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Analysis of a spatial gene expression database for sea anemone Nematostella vectensis during early development.

Botman D, Jansson F, Röttinger E, Martindale MQ, de Jong J, Kaandorp JA - BMC Syst Biol (2015)

Bottom Line: A correlation analysis has been performed on the resulting numerical gene expression profiles for each stage.Early determination in N. vectensis occurs in two stages: expression in broad circles and rings in the blastula is consolidated during gastrulation, and more complex expression patterns appear in the planula within these broad regions.Quantification and comparison of gene expression patterns across a database can generate hypotheses about collective cell movements before these movements are measured directly.

View Article: PubMed Central - PubMed

Affiliation: Computational Science, University of Amsterdam, Science Park 904, Amsterdam, The Netherlands. d.botman@uva.nl.

ABSTRACT

Background: The spatial distribution of many genes has been visualized during the embryonic development in the starlet sea anemone Nematostella vectensis in the last decade. In situ hybridization images are available in the Kahi Kai gene expression database, and a method has been developed to quantify spatial gene expression patterns of N. vectensis. In this paper, gene expression quantification is performed on a wide range of gene expression patterns from this database and descriptions of observed expression domains are stored in a separate database for further analysis.

Methods: Spatial gene expression from suitable in situ hybridization images has been quantified with the GenExp program. A correlation analysis has been performed on the resulting numerical gene expression profiles for each stage. Based on the correlated clusters of spatial gene expression and detailed descriptions of gene expression domains, various mechanisms for developmental gene expression are proposed.

Results: In the blastula and gastrula stages of development in N. vectensis, its continuous sheet of cells is partitioned into correlating gene expression domains. During progressing development, these regions likely correspond to different fates. A statistical analysis shows that genes generally remain expressed during the planula stages in those major regions that they occupy at the end of gastrulation.

Discussion: Observed shifts in gene expression domain boundaries suggest that elongation in the planula stage mainly occurs in the vegetal ring under the influence of the gene Rx. The secondary body axis in N. vectensis is proposed to be determined at the mid blastula transition.

Conclusions: Early gene expression domains in N. vectensis appear to maintain a positional order along the primary body axis. Early determination in N. vectensis occurs in two stages: expression in broad circles and rings in the blastula is consolidated during gastrulation, and more complex expression patterns appear in the planula within these broad regions. Quantification and comparison of gene expression patterns across a database can generate hypotheses about collective cell movements before these movements are measured directly.

No MeSH data available.


Related in: MedlinePlus

Proposed interactions between gene clusters in various expression regions. Early expression clusters activate or develop into later expression clusters in corresponding regions (green arrows). Neighboring expression clusters inhibit each other (red arrows). The blastula domains developing into the body wall ectoderm region are derived from a single gene expression pattern (see text). For this reason, the proposed interactions with the body wall ectoderm are indicated with dashed arrows
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Fig21: Proposed interactions between gene clusters in various expression regions. Early expression clusters activate or develop into later expression clusters in corresponding regions (green arrows). Neighboring expression clusters inhibit each other (red arrows). The blastula domains developing into the body wall ectoderm region are derived from a single gene expression pattern (see text). For this reason, the proposed interactions with the body wall ectoderm are indicated with dashed arrows

Mentions: Central domain expression is generally persistent in the endoderm, while expression in the central and external rings is often limited to the oral ectoderm during and after gastrulation. The first entry in Table 1 shows that the early gastrula expression pattern is known for 23 genes that are expressed exclusively in the central domain in the blastula stage. Out of these 23 genes, 21 are expressed in the presumptive endoderm in the early gastrula stage. Similarly, all 8 genes expressed exclusively in the central or external ring in the blastula with known expression in the early gastrula, are expressed in the blastoporal ectoderm in the latter stage as summarized in the first entry in Table 2. Moreover, expression is observed exclusively in the same major domain in the next available stage for at least 69 % of all instances of expression limited to either of these two major domains, as indicated in the last column of Tables 4 and 5. These observations are a strong indication that the central domain differentiates into the later endoderm and that the central and external rings become oral ectoderm. The vegetal hemisphere likely becomes aboral ectoderm, but this is based on a small number of expression patterns (Table 6). These differentiation regions are in agreement with the locations of a dye injected into an N. vectensis egg and recorded during embryonic development [11]. Injection of lineage tracers into individual cells of developing N. vectensis embryos results in contiguous clones of labeled cells without long distant migration of individual cells (Martindale, unpublished observations). Based on the statistical stability of the main gene expression regions, a regulation mechanism is proposed where genes in early regions activate genes in corresponding later regions, while genes in adjacent regions repress one another (Fig. 21).Fig. 21


Analysis of a spatial gene expression database for sea anemone Nematostella vectensis during early development.

Botman D, Jansson F, Röttinger E, Martindale MQ, de Jong J, Kaandorp JA - BMC Syst Biol (2015)

Proposed interactions between gene clusters in various expression regions. Early expression clusters activate or develop into later expression clusters in corresponding regions (green arrows). Neighboring expression clusters inhibit each other (red arrows). The blastula domains developing into the body wall ectoderm region are derived from a single gene expression pattern (see text). For this reason, the proposed interactions with the body wall ectoderm are indicated with dashed arrows
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4581490&req=5

Fig21: Proposed interactions between gene clusters in various expression regions. Early expression clusters activate or develop into later expression clusters in corresponding regions (green arrows). Neighboring expression clusters inhibit each other (red arrows). The blastula domains developing into the body wall ectoderm region are derived from a single gene expression pattern (see text). For this reason, the proposed interactions with the body wall ectoderm are indicated with dashed arrows
Mentions: Central domain expression is generally persistent in the endoderm, while expression in the central and external rings is often limited to the oral ectoderm during and after gastrulation. The first entry in Table 1 shows that the early gastrula expression pattern is known for 23 genes that are expressed exclusively in the central domain in the blastula stage. Out of these 23 genes, 21 are expressed in the presumptive endoderm in the early gastrula stage. Similarly, all 8 genes expressed exclusively in the central or external ring in the blastula with known expression in the early gastrula, are expressed in the blastoporal ectoderm in the latter stage as summarized in the first entry in Table 2. Moreover, expression is observed exclusively in the same major domain in the next available stage for at least 69 % of all instances of expression limited to either of these two major domains, as indicated in the last column of Tables 4 and 5. These observations are a strong indication that the central domain differentiates into the later endoderm and that the central and external rings become oral ectoderm. The vegetal hemisphere likely becomes aboral ectoderm, but this is based on a small number of expression patterns (Table 6). These differentiation regions are in agreement with the locations of a dye injected into an N. vectensis egg and recorded during embryonic development [11]. Injection of lineage tracers into individual cells of developing N. vectensis embryos results in contiguous clones of labeled cells without long distant migration of individual cells (Martindale, unpublished observations). Based on the statistical stability of the main gene expression regions, a regulation mechanism is proposed where genes in early regions activate genes in corresponding later regions, while genes in adjacent regions repress one another (Fig. 21).Fig. 21

Bottom Line: A correlation analysis has been performed on the resulting numerical gene expression profiles for each stage.Early determination in N. vectensis occurs in two stages: expression in broad circles and rings in the blastula is consolidated during gastrulation, and more complex expression patterns appear in the planula within these broad regions.Quantification and comparison of gene expression patterns across a database can generate hypotheses about collective cell movements before these movements are measured directly.

View Article: PubMed Central - PubMed

Affiliation: Computational Science, University of Amsterdam, Science Park 904, Amsterdam, The Netherlands. d.botman@uva.nl.

ABSTRACT

Background: The spatial distribution of many genes has been visualized during the embryonic development in the starlet sea anemone Nematostella vectensis in the last decade. In situ hybridization images are available in the Kahi Kai gene expression database, and a method has been developed to quantify spatial gene expression patterns of N. vectensis. In this paper, gene expression quantification is performed on a wide range of gene expression patterns from this database and descriptions of observed expression domains are stored in a separate database for further analysis.

Methods: Spatial gene expression from suitable in situ hybridization images has been quantified with the GenExp program. A correlation analysis has been performed on the resulting numerical gene expression profiles for each stage. Based on the correlated clusters of spatial gene expression and detailed descriptions of gene expression domains, various mechanisms for developmental gene expression are proposed.

Results: In the blastula and gastrula stages of development in N. vectensis, its continuous sheet of cells is partitioned into correlating gene expression domains. During progressing development, these regions likely correspond to different fates. A statistical analysis shows that genes generally remain expressed during the planula stages in those major regions that they occupy at the end of gastrulation.

Discussion: Observed shifts in gene expression domain boundaries suggest that elongation in the planula stage mainly occurs in the vegetal ring under the influence of the gene Rx. The secondary body axis in N. vectensis is proposed to be determined at the mid blastula transition.

Conclusions: Early gene expression domains in N. vectensis appear to maintain a positional order along the primary body axis. Early determination in N. vectensis occurs in two stages: expression in broad circles and rings in the blastula is consolidated during gastrulation, and more complex expression patterns appear in the planula within these broad regions. Quantification and comparison of gene expression patterns across a database can generate hypotheses about collective cell movements before these movements are measured directly.

No MeSH data available.


Related in: MedlinePlus