The Evolution of Branching in Land Plants: Between Conservation and Diversity

Coudert, Yoan

doi:10.1007/978-3-319-33038-9_63-1

Cited by 2 publications

(6 citation statements)

References 28 publications

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“…Importantly, these principles are not restricted to filamentous organisms. Lateral inhibition also governs branching morphogenesis in animal organs or plant root systems [62,68], and apical dominance represents a major control mechanism of the three-dimensional architecture of plant shoot systems [8,69,70,81,125]. Although it is less clear how long-range inhibitory signaling affects morphogenesis in branched animal organs, this raises the question of whether branching may be a 'default mode' and inhibitory cues dominate over branch promoting factors.…”

Section: Discussionmentioning

confidence: 99%

“…It is well established that auxin, a small indole-derived signaling molecule, produced in shoot tips inhibits branch development at a distance and is a conserved regulator of apical dominance in land plant leafy shoots [8,70]. In moss, auxin promotes the differentiation of growing chloronemal cells into caulonemal cells Like multicellular brown algae, green algae, and plants, most fungi are sessile organisms.…”

Section: Auxin Inhibitory Gradientsmentioning

confidence: 99%

“…Branching is also a conspicuous morphological feature of multicellular organisms with parenchymatous bodies of varying complexity, including land plants [8], and numerous vertebrate and invertebrate animal organs such as the lung, kidney, mammary gland, prostate gland, vasculature (blood vessels) and tracheal system [9,10]. The regulation of their morphogenesis has been extensively investigated at the molecular and cellular levels, and exhaustive reviews have been written on these topics (see for example [9][10][11][12][13] for animal organs, and [14][15][16] for plants).…”

Section: Introductionmentioning

confidence: 99%

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Design Principles of Branching Morphogenesis in Filamentous Organisms

2019

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Auxin Inhibitory Gradientsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Design Principles of Branching Morphogenesis in Filamentous Organisms

2019

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“…Understanding the mechanisms that determine the shape of living organisms is a central goal of biology. In plants, branching patterns are a major determinant of shape diversity 6,7 . Indeed, most plant shoots have the capacity to develop indeterminately, which allows for the continuous production of new growth axes, or branches, throughout their lifetime 7 .…”

Section: Introductionmentioning

confidence: 99%

“…In plants, branching patterns are a major determinant of shape diversity 6,7 . Indeed, most plant shoots have the capacity to develop indeterminately, which allows for the continuous production of new growth axes, or branches, throughout their lifetime 7 . Apical dominance, the inhibitory effect exerted by shoot apices on the initiation or outgrowth of distant lateral buds, is a fundamental regulatory mechanism of branching form development.…”

Section: Introductionmentioning

confidence: 99%

Apical and basal auxin sources pattern shoot branching in a moss

Thelander

Landberg

Muller

et al. 2022

Preprint

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Shoot branching mechanisms where branches arise in association with leaves – referred to as lateral or axillary branching – evolved by convergence in the sporophyte of vascular plants and the gametophyte of bryophytes, and accompanied independent events of plant architectural diversification. Previously, we showed that three hormonal cues, including auxin, have been recruited independently to co-ordinate branch patterning in flowering plant leafy shoots and moss gametophores (Coudert, Palubicki et al., 2015). Moreover, auxin-mediated apical dominance, which relies on local auxin production, has been proposed as a unifying molecular regulatory mechanism of branch development across land plants. Whilst our previous work in the moss Physcomitrium patens has gathered indirect evidence supporting the notion that auxin synthesized in gametophore apices regulates branch formation at a distance, direct genetic evidence for a role of auxin biosynthesis in gametophore branching control is still lacking. Here, we show that gametophore apex decapitation promotes branch emergence through massive and rapid transcriptional reprogramming of auxin-responsive genes and altering auxin biosynthesis gene activity. Specifically, we identify a subset of P. patens TRYPTOPHAN AMINO-TRANSFERASE (TAR) and YUCCA FLAVIN MONOOXYGENASE-LIKE (YUC) auxin biosynthesis genes expressed in apical and basal regions of the gametophore, and show that they are essential for branch initiation and outgrowth control. Our results demonstrate that local auxin biosynthesis coordinates branch patterning in moss and thus constitutes a shared and ancient feature of shoot architecture control in land plants.

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The Evolution of Branching in Land Plants: Between Conservation and Diversity

Cited by 2 publications

References 28 publications

Design Principles of Branching Morphogenesis in Filamentous Organisms

Design Principles of Branching Morphogenesis in Filamentous Organisms

Apical and basal auxin sources pattern shoot branching in a moss

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