Abstract
Author SummaryA major challenge in developmental biology is to understand how patterns of gene activity are translated into complex three-dimensional forms, like hearts, wings, or flowers. Addressing this problem has not been easy, partly because of the difficulties in quantifying the effects of genes on shape and also because we lack frameworks that allow hypotheses about underlying mechanisms to be evaluated. Here we address this issue through a combination of experimental and computational approaches, using the Snapdragon flower as a model system. By quantifying the shapes of these flowers in a range of mutants with reduced or increased activity of particular genes, we show how the complex floral shape depends on the way genes act in combination in each petal region. The proposed interactions were tested by incorporating them into a computational model of the growing flower. Quantitative comparisons reveal a good agreement between the shapes generated by the model and those observed experimentally, confirming our underlying hypothesis. The Snapdragon flower, with its tightly fitting upper and lower petals, has evolved as a specialised mechanism for targeting pollinators. Our article shows how the development and evolution of such forms may have arisen by natural tinkering with the local effects of genes on growth.
Highlights
Major progress has been made in the genetic dissection of organ and appendage development, the process whereby gene activities lead to particular tissue shapes is still poorly understood
Wing morphogenesis in Drosophila is one of the best defined developmental systems [1], yet little is known about how regional gene activities in the imaginal disc are translated into final wing shape [2]
A major challenge in developmental biology is to understand how patterns of gene activity are translated into complex three-dimensional forms, like hearts, wings, or flowers
Summary
Major progress has been made in the genetic dissection of organ and appendage development, the process whereby gene activities lead to particular tissue shapes is still poorly understood. Wing morphogenesis in Drosophila is one of the best defined developmental systems [1], yet little is known about how regional gene activities in the imaginal disc are translated into final wing shape [2]. Addressing this problem has not been easy for several reasons. Genes that modify shape are normally identified through their overall phenotypic effects, making it difficult to establish how particular regions of the tissue are affected. Shape is often described in qualitative terms like ‘‘rounder’’ or ‘‘more elongated,’’ making it difficult to quantify and compare the effects of different gene combinations. We lack modelling frameworks that allow hypotheses for how genes control morphogenesis to be evaluated quantitatively
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