Cellularization across eukaryotes: Conserved mechanisms and novel strategies

McCartney, Brooke M.; Dudin, Omaya

doi:10.1016/j.ceb.2023.102157

Cited by 13 publications

(11 citation statements)

References 101 publications

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“…Our results show that C. perkinsii undergoes palintomic division (Fig. 4F), involving cell cleavages coupled to open mitosis, diverging from the coenocytic development and cellularization in other studied ichthyosporeans ( 52 ). Notably, the development of C. perkinsii is stereotypical and occurs independently of apparent external trigger, leading to the formation of colonies harboring hundreds of cells (Fig.…”

Section: Discussionmentioning

confidence: 60%

“…1A) ( 46 , 47 ), exhibit a variety of life cycles that combine fungal-like characteristics with transient multicellular stages reminiscent of early animal development ( 47 ). Most ichthyophonids, including the model Sphaeroforma arctica , undergo coenocytic development, characterized by synchronized nuclear divisions without cytokinesis ( 48–52 ). This process depends on an acentriolar microtubule organizing centre (MTOC) that drives a fungal-like closed mitosis ( 53 ).…”

Section: Introductionmentioning

confidence: 99%

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A multicellular developmental program in a close animal relative

Olivetta,

Bhickta,

Chiaruttini

et al. 2024

Preprint

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All animals develop from a single-celled zygote into a complex multicellular organism through a series of precisely orchestrated processes. Despite the remarkable conservation of early embryogenesis across animals, the evolutionary origins of this process remain elusive. By combining time-resolved imaging and transcriptomic profiling, we show that single cells of the ichthyosporean Chromosphaera perkinsii - a close relative that diverged from animals approximately 1 billion years ago - undergo symmetry breaking and develop through cleavage divisions to produce a prolonged multicellular colony with distinct co-existing cell types. Our findings about the autonomous developmental program of C. perkinsii, hint that such animal-like multicellular development is either much older than previously thought or evolved convergently in ichthyosporeans.

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Section: Discussionmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

A multicellular developmental program in a close animal relative

Olivetta,

Bhickta,

Chiaruttini

et al. 2024

Preprint

Self Cite

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“…Switching between unicellular and multicellular organization is thus a common part of the development of multicellular fungi and their lifestyles and helps these organisms to either adapt to or escape from unfavorable living conditions. Multinucleated cells are also frequent in animals [ 130 ]. They can be formed by cell–cell fusion and are then referred to as syncytia.…”

Section: Cellular Structuresmentioning

confidence: 99%

Looking outside the box: a comparative cross-kingdom view on the cell biology of the three major lineages of eukaryotic multicellular life

Panstruga

Antonin

Lichius

2023

Cell. Mol. Life Sci.

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Many cell biological facts that can be found in dedicated scientific textbooks are based on findings originally made in humans and/or other mammals, including respective tissue culture systems. They are often presented as if they were universally valid, neglecting that many aspects differ—in part considerably—between the three major kingdoms of multicellular eukaryotic life, comprising animals, plants and fungi. Here, we provide a comparative cross-kingdom view on the basic cell biology across these lineages, highlighting in particular essential differences in cellular structures and processes between phyla. We focus on key dissimilarities in cellular organization, e.g. regarding cell size and shape, the composition of the extracellular matrix, the types of cell–cell junctions, the presence of specific membrane-bound organelles and the organization of the cytoskeleton. We further highlight essential disparities in important cellular processes such as signal transduction, intracellular transport, cell cycle regulation, apoptosis and cytokinesis. Our comprehensive cross-kingdom comparison emphasizes overlaps but also marked differences between the major lineages of the three kingdoms and, thus, adds to a more holistic view of multicellular eukaryotic cell biology.

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“…Multinucleated cells, also known as syncytia, are found across the tree of life (Ogle et al, 2005; Mela et al, 2020; Olsen, 2020; McCartney and Dudin, 2023). Syncytia can arise in two ways; through nuclear division in the absence of cytokinesis or through cell-cell fusion.…”

Section: Introductionmentioning

confidence: 99%

Molecular compartmentalization in a syncytium: restricted mobility of proteins within the sea urchin skeletogenic mesenchyme

Khor

Guerrero-Santoro

Ettensohn

2023

Preprint

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Multinucleated cells, or syncytia, are found in diverse taxa. Their biological function is often associated with the compartmentalization of biochemical or cellular activities within the syncytium. How such compartments are generated and maintained is poorly understood. The sea urchin embryonic skeleton is secreted by a syncytium, and local patterns of skeletal growth are associated with distinct sub-domains of gene expression within the syncytium. For such molecular compartments to be maintained and to control local patterns of skeletal growth: 1) the mobility of TFs must be restricted to produce stable differences in the transcriptional states of nuclei within the syncytium, and 2) the mobility of biomineralization proteins must also be restricted to produce regional differences in skeletal growth patterns. To test these predictions, we expressed fluorescently-tagged forms of transcription factors and biomineralization proteins in sub-domains of the skeletogenic syncytium. We found that both classes of proteins have restricted mobility within the syncytium and identified motifs that limit their mobility. Our findings have general implications for understanding the functional and molecular compartmentalization of syncytia.

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Cellularization across eukaryotes: Conserved mechanisms and novel strategies

Cited by 13 publications

References 101 publications

A multicellular developmental program in a close animal relative

A multicellular developmental program in a close animal relative

Looking outside the box: a comparative cross-kingdom view on the cell biology of the three major lineages of eukaryotic multicellular life

Molecular compartmentalization in a syncytium: restricted mobility of proteins within the sea urchin skeletogenic mesenchyme

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