Analysis of pattern precision shows that Drosophila segmentation develops substantial independence from gradients of maternal gene products

Abstract

We analyze the relation between maternal gradients and segmentation in Drosophila, by quantifying spatial precision in protein patterns. Segmentation is first seen in the striped expression patterns of the pair-rule genes, such as even-skipped (eve). We compare positional precision between Eve and the maternal gradients of Bicoid (Bcd) and Caudal (Cad) proteins, showing that Eve position could be initially specified by the maternal protein concentrations but that these do not have the precision to specify the mature striped pattern of Eve. By using spatial trends, we avoid possible complications in measuring single boundary precision (e.g., gap gene patterns) and can follow how precision changes in time. During nuclear cleavage cycles 13 and 14, we find that Eve becomes increasingly correlated with egg length, whereas Bcd does not. This finding suggests that the change in precision is part of a separation of segmentation from an absolute spatial measure, established by the maternal gradients, to one precise in relative (percent egg length) units.

Canalization of segmentation and its evolution in Drosophila

“…Scaling of gene expression patterns for both gap and pair-rule genes echoes results on Bcd and Hb expression (1,4,7) and suggests that the absolute shift in gene expression between the large-and small-embryo lines is established early in embryogenesis. To test whether scaling is a maternal or zygotic property, we analyzed stripe locations in F 1 , F 2 , and F 3 embryos from reciprocal crosses between the Ind and Fra lines (Fig.…”

“…One such trait is the well studied pathway for establishing the anterior-posterior (A-P) axis in Drosophila, which has come into focus with renewed interest in the genetic basis of phenotypic robustness (1)(2)(3)(4)(5). In a seminal paper, Houchmandzedah, Wieschaus, and Leibler (1) measured spatiotemporal variability in the Bicoid (Bcd) diffusion gradient and its downstream target hunchback (hb).…”

“…Scaling, the expression of segmentation genes at the same relative position along the length of the embryo independent of embryo length, is a second reported property of the A-P patterning system (1,4). The molecular or genetic basis for this feature of the patterning system is not known.…”

“…The molecular or genetic basis for this feature of the patterning system is not known. A study of gene expression through the developmental stages during which Bcd activates hb expression (4,5) indicates that the Bcd gradient is established along an absolute coordinate system, independent of (intrastrain) egg length, whereas Hb and even-skipped (Eve) patterns scale with embryo length. The establishment of spatial precision, as reflected in Hb and Eve expression, coincides with this transformation of scale (4).…”

“…A study of gene expression through the developmental stages during which Bcd activates hb expression (4,5) indicates that the Bcd gradient is established along an absolute coordinate system, independent of (intrastrain) egg length, whereas Hb and even-skipped (Eve) patterns scale with embryo length. The establishment of spatial precision, as reflected in Hb and Eve expression, coincides with this transformation of scale (4). On the other hand, the Bcd gradient and Hb expression have also been investigated in three distantly related Dipteran species with egg sizes differing by a factor of five; Bcd gradients were found to scale with embryo size (5).…”