A New Scaling Measure Quantifies the Conservation of Proportions of Gene Expression Profiles in Developing Organic Shapes

Most organisms and organs go through a developmental phase before they reach their adult size and proportions. We studied the scaling properties of the fruit fly embryo and its wing. Even in batches of genetically identical embryos their length fluctuates about 10% around its mean value of 0.5mm. Yet, expression domains of certain genes that define the adult body plan of the fly extend over areas proportional to embryo length. This kind of scaling property makes sure that while flies may have different sizes, the proportionality of their respective body parts are extremely well conserved, thus ensuring their functionality. A similar phenomenon is observed for the wing, which evolves from a growing tissue known as the imaginal wing disk. Again expression patterns of many genes responsible for the later cell differentiation scale with the growing total size of the wing disk. Here we focus on how scaling of graded expression profiles can be quantified properly in growing tissues. This extends our previous work for the quantification of scaling of discrete expression domains (Mol. Syst. Biol.: 2010, 6;351).

[1]  Johannes Jaeger,et al.  On the dynamic nature of positional information. , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[2]  F. Crick Diffusion in Embryogenesis , 1970, Nature.

[3]  C. Pantin Problems of Relative Growth , 1932, Nature.

[4]  S. Bergmann,et al.  Pre-Steady-State Decoding of the Bicoid Morphogen Gradient , 2007, PLoS biology.

[5]  Olivier Pourquié,et al.  fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo , 2004, Nature.

[6]  C. Nüsslein-Volhard,et al.  A gradient of bicoid protein in Drosophila embryos , 1988, Cell.

[7]  Olivier Pourquié,et al.  Segmental patterning of the vertebrate embryonic axis , 2008, Nature Reviews Genetics.

[8]  E. Davidson,et al.  Gene regulatory networks for development. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  S. Bergmann,et al.  Precision and scaling in morphogen gradient read-out , 2010, Molecular systems biology.

[10]  Marcos Nahmad,et al.  Dynamic Interpretation of Hedgehog Signaling in the Drosophila Wing Disc , 2009, PLoS biology.

[11]  Douglas J Emlen,et al.  Size and shape: the developmental regulation of static allometry in insects , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[12]  David H. Sharp,et al.  Dynamic control of positional information in the early Drosophila embryo , 2004, Nature.

[13]  C. Nüsslein-Volhard,et al.  The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner , 1988, Cell.

[14]  J. Huxley Problems of relative growth , 1932 .

[15]  D'arcy W. Thompson On growth and form i , 1943 .

[16]  L. Wolpert Positional information and the spatial pattern of cellular differentiation. , 1969, Journal of theoretical biology.

[17]  Tetsuya Tabata,et al.  Morphogens, their identification and regulation , 2004, Development.

[18]  Y. Kawakami,et al.  Cell lineage transport: a mechanism for molecular gradient formation , 2006, Molecular systems biology.

[19]  A. Kicheva,et al.  Temporal dynamics of patterning by morphogen gradients. , 2009, Current opinion in genetics & development.

[20]  Y. Kalaidzidis,et al.  Kinetics of Morphogen Gradient Formation , 2007, Science.

[21]  Alexander Spirov,et al.  Formation of the bicoid morphogen gradient: an mRNA gradient dictates the protein gradient , 2009, Development.

[22]  N. Barkai,et al.  Robustness of the BMP morphogen gradient in Drosophila embryonic patterning , 2022 .

[23]  T. Morgan REGENERATION AND LIABILITY TO INJURY. , 1898, Science.

[24]  James Briscoe,et al.  Dynamic Assignment and Maintenance of Positional Identity in the Ventral Neural Tube by the Morphogen Sonic Hedgehog , 2010, PLoS biology.

[25]  D'arcy W. Thompson,et al.  On Growth and Form , 1917, Nature.

[26]  M. Strigini Mechanisms of morphogen movement. , 2005, Journal of neurobiology.

[27]  H. Nijhout,et al.  The Cellular and Physiological Mechanism of Wing-Body Scaling in Manduca sexta , 2010, Science.

[28]  D. Emlen,et al.  The developmental basis for allometry in insects. , 1999, Development.

[29]  Naama Barkai,et al.  Self-enhanced ligand degradation underlies robustness of morphogen gradients. , 2003, Developmental cell.

[30]  A. Kicheva,et al.  Dynamics of Dpp Signaling and Proliferation Control , 2011, Science.

[31]  B. Edgar How flies get their size: genetics meets physiology , 2006, Nature Reviews Genetics.