed 12 times, suggesting the existence of a cod egg-specific antifreeze protein.
Keywords: cDNA, cod, EST, genomic, Godus morhua, library, ovary, reproduction
Received 13 June 2004; accepted 26 October 2005.
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Introduction |
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 Top Introduction Material and methodsResults and discussionConclusionReferences |
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Worldwide decreases in wild stocks of cod have led to enhanced interest in the cultivation of this species (Brown et al., 2003). While many aspects of cod mariculture have been addressed, there are still issues that will be pivotal to the successful economic development of cod culture including the enhancement of growth, resistance to disease, and gamete quality. Many of these issues will require the selection of desirable traits in broodstocks or an understanding of the basic physiology and genetics of cod. Genetic selection will require a good understanding of the cod genome. In certain intensively reared fish groups such as salmonids, there has been significant progress in developing genomic tools such as complimentary DNA (cDNA) and bacterial artificial chromosome (BAC) libraries, expressed sequence tags (ESTs), micro-arrays, and genetic maps (Nichols et al., 2003; Rexroad et al., 2003; Rise et al., 2004). However, with the exception of mitochondrial sequencing for phylogenetic investigations (Johansen and Bakke, 1996; Sigurgislason and Arnason, 2003), there have been virtually no comparable tools developed for cod.
Several aspects of reproduction, including egg quality, out-of-season spawning, and the effects of gonadal development (e.g. puberty) on somatic growth are important issues for successful cod mariculture. While cod reproduce seasonally, females can theoretically spawn multiple batches of eggs during the yearly reproductive period. For example, in captive cod, females shed from 1 to 19 batches of eggs depending on the individual (Kjesbu, 1989). In addition, wild stocks of cod living in very similar temperate regions can spawn at very different times of the year. To acquire a more complete understanding of cod reproduction, we have been studying the endocrine regulation of the gonad. For those investigations, we first developed stage-specific cDNA libraries of the cod ovary and used them to isolate and characterize genes involved in the regulation of steroid synthesis (Goetz et al., 2004). Here we describe the use of these libraries to develop ESTs for cod reproduction. Expressed sequence tags are the partial sequencing and analysis of clones obtained from the random plating of cDNA libraries. Since cDNA libraries are composed of the RNA transcripts expressed in a given tissue, ESTs represent the sequences of these transcripts; hence the name "expressed". For organisms in which gene sequence information is lacking, the analysis of ESTs is particularly useful to provide an initial survey of genes expressed in a given tissue. Subsequently, that information can be used for more directed studies of gene expression (e.g. candidate gene approaches) or for more global expression analysis (e.g. cDNA micro-arrays).
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Material and methods |
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TopIntroductionMaterial and methodsResults and discussionConclusionReferences |
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Animals
Larvae of coastal Atlantic cod were hatched in 1999 (winter) and reared in a seawater pond (Parisvatnet) located outside Bergen. The cod were transported to Austevoll, Norway, in September 1999 and kept in indoor tanks under a simulated natural photoperiod until May the following year when they were transferred to an outdoor, 5 x 5 m cage. The fish were fed ad libitum and kept in the sea cage under a natural photoperiod until sampling. From these stocks, mature, 2-year-old female cod were sacrificed in February 2001, and ovarian samples were collected. Fish were sampled at stages IV (late vitellogenesis), V (spawning), and VI (spent), defined according to a previously reported classification (Kjesbu, 1991). Cod are periodic (batch) spawners that may undergo 15–20 ovulatory cycles during their spawning period (Kjesbu, 1989; Kjesbu et al., 1990). Thus, the fish in stage V were further divided into three sub-stages: (i) females sampled early in the spawning period containing ovaries with oocytes undergoing final oocyte maturation (V1); (ii) ovulating fish (V2); and (iii) females sampled in the middle to late stages of the spawning period with ovaries containing oocytes undergoing final oocyte maturation (V3). All ovaries were snap-frozen on dry ice and maintained frozen at –80°C prior to RNA extraction.
RNA extraction and library construction
Ovarian tissue from several reproductive stages was homogenized with a TissueTearor (Biospec), and RNA was extracted using Tri Reagent (Molecular Research Center, Inc.) at a ratio of 100 mg tissue/1.0 ml of reagent as previously described (Chomcynski and Sacchi, 1987; Chomcynski, 1993). Poly(A+) RNA was isolated using the PolyAtract mRNA Isolation System (Promega). Messenger ribonucleic acid (5.0 µg) derived from 4–5 females/reproductive stage, was used to construct individual cDNA libraries of each reproductive stage (I–V) in Zap Express (Stratagene). Libraries obtained from stages V1, V2, and V3 were mass excised to pBK-CMV phagemids and plated at low density. Individual colonies were randomly picked, and plasmid preparations were made using the RevPrep Orbit (GeneMachines). Plasmid preparations were sequenced from the 5' end using the dideoxy chain termination method with "Big Dye Terminator" (Applied Biosystems) and the BK reverse vector primer. The reactions were precipitated and resuspended in "Hi-Di Formamide with EDTA" (Applied Biosystems) and run on an ABI Prism 3730 automated sequencer (Applied Biosystems).
Sequence data analysis
Sequence chromatogram files were trimmed for quality using phred (http://www.phrap.org/phrap.docs/phred.html), vector screened using cross-match (http://www.phrap.org/phrap.docs/phrap.html), and analysed locally using (i) blastx against the NCBI non-redundant (nr) protein database, (ii) blastn against the NCBI nucleotide (nt) database, and (iii) blastn against the NCBI EST (dbEST) database. In general, "blast" analyses can be used to compare the translated and/or nucleotide sequences of an unknown sequence (e.g. an EST) against known NCBI sequences to provide an initial identification based on the degree of identity. Specifically, the blastx analysis provides an amino acid sequence comparison of each cod EST translated in six reading frames against the NCBI non-redundant protein database. The blastn analysis against the nt database compares the nucleotide sequence of each cod EST against all nucleotide sequences at NCBI, and the blastn analysis against the NCBI EST database compares the nucleotide sequence of all cod ESTs against the entire NCBI EST database. All sequences were grouped by category (GO database), and tentative identification was based initially on a blastx similarity score of <10–3 or, in the case of blastx scores of >10–3, a blastn score of <10–5. All sequences were collectively analysed for redundancy using CAP3 (Huang and Madan, 1999). Sequences for all of the cod ESTs are currently available at NCBI (accession numbers CO541452
[GenBank]
–CO54294, AY70611–AY70614, AY584595
[GenBank]
).
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Results and discussion |
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TopIntroductionMaterial and methodsResults and discussionConclusionReferences |
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General
Of the 1417 clones initially sequenced from the cod ovarian libraries, there were 1361 sequences
100 bp that were annotated and reported here. The average sequence length was 645 bp, and when analysed for redundancy by CAP3, there were 208 contigs (of two or greater) and 659 singletons. As might be expected, a significant number of sequences were homologous to genes encoding proteins involved in metabolism, and ribosomal and structural proteins (Table 1). In addition, approximately 14% of the ESTs coded for peptides that could be grouped as "Regulatory Proteins" that are involved in the control of cell division, transcription, translation, signalling, apoptosis, and development (Table 1).
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Structural proteins
A major group of structural genes coding for egg membrane proteins was observed; there were 18 ESTs for egg proteins that, based on contig analysis, theoretically represent five unique sequences aligning to choriogenin L (CO542190 [GenBank] ), ZPC2 (CO542098 [GenBank] ), ZPAX (CO542010 [GenBank] ), ZPC (CO542603 [GenBank] ), and ZPA (CO542593 [GenBank] ). In fish, the nomenclature for these egg proteins is inconsistent, but they are extremely important because they constitute the inner portion or zona radiata of the egg envelope (Arukwe and Goksoyr, 2003). Other structural genes observed several times were beta 1 tubulin (CO541590 [GenBank] ) and a profiling-2 like EST (CO541946 [GenBank] ). ESTs (AY584595 [GenBank] ) for a protein that had greatest similarity with an antifreeze protein described from the longhorn sculpin (Zhao et al., 1998) were observed 12 times in the ovarian libraries (Table 2). There are several classes of naturally occurring antifreeze proteins that act to depress the temperature at which ice grows in a non-colligative manner, thereby exhibiting what is termed thermal hysteresis. In gadids, the antifreeze proteins that have been reported are representative of a group called "antifreeze glycoproteins" (Harding et al., 2003). These glycoproteins are distinct from the type of antifreeze proteins reported in the longhorn sculpin and the protein presumably encoded by the ESTs observed in the cod ovarian cDNA libraries. However, the cod ovarian protein also has sequence similarity with apolipoproteins, so it is unclear if it acts as an antifreeze protein or has other functions in the egg/ovary.
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Cell division/cell cycle regulators
Because the cod ovaries that were used for library construction were taken from fish at several stages of oocyte maturation and ovulation, we expected to see genes encoding proteins that are involved with the control of meiosis and cell division. Prominent among these proteins were cyclin B1 (CO541540 [GenBank] ) and B2 (CO541792 [GenBank] ), each observed several times (Table 2). Cyclins are factors expressed in cells that modulate the kinase activity of cyclin-dependent kinases, directing the progression through the cell cycle (Obaya and Sedivy, 2002). They are unified by the presence of a "cyclin box" in their amino acid sequence. Cyclin B and the Cdc2 kinase make up the maturational promoting factor (MPF) that induces oocyte final maturation and the resumption of meiosis (Kishimoto, 2003). Specifically, MPF acts at the G2/M transition of the cell cycle. In zebrafish, cyclin B1 was expressed in all tissues observed (including the ovary), but cyclin B2 expression was only observed in the ovary and testes, consistent with a role in the control of meiosis (Bauer, 2001). It is likely that one of the cyclin B sequences observed in the ESTs represent the cyclin component of the MPF in the cod ovary, and therefore, is of considerable importance.
Other ESTs that potentially are involved in regulating the cell cycle include a Wee1-like cDNA (CO542429 [GenBank] ), one of the kinases that phosphorylates the Cdc2 kinase of MPF (Mueller et al., 1995); Pin 1 (CO541689 [GenBank] ), an enzyme required in mammals for mitosis progression (Fujimori et al., 1999) and recently shown to regulate primordial germ cell proliferation in mice (Atchison et al., 2003); and several genes encoding proteins associated with mitotic spindles including the Protein Regulator of Cytokinesis (PRC1; CO542004 [GenBank] ) (Jiang et al., 1998) and a mitotic spindle assembly checkpoint protein homolog (MAD2B; CO542663 [GenBank] ) (van den Hurk et al., 2004).
Cell signaling/apoptosis
ESTs for a number of genes involved in apoptosis and cell proliferation were also identified. These included several nucleoside diphosphate kinases (CO542766
[GenBank]
and CO542513
[GenBank]
) that are biochemically responsible for the synthesis of nucleoside triphosphates but also have been implicated in a number of regulatory roles including oncogenic transformation and metastasis (Roymans et al., 2002). Other ESTs encoding proteins theoretically involved with apoptosis were a cDNA (CO542330
[GenBank]
), encoding a novel Bcl-2 family member called Bok (Bcl-2 related ovarian killer) that has restricted expression to reproductive tissues and is pro-apoptotic (Hsu et al., 1997); an EST (CO542111
[GenBank]
) similar to SARPs (secreted apoptosis related proteins) that are anti-apoptotic (Melkonyan et al., 1997); an EST (CO542251
[GenBank]
) encoding a protein with similarity to caspases (Uren et al., 2000); and a cDNA (CO541487
[GenBank]
) for BID (BH3 interacting death domain agonist) that promotes cell death (Wang et al., 1996).
Developmental regulators
Since maternal oocyte mRNA undoubtedly made up a large portion of the transcripts in the ovarian cDNA libraries, we also expected to see a number of genes that have already been specifically implicated in the regulation of embryonic development. These included genes such as derriere (CO542177
[GenBank]
), a TGF-beta super-family member involved in directing the fate of posterior development (Sun et al., 1999), and geminin (CO542557
[GenBank]
), a protein that plays an early role in establishing the neural plate during gastrulation (Kroll et al., 1998). However, there were also several genes found in high copy number that have been established only recently in the regulation of development. These included cDNAs (CO541612
[GenBank]
) with strong similarity to the zygote arrest 1 gene. The seven ESTs of this gene could be separated into two distinct contigs. In mice and humans, the zygote arrest gene is oocyte-specific, and in mice lacking this gene, embryos are arrested at the one cell stage (Wu et al., 2003a). In other species, it may not be specific to the oocyte (Wu et al., 2003b). Several copies of ESTs for stathmin (CO542152
[GenBank]
), that appear to play a pivotal role in early neurogenesis directing the early migration of neurons in the brain (Jin et al., 2004), were observed. While stathmin is preferentially expressed in the brain, it also appears to be involved in implantation of the embryo in the uterus (Tamura et al., 2003).
Others
Given the extensive hormonal control of the ovary, we expected to see ESTs for hormone receptors or for genes involved in hormone synthesis. Guanine nucleotide-binding proteins (G-proteins) are involved in the signal transduction of stimuli directed through receptors present on the outer surface of a cell membrane. They are composed of three subunits: alpha, beta, and gamma. Cod homologs of all three subunits (gamma: CO541764
[GenBank]
, beta: CO542763
[GenBank]
, and alpha: CO541729
[GenBank]
) of these G-proteins were present in the ESTs (Table 2). An EST (CO542479
[GenBank]
) for the cAMP response element binding (CREB) protein transcription factor that binds to CRE elements in DNA and modulates gene transcription under cAMP stimulation was observed several times. The cod homolog (CO541987
[GenBank]
) of the regulatory subunit of AMP-activated protein kinase was also identified.
There were several ESTs that had sequence similarity to genes encoding cytochrome P450 enzymes, a super-family of proteins that are involved in the oxidative, peroxidative, and reductive metabolism of many compounds, including steroids, bile acids, fatty acids, prostaglandins, and xenobiotics (Hukkanen, 2000). Thus, some P450 enzymes are involved in steroid hormone synthesis in the gonads or other steroidogenic tissues (e.g. CYP11 and CPY17), while others are involved in the metabolism of environmental pollutants (e.g. CYP1A). Based on amino acid sequence similarity, one of these, cytochrome P450 11A1 (AY706102 [GenBank] ), is most likely the cod homolog of the cholesterol side-chain cleavage enzyme. Another EST (AY706101 [GenBank] ) is very similar in structure to a novel 3-beta hydroxysteroid dehydrogenase (3-beta HSD) that was characterized as the causative gene in several mouse mutations involving abnormalities in cholesterol synthesis (Liu et al., 1999). Determining whether the EST is truly a novel form of 3-beta HSD or the actual form responsible for the conversion of 3-beta-hydroxy-5-ene steroids into 3-keto-4-ene steroids will require complete sequence analysis. ESTs (AY706104 [GenBank] and AY706103 [GenBank] ) for two other cytochrome P450 enzymes of unknown function were also observed.
Finally, ESTs for novel transcripts encoding proteins that might have a specific involvement with changes in the egg at oocyte maturation/ovulation/fertilization were observed (Table 2). These include an EST (CO542550 [GenBank] ) for hyosophorin, a protein that has been shown to be cleaved and exocytosed into the perivitelline space during the cortical reaction at fertilization (Tsao et al., 1999); an EST (CO542059 [GenBank] ) for alveolin, a metalloproteinase that is believed to induce chorion hardening at fertilization in medaka (Shibata et al., 2000); and an EST (CO542075 [GenBank] ) for a transcript encoding a protein that has been shown to regulate chloride conductance through the membrane (Krapivinsky et al., 1994), and therefore, may be involved in oocyte volume regulation.
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Conclusion |
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TopIntroductionMaterial and methodsResults and discussionConclusionReferences |
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To our knowledge, the ESTs reported here are the first to be submitted to Genbank for cod. Even though there were relatively few ESTs in this project compared with other surveys, several pivotal ovarian genes such as the B cyclins and steroidogenic enzymes have already been uncovered that can be used for future research on the endocrine control of reproduction in cod. When we initiated this EST project, we did not consider the proportion of mRNA from the oocyte vs. follicle and stromal tissue that would be present in the libraries. However, after sequencing a number of clones, it is now clear that the contribution of oocyte mRNA is extremely high in comparison to other tissue sources such as the follicle wall. As a result, we probably obtained ESTs for transcripts that were mainly of oocyte origin. To obtain more transcripts that would come from the follicle wall or stroma, it might be necessary to sequence a very large number of ESTs from the libraries. It is clear that follicle wall genes are present in these cod libraries because, for example, we have used the same cDNA libraries to isolate follicle cell regulators of steroidogenesis such as StAR (steroidogenic acute regulatory protein) (Goetz et al., 2004). However, the magnitude of the disparity in genes originating from the oocyte vs. the follicle wall is demonstrated by the fact that StAR is very highly upregulated at oocyte maturation in cod, yet it was not identified in the
1300 sequences in this study. Alternatively, we might need to prepare new libraries in which egg cytoplasm has been removed first so that the extra-oocyte components can be enriched. We did this previously with yellow perch (Perca flavescens), to enrich libraries for follicle wall genes involved in ovulation (Langenau et al., 1999). However, this procedure is difficult for species in which the oocytes are small.
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Footnotes |
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1 This work was supported in part by grant #139630/140 from the Research Council of Norway to BN and USDA grant #2004-35204-14232 to FWG.
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