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Two frizzled planar cell polarity signals in the Drosophila wing are differentially organized by the Fat/Dachsous pathway.

Hogan J, Valentine M, Cox C, Doyle K, Collier S - PLoS Genet. (2011)

Bottom Line: There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein.The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model.Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Marshall University, Huntington, West Virginia, United States of America.

ABSTRACT
The regular array of distally pointing hairs on the mature Drosophila wing is evidence for the fine control of Planar Cell Polarity (PCP) during wing development. Normal wing PCP requires both the Frizzled (Fz) PCP pathway and the Fat/Dachsous (Ft/Ds) pathway, although the functional relationship between these pathways remains under debate. There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein. The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model. Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

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Over-expression of Ft/Ds pathway genes modifies the pkpk hair polarity phenotype.All micrographs are of the female dorsal wing surface. Arrows indicate local hair polarity. Red shaded ovals represent regions where hair polarity differs from wild-type. Red arrows indicate where local hair polarity differs from that seen on a pkpk30 homozygous wing. (A) Wild-type wing. (B) MS1096-gal4; UAS-ft wing. (C) MS1096-gal4; UAS-ds wing. (D) MS1096-gal4; UAS-fj wing. (E) pkpk30/pkpk30 wing. (F) MS1096-gal4; UAS-ft, pkpk30/pkpk30 wing. (G) MS1096-gal4; pkpk30/pkpk30; UAS-ds wing. (H) MS1096-gal4; UAS-fj, pkpk30/pkpk30 wing.
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pgen-1001305-g005: Over-expression of Ft/Ds pathway genes modifies the pkpk hair polarity phenotype.All micrographs are of the female dorsal wing surface. Arrows indicate local hair polarity. Red shaded ovals represent regions where hair polarity differs from wild-type. Red arrows indicate where local hair polarity differs from that seen on a pkpk30 homozygous wing. (A) Wild-type wing. (B) MS1096-gal4; UAS-ft wing. (C) MS1096-gal4; UAS-ds wing. (D) MS1096-gal4; UAS-fj wing. (E) pkpk30/pkpk30 wing. (F) MS1096-gal4; UAS-ft, pkpk30/pkpk30 wing. (G) MS1096-gal4; pkpk30/pkpk30; UAS-ds wing. (H) MS1096-gal4; UAS-fj, pkpk30/pkpk30 wing.

Mentions: To complement the studies described above, we looked at the effect of over-expressing Ft/Ds pathway genes on the Early Fz(Sple) and Late Fz(Pk) signals. Uniform over-expression of ft (MS1096-gal4; UAS-ft) results in similar wing morphology to loss of ft activity (Figure 5B) and alters posterior ridges. ft over-expression alters hair polarity in the same proximal region of the wing affected by reduced Ft/Ds pathway gene activity (see Figure 3), but also generates variable hair polarity changes in more distal regions of the wing (red ovals in Figure 5B). Uniform over-expression of ds or fj results in a similar wing shape, posterior ridge and hair polarity phenotype to reduced activity of the same genes (Figure 5C and 5D). When ft, ds or fj are uniformly over-expressed in a pkpk mutant wing, the pkpk wing hair phenotype is modified to a more distal polarity in the anterior wing and in distal regions of the posterior wing (Figure 5F, 5G and 5H). These modifications of the pkpk hair phenotype are similar to those generated by reduced activity of the same Ft/Ds pathway genes (see Figure 4).


Two frizzled planar cell polarity signals in the Drosophila wing are differentially organized by the Fat/Dachsous pathway.

Hogan J, Valentine M, Cox C, Doyle K, Collier S - PLoS Genet. (2011)

Over-expression of Ft/Ds pathway genes modifies the pkpk hair polarity phenotype.All micrographs are of the female dorsal wing surface. Arrows indicate local hair polarity. Red shaded ovals represent regions where hair polarity differs from wild-type. Red arrows indicate where local hair polarity differs from that seen on a pkpk30 homozygous wing. (A) Wild-type wing. (B) MS1096-gal4; UAS-ft wing. (C) MS1096-gal4; UAS-ds wing. (D) MS1096-gal4; UAS-fj wing. (E) pkpk30/pkpk30 wing. (F) MS1096-gal4; UAS-ft, pkpk30/pkpk30 wing. (G) MS1096-gal4; pkpk30/pkpk30; UAS-ds wing. (H) MS1096-gal4; UAS-fj, pkpk30/pkpk30 wing.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3040658&req=5

pgen-1001305-g005: Over-expression of Ft/Ds pathway genes modifies the pkpk hair polarity phenotype.All micrographs are of the female dorsal wing surface. Arrows indicate local hair polarity. Red shaded ovals represent regions where hair polarity differs from wild-type. Red arrows indicate where local hair polarity differs from that seen on a pkpk30 homozygous wing. (A) Wild-type wing. (B) MS1096-gal4; UAS-ft wing. (C) MS1096-gal4; UAS-ds wing. (D) MS1096-gal4; UAS-fj wing. (E) pkpk30/pkpk30 wing. (F) MS1096-gal4; UAS-ft, pkpk30/pkpk30 wing. (G) MS1096-gal4; pkpk30/pkpk30; UAS-ds wing. (H) MS1096-gal4; UAS-fj, pkpk30/pkpk30 wing.
Mentions: To complement the studies described above, we looked at the effect of over-expressing Ft/Ds pathway genes on the Early Fz(Sple) and Late Fz(Pk) signals. Uniform over-expression of ft (MS1096-gal4; UAS-ft) results in similar wing morphology to loss of ft activity (Figure 5B) and alters posterior ridges. ft over-expression alters hair polarity in the same proximal region of the wing affected by reduced Ft/Ds pathway gene activity (see Figure 3), but also generates variable hair polarity changes in more distal regions of the wing (red ovals in Figure 5B). Uniform over-expression of ds or fj results in a similar wing shape, posterior ridge and hair polarity phenotype to reduced activity of the same genes (Figure 5C and 5D). When ft, ds or fj are uniformly over-expressed in a pkpk mutant wing, the pkpk wing hair phenotype is modified to a more distal polarity in the anterior wing and in distal regions of the posterior wing (Figure 5F, 5G and 5H). These modifications of the pkpk hair phenotype are similar to those generated by reduced activity of the same Ft/Ds pathway genes (see Figure 4).

Bottom Line: There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein.The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model.Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Marshall University, Huntington, West Virginia, United States of America.

ABSTRACT
The regular array of distally pointing hairs on the mature Drosophila wing is evidence for the fine control of Planar Cell Polarity (PCP) during wing development. Normal wing PCP requires both the Frizzled (Fz) PCP pathway and the Fat/Dachsous (Ft/Ds) pathway, although the functional relationship between these pathways remains under debate. There is strong evidence that the Fz PCP pathway signals twice during wing development, and we have previously presented a Bidirectional-Biphasic Fz PCP signaling model which proposes that the Early and Late Fz PCP signals are in different directions and employ different isoforms of the Prickle protein. The goal of this study was to investigate the role of the Ft/Ds pathway in the context of our Fz PCP signaling model. Our results allow us to draw the following conclusions: (1) The Early Fz PCP signals are in opposing directions in the anterior and posterior wing and converge precisely at the site of the L3 wing vein. (2) Increased or decreased expression of Ft/Ds pathway genes can alter the direction of the Early Fz PCP signal without affecting the Late Fz PCP signal. (3) Lowfat, a Ft/Ds pathway regulator, is required for the normal orientation of the Early Fz PCP signal but not the Late Fz PCP signal. (4) At the time of the Early Fz PCP signal there are symmetric gradients of dachsous (ds) expression centered on the L3 wing vein, suggesting Ds activity gradients may orient the Fz signal. (5) Localized knockdown or over-expression of Ft/Ds pathway genes shows that boundaries/gradients of Ft/Ds pathway gene expression can redirect the Early Fz PCP signal specifically. (6) Altering the timing of ds knockdown during wing development can separate the role of the Ft/Ds pathway in wing morphogenesis from its role in Early Fz PCP signaling.

Show MeSH