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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

Progressing embryo morphology during N. vectensis development. The table estimates the time of development at two different temperatures for the stages until the late planula. Table entries indicate the hours after fertilization derived from [11, 18, 21]. The annotations in the schematic morphologies are guidelines for researchers to describe expression domains in their hybridization images. AnHe = animal hemisphere, VeHe = vegetal hemisphere, An = animal pole, Cd = central domain, Cr = central ring, Er = external ring, Ve = vegetal pole, pEn = presumptive endoderm, bEc = blastoporal ectoderm, Ec = ectoderm, OrHe = oral hemisphere, AbHe = aboral hemisphere, OrEc = oral ectoderm, En = endoderm, AbEc = aboral ectoderm, PhEc = pharyngeal ectoderm, PhEn = pharyngeal endoderm, AtEn = apical tuft endoderm, AtEc = apical tuft ectoderm, At = apical tuft, M = mouth, BwEc = body wall ectoderm, BwEn = body wall endoderm, MeEc = mesentery ectoderm, MeEn = mesentery endoderm, TeB = tentacle bud, TeEc = tentacle ectoderm, TeEn = tentacle endoderm, Si = siphonoglyph, TeTi = tentacle tip, TeBa = tentacle base (The original nomenclature in [9] has been adapted to the more detailed denotations for the blastula stage in [15].)
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Fig1: Progressing embryo morphology during N. vectensis development. The table estimates the time of development at two different temperatures for the stages until the late planula. Table entries indicate the hours after fertilization derived from [11, 18, 21]. The annotations in the schematic morphologies are guidelines for researchers to describe expression domains in their hybridization images. AnHe = animal hemisphere, VeHe = vegetal hemisphere, An = animal pole, Cd = central domain, Cr = central ring, Er = external ring, Ve = vegetal pole, pEn = presumptive endoderm, bEc = blastoporal ectoderm, Ec = ectoderm, OrHe = oral hemisphere, AbHe = aboral hemisphere, OrEc = oral ectoderm, En = endoderm, AbEc = aboral ectoderm, PhEc = pharyngeal ectoderm, PhEn = pharyngeal endoderm, AtEn = apical tuft endoderm, AtEc = apical tuft ectoderm, At = apical tuft, M = mouth, BwEc = body wall ectoderm, BwEn = body wall endoderm, MeEc = mesentery ectoderm, MeEn = mesentery endoderm, TeB = tentacle bud, TeEc = tentacle ectoderm, TeEn = tentacle endoderm, Si = siphonoglyph, TeTi = tentacle tip, TeBa = tentacle base (The original nomenclature in [9] has been adapted to the more detailed denotations for the blastula stage in [15].)

Mentions: The change in N. vectensis morphology during development is schematically displayed in Fig. 1. The nucleus in the egg is located at the future oral pole, which means that the primary (oral-aboral) axis is already determined before fertilization [10, 11]. The determination of the secondary axis, which is defined by the location of the syphonoglyph, is unclear. The first structures that appear along this axis are the primary mesenteries, but differential gene expression is already observed during gastrulation [12, 13]. Based on the early symmetry break in various gene expression patterns and on early N. vectensis morphogenesis, a mechanism is proposed for secondary axis determination. Spatial gene expression patterns in early stages of development are necessary to study the determination and formation of the secondary axis.Fig. 1


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)

Progressing embryo morphology during N. vectensis development. The table estimates the time of development at two different temperatures for the stages until the late planula. Table entries indicate the hours after fertilization derived from [11, 18, 21]. The annotations in the schematic morphologies are guidelines for researchers to describe expression domains in their hybridization images. AnHe = animal hemisphere, VeHe = vegetal hemisphere, An = animal pole, Cd = central domain, Cr = central ring, Er = external ring, Ve = vegetal pole, pEn = presumptive endoderm, bEc = blastoporal ectoderm, Ec = ectoderm, OrHe = oral hemisphere, AbHe = aboral hemisphere, OrEc = oral ectoderm, En = endoderm, AbEc = aboral ectoderm, PhEc = pharyngeal ectoderm, PhEn = pharyngeal endoderm, AtEn = apical tuft endoderm, AtEc = apical tuft ectoderm, At = apical tuft, M = mouth, BwEc = body wall ectoderm, BwEn = body wall endoderm, MeEc = mesentery ectoderm, MeEn = mesentery endoderm, TeB = tentacle bud, TeEc = tentacle ectoderm, TeEn = tentacle endoderm, Si = siphonoglyph, TeTi = tentacle tip, TeBa = tentacle base (The original nomenclature in [9] has been adapted to the more detailed denotations for the blastula stage in [15].)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig1: Progressing embryo morphology during N. vectensis development. The table estimates the time of development at two different temperatures for the stages until the late planula. Table entries indicate the hours after fertilization derived from [11, 18, 21]. The annotations in the schematic morphologies are guidelines for researchers to describe expression domains in their hybridization images. AnHe = animal hemisphere, VeHe = vegetal hemisphere, An = animal pole, Cd = central domain, Cr = central ring, Er = external ring, Ve = vegetal pole, pEn = presumptive endoderm, bEc = blastoporal ectoderm, Ec = ectoderm, OrHe = oral hemisphere, AbHe = aboral hemisphere, OrEc = oral ectoderm, En = endoderm, AbEc = aboral ectoderm, PhEc = pharyngeal ectoderm, PhEn = pharyngeal endoderm, AtEn = apical tuft endoderm, AtEc = apical tuft ectoderm, At = apical tuft, M = mouth, BwEc = body wall ectoderm, BwEn = body wall endoderm, MeEc = mesentery ectoderm, MeEn = mesentery endoderm, TeB = tentacle bud, TeEc = tentacle ectoderm, TeEn = tentacle endoderm, Si = siphonoglyph, TeTi = tentacle tip, TeBa = tentacle base (The original nomenclature in [9] has been adapted to the more detailed denotations for the blastula stage in [15].)
Mentions: The change in N. vectensis morphology during development is schematically displayed in Fig. 1. The nucleus in the egg is located at the future oral pole, which means that the primary (oral-aboral) axis is already determined before fertilization [10, 11]. The determination of the secondary axis, which is defined by the location of the syphonoglyph, is unclear. The first structures that appear along this axis are the primary mesenteries, but differential gene expression is already observed during gastrulation [12, 13]. Based on the early symmetry break in various gene expression patterns and on early N. vectensis morphogenesis, a mechanism is proposed for secondary axis determination. Spatial gene expression patterns in early stages of development are necessary to study the determination and formation of the secondary axis.Fig. 1

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