Design Principles of Branching Morphogenesis in Filamentous Organisms

Abstract

The radiation of life on Earth was accompanied by the diversification of multicellular body plans in the eukaryotic kingdoms Animalia, Plantae, Fungi and Chromista. Branching forms are ubiquitous in nature and evolved repeatedly in the above lineages. The developmental and genetic basis of branch formation is well studied in the three-dimensional shoot and root systems of land plants, and in animal organs such as the lung, kidney, mammary gland, vasculature, etc. Notably, recent thought-provoking studies combining experimental analysis and computational modeling of branching patterns in whole animal organs have identified global patterning rules and proposed unifying principles of branching morphogenesis. Filamentous branching forms represent one of the simplest expressions of the multicellular body plan and constitute a key step in the evolution of morphological complexity. Similarities between simple and complex branching forms distantly related in evolution are compelling, raising the question whether shared mechanisms underlie their development. Here, we focus on filamentous branching organisms that represent major study models from three distinct eukaryotic kingdoms, including the moss Physcomitrella patens (Plantae), the brown alga Ectocarpus sp. (Chromista), and the ascomycetes Neurospora crassa and Aspergillus nidulans (Fungi), and bring to light developmental regulatory mechanisms and design principles common to these lineages. Throughout the review we explore how the regulatory mechanisms of branching morphogenesis identified in other models, and in particular animal organs, may inform our thinking on filamentous systems and thereby advance our understanding of the diverse strategies deployed across the eukaryotic tree of life to evolve similar forms. Gross morphology of single clones (A-C) and dissected branching filaments (D-F) in the moss Physcomitrella patens (A,D), the brown alga Ectocarpus sp. (B,E), and the filamentous fungus Aspergillus nidulans (C,F). Fungal hyphae were fixed and stained with Hoechst 33258 and Calcofluor to visualize nuclei and septa, respectively.

Acquisition of cell identity in the brown alga Ectocarpus: which of time, cell shape or position matters most?

“…Adult Physcomitrium (former Physcomitrella) gametophytes are comprised of branched uniseriate filaments growing apically. Interestingly, the first cell types differentiating from the spore, the chloronemata, are slow growing and committed mainly to photosynthetic assimilatory function, while the second cell type, the caulonemata, are fast growing and forage for water and nutrients (Coudert et al, 2019;Cove, 2005). Nicely, this spatial distribution of functions is reminiscent of what is observed in Ectocarpus.…”

Theory of branching morphogenesis by local interactions and global guidance

“…This is strengthened by our findings that the predictions of the model are similar in both 2D and 3D settings. Interestingly, it has recently been proposed that the types of stochastic rules governing tip growth that we model here are conserved for the morphogenesis of various filamentous organisms such as plants or Fungi 52 . Understanding quantitatively the relative contribution of each mechanism is also of key importance for the morphogenesis of branched mammalian organs 53 : Mammary gland, pancreas or late-kidney morphogenesis have been proposed to follow a simpler form of these stochastic models in the absence of external guidance 22 , although kidney morphogenesis has been suggested to require stronger self-avoidance (denoted by the parameter f s in our framework) at early stages to avoid premature termination 54 .…”

Theory of branching morphogenesis by local interactions and global guidance

“…This theoretical framework, although we have applied it here to a specific geometry in neuronal branching, is highly general and could be applied to any branching structure such as in angiogenesis or the branching of epithelial organs, where similar questions on external guidance vs. local self-organization rules arise [48][49][50]. Similarly, it has recently been proposed that these types of stochastic tip interaction mechanisms are conserved for the morphogenesis of various filamentous organisms such as plants or Fungi [51]. Understanding quantitatively the relative contribution of each mechanism is also of key importance for the morphogenesis of branched mammalian organs: Mammary gland or late-kidney morphogenesis have been proposed to follow a simpler form of these stochastic models in the absence of external guidance [22], although kidney morphogenesis has been suggested to require larger amount of self-avoidance strength (denoted by the parameter f s in our framework) at early stages to avoid premature termination [52].…”