The problem of morphogenesis: unscripted biophysical control systems in plants

Abstract

The relative simplicity of plant developmental systems, having evolved within the universal constraints imposed by the plant cell wall, may allow us to outline a consistent developmental narrative that is not currently possible in the animal kingdom. In this article, I discuss three aspects of the development of the mature form in plants, approaching them in terms of the role played by the biophysics and mechanics of the cell wall during growth. First, I discuss axis extension in terms of a loss of stability-based model of cell wall stress relaxation and I introduce the possibility that cell wall stress relaxation can be modeled as a binary switch. Second, I consider meristem shape and surface conformation as a controlling element in the morphogenetic circuitry of plant organogenesis at the apex. Third, I approach the issue of reproductive differentiation and propose that the multicellular sporangium, a universal feature of land plants, acts as a stress-mechanical lens, focusing growth-induced stresses to create a geometrically precise mechanical singularity that can serve as an inducing developmental signal triggering the initiation of reproductive differentiation. Lastly, I offer these three examples of biophysically integrated control processes as entry points into a narrative that provides an independent, nongenetic context for understanding the evolution of the apoplast and the morphogenetic ontogeny of multicellular land plants.

Fig. 1

LOS-driven stress relaxation in a cylindrical cell is limited by the increase in volume and the resulting pressure drop. The turgor pressure P _CR at which stress relaxation will occur is a function of the geometry and material properties of the cell wall

Fig. 2

Surface topology is a critical element in the cycle of shape changes that characterize apical morphogenesis. Cell division and growth leads to distortion of the apical surface, which redirects growth stress and reorients new partition walls

Fig. 3

Immature sporangia of the fern Cyrtomium sp. All land plant sporangia share common features. Note the distinct sporangial wall cells and central sporogenous region. Scale bar = 50 μ

Fig. 4

Lilium sp. premeiotic anther sacs. Early anther development in the flowering plants shows striking similarities to sporangial development throughout the plant kingdom. Scale bar = 100 μ