Abstract

During development, Arabidopsis thaliana sepal primordium cells grow, divide and interact with their neighbours, giving rise to a sepal with the correct size, shape and form. Arabidopsis sepals have proven to be a good system for elucidating the emergent processes driving morphogenesis due to their simplicity, their accessibility for imaging and manipulation, and their reproducible development. Sepals undergo a basipetal gradient of growth, with cessation of cell division, slow growth and maturation starting at the tip of the sepal and progressing to the base. In this review, I discuss five recent examples of processes during sepal morphogenesis that yield emergent properties: robust size, tapered tip shape, laminar shape, scattered giant cells and complex gene expression patterns. In each case, experiments examining the dynamics of sepal development led to the hypotheses of local rules. In each example, a computational model was used to demonstrate that these local rules are sufficient to give rise to the emergent properties of morphogenesis.

Highlights

  • During development, Arabidopsis thaliana sepal primordium cells grow, divide and interact with their neighbours, giving rise to a sepal with the correct size, shape and form

  • For the past 15 years or so, biologists have become increasingly aware that reductionist experimental approaches, while certainly useful, have not been sufficient to understand the complexity of biological systems, their emergent properties

  • Systems biology came of age at the same time as functional-omics technologies were exploding

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Summary

Morphogenesis as an emergent process

How does a flower develop from a few cells to its final beautiful and elaborate shape? Morphogenesis is the development of size, shape, structure and form, which has long fascinated developmental biologists. Plant biologists have shown that the spiral pattern of primordia forming around the meristem can emerge from a simple local rule together with growth and cell division (Figure 1a). The models of phyllotaxy were developed following extensive analysis of PIN1 polarisation, live imaging of PIN1 dynamics in the developing meristem (Heisler et al, 2005; Reinhardt et al, 2003) Extracting information from these complex imaging datasets requires sophisticated computational image processing (Barbier de Reuille et al, 2015; Fernandez et al, 2010; Roeder, Cunha, Burl, & Meyerowitz, 2012; Wolny et al, 2020). Deciphering the emergent processes that drive morphogenesis requires iterative rounds of modelling and dynamic experimentation, with both refining and informing each other (Chickarmane et al, 2010; Roeder et al, 2011)

F Spatial gene expression patterns
Sepal definition
Advantages of Arabidopsis sepals as a model system for morphogenesis
The outcome of morphogenesis
Arabidopsis sepal development and staging
Growth pattern of sepals
Case studies of emergent processes in sepal morphogenesis
Emergence example 1
Emergence example 2
Emergence example 3
Emergence example 4
Emergence example 5
Findings
Conclusion
Full Text
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