Effect of the oxidative phosphorylation uncoupler 2,4-dinitrophenol on hypoxia-inducible factor-regulated gene expression in bovine blastocysts

In cattle embryos, development to the blastocyst stage is improved in the presence of 10 μm 2,4-dinitrophenol (DNP), an uncoupler of oxidative phosphorylation, coincident with an increase in glycolytic activity following embryonic genome activation. The present study examined redox-sensitive gene expression and embryo development in response to the addition of DNP post-compaction. 2,4-Dinitrophenol increased the expression of hypoxia-inducible factor 1α and 2α (HIF1α, HIF2α) mRNA. Although HIF1α protein remained undetectable in bovine blastocysts, HIF2α protein was localised within the nucleus of trophectoderm and inner cell mass (ICM) cells of blastocysts cultured in the presence or absence of DNP, with a slight increase in staining evident within the ICM in blastocysts cultured in the presence of DNP. However, the expression of GLUT1 and VEGF mRNA, genes known to be regulated by HIFs, was unaffected by the addition of DNP to the culture. Although the development of Grade 1 and 2 blastocysts was unaltered by the addition of DNP post compaction in the present study, a significant increase in the proportion of ICM cells was observed. Results indicate that 10 μm DNP improves the quality of bovine embryos, coincident with increased HIF2α protein localisation within ICM cells and increased HIFα mRNA levels. Therefore, the results demonstrate redox-regulated expression of HIF2.

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Haemoglobin expression in in vivo murine preimplantation embryos suggests a role in oxygen-regulated gene expression

Reproduction Fertility and Development ◽

10.1071/rd17321 ◽

2019 ◽

Vol 31 (4) ◽

pp. 724 ◽

Cited By ~ 1

Author(s):

M. Lim ◽

H. M. Brown ◽

K. L. Kind ◽

J. Breen ◽

M. R. Anastasi ◽

...

Keyword(s):

Gene Expression ◽

Glucose Transporter ◽

Preimplantation Embryo ◽

Inner Cell Mass ◽

Cell Mass ◽

Specific Effect ◽

Blastocyst Stage ◽

High Expression ◽

Preimplantation Embryos ◽

Regulated Gene Expression

Haemoglobin expression is not restricted to erythroid cells. We investigated the gene expression of the haemoglobin subunits haemoglobin, alpha adult chain 1 (Hba-a1) and haemoglobin, beta (Hbb), 2,3-bisphosphoglycerate mutase (Bpgm) and the oxygen-regulated genes BCL2/adenovirus E1B interacting protein 3 (Bnip3), solute carrier family 2 (facilitated glucose transporter), member 1 (Slc2a1) and N-myc downstream regulated gene 1 (Ndrg1) in the murine preimplantation embryo, comparing invivo to invitro gene expression. Relatively high levels of Hba-a1 and Hbb were expressed invivo from the 2-cell to blastocyst stage; in contrast, little or no expression occurred invitro. We hypothesised that the presence of haemoglobin invivo creates a low oxygen environment to induce oxygen-regulated gene expression, supported by high expression of Slc2a1 and Ndrg1 in invivo relative to invitro embryos. In addition, analysis of an invitro-derived human embryo gene expression public dataset revealed low expression of haemoglobin subunit alpha (HBA) and HBB, and high expression of BPGM. To explore whether there was a developmental stage-specific effect of haemoglobin, we added exogenous haemoglobin either up to the 4-cell stage or throughout development to the blastocyst stage, but observed no difference in blastocyst rate or the inner cell mass to trophectoderm cell ratio. We conclude that haemoglobin in the invivo preimplantation embryo raises an interesting premise of potential mechanisms for oxygen regulation, which may influence oxygen-regulated gene expression.

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The absence of a Ca2+ signal during mouse egg activation can affect parthenogenetic preimplantation development, gene expression patterns, and blastocyst quality

Reproduction ◽

10.1530/rep.1.01059 ◽

2006 ◽

Vol 132 (1) ◽

pp. 45-57 ◽

Cited By ~ 41

Author(s):

N T Rogers ◽

G Halet ◽

Y Piao ◽

J Carroll ◽

M S H Ko ◽

...

Keyword(s):

Gene Expression ◽

Inner Cell Mass ◽

Expression Patterns ◽

Cell Mass ◽

Blastocyst Stage ◽

Distinct Pattern ◽

Egg Activation ◽

Cell Stage ◽

Embryonic Genome ◽

Genome Activation

A series of Ca2+ oscillations during mammalian fertilization is necessary and sufficient to stimulate meiotic resumption and pronuclear formation. It is not known how effectively development continues in the absence of the initial Ca2+ signal. We have triggered parthenogenetic egg activation with cycloheximide that causes no Ca2+ increase, with ethanol that causes a single large Ca2+ increase, or with Sr2+ that causes Ca2+ oscillations. Eggs were co-treated with cytochalasin D to make them diploid and they formed pronuclei and two-cell embryos at high rates with each activation treatment. However, far fewer of the embryos that were activated by cycloheximide reached the blastocyst stagecompared tothose activated by Sr2+ orethanol. Any cycloheximide-activated embryos that reached the blastocyst stage had a smaller inner cell mass number and a greater rate of apoptosis than Sr2+-activated embryos. The poor development of cycloheximide-activated embryos was due to the lack of Ca2+ increase because they developed to blastocyst stages at high rates when co-treated with Sr2+ or ethanol. Embryos activated by either Sr2+ or cycloheximide showed similar signs of initial embryonic genome activation (EGA) when measured using a reporter gene. However, microarray analysis of gene expression at the eight-cell stage showed that activation by Sr2+ leads to a distinct pattern of gene expression from that seen with embryos activated by cycloheximide. These data suggest that activation of mouse eggs in the absence of a Ca2+ signal does not affect initial parthenogenetic events, but can influence later gene expression and development.

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Position- and Hippo signaling-dependent plasticity during lineage segregation in the early mouse embryo

eLife ◽

10.7554/elife.22906 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 55

Author(s):

Eszter Posfai ◽

Sophie Petropoulos ◽

Flavia Regina Oliveira de Barros ◽

John Paul Schell ◽

Igor Jurisica ◽

...

Keyword(s):

Gene Expression ◽

Inner Cell Mass ◽

Cell Mass ◽

Global Gene Expression ◽

Blastocyst Stage ◽

Egfp Expression ◽

Hippo Signaling ◽

Ability To Regenerate ◽

Early Mouse ◽

Cell Commitment

The segregation of the trophectoderm (TE) from the inner cell mass (ICM) in the mouse blastocyst is determined by position-dependent Hippo signaling. However, the window of responsiveness to Hippo signaling, the exact timing of lineage commitment and the overall relationship between cell commitment and global gene expression changes are still unclear. Single-cell RNA sequencing during lineage segregation revealed that the TE transcriptional profile stabilizes earlier than the ICM and prior to blastocyst formation. Using quantitative Cdx2-eGFP expression as a readout of Hippo signaling activity, we assessed the experimental potential of individual blastomeres based on their level of Cdx2-eGFP expression and correlated potential with gene expression dynamics. We find that TE specification and commitment coincide and occur at the time of transcriptional stabilization, whereas ICM cells still retain the ability to regenerate TE up to the early blastocyst stage. Plasticity of both lineages is coincident with their window of sensitivity to Hippo signaling.

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Nuclear transplantation of male primordial germ cells in the mouse

Development ◽

10.1242/dev.107.2.407 ◽

1989 ◽

Vol 107 (2) ◽

pp. 407-411 ◽

Cited By ~ 3

Author(s):

Y. Tsunoda ◽

T. Tokunaga ◽

H. Imai ◽

T. Uchida

Keyword(s):

Germ Cells ◽

Inner Cell Mass ◽

Primordial Germ Cells ◽

Cell Mass ◽

Blastocyst Stage ◽

Nuclear Transplantation ◽

Embryonic Genome ◽

Donor Nucleus ◽

Implantation Sites ◽

Genome Activation

We examined the developmental ability of enucleated eggs receiving embryonic nuclei and male primordial germ cells (PGCs) in the mouse. Reconstituted eggs developed into the blastocyst stage only when an earlier 2-cell nucleus was transplanted (36%) but very rarely if the donor nucleus was derived from a later 2-cell, 8-cell, or inner cell mass of a blastocyst (0–3%). 54–100%, 11–67%, 6–43% and 6–20% of enucleated eggs receiving male PGCs developed to 2-cell, 4-cell, 8-cell and blastocyst stage, respectively, in culture. The overall success rate when taking into account the total number of attempts at introducing germ cells was actually 0–6%. Live fetuses were not obtained after transfer of reconstituted eggs to recipients, although implantation sites were observed. The developmental ability of reconstituted eggs in relation to embryonic genome activation and genomic imprinting is discussed.

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Lipid Stores and Lipid Metabolism Associated Gene Expression in Porcine and Bovine Parthenogenetic Embryos Revealed by Fluorescent Staining and RNA-seq

International Journal of Molecular Sciences ◽

10.3390/ijms21186488 ◽

2020 ◽

Vol 21 (18) ◽

pp. 6488

Author(s):

Arkadiusz Kajdasz ◽

Ewelina Warzych ◽

Natalia Derebecka ◽

Zofia E. Madeja ◽

Dorota Lechniak ◽

...

Keyword(s):

Gene Expression ◽

Lipid Metabolism ◽

Inner Cell Mass ◽

Mammalian Species ◽

Cell Mass ◽

Blastocyst Stage ◽

Preimplantation Embryos ◽

Rna Seq ◽

Expression Of Genes ◽

Bovine Blastocyst

Compared to other mammalian species, porcine oocytes and embryos are characterized by large amounts of lipids stored mainly in the form of droplets in the cytoplasm. The amount and the morphology of lipid droplets (LD) change throughout the preimplantation development, however, relatively little is known about expression of genes involved in lipid metabolism of early embryos. We compared porcine and bovine blastocyst stage embryos as well as dissected inner cell mass (ICM) and trophoblast (TE) cell populations with regard to lipid droplet storage and expression of genes functionally annotated to selected lipid gene ontology terms using RNA-seq. Comparing the number and the volume occupied by LD between bovine and porcine blastocysts, we have found significant differences both at the level of single embryo and a single blastomere. Aside from different lipid content, we found that embryos regulate the lipid metabolism differentially at the gene expression level. Out of 125 genes, we found 73 to be differentially expressed between entire porcine and bovine blastocyst, and 36 and 51 to be divergent between ICM and TE cell lines. We noticed significant involvement of cholesterol and ganglioside metabolism in preimplantation embryos, as well as a possible shift towards glucose, rather than pyruvate dependence in bovine embryos. A number of genes like DGAT1, CD36 or NR1H3 may serve as lipid associated markers indicating distinct regulatory mechanisms, while upregulated PLIN2, APOA1, SOAT1 indicate significant function during blastocyst formation and cell differentiation in both models.

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142 DYNAMICS OF Tet FAMILY DURING PRE-IMPLANTATION DEVELOPMENT OF PORCINE EMBRYOS

Reproduction Fertility and Development ◽

10.1071/rdv24n1ab142 ◽

2012 ◽

Vol 24 (1) ◽

pp. 183 ◽

Cited By ~ 2

Author(s):

J. Teson ◽

K. Lee ◽

L. Spate ◽

R. S. Prather

Keyword(s):

Gene Expression ◽

Embryo Development ◽

Expression Profile ◽

Inner Cell Mass ◽

Cell Mass ◽

Blastocyst Stage ◽

Dna Demethylation ◽

Dimensional Structure ◽

Cell Stage ◽

Donor Cells

One of the key regulators of gene expression in mammals is DNA methylation. The Tet family (Tet1–3) is suggested to be involved in regulating the level of methylation by hydroxylating a methyl group from 5-methylcytosine to form 5-hydroxymethylcystosine. This hydroxylation alters the 3-dimensional structure of the DNA and results in altered gene expression. Previous studies conducted in the mouse have shown that Tet1 is important for inner cell mass specification by regulating the apparent level of methylation on a specific promoter region in blastocysts and Tet3 is related to the apparent paternal DNA demethylation after fertilization by hydroxylating the paternal genome. The objective of this study was to investigate the expression profile of the Tet family in porcine oocytes and pre-implantation-stage embryos derived from IVF and somatic cell nuclear transfer (SCNT). The RNA was isolated from donor cells, germinal vesicle (GV), MII and 2-cell and blastocyst stage embryos (20 oocytes or embryos per group). Levels of mRNA for each Tet gene were measured by quantitative real-time RT-PCR. The levels of each mRNA transcript were compared to YWHAG, a housekeeping gene that shows a constant level of expression throughout pre-implantation embryo development and normalized to the GV stage. The analysis was repeated with 3 biological replications and 2 experimental replications. Differences in gene expression were compared by ANOVA and P < 0.05 was considered significant. No difference was found in the levels of the Tet family members between GV and MII stage oocytes. Compared with GV stage oocytes, up-regulation of Tet3 at the 2-cell stage was detected in both IVF and SCNT embryos, 4.7 and 6.2 fold, respectively. A dramatic increase in Tet1 was also observed at the blastocyst stage in IVF and SCNT embryos when compared with the GV stage, 65.7 and 79.7 fold increases, respectively. Interestingly, the level of Tet3 was down-regulated in blastocyst embryos at a 25 or more fold decrease compared with GV. The level of Tet2 remained constant throughout embryo development. Embryos (2-cell and blastocyst) compared from IVF and SCNT showed no difference in Tet expression levels. Donor cells had significantly lower levels of Tet2 and Tet3 when compared with GV. Our results indicate that the Tet family shows a dynamic expression profile during porcine pre-implantation embryo development. High expression of Tet3 in 2-cell stage embryos suggests its importance during the post-activation demethylation process. The increase of Tet1 transcript in blastocysts suggests that Tet1 is involved in regulating the type of methylation at the blastocyst stage. These results are consistent with results from previous mouse studies. There was no misregulated expression of the Tet family in SCNT embryos compared with IVF embryos, thus indicating successful reprogramming of the Tet family after SCNT. Lower levels of Tet2 and Tet3 would indicate that Tet1 is important for maintaining type of methylation in donor cells. This is the first report on the profile of the Tet family during porcine pre-implantation embryo development and further studies are needed to clarify their role during this stage.

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221 TYPICAL HIF1-REGULATED GENES ARE UNALTERED BY OXYGEN IN BOVINE BLASTOCYSTS

Reproduction Fertility and Development ◽

10.1071/rdv17n2ab221 ◽

2005 ◽

Vol 17 (2) ◽

pp. 261

Author(s):

A. Harvey ◽

K. Kind ◽

J. Thompson

Keyword(s):

Gene Expression ◽

Oxygen Concentration ◽

Hypoxia Inducible Factor ◽

Fold Increase ◽

Blastocyst Stage ◽

Bovine Embryo ◽

Bovine Embryos ◽

Expression Of Genes ◽

Regulated Gene Expression

Oxygen-regulated gene expression in the bovine embryo contrasts markedly with that observed in the mouse. Under low (2%) post-compaction oxygen conditions moderate changes in gene expression are observed in the bovine blastocyst (Harvey et al. 2004 Biol. Reprod. 71, in press), compared with 3–4 fold increases in the mouse (Kind et al. 2004 Mol. Reprod. Dev., in press). Specifically, GLUT-1 (Harvey et al. 2004), myotrophin, and anaphase-promoting complex 1 (Harvey et al., unpublished) mRNAs are increased in bovine blastocysts following 2% oxygen culture, compared with those cultured under 20% oxygen. These oxygen-mediated differences in gene expression in the bovine are most likely regulated by hypoxia-inducible factor (HIF)2 transcription factor activity, as we have previously observed that HIF1α protein is not detectable in bovine embryos whereas HIF2α is readily detectable (Harvey et al. 2004). The aim of this study was to determine the effect of post-compaction oxygen concentration on the expression of typically HIF1-regulated and potential HIF2-regulated (suggested from a mouse knockout study; Scortegagna et al. 2003 Nat. Genet. 35, 371) genes in bovine blastocysts. In vitro-produced bovine embryos were generated using standard protocols. Compact morulae were randomly allocated to treatments under 2%, 7%, or 20% oxygen for 72 h from Day 5. Blastocyst RNA was isolated using TriReagent (Molecular Research Center, Inc., Cincinnati, OH, USA) and samples were reverse-transcribed using Superscript II (Invitrogen, Melbourne, Australia). Amplification and analysis of cDNA was achieved by real-time PCR using specific primers and Sybr green PCR master mix (Applied BioSystems, Melbourne, Australia). Statistically significant differences in gene expression were analyzed by ANOVA, P < 0.05. Examination of expression of genes known to be regulated by HIF1 in somatic cells (reviewed by Semenza 2002 Biochem. Pharm. 64, 993) revealed no oxygen-mediated alteration in expression of aldose reductase, cyclooxygenase 2, or inducible nitric oxide synthase. However, the expression of lactate dehydrogenase A (LDHA) displayed a 4-fold increase under 2% oxygen, compared with 7% and 20% oxygen (P < 0.001). Expression of glutathione peroxidase, and CuZn- and Mn-superoxide dismutase (putative HIF2-regulated genes) was not influenced by oxygen concentration post-compaction. This study suggests that typical HIF1-regulated genes are not influenced by alterations in the external oxygen environment in the bovine embryo. These results complement previous observations that HIF1α protein is not detectable in blastocyst-stage bovine embryos, and suggest that LDHA may be an HIF2 target gene in the bovine embryo. As embryo development is influenced by oxygen concentration, levels of LDHA at the blastocyst stage may be used as a marker of oxygen responsiveness.

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62 Investigating differences in gene expression between invitro-produced bovine embryos and parthenotes

Reproduction Fertility and Development ◽

10.1071/rdv33n2ab62 ◽

2021 ◽

Vol 33 (2) ◽

pp. 138

Author(s):

K. Stoecklein ◽

K. Clark ◽

K. Pohler ◽

M. S. Ortega

Keyword(s):

Gene Expression ◽

Inner Cell Mass ◽

Cell Mass ◽

Male Gamete ◽

Rna Isolation ◽

Blastocyst Stage ◽

Suitable Model ◽

Cleavage Rate ◽

Paternal Genome ◽

Cellular Division

Parthenogenic activation allows for the development of an oocyte without male gamete contribution and may serve as a suitable model for understanding maternal and paternal contributions during development. In the bovine, parthenotes lack the ability to survive to term once transferred into females. The goal of this study was to investigate the gene expression profile at the blastocyst stage in parthenotes and embryos by characterising expression of developmentally important genes, such as markers for pluripotency (OCT4, NANOG), hypoblast (GATA6), epiblast (SOX2), trophectoderm (CDX2), and maternal-embryo communication (IFNT2). To test this, IVM oocytes were either fertilized to a bull with known fertility invitro or activated. To activate, oocytes were denuded, and placed in ionomycin calcium salt for 5min. They were incubated for 3h in 6-(dimethylamino)purine (6-DMAP) and placed in synthetic oviductal fluid (SOF). Putative zygotes and activated oocytes were cultured in SOF for 8 days. Cleavage (at least one cellular division) was recorded on Day 3 and development to the blastocyst stage was recorded on Day 8 after insemination or activation. Cleavage rate was 85.9% and 83.2% for parthenotes and embryos, respectively. Both groups produced a similar blastocyst rate, 32.3% for parthenotes and 33.7% for embryos. On Day 8, blastocyst stage parthenotes and embryos were collected. Data were analysed by ANOVA (Tukey HSD post hoc test) using the GLM procedure of SAS version 9.4. Pools of 5 embryos or parthenotes (3 replicates) were flash frozen and stored until RNA isolation (PicoPure™ RNA Isolation Kit). Real-time PCR was used for quantification of gene expression. Genes were analysed relative to a housekeeping gene, GAPDH. There was no difference in gene expression detected for OCT4 (P=0.25), NANOG (P=0.11), GATA6 (P=0.32), SOX2 (P=0.25), or IFNT2 (P=0.52). Expression of CDX2 was lower in the parthenotes than the embryos (P=0.05). In a second experiment, the proteins GATA6, NANOG, and CDX2 were immunolocalized in 17 parthenotes and 15 embryos. Fixed embryos were permeabilized, blocked, and placed in primary antibodies overnight. After, they were placed into the secondary antibody for 1h, followed by nuclear stain. There was a decreased mean intensity of CDX2 in the parthenotes compared to embryos (P=0.005). No difference (P>0.05) in GATA6 or NANOG was observed between the 2 groups. The ratio of inner cell mass to trophectoderm was higher (P=0.04) in the parthenotes (2.5±0.23) than in the embryos (1.7±0.25). Here we analysed and confirmed the expression of developmentally important genes at the blastocyst stage in embryos and parthenotes. CDX2, a marker of the trophectoderm that will later give rise to the placenta, was downregulated in parthenotes. This highlights the importance of the contribution of the paternal genome to development. Further research is necessary to elucidate the ability of the parthenotes to establish and maintain pregnancy. This research was supported by the National Needs Fellowship funded by USDA NIFA Grant 2019-38420-28972.

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Analysis of gene transcription alterations at the blastocyst stage related to the long-term consequences of in vitro culture in mice

Reproduction ◽

10.1530/rep-08-0265 ◽

2009 ◽

Vol 137 (2) ◽

pp. 271-283 ◽

Cited By ~ 46

Author(s):

Raúl Fernández-González ◽

Juan de Dios Hourcade ◽

Irene López-Vidriero ◽

Alberto Benguría ◽

Fernando Rodríguez De Fonseca ◽

...

Keyword(s):

Gene Expression ◽

Inner Cell Mass ◽

Cell Mass ◽

Blastocyst Stage ◽

Epigenetic Mechanisms ◽

Long Term Effects ◽

Long Term Consequences

We have reported thatin vitroculture (IVC) of preimplantation mouse embryos in the presence of FCS produces long-term effects (LTE) on development, growth and behaviour of the offspring at adult age. To analyse the mechanisms underlying this phenomenon, we have examined development and global alterations in gene expression in the mouse blastocysts produced in the presence of FCS, conditions known to be suboptimal and that generate LTE. Embryos culturedin vitroin KSOM and in KSOM+FCS had a reduced number of cells in the inner cell mass at the blastocyst stage compared within vivoderived embryos; however, only culture in KSOM+FCS leads to a reduction in the number of trophoblast cells. Gene expression levels were measured by comparison among three groups of blastocysts (in vivo, IVC in KSOM and IVC in KSOM+FCS). Different patterns of gene expression and development were found between embryos culturedin vitroorin vivo. Moreover, when we compared the embryos produced in KSOM versus KSOM+FCS, we observed that the presence of FCS affected the expression of 198 genes. Metabolism, proliferation, apoptosis and morphogenetic pathways were the most common processes affected by IVC. However, the presence of FCS during IVC preferentially affected genes associated with certain molecular and biological functions related to epigenetic mechanisms. These results suggest that culture-induced alterations in transcription at the blastocyst stage related to epigenetic mechanisms provide a foundation for understanding the molecular origin at the time of preimplantation development of the long-term consequences of IVC in mammals.

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Revealing the dynamics of gene expression during embryonic genome activation and first differentiation in the rabbit embryo with a dedicated array screening

Physiological Genomics ◽

10.1152/physiolgenomics.90310.2008 ◽

2009 ◽

Vol 36 (2) ◽

pp. 98-113 ◽

Cited By ~ 20

Author(s):

R. D. Léandri ◽

C. Archilla ◽

L. C. Bui ◽

N. Peynot ◽

Z. Liu ◽

...

Keyword(s):

Gene Expression ◽

Inner Cell Mass ◽

Cell Mass ◽

Gene Expression Pattern ◽

Cdna Array ◽

Epigenetic Modifications ◽

Embryonic Cells ◽

Embryonic Genome Activation ◽

Embryonic Genome ◽

Genome Activation

Early mammalian development is characterized by extensive changes in nuclear functions that result from epigenetic modifications of the newly formed embryonic genome. While the first embryonic cells are totipotent, this status spans only a few cell cycles. At the blastocyst stage, the embryo already contains differentiated trophectoderm cells and pluripotent inner cell mass cells. Concomitantly, the embryonic genome becomes progressively transcriptionally active. During this unique period of development, the gene expression pattern has been mainly characterized in the mouse, in which embryonic genome activation (EGA) spans a single cell cycle after abrupt epigenetic modifications. To further characterize this period, we chose to analyze it in the rabbit, in which, as in most mammals, EGA is more progressive and occurs closer to the first cell differentiation events. In this species, for which no transcriptomic arrays were available, we focused on genes expressed at EGA and first differentiation and established a 2,000-gene dedicated cDNA array. Screening this with pre-EGA, early post-EGA, and blastocyst embryos divided genes into seven clusters of expression according to their regulation during this period and revealed their dynamics of expression during EGA and first differentiation. Our results point to transient properties of embryo transcriptome at EGA, due not only to the transition between maternal and embryonic transcripts but also to the transient expression of a subset of embryonic genes whose functions remained largely uncharacterized. They also provide a first view of the functional consequences of the changes in gene expression program.

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