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Caudal regulates the spatiotemporal dynamics of pair-rule waves in Tribolium.

El-Sherif E, Zhu X, Fu J, Brown SJ - PLoS Genet. (2014)

Bottom Line: However, neither a molecular candidate nor a functional role has been identified to date for such a frequency gradient, either in vertebrates or elsewhere.We show this by analyzing the spatiotemporal dynamics of Tc-even-skipped expression in strong and mild knockdown of Tc-caudal, and by correlating the extension, level and slope of the Tc-caudal expression gradient to the spatiotemporal dynamics of Tc-even-skipped expression in wild type as well as in different RNAi knockdowns of Tc-caudal regulators.Our results highlight the role of frequency gradients in pattern formation.

View Article: PubMed Central - PubMed

Affiliation: Genetics Program, Kansas State University, Manhattan, Kansas, United States of America.

ABSTRACT
In the short-germ beetle Tribolium castaneum, waves of pair-rule gene expression propagate from the posterior end of the embryo towards the anterior and eventually freeze into stable stripes, partitioning the anterior-posterior axis into segments. Similar waves in vertebrates are assumed to arise due to the modulation of a molecular clock by a posterior-to-anterior frequency gradient. However, neither a molecular candidate nor a functional role has been identified to date for such a frequency gradient, either in vertebrates or elsewhere. Here we provide evidence that the posterior gradient of Tc-caudal expression regulates the oscillation frequency of pair-rule gene expression in Tribolium. We show this by analyzing the spatiotemporal dynamics of Tc-even-skipped expression in strong and mild knockdown of Tc-caudal, and by correlating the extension, level and slope of the Tc-caudal expression gradient to the spatiotemporal dynamics of Tc-even-skipped expression in wild type as well as in different RNAi knockdowns of Tc-caudal regulators. Further, we show that besides its absolute importance for stripe generation in the static phase of the Tribolium blastoderm, a frequency gradient might serve as a buffer against noise during axis elongation phase in Tribolium as well as vertebrates. Our results highlight the role of frequency gradients in pattern formation.

No MeSH data available.


Related in: MedlinePlus

Spatial characteristics of Tc-eve waves over time in WT and RNAi knockdowns.(A, B, C, D, E, F) average position of the anterior border of Tc-eve expression over time in mild Tc-cad (A), Tc-lgs (B), Tc-pan (C), Tc-apc1 (D), Tc-zen1 (E) and Tc-lgs;Tc-zen1 (F) RNAi embryos (red) compared to WT (blue; along with Tc-lgs RNAi in case of Tc-lgs;Tc-zen1, green). Same comparisons were performed for average width of first (A′, B′, C′, D′, E′, F′) and second (A″, B″, C″, D″, E″, F″) Tc-eve stripes. At top is a depiction of Tc-eve expression (black stripes) in a WT Tribolium embryo at late blastoderm stage; anterior to the left. All measurements were normalized to AP axis lengths (Text S3 and Figure S5). A missing data point for a certain stripe indicates that stripe has not formed yet; a stripe proper should have both anterior and posterior borders. Error bars represent 95% confidence intervals.
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pgen-1004677-g004: Spatial characteristics of Tc-eve waves over time in WT and RNAi knockdowns.(A, B, C, D, E, F) average position of the anterior border of Tc-eve expression over time in mild Tc-cad (A), Tc-lgs (B), Tc-pan (C), Tc-apc1 (D), Tc-zen1 (E) and Tc-lgs;Tc-zen1 (F) RNAi embryos (red) compared to WT (blue; along with Tc-lgs RNAi in case of Tc-lgs;Tc-zen1, green). Same comparisons were performed for average width of first (A′, B′, C′, D′, E′, F′) and second (A″, B″, C″, D″, E″, F″) Tc-eve stripes. At top is a depiction of Tc-eve expression (black stripes) in a WT Tribolium embryo at late blastoderm stage; anterior to the left. All measurements were normalized to AP axis lengths (Text S3 and Figure S5). A missing data point for a certain stripe indicates that stripe has not formed yet; a stripe proper should have both anterior and posterior borders. Error bars represent 95% confidence intervals.

Mentions: To examine a possible role of Tc-cad in regulating Tc-eve, we characterized the dynamics of Tc-eve expression in WT and Tc-cad RNAi embryos. Strong Tc-cad RNAi completely abolished Tc-eve expression (Figure S3 A). We produced milder effects by injecting lower concentrations of Tc-cad dsRNA. In these embryos, waves of Tc-eve expression propagated from posterior to anterior (Figure 3 B); however, the final positions of the Tc-eve stripes were shifted posteriorly compared to WT (compare Figure 3 B with Figure 3 A; Figure 4 A).


Caudal regulates the spatiotemporal dynamics of pair-rule waves in Tribolium.

El-Sherif E, Zhu X, Fu J, Brown SJ - PLoS Genet. (2014)

Spatial characteristics of Tc-eve waves over time in WT and RNAi knockdowns.(A, B, C, D, E, F) average position of the anterior border of Tc-eve expression over time in mild Tc-cad (A), Tc-lgs (B), Tc-pan (C), Tc-apc1 (D), Tc-zen1 (E) and Tc-lgs;Tc-zen1 (F) RNAi embryos (red) compared to WT (blue; along with Tc-lgs RNAi in case of Tc-lgs;Tc-zen1, green). Same comparisons were performed for average width of first (A′, B′, C′, D′, E′, F′) and second (A″, B″, C″, D″, E″, F″) Tc-eve stripes. At top is a depiction of Tc-eve expression (black stripes) in a WT Tribolium embryo at late blastoderm stage; anterior to the left. All measurements were normalized to AP axis lengths (Text S3 and Figure S5). A missing data point for a certain stripe indicates that stripe has not formed yet; a stripe proper should have both anterior and posterior borders. Error bars represent 95% confidence intervals.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4199486&req=5

pgen-1004677-g004: Spatial characteristics of Tc-eve waves over time in WT and RNAi knockdowns.(A, B, C, D, E, F) average position of the anterior border of Tc-eve expression over time in mild Tc-cad (A), Tc-lgs (B), Tc-pan (C), Tc-apc1 (D), Tc-zen1 (E) and Tc-lgs;Tc-zen1 (F) RNAi embryos (red) compared to WT (blue; along with Tc-lgs RNAi in case of Tc-lgs;Tc-zen1, green). Same comparisons were performed for average width of first (A′, B′, C′, D′, E′, F′) and second (A″, B″, C″, D″, E″, F″) Tc-eve stripes. At top is a depiction of Tc-eve expression (black stripes) in a WT Tribolium embryo at late blastoderm stage; anterior to the left. All measurements were normalized to AP axis lengths (Text S3 and Figure S5). A missing data point for a certain stripe indicates that stripe has not formed yet; a stripe proper should have both anterior and posterior borders. Error bars represent 95% confidence intervals.
Mentions: To examine a possible role of Tc-cad in regulating Tc-eve, we characterized the dynamics of Tc-eve expression in WT and Tc-cad RNAi embryos. Strong Tc-cad RNAi completely abolished Tc-eve expression (Figure S3 A). We produced milder effects by injecting lower concentrations of Tc-cad dsRNA. In these embryos, waves of Tc-eve expression propagated from posterior to anterior (Figure 3 B); however, the final positions of the Tc-eve stripes were shifted posteriorly compared to WT (compare Figure 3 B with Figure 3 A; Figure 4 A).

Bottom Line: However, neither a molecular candidate nor a functional role has been identified to date for such a frequency gradient, either in vertebrates or elsewhere.We show this by analyzing the spatiotemporal dynamics of Tc-even-skipped expression in strong and mild knockdown of Tc-caudal, and by correlating the extension, level and slope of the Tc-caudal expression gradient to the spatiotemporal dynamics of Tc-even-skipped expression in wild type as well as in different RNAi knockdowns of Tc-caudal regulators.Our results highlight the role of frequency gradients in pattern formation.

View Article: PubMed Central - PubMed

Affiliation: Genetics Program, Kansas State University, Manhattan, Kansas, United States of America.

ABSTRACT
In the short-germ beetle Tribolium castaneum, waves of pair-rule gene expression propagate from the posterior end of the embryo towards the anterior and eventually freeze into stable stripes, partitioning the anterior-posterior axis into segments. Similar waves in vertebrates are assumed to arise due to the modulation of a molecular clock by a posterior-to-anterior frequency gradient. However, neither a molecular candidate nor a functional role has been identified to date for such a frequency gradient, either in vertebrates or elsewhere. Here we provide evidence that the posterior gradient of Tc-caudal expression regulates the oscillation frequency of pair-rule gene expression in Tribolium. We show this by analyzing the spatiotemporal dynamics of Tc-even-skipped expression in strong and mild knockdown of Tc-caudal, and by correlating the extension, level and slope of the Tc-caudal expression gradient to the spatiotemporal dynamics of Tc-even-skipped expression in wild type as well as in different RNAi knockdowns of Tc-caudal regulators. Further, we show that besides its absolute importance for stripe generation in the static phase of the Tribolium blastoderm, a frequency gradient might serve as a buffer against noise during axis elongation phase in Tribolium as well as vertebrates. Our results highlight the role of frequency gradients in pattern formation.

No MeSH data available.


Related in: MedlinePlus