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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.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.


Characterization of Tc-cad gradient in WT and RNAi knockdowns.(A, A′) Tc-cad gradient in WT. (B) A model for Tc-cad regulation in the Tribolium blastoderm. (C–D″) Tc-cad gradient expression in a Tc-lgs RNAi embryo (C, C′), and the average of its three descriptors normalized to WT values (Text S3) in 14–17 AEL (D) and 17–20 AEL (D′). As inferred from (D, D′), a comparison between the spatial distribution of Tc-cad gradient in Tc-lgs RNAi embryos and that of WT is summarized in D″ (not to scale). The same was performed for Tc-pan (E–F″), Tc-apc1 (G–H″; in H″: dashed curve for 14–17 AEL and solid curve for 17–20 AEL), Tc-zen1 (I–J″), and Tc-lgs;Tc-zen1 (K–L″) RNAi embryos. (M–M″) the average of the three descriptors of the Tc-cad expression gradient in Tc-pan RNAi normalized to Tc-lgs RNAi values (Text S3). (N–N″) the average of the three descriptors of the Tc-cad expression gradient in Tc-lgs;Tc-zen1 RNAi normalized to Tc-lgs RNAi values. Anterior to the left. Error bars represent 95% confidence intervals. Asterisk (*) represents p-value<0.05.
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pgen-1004677-g002: Characterization of Tc-cad gradient in WT and RNAi knockdowns.(A, A′) Tc-cad gradient in WT. (B) A model for Tc-cad regulation in the Tribolium blastoderm. (C–D″) Tc-cad gradient expression in a Tc-lgs RNAi embryo (C, C′), and the average of its three descriptors normalized to WT values (Text S3) in 14–17 AEL (D) and 17–20 AEL (D′). As inferred from (D, D′), a comparison between the spatial distribution of Tc-cad gradient in Tc-lgs RNAi embryos and that of WT is summarized in D″ (not to scale). The same was performed for Tc-pan (E–F″), Tc-apc1 (G–H″; in H″: dashed curve for 14–17 AEL and solid curve for 17–20 AEL), Tc-zen1 (I–J″), and Tc-lgs;Tc-zen1 (K–L″) RNAi embryos. (M–M″) the average of the three descriptors of the Tc-cad expression gradient in Tc-pan RNAi normalized to Tc-lgs RNAi values (Text S3). (N–N″) the average of the three descriptors of the Tc-cad expression gradient in Tc-lgs;Tc-zen1 RNAi normalized to Tc-lgs RNAi values. Anterior to the left. Error bars represent 95% confidence intervals. Asterisk (*) represents p-value<0.05.

Mentions: Manipulating Wnt activity affected Tc-cad expression in the Tribolium blastoderm. Knocking down Tc-lgs (a positive Wnt regulator) by means of maternal RNAi (Methods) shifted the Tc-cad expression gradient posteriorly (compare Figure 2 C–C′ to Figure 2 A–A′). In addition, the posterior maximum value of Tc-cad and slope of the gradient were reduced in Tc-lgs RNAi embryos compared to WT (Figure 2 D–D″).


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

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

Characterization of Tc-cad gradient in WT and RNAi knockdowns.(A, A′) Tc-cad gradient in WT. (B) A model for Tc-cad regulation in the Tribolium blastoderm. (C–D″) Tc-cad gradient expression in a Tc-lgs RNAi embryo (C, C′), and the average of its three descriptors normalized to WT values (Text S3) in 14–17 AEL (D) and 17–20 AEL (D′). As inferred from (D, D′), a comparison between the spatial distribution of Tc-cad gradient in Tc-lgs RNAi embryos and that of WT is summarized in D″ (not to scale). The same was performed for Tc-pan (E–F″), Tc-apc1 (G–H″; in H″: dashed curve for 14–17 AEL and solid curve for 17–20 AEL), Tc-zen1 (I–J″), and Tc-lgs;Tc-zen1 (K–L″) RNAi embryos. (M–M″) the average of the three descriptors of the Tc-cad expression gradient in Tc-pan RNAi normalized to Tc-lgs RNAi values (Text S3). (N–N″) the average of the three descriptors of the Tc-cad expression gradient in Tc-lgs;Tc-zen1 RNAi normalized to Tc-lgs RNAi values. Anterior to the left. Error bars represent 95% confidence intervals. Asterisk (*) represents p-value<0.05.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004677-g002: Characterization of Tc-cad gradient in WT and RNAi knockdowns.(A, A′) Tc-cad gradient in WT. (B) A model for Tc-cad regulation in the Tribolium blastoderm. (C–D″) Tc-cad gradient expression in a Tc-lgs RNAi embryo (C, C′), and the average of its three descriptors normalized to WT values (Text S3) in 14–17 AEL (D) and 17–20 AEL (D′). As inferred from (D, D′), a comparison between the spatial distribution of Tc-cad gradient in Tc-lgs RNAi embryos and that of WT is summarized in D″ (not to scale). The same was performed for Tc-pan (E–F″), Tc-apc1 (G–H″; in H″: dashed curve for 14–17 AEL and solid curve for 17–20 AEL), Tc-zen1 (I–J″), and Tc-lgs;Tc-zen1 (K–L″) RNAi embryos. (M–M″) the average of the three descriptors of the Tc-cad expression gradient in Tc-pan RNAi normalized to Tc-lgs RNAi values (Text S3). (N–N″) the average of the three descriptors of the Tc-cad expression gradient in Tc-lgs;Tc-zen1 RNAi normalized to Tc-lgs RNAi values. Anterior to the left. Error bars represent 95% confidence intervals. Asterisk (*) represents p-value<0.05.
Mentions: Manipulating Wnt activity affected Tc-cad expression in the Tribolium blastoderm. Knocking down Tc-lgs (a positive Wnt regulator) by means of maternal RNAi (Methods) shifted the Tc-cad expression gradient posteriorly (compare Figure 2 C–C′ to Figure 2 A–A′). In addition, the posterior maximum value of Tc-cad and slope of the gradient were reduced in Tc-lgs RNAi embryos compared to WT (Figure 2 D–D″).

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.