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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

Tc-eve expression in WT and RNAi knockdowns.Tc-eve expression waves in WT (A), mild Tc-cad (B), Tc-lgs (C), Tc-pan (D), Tc-apc1 (E), Tc-zen1 (F) and Tc-lgs;Tc-zen1 (G) RNAi embryos (First cycle/wave/stripe in red, second in gold, and third in green). Tc-eve expression patterns were classified according to the cycle of Tc-eve oscillation in the posterior end of the embryo (roman numerals) and the phase of the cycle (1 for high phase, and 0 for low; e.g. I.1: high phase of the first cycle). Embryos were mapped on the time axis according to timing data (see text). Arrows indicate the position of the anterior border of Tc-eve expression at 20–23 hours AEL in WT (black arrow) and in different knockdowns (white arrows). Shown also are snapshots of computer simulations of a Tc-eve oscillator the frequency of which is modulated by the Tc-cad gradient of WT (A′; see Movie S1, upper panel), mild Tc-cad and Tc-lgs RNAi (C′; see Movie S2, lower panel), Tc-pan RNAi (D′; see Movie S3, lower panel), Tc-apc1 (E′; see Movie S4, lower panel), Tc-zen1 (F′; see Movie S5, lower panel), and Tc-lgs;Tc-zen1 (G′; see Movie S6, lower panel) RNAi embryos; blue: Tc-eve expression, red curve: Tc-cad expression gradient. Snapshots were taken at the end of the corresponding simulations. Anterior to the left. Simulations were performed using Matlab (code is available in Text S1).
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pgen-1004677-g003: Tc-eve expression in WT and RNAi knockdowns.Tc-eve expression waves in WT (A), mild Tc-cad (B), Tc-lgs (C), Tc-pan (D), Tc-apc1 (E), Tc-zen1 (F) and Tc-lgs;Tc-zen1 (G) RNAi embryos (First cycle/wave/stripe in red, second in gold, and third in green). Tc-eve expression patterns were classified according to the cycle of Tc-eve oscillation in the posterior end of the embryo (roman numerals) and the phase of the cycle (1 for high phase, and 0 for low; e.g. I.1: high phase of the first cycle). Embryos were mapped on the time axis according to timing data (see text). Arrows indicate the position of the anterior border of Tc-eve expression at 20–23 hours AEL in WT (black arrow) and in different knockdowns (white arrows). Shown also are snapshots of computer simulations of a Tc-eve oscillator the frequency of which is modulated by the Tc-cad gradient of WT (A′; see Movie S1, upper panel), mild Tc-cad and Tc-lgs RNAi (C′; see Movie S2, lower panel), Tc-pan RNAi (D′; see Movie S3, lower panel), Tc-apc1 (E′; see Movie S4, lower panel), Tc-zen1 (F′; see Movie S5, lower panel), and Tc-lgs;Tc-zen1 (G′; see Movie S6, lower panel) RNAi embryos; blue: Tc-eve expression, red curve: Tc-cad expression gradient. Snapshots were taken at the end of the corresponding simulations. Anterior to the left. Simulations were performed using Matlab (code is available in Text S1).

Mentions: In Tribolium, Tc-eve is expressed in waves that shrink while propagating from posterior to anterior (Figure 3 A) [13]. Tc-eve and Tc-cad RNAi embryo display similar phenotypes lacking all post oral segments, and previous studies implicate cad in the regulation of eve in arthropods [24], [25].


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

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

Tc-eve expression in WT and RNAi knockdowns.Tc-eve expression waves in WT (A), mild Tc-cad (B), Tc-lgs (C), Tc-pan (D), Tc-apc1 (E), Tc-zen1 (F) and Tc-lgs;Tc-zen1 (G) RNAi embryos (First cycle/wave/stripe in red, second in gold, and third in green). Tc-eve expression patterns were classified according to the cycle of Tc-eve oscillation in the posterior end of the embryo (roman numerals) and the phase of the cycle (1 for high phase, and 0 for low; e.g. I.1: high phase of the first cycle). Embryos were mapped on the time axis according to timing data (see text). Arrows indicate the position of the anterior border of Tc-eve expression at 20–23 hours AEL in WT (black arrow) and in different knockdowns (white arrows). Shown also are snapshots of computer simulations of a Tc-eve oscillator the frequency of which is modulated by the Tc-cad gradient of WT (A′; see Movie S1, upper panel), mild Tc-cad and Tc-lgs RNAi (C′; see Movie S2, lower panel), Tc-pan RNAi (D′; see Movie S3, lower panel), Tc-apc1 (E′; see Movie S4, lower panel), Tc-zen1 (F′; see Movie S5, lower panel), and Tc-lgs;Tc-zen1 (G′; see Movie S6, lower panel) RNAi embryos; blue: Tc-eve expression, red curve: Tc-cad expression gradient. Snapshots were taken at the end of the corresponding simulations. Anterior to the left. Simulations were performed using Matlab (code is available in Text S1).
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Related In: Results  -  Collection

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pgen-1004677-g003: Tc-eve expression in WT and RNAi knockdowns.Tc-eve expression waves in WT (A), mild Tc-cad (B), Tc-lgs (C), Tc-pan (D), Tc-apc1 (E), Tc-zen1 (F) and Tc-lgs;Tc-zen1 (G) RNAi embryos (First cycle/wave/stripe in red, second in gold, and third in green). Tc-eve expression patterns were classified according to the cycle of Tc-eve oscillation in the posterior end of the embryo (roman numerals) and the phase of the cycle (1 for high phase, and 0 for low; e.g. I.1: high phase of the first cycle). Embryos were mapped on the time axis according to timing data (see text). Arrows indicate the position of the anterior border of Tc-eve expression at 20–23 hours AEL in WT (black arrow) and in different knockdowns (white arrows). Shown also are snapshots of computer simulations of a Tc-eve oscillator the frequency of which is modulated by the Tc-cad gradient of WT (A′; see Movie S1, upper panel), mild Tc-cad and Tc-lgs RNAi (C′; see Movie S2, lower panel), Tc-pan RNAi (D′; see Movie S3, lower panel), Tc-apc1 (E′; see Movie S4, lower panel), Tc-zen1 (F′; see Movie S5, lower panel), and Tc-lgs;Tc-zen1 (G′; see Movie S6, lower panel) RNAi embryos; blue: Tc-eve expression, red curve: Tc-cad expression gradient. Snapshots were taken at the end of the corresponding simulations. Anterior to the left. Simulations were performed using Matlab (code is available in Text S1).
Mentions: In Tribolium, Tc-eve is expressed in waves that shrink while propagating from posterior to anterior (Figure 3 A) [13]. Tc-eve and Tc-cad RNAi embryo display similar phenotypes lacking all post oral segments, and previous studies implicate cad in the regulation of eve in arthropods [24], [25].

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