Genome-wide microarray analysis of Atlantic cod (Gadus morhua) oocyte and embryo
© Škugor et al.; licensee BioMed Central Ltd. 2014
Received: 3 February 2014
Accepted: 9 July 2014
Published: 14 July 2014
Regulation of gene expression plays a central role in embryonic development. Early stages are controlled by gametic transcripts, which are subsequently substituted with transcripts from the genome of the zygote. Transcriptomic analyses provide an efficient approach to explore the temporal gene expression profiles in embryos and to search for the developmental regulators. We report a study of early Atlantic cod development that used a genome-wide oligonucleotide microarray to examine the composition and putative roles of polyadenylated transcripts.
The analyses were carried out in unfertilized oocytes, newly fertilized oocytes and embryos at the stages of mid-blastula transition and segmentation. Numerous genes transcribed in oocytes are involved in multiple aspects of cell maintenance and protection, including metabolism, signal perception and transduction, RNA processing, cell cycle, defense against pathogens and DNA damage. Transcripts found in unfertilized oocytes also encoded a large number of proteins implicated in cell adherence, tight junction and focal adhesion, suggesting high complexity in terms of structure and cellular interactions in embryos prior to midblastula transition (MBT). Prezygotic transcripts included multiple regulators that are most likely involved in developmental processes that take place long after fertilization, such as components of ErbB, hedgehog, notch, retinoid, TGFb, VEGF and Wnt signaling pathways, as well as transcripts involved in the development of nervous system. The major event of MBT was the activation of a large group of histones and other genes that modify chromatin structure preceding massive gene expression changes. A hallmark of events observed during segmentation was the induction of multiple transcription factors, including a large group of homeobox proteins in pace with decay of a large fraction of maternal transcripts. Microarray analyses detected a suite of master developmental regulators that control differentiation and maintenance of diverse cell lineages.
Transcriptome profiling of the early stages in Atlantic cod revealed the presence of transcripts involved in patterning and development of tissues and organs long before activation of the zygotic genome. The switch from maternal to zygotic developmental programs is associated with large-scale modification of chromosomes.
Early ontogeny is associated with dramatic gene expression changes that underlie and determine the developmental processes. Transcription terminates by the end of oogenesis when the maturing oocyte is arrested in the metaphase of its second meiotic division [1, 2]. The oocyte is loaded with maternal mRNAs and proteins that control the cell maintenance and fate and the formation of the body plan prior to the onset of zygotic genome expression [3, 4]. Important transcripts can be also contributed by sperm cell, as was recently shown in Drosophila and mammals [5, 6]. Today, it is generally thought that the combination of determinants deposited by the mother during oogenesis and the inductive signals between different cells trigger the specification of different cell lineages during development of the embryo [7, 8]. Maternal to zygotic transition (MZT) is the key event during embryogenesis marked by the switch of control from the maternal and possibly paternal transcripts to the newly synthesized embryonic gene products [9–11]. Degradation of maternal transcripts and zygotic genome activation is characterized by striking changes in the transcriptome profiles. MZT timing is species-specific according to the extent and form of maternal contributions and generally occurs earlier in mammals [12–15] compared to fish, Drosophila and Xenopus[16–19]. In a number of animal species, MZT roughly coincides with the mid-blastula transition (MBT)  when cells become motile and divide asynchronously. The three germ layers and the body plan of the mature organism are established during gastrulation, and the period is characterized by extensive cell movements and intracellular communications [21, 22]. During the following segmentation stage major events in the formation of tissues and organs take place.
Knowledge of the genetic networks controlling embryogenesis has been obtained principally by mutagenesis screens in model species. Multiple mutations affecting embryonic development have been induced by chemical and insertional mutagenesis resulting in the identification of genes with important roles in development in Drosophila[23–25]. Similarly, large-scale genetic screens in zebrafish have enhanced the overall understanding of critical steps and pathways during embryogenesis, and forward genetics revealed a number of developmentally regulated genes [26–28]. Despite high power, this research strategy encounters limitations because only indispensable genes whose loss cannot be compensated by functionally related genes are found, leaving many important actors undetected. A complementary approach is transcriptome profiling that reveals genes with characteristic temporal expression patterns. The completion of the Atlantic cod whole-genome sequencing project  enabled the development of novel tools for gene expression profiling of this ecologically and commercially important marine species sustaining wild fisheries and aquaculture. DNA microarrays are used for analyses of polyadenylated mRNA and a transcriptome study of Atlantic cod embryogenesis using a cDNA microarray was recently reported . We present herein the use of the Atlantic cod genome-wide oligonucleotide microarray for investigation of transcriptome changes associated with the key events of early development from unfertilized oocytes to late somitogenesis with focus on changes during MZT. Contribution of transcripts with different temporal profiles in diverse processes associated with maintenance and development was assessed and compared.
An overview of oocyte and embryo transcriptome
Division of genes in groups by temporal expression profiles
log2-ER > 0.8 in UFO
Prezygotic 2 hpf-
log2-ER < 0.3 in 2 hpf
log2-ER < 0.3 in MBT
log2-ER < 0.3 in SGM
The rest prezygotic
log2-ER < 0.8 in UFO
Zygotic 2 hpf+
log2-ER > 0.8 in 2 hpf
log2-ER > 0.8 in MBT
log2-ER > 0.8 in SGM
Metabolism, cell maintenance, proliferation and protection
Early fish embryos possess a multifaceted defence system. A suite of immune genes was expressed at high levels already in UFO. This group included complement components, cytokines, chemokines and their receptors, IFN and TNF-related genes, together with three negative regulators of immunity from the SOCS family. Several immune genes including myeloperoxidase were activated during SGM. While protection from DNA damage was driven mainly by the maternal transcripts, responses to oxidative stress were switched on later, and seven of eight genes involved in regulation of redox homeostasis were induced during SGM (Figure 2C). Marked developmental regulation was shown by glutathione peroxidases and oxidation resistance protein coding genes.
Cell-to-cell and cell-to-extracellular matrix (ECM) interactions
Transcriptional repression/activation and chromosomal remodeling
Regulation of early cellular differentiation and signaling
A suite of genes known for their roles in neurogenesis was detected already in UFO (Figure 6B). Greatest difference with adult tissues (59-, 34- and 33-fold) was shown by neural cell adhesion molecule L1-like protein (chl1) implicated in cell migration and neuronal positioning, neuropilin and contactin-1a, a neuronal cell adhesion molecule important for the formation of axon connections during the nervous system development [49, 50]. Maternally provided transcripts also included neurogenic differentiation factors (5 genes), which are involved in neuroepithelial stem cell differentiation and neurogenesis, the synaptic protein and receptor of neurotransmitters neuronal pentraxin-1 precursor (nptx1) and two ephrins and ephrin type-B receptors (4 genes), that play a crucial part in migration of axons. Interestingly, switch of ephrin and ephrin receptor isoforms took place at SGM. Maternal transcripts also encoded receptors of the dopamine and acetylcholine neurotransmitters.
Master regulators of embryogenesis
Validation of microarray data
Genome sequencing enabled construction of oligonucleotide microarrays that may provide complete coverage of the polyadenylated fraction of transcriptomes; microarray analyses evaluate abundance of mature mRNA, which is capable for translation. While a genome-wide platform was used for evaluating the abundance of mature mRNA during zebrafish development , we report the first study performed with an aquaculture fish species. The main issue was the presentation of pathways and functional groups among the transcripts displayinh different temporal profiles. High complexity of the transcriptome in unfertilized cod oocytes is consistent with similar studies in both invertebrates and vertebrates [10, 59, 60]. Maternally provided mRNA comprised the major part of prezygotic transcripts while the putative paternal contribution was small, but sperm transcripts might play important roles of in the establishing of early embryonic gene expression profiles [5, 61, 62]. Fertilized cod eggs contained a suite of transcripts for proteins involved in chromatin remodeling and regulation of transcription, cell cycle control and cellular transport. However, it is unknown whether these genes have any developmental roles. In general, maternal transcripts support basic requirements of the embryo prior to the onset of zygotic expression. Interestingly, we got evidence that processing of mRNA continues even in absence of transcription that is in line with recent report on large-scale maturation of maternal transcripts in zebrafish embryos [57, 63]. In addition to maintenance of metabolism, cell structure and proliferation, transcripts of oocytes provide immune protection against pathogens and a suite of genes is expressed at higher level in comparison with adult tissues. Maternal transfer of complement factors and their protective roles was reported in wolffish, rainbow trout and zebrafish [64–67]. The female fish also provide offspring with immunoglobulins, lysozymes, protease inhibitors and different types of lectins [68, 69]. The observed prevalence of immune genes involved in signaling suggests that embryos are capable to regulate responses to pathogens. Presentation of multiple signal transduction pathways points to active perception of external cues and complex interactions between early embryos and environment.
Differentiation presumes acquisition of specific properties by cells and increase of their heterogeneity. A large number of transcripts for proteins involved in cell contacts were abundant in UFO being eliminated at SGM. Cadherins are transmembrane cell adhesion proteins that mediate various processes during development including cellular migration and tissue organization . Interestingly, this study identified a large number of cadherin paralogs that are likely involved in cell sorting and tissue morphogenesis . UFO included many transcripts that can be involved in the control of processes taking place long after fertilization, such as components of Wnt, Notch, hedgehog, ErbB, TGF beta and VEGF signaling pathways and markers of specialized cell lines [72, 73]. We also identified multiple transcripts that may regulate neurogenesis or encode proteins known as highly specific for neural tissue, in agreement with a few studies reporting maternal deposition of transcripts later expressed in the CNS (e.g. Drosophila, zebrafish and axolotl [74–76]). This finding can partly be accounted for by the bias in annotation, since a number of genes with pleiotropic functions have been studied mainly in the context of nervous system. Furthermore, some genes could change functions in course of the vertebrate evolution as demonstrated by the identification several genes known as neural specific in mammals were primarily involved in innate antiviral responses in fish [77, 78].
Transcriptome analyses suggested that the onset of zygotic expression is preceded by large scale modification of chromosomes. Histones comprise a major fraction of genes activated during MBT while the number of transcription factors in this group was small. The pre-MBT transcripts encoded several proteins that modify histones and DNA and are known as positive and negative regulators (e.g. myst2, brd2, n6amt1, rsf1, ehmt3, scml-1, 2 and 4). Transcripts coding for histone methyltransferases and members of the polycomb repressors were highly abundant in unfertilized and fertilized oocytes, but showed a decrease in expression after MBT and coincided with the chromatin remodeling prior to the activation of transcription. Preparation of transcriptional machinery to the large-scale activation of gene expression appears a major developmental event that takes place during MBT. In most studied vertebrates this period coincides with the degradation of maternal transcripts and activation of the zygotic genome which takes over the genetic control of embryogenesis [10, 79]. Furthermore, accumulated studies reveal the dynamic nature of chromatin regulation and the importance of its modifications during transitions from maternal to zygotic control of development [20, 42, 80]. Our data are consistent with recent studies reporting the activation of zygotic transcription at MBT in Atlantic cod [30, 81]. As large fraction of genome is transcriptionally inactive, rearrangement of chromatin is essential to provide an access of transcription factors to the cis-regulatory elements . Microarray analyses are insufficient for accurate timing of the onset of transcription. Part of transcripts appear in the polyadenylated fraction due to maturation of maternal RNA [57, 63]. However, given modification of chromosomes during MBT and the size of the the SGM group, it is likely that a large part of mRNA denoted as zygotic was indeed transcribed from the zygotic genome. The SGM group was complex by composition and contained numerous developmental regulators. Massive upregulation of homeobox genes at SGM is consistent with their involvement in the establishment of body plan and formation of anterior-posterior axis of the embryo [83, 84]. Homeobox transcription factors and cell signaling pathways cooperate to pattern tissues and organs and to specify the fate of a variety of cell types. However, none of the functional groups and pathways was restricted to the post-MBT period and all were largely represented among UFO.
Transcriptome profiling of the oocytes and embryos of Atlantic cod with an aid of genome-wide microarray provided an insight in events taking place in early development and the roles of parental and zygotic transcripts. Maternal transcripts are involved in cellular metabolism, signal perception and transduction, defence, communication and contacts between cells. High representation of pathways and genes that control development suggest early cell fate specification and patterning of tissues and organs, especially of the neuronal lineage. The key event of zygotic genome activation at MBT was extensive chromatin rearrangements followed by expression of multiple developmental regulators.
The study was approved by the Norwegian Animal Research Authority and conducted according to the prevailing animal welfare regulations: FOR-1996-01-15-23 (Norway), European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (Strasbourg, 18.III.1986) and COUNCIL DIRECTIVE of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes (86/609/EEC).
Atlantic cod eggs and embryos were obtained from farmed fish at the National Cod Breeding Centre (Kraknes, Tromsø, Norway). Eggs were hand stripped, fertilized in vitro and transferred to seawater rearing tanks at an average temperature of 4.5°C and 100% oxygen saturation. The following stages were selected for analyses: 1) unfertilized (UFO) and 2) newly fertilized oocytes, 2 hpf and embryos at 3) mid-blastula (MBT), 4) 12 somites and 5) 52 somites (end of somitogenesis). Embryonic stages were determined based on description of Atlantic cod development with precise timing . Tissues from adult male and female cod were used as a reference in the microarray analyses. Eggs and tissue samples were stored in RNAlater (Ambion, Austin, Texas, USA).
Total RNA was extracted from Atlantic cod eggs and tissues using TRIzol (Life Technologies) and PureLinkTM RNA mini kit (Ambion, Austin, Texas, USA). For each developmental stage, 10 oocytes/embryos were pooled for the analyses. On-column DNase treatment was performed using PureLinkTM DNase (Life Technologies) in order to remove traces of DNA and impurities. The concentration was analyzed by NanoDrop ND-1000 spectrophotometer (Thermo Fisher Scientific, Wilmington, USA). The total RNA quality was assessed with Agilent 2100 Bioanalyzer (Agilent 2100 Bioanalyzer, Agilent Technologies, Waldbronn, Germany) and only the samples of high quality (RIN ≥ 8) were selected for analysis.
The Nofima’s Atlantic cod oligonucleotide microarray (ACIQ-2) produced by Agilent Technologies in the 4 × 44 k format included 60-mer probes to the unique transcripts from Ensembl and Unigene which were annotated by functional categories of GO and pathways of KEGG using bioinformatics package STARS [78, 86]. The genes were assigned to the orthology groups of OrthoDB . Three and two biological replicates of the respectively three first and two last stages were analyzed in a total of 13 microarrays. Reference RNA was prepared by pooling equal amounts of RNA from pyloric caeca, liver, muscle, brain and male and female gonad to identify genes with increased expression in oocytes and embryos or developmentally regulated genes. The common reference design also made possible comparison between stages and finding of stage-specific genes. RNA amplification, labeling and fragmentation were performed using Two-Colour Quick Amp Labeling Kit and Gene Expression Hybridization kit following the manufacturer's instructions (Agilent Technologies). The input of total RNA used in each reaction was 100 ng. Individual samples were compared to the common reference; assignment of fluorescent labels (Cy5 and Cy3) was changed in each hybridization performed at 65°C at the rotation speed of 10 rpm for 17 hours in the oven (Agilent Technologies). The slides were washed with Gene Expression Wash Buffers 1 and 2 as described by the manufacturer and scanning was performed at 5 μm resolution using a GenePix Personal 4100A scanner (Molecular Devices, Sunnyvale, CA, USA). The laser power was manually adjusted and the “auto PMT” was enabled to adjust PMT for each channel such that less than 0.1% of features were saturated and that the mean intensity ratio of the Cy3 and Cy5 signals was close to one. Nofima’s bioinformatic package STARS was used for data processing and mining. After filtration of low quality spots flagged by FE, lowess normalization of log2-expression ratios (ER) was performed. Results for the two last developmental stages were highly similar and these samples were therefore merged and denoted as SGM (segmentation). Features that passed quality control in all samples of at least one stage and showed over 2-fold difference from reference were selected (Additional file 1). Further, the features were assigned to groups with different temporal profiles (Figure 1) according to criteria presented in Table 1 with minor manual editing. Data were submitted to GEO Omnibus (GSE58392).
Quantitative real-time RT-PCR
Primer list for real-time qPCR
Sequence (5′- 3′)
Product length, bp
Heat shock 70 kDa protein 4
Heat shock 90 kDa beta
Stress-induced-phosphoprotein 1 (Hsp70/Hsp90-organizing)
Formin-binding protein 4
ATP synthase subunit s mitochondrial
Eukaryotic translation initiation factor 3 subunit 3 gamma 40 kDa isoform CRA b
Tetratricopeptide repeat protein 39C
Dehydrogenase/reductase SDR family member 11
We would like to thank the Norwegian Research Council (project no: 190371) for providing necessary financial support.
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