Contact area–dependent cell communication and the morphological invariance of ascidian embryogenesis

Guignard, Léo; Fiúza, Ulla-Maj; Leggio, Bruno; Laussu, Julien; Faure, Emmanuel; Michelin, Gaël; Biasuz, Kilian; Hufnagel, Lars; Malandain, Grégoire; Godin, Christophe; Lemaire, Patrick

doi:10.1126/science.aar5663

Cited by 108 publications

(145 citation statements)

References 133 publications

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“…To demonstrate the benefits of the protocol for conducting a quantitative study of LB deconstruction, we show how a quantitative method using image segmentation and tracking can extract information at the tissular scale. Similar approaches have previously allowed the establishment of computational frameworks, leading to significant advances in multicellular plant and animal organisms [9,10]. Therefore, our imaging protocol can be a foundation to understanding hydrolysis at the yet little-explored tissular scale with unprecedented detail.…”

Section: Introductionmentioning

confidence: 87%

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Three-Dimensional Imaging of Plant Cell Wall Deconstruction Using Fluorescence Confocal Microscopy

Zoghlami

Refahi

Terryn

et al. 2020

Sustainable Chemistry

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Lignocellulosic biomass (LB) is recalcitrant to enzymatic hydrolysis due to its compact and complex cell wall structure. To identify the parameters behind LB recalcitrance, experimental data over hydrolysis time must be collected. Here, we describe a novel method to collect time-lapse images during cell wall deconstruction by enzymatic hydrolysis. The protocol includes instructions for sample preparation, layout of a custom designed incubation chamber and instructions for confocal time lapse acquisition. The protocol sets out a detailed plan where cross-sections of untreated and pretreated poplar samples are mounted in a sealed frame containing a buffer and an enzymatic cocktail. The sealed frame is then placed into an incubator to maintain the sample at a constant temperature of 50 °C, which is optimal for enzymatic reaction while avoiding enzymatic cocktail evaporation. Using lignin natural autofluorescence, confocal z-stacks of untreated and pretreated samples were acquired at regular time intervals during enzymatic hydrolysis for 24 h. Acquisition parameters were optimized to compromise between image resolution and reduced photo-bleaching. The acquired image might then be processed by further development of algorithms to extract precise quantitative information on cell wall deconstruction. This protocol is an important first step towards elucidating the underlying parameters of LB recalcitrance by allowing the acquisition of high-quality images of LB hydrolysis for extracting quantitative data on LB deconstruction.

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Section: Introductionmentioning

confidence: 87%

“…Below, "PAUSE STEP" indicates some critical technical details used to apply the procedure correctly. (10,15 and 20 min) were tested. Incubation time and temperature were selected in order to improve the enzymatic hydrolysis while conserving plant cell structure.…”

Section: Methodsmentioning

confidence: 99%

Three-Dimensional Imaging of Plant Cell Wall Deconstruction Using Fluorescence Confocal Microscopy

Zoghlami

Refahi

Terryn

et al. 2020

Sustainable Chemistry

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“…However, it remains an important challenge to generate such faithful digital representations. Substantial efforts in animal developmental biology did not achieve single-cell resolution (Lein et al, 2007, 2007; Rein et al, 2002; Lein et al, 2007; Dreyer et al, 2010; Asadulina et al, 2012; Anderson et al, 2019), except for C. elegans (Long et al, 2009) and the early embryo of the ascidian Phallusia mammillata (Guignard et al, 2020; Sladitschek et al, 2020). Model plants, such as Arabidopsis thaliana , are uniquely suited for this task.…”

Section: Introductionmentioning

confidence: 99%

A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule

Vijayan

Tofanelli

Strauss

et al. 2020

Preprint

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A fundamental question in biology is how morphogenesis integrates the multitude of distinct processes that act at different scales, ranging from the molecular control of gene expression to cellular coordination in a tissue. Investigating morphogenesis of complex organs strongly benefits from three-dimensional representations of the organ under study. Here, we present a digital analysis of ovule development from Arabidopsis thaliana as a paradigm for a complex morphogenetic process. Using machine-learning-based image analysis we generated a three-dimensional atlas of ovule development with cellular resolution. It allows quantitative stage- and tissue-specific analysis of cellular patterns. Exploiting a fluorescent reporter enabled precise spatial determination of gene expression patterns, revealing subepidermal expression of WUSCHEL. Underlying the power of our approach, we found that primordium outgrowth progresses evenly, discovered a novel mode of forming a new cell layer, and detected a new function of INNER NO OUTER in restricting cell proliferation in the nucellus. Moreover, we identified two distinct subepidermal cell populations that make crucial contributions to ovule curvature. Our work demonstrates the expedience of a three-dimensional digital representation when studying the morphogenesis of an organ of complex cellular architecture and shape that eventually consists of 1,900 cells.

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“…Geometric and cell contact constraints have been suggested to drive invariant development in ascidians with links to asymmetric cell division and cell fate specification 40 . Seam cells are highly dynamic and reconnect to each other after every round of cell division.…”

Section: Discussionmentioning

confidence: 99%

A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans

Koneru

Quah

Ghose

et al. 2021

Sci Rep

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Developmental patterning in Caenorhabditis elegans is known to proceed in a highly stereotypical manner, which raises the question of how developmental robustness is achieved despite the inevitable stochastic noise. We focus here on a population of epidermal cells, the seam cells, which show stem cell-like behaviour and divide symmetrically and asymmetrically over post-embryonic development to generate epidermal and neuronal tissues. We have conducted a mutagenesis screen to identify mutants that introduce phenotypic variability in the normally invariant seam cell population. We report here that a null mutation in the fusogen eff-1 increases seam cell number variability. Using time-lapse microscopy and single molecule fluorescence hybridisation, we find that seam cell division and differentiation patterns are mostly unperturbed in eff-1 mutants, indicating that cell fusion is uncoupled from the cell differentiation programme. Nevertheless, seam cell losses due to the inappropriate differentiation of both daughter cells following division, as well as seam cell gains through symmetric divisions towards the seam cell fate were observed at low frequency. We show that these stochastic errors likely arise through accumulation of defects interrupting the continuity of the seam and changing seam cell shape, highlighting the role of tissue homeostasis in suppressing phenotypic variability during development.

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Contact area–dependent cell communication and the morphological invariance of ascidian embryogenesis

Cited by 108 publications

References 133 publications

Three-Dimensional Imaging of Plant Cell Wall Deconstruction Using Fluorescence Confocal Microscopy

Three-Dimensional Imaging of Plant Cell Wall Deconstruction Using Fluorescence Confocal Microscopy

A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule

A role for the fusogen eff-1 in epidermal stem cell number robustness in Caenorhabditis elegans

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