Limits...
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.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.

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.


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
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).


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.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.

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.