Generation of shape complexity through tissue conflict resolution
Alexandra B Rebocho Paul Southam J Richard Kennaway J Andrew Bangham Enrico Coen
John Innes Centre, England; University of East Anglia, England
Published February 7, 2017
Cite as eLife 2017;6:e20156
Out-of-plane tissue deformations are key morphogenetic events during plant and animal development that generate 3D shapes, such as flowers or limbs. However, the mechanisms by which spatiotemporal patterns of gene expression modify cellular behaviours to generate such deformations remain to be established. We use the Snapdragon flower as a model system to address this problem. Combining cellular analysis with tissue-level modelling, we show that an orthogonal pattern of growth orientations plays a key role in generating out-of-plane deformations. This growth pattern is most likely oriented by a polarity field, highlighted by PIN1 protein localisation, and is modulated by dorsoventral gene activity. The orthogonal growth pattern interacts with other patterns of differential growth to create tissue conflicts that shape the flower. Similar shape changes can be generated by contraction as well as growth, suggesting tissue conflict resolution provides a flexible morphogenetic mechanism for generating shape diversity in plants and animals.
Plant and animal organs come in many different shapes, from pitcher-shaped leaves and butterfly wings, to orchid flowers and the convoluted shape of the brain. Unlike pottery or sculpture, no external hand guides the formation of these biological structures; they arise on their own, through sheets of cells developing into particular three-dimensional shapes. But how does this process of self-making operate? We know that patterns of gene activity are important, because mutations that disrupt these patterns change the shape of the organ. But it is not clear how these patterns lead to sheets of cells curving and bending themselves into their characteristic three-dimensional shapes.
Plants are particularly useful tools for studying how three-dimensional organs form because, unlike animals, their cells do not slide relative to each other, which makes the analysis simpler. Rebocho et al. used a combination of computational modelling and cell analysis to study how the intricately shaped flowers of plants known as Snapdragons form. The experiments show that genes control the shape of Snapdragon flowers by causing groups of cells to grow at different rates and in different directions. This pattern of growth creates internal conflicts that are resolved by sheets of cells curving in particular ways, accounting for the three-dimensional shape.
Rebocho et al. propose that the principles of tissue conflict resolution described in this work may also underlie the development and evolution of many other plant and animal organ shapes. A future challenge is to identify the cellular mechanisms that link patterns of gene activity to the generation and resolution of conflicting cell behaviours.
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