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 eukary-otic 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. Introduction The evolution of multicellularity was a prerequisite to the diversification of complex morphologies in living organisms. The multi-cellular body plan (as defined in [1]) has three basic variants that can be described by the number of planes that orient cell division , which is typically mirrored in development by the dimen-sionality of tissue growth. A single cell that cleaves repeatedly in one plane gives rise to unbranched uniseriate filaments, cleav-age in two planes gives rise to branching uniseriate filaments or pseudo-parenchymatous tissues, and cleavage in three planes leads to parenchymatous tissues [2-5]. Unicellularity represents the morphological condition preceding the origin of multicellular forms across the tree of life. The unbranched filament is likely the simplest and most ancient variant of the multicellular body plan, and filamentous branching forms represent a key step in the evolution of complex three-dimensional multicellular morphologies [6]. It is noteworthy that despite the constraints imposed by cell division patterns, development may also occur in three dimensions in branching filaments through the establishment of new growth directions when branch points are specified. Multi-cellularity arose repeatedly in the different eukaryotic kingdoms, leading to multiple independent acquisitions of branched fila-mentous forms. These forms have been maintained as a dominant (e.g., brown, red and green algae, fungi) or transient state
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Yoan Coudert, Steven Harris, Bénédicte Charrier. Design Principles of Branching Morphogenesis in Filamentous Organisms. Current Biology - CB, Elsevier, 2019, 29 (21), pp.R1149-R1162. ⟨10.1016/j.cub.2019.09.021⟩. ⟨hal-02352988⟩

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