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Microtubules sustain the fidelity of cellularization in a coenocytic relative of animals

Margarida Araújo, Marine Olivetta, Paolo Ronchi, Viola Oorschot, Arif Khan, Christian Tischer, Hiral Shah, Gautam Dey, Omaya Dudin

Posted on: 17 August 2026 , updated on: 18 August 2026

Preprint posted on 17 February 2026

Cellularization as a mechanism to build cells

Selected by Girish Kale, preLights peer support

Categories: cell biology, developmental biology

Written by: Anne Ruess (Bachelor student at the University of Hohenheim, Stuttgart. Germany)

Background:

A coenocyte is a cell with many nuclei inside, produced through nuclear divisions, all sharing the same cytoplasm. During cellularization, each of these nuclei must end up in its own individual cell. To do this, the cell grows membrane furrows inward to wrap around each nucleus separately. But how does the cell know where to put these furrows? That is exactly what this study aimed to find out.

What I find fascinating about this is how a structure that complex can organize itself so precisely. The fact that this works at all is, frankly, remarkable. Understanding its underlying mechanisms therefore has a big relevance to cell and developmental biology. Cellularization as a feature is shared with animal embryos and certain fungal systems, but they appear to reach it via independent evolutionary paths. Taken together, this makes cellularization not only a recurrent theme across distant lineages, but also a key process in understanding how multicellularity may have first emerged. The species of interest in this preprint, Sphaeroforma arctica, therefore represents a particularly powerful and underexplored model system for studying this process. As a member of the Ichthyosporea, it belongs to one of the closest relatives of animals and undergoes a multinucleate life cycle. This phylogenetic position, neither a classical animal nor a plant model, makes it a valuable system for asking which features of this process are ancient and shared, and which ones evolved separately in different lineages.

Evolution of cellularization, with a focus on ichthyosporea (adapted from Figure 1 in the preprint)

Previous work (Dudin et al., 2019) had already shown that actin is essential for cellularization in S. arctica and hinted that microtubules might play a role in nuclear organization, but what exactly they do was never really looked at. That is exactly the gap this study fills.

The preprint authors set out to investigate what role microtubules (MTs) play in coordinating and executing cellularization in S. arctica, while also exploring the evolutionary implications of these findings. The authors combined live-cell imaging, ultrastructure expansion microscopy (U-ExM), and volume electron microscopy with pharmacological perturbations to dissect microtubule function.

Key findings:

To investigate the role of microtubules in cellularization, the authors asked a simple but powerful question: What happens when you take them away? By treating S. arctica coenocytes during cellularization with carbendazim (MBC), a drug that causes MT depolymerization, and following the process by live-cell imaging with the membrane dye FM4-64, they obtained a clear and surprising result. Cellularization still initiated, the furrows were still formed, but the precision with which they did so was dramatically compromised.

The process became spatially disorganized without MT, and instead of uniform furrows growing steadily inward to enclose individual nuclei, furrows adopted diagonal trajectories, bifurcated, or progressed at irregular speeds. The consequences were that some compartments ended up enclosing multiple nuclei, while others ended up without a nucleus. Ultrastructural analysis by TEM tomography confirmed that furrow morphology itself was affected. The cells displayed convoluted, branched, and irregular furrow profiles. Against this background, the authors came to the conclusion that MT are not required to initiate cellularization, but they are essential for its coordination.

To look at the organizational role of MT, the authors turned to U-ExM, a technique that physically expands the biological sample to reveal details below the diffraction limit of conventional light microscopy. Combined with a newly developed tool, the HAK-actin probe, they could simultaneously visualize actin and MT networks in S. arctica at near-nanoscale resolution. This represents a significant technical advance for the field. The images revealed that, outward from MT- organizing centres (MTOCs), MT were sitting directly adjacent to each nucleus, extending all the way to the cell cortex. By comparing different stages of cellularization, the authors found that MT dynamically reorganize the furrows and follow the membrane invaginations by tracking their inward progression. Quantitative analysis confirmed a positive correlation between cortical MT length and furrow depth, suggesting that MT elongation and furrow ingression are tightly coupled. Through ingression, the actin accumulates at the base of the furrows.

By spinning coenocytes in the cellularization stage to displace the nuclei towards one pole of the cell, and without otherwise disrupting the cellularization machinery, the authors tested whether nuclear position instructs furrow placement. The result was pretty clear: cortical regions overlying the nuclei-enriched pole showed normal, deep furrow ingression, while nuclei-depleted regions produced only shallow, poorly progressing furrows. Furrow kinetics in nuclei-enriched areas were comparable to unperturbed controls, confirming that the core ingression machinery remained intact. This experiment shows a direct causal link between nuclear position and furrow placement. The nucleus-MTOC unit acts as a spatial organizer, defining where the coenocytic cell will build its new boundaries.

Finally, the authors investigated the role of vesicles and asked whether membrane trafficking contributes to cellularization, independently of microtubule-based nuclear positioning. Treatment with Brefeldin A (BfA), a drug that blocks the Golgi apparatus from dispatching membrane vesicles to the furrow front, revealed that Golgi-derived vesicle trafficking supplies the membrane material needed for furrow growth. This parallels the situation in Drosophila, and the module operates independently from the MT-dependent spatial patterning system. The authors bring these findings together in a two-module model. First, the nucleus MTOC complex and its associated microtubule arrays establish the spatial blueprint of cellularization, while secondly, actin dynamics and membrane trafficking execute the mechanical work of building the furrows.

Why I like this preprint:

This study caught my attention for several reasons. As someone still learning the field, I found it remarkable how much information the authors were able to extract by combining live-cell imaging, drug treatments, and centrifugation, with cutting-edge techniques like U-ExM and TEM tomography. The centrifugation experiment was the most elegant in my opinion. By simply spinning the cells, the authors could physically move nuclei around and directly show that where the nucleus goes, the furrow follows. It is a beautifully simple way to demonstrate the role of the nuclei by pushing them away without disrupting the cellularization machinery.

Beyond the specific findings, I think this study is important for another reason. It adds a genuinely new perspective on the evolution of cellularization. S. arctica is neither an animal nor a plant. It sits in a unique phylogenetic position as one of the closest unicellular relatives of animals yet reaches cellularization through an independent evolutionary path. This makes it a particularly valuable system for asking which features of cellularization are truly ancient and which have been independently invented in different lineages. The parallel the authors draw with Drosophila raises the possibility that nucleus-based spatial patterning may be a deeply conserved solution to the geometric challenge of dividing a shared cytoplasm.

The authors show a completely new biological function of S. arctica, which is great. But I feel the evolutionary dimension could be explored even further. The paper leaves me wondering how this compares to other Ichthyosporean species, and whether the two-module model described here is a general principle or specific to this organism. Also, I wanted to know a little more about the linked mechanism between plants, animals, and the Ichthyosporean altogether. Are there shared genetic regulators underlying these parallels? I hope future work will take up these questions, and I am looking forward to reading about it.

Questions for the authors:

  1. The work beautifully dissects the roles of microtubules, actin, and membrane trafficking as separable but coordinated modules. What is your speculation on how these modules are regulated? What signals or molecular players coordinate the timing of their sequential activation to ensure cellularization proceeds with spatial and temporal precision?
  2. S. arctica has a fascinating phylogenetic position. It is neither an animal nor a plant, but one of the closest unicellular relatives of animals. Do you think the MT-dependent spatial patterning module described here represents an ancestral feature shared with the animal lineage, or rather an independent evolutionary solution to the same geometric challenge?
  3. In my opinion, the centrifugation experiment is a highlight of the study. However, as a reader, I wondered whether spinning the cells could have introduced mechanical stress or secondary effects on the cellularization process beyond simply displacing the nuclei. How confident are you that the observed changes in furrow behaviour reflect nuclear mispositioning specifically, rather than a more general perturbation of the cell?

 

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Author's response

Omaya Dudin, Hiral Shah, and Gautam Dey shared

1) We strongly suspect that the coordination of microtubules, actin–myosin, and membrane trafficking during Sphaeroforma cellularization is primarily intrinsically regulated. Extrinsic parameters such as calcium, magnesium, lipid composition, temperature, or salt concentration can certainly modulate the process, as they do in other systems, but the timing and sequence of module activation look to us like the output of an internal program that each life cycle must execute reliably.

Two intrinsic cues stand out from our work. First, cellularization initiates at a defined nuclear-to-cytoplasmic (N/C) ratio, and perturbing this ratio shifts both the timing and outcome of development. This, together with transcriptional waves that upregulate actin, myosins, and other cellularization genes at or just before onset, suggests that the N/C ratio gates a dedicated transcriptional program, conceptually analogous to zygotic genome activation in animal embryos. Mechanistically, we imagine the rising N/C ratio titrating cytoplasmic repressors (or diluting them at the cortex), thereby lowering a threshold that switches on a “cellularization module” of genes. Importantly, we have evidence that the N/C ratio is sensed at the cortex in a phosphatase-dependent manner, so we think cortical phosphatases (and opposing kinases) act as key integrators that convert N/C ratio information into local changes in phosphorylation state that permit actin–myosin remodeling, microtubule reorganization, and membrane trafficking to proceed in sequence.

Second, recent work in collaboration with the Aydogan lab shows that a mitochondrial H₂O₂ burst acts as a metabolic switch that licenses the onset of morphogenesis in animals and in Sphaeroforma itself. In this view, mitochondrial Complex III–derived H₂O₂ is not just a byproduct of respiration but a conserved, intrinsic signal that permits chromatin decondensation, cytoskeletal remodeling, and progression into morphogenesis. We therefore speculate that a similar redox “go” signal could act as a metabolic checkpoint in Sphaeroforma, allowing the cellularization program to run once the N/C ratio threshold is reached. Because H₂O₂ can directly modulate the activity of redox-sensitive phosphatases and kinases, we imagine this burst helping to tip the cortical phosphorylation balance toward the dephosphorylation (or phosphorylation) states that are permissive for each cytoskeletal and trafficking module.

Within this intrinsically timed framework, we see ionic, lipid, and physical cues (Ca²⁺/Mg²⁺, membrane composition, temperature, tension) as local modulators that refine when and where each module is deployed, rather than as primary timers. In short: the N/C ratio and a mitochondrial H₂O₂ switch set the global “when” and “go,” cortical phosphatases/kinases translate these into local phosphorylation states that gate module activation, and extrinsic biochemical/mechanical signals fine‑tune the “where” and “how fast” to ensure spatially and temporally precise cellularization.

2) We lean toward this being a conserved feature rather than a purely independent solution. The functional coupling between microtubules and membrane trafficking is ancient and widespread, showing up in diverse unicellular and multicellular systems where microtubules organize organelles, direct long-range trafficking, and help position membranes during division and morphogenesis. In Sphaeroforma, microtubules position nuclei and guide nascent furrows to ensure faithful nuclear and cytoplasmic partitioning, in ways that echo microtubule roles in other cellularization and cytokinesis contexts. From that perspective, the MT-dependent spatial patterning module we describe fits naturally into a broader, deeply rooted toolkit for coordinating cytoskeleton and membrane dynamics.

That said, whether this reflects direct homology with animal cellularization or convergent tuning to similar geometric constraints is hard to say, and, in a way, both outcomes are equally exciting from an evolutionary standpoint. What feels more exciting to us from an evolutionary cell biology perspective is the question of how this coordination is achieved across many cells so that they all cellularize at the same pace. The module itself, microtubules guiding membrane furrows, may well be conserved, but the deeper puzzle is how hundreds of nuclei and their surrounding cortices stay in sync, avoiding stragglers and misaligned furrows. This also makes us wonder why microtubules in Sphaeroforma, and in many animal embryos, contribute more to spatial patterning and membrane guidance, while actin takes the lead in the mechanics of cytokinesis and cortical contractility. Would a cellularizing relative of plants rely more on actin or on microtubules for equivalent steps? Understanding the logic of this cytoskeletal “choice,” and how it is wired into the intrinsic timing programs we discussed, feels like the more pressing and broadly relevant puzzle. In other words, the interesting evolutionary question may not only be whether the module itself is conserved, but how ancient cytoskeletal systems have been adapted and coordinated to solve the same fundamental problem of organizing space, mechanics, and timing during cellularization.

3) This is a very reasonable concern, and we cannot completely exclude the possibility that centrifugation introduces some degree of mechanical stress or other secondary effects. From previous experiments, we know that sufficiently strong or prolonged centrifugation can indeed compromise cell viability. However, under the conditions we use here, the cells remain viable and continue to progress through cellularization. Importantly, we observe the same overall invagination dynamics, and the cytoskeleton still forms within the cells, although it is displaced together with the nuclei.

These observations make us think that the phenotype is not simply a consequence of a general perturbation of the cells. Rather, the fact that the cells continue to cellularize, while the nuclei and associated cytoskeletal organization are specifically repositioned, is consistent with the idea that the altered furrow behaviour results primarily from nuclear mispositioning. That said, we think it is fair to acknowledge that we cannot completely disentangle nuclear mispositioning from all possible mechanical effects of centrifugation, and we therefore interpret the experiment as strong evidence for a role of nuclear position rather than as a perfectly specific manipulation of nuclear position alone.

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The Keystone Symposium on Stem Cell Models in Embryology, 2026, was organised by Jun Wu (UT Southwestern), Jianping Fu (University of Michigan) and Miki Ebisuya (TU Dresden) and held at Asilomar Conference Grounds in California (US). The meeting discussed recent advances made in establishing stem-cell-based embryo models, what fundamental insights into developmental processes have been gleaned from them, as well as how they are beginning to be applied more widely. This prelist contains preprints by presenters at the talk and poster sessions at the conference, which our Reviews Editor in attendance spotted. Please do reach out to preLights@biologists.com if you notice any that we’ve missed.

 



List by Ingrid Tsang

November in preprints – DevBio & Stem cell biology

preLighters with expertise across developmental and stem cell biology have nominated a few developmental and stem cell biology (and related) preprints posted in November they’re excited about and explain in a single paragraph why. Concise preprint highlights, prepared by the preLighter community – a quick way to spot upcoming trends, new methods and fresh ideas.

 



List by Aline Grata et al.

October in preprints – DevBio & Stem cell biology

Each month, preLighters with expertise across developmental and stem cell biology nominate a few recent developmental and stem cell biology (and related) preprints they’re excited about and explain in a single paragraph why. Short, snappy picks from working scientists — a quick way to spot fresh ideas, bold methods and papers worth reading in full. These preprints can all be found in the October preprint list published on the Node.

 



List by Deevitha Balasubramanian et al.

October in preprints – Cell biology edition

Different preLighters, with expertise across cell biology, have worked together to create this preprint reading list for researchers with an interest in cell biology. This month, most picks fall under (1) Cell organelles and organisation, followed by (2) Mechanosignaling and mechanotransduction, (3) Cell cycle and division and (4) Cell migration

 



List by Matthew Davies et al.

June in preprints – the CellBio edition

A group of preLighters, with expertise in different areas of cell biology, have worked together to create this preprint reading lists for researchers with an interest in cell biology. This month, categories include: (1) Cell organelles and organisation (2) Cell signaling and mechanosensation (3) Genetics/gene expression (4) Biochemistry (5) Cytoskeleton

 



List by Barbora Knotkova et al.

Keystone Symposium – Metabolic and Nutritional Control of Development and Cell Fate

This preList contains preprints discussed during the Metabolic and Nutritional Control of Development and Cell Fate Keystone Symposia. This conference was organized by Lydia Finley and Ralph J. DeBerardinis and held in the Wylie Center and Tupper Manor at Endicott College, Beverly, MA, United States from May 7th to 9th 2025. This meeting marked the first in-person gathering of leading researchers exploring how metabolism influences development, including processes like cell fate, tissue patterning, and organ function, through nutrient availability and metabolic regulation. By integrating modern metabolic tools with genetic and epidemiological insights across model organisms, this event highlighted key mechanisms and identified open questions to advance the emerging field of developmental metabolism.

 



List by Virginia Savy, Martin Estermann

Biologists @ 100 conference preList

This preList aims to capture all preprints being discussed at the Biologists @100 conference in Liverpool, UK, either as part of the poster sessions or the (flash/short/full-length) talks.

 



List by Reinier Prosee, Jonathan Townson

BSDB/GenSoc Spring Meeting 2024

A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.

 



List by Joyce Yu, Katherine Brown

GfE/ DSDB meeting 2024

This preList highlights the preprints discussed at the 2024 joint German and Dutch developmental biology societies meeting that took place in March 2024 in Osnabrück, Germany.

 



List by Joyce Yu

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

The Society for Developmental Biology 82nd Annual Meeting

This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.

 



List by Joyce Yu, Katherine Brown

CSHL 87th Symposium: Stem Cells

Preprints mentioned by speakers at the #CSHLsymp23

 



List by Alex Eve

Journal of Cell Science meeting ‘Imaging Cell Dynamics’

This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.

 



List by Helen Zenner

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Alumni picks – preLights 5th Birthday

This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.

 



List by Sergio Menchero et al.

CellBio 2022 – An ASCB/EMBO Meeting

This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.

 



List by Nadja Hümpfer et al.

2nd Conference of the Visegrád Group Society for Developmental Biology

Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)

 



List by Nándor Lipták

Fibroblasts

The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!

 



List by Osvaldo Contreras

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

Single Cell Biology 2020

A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.

 



List by Alex Eve

Society for Developmental Biology 79th Annual Meeting

Preprints at SDB 2020

 



List by Irepan Salvador-Martinez, Martin Estermann

FENS 2020

A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020

 



List by Ana Dorrego-Rivas

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

 



List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.

 



List by Paul Gerald L. Sanchez and Stefano Vianello

ASCB EMBO Annual Meeting 2019

A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)

 



List by Madhuja Samaddar et al.

EDBC Alicante 2019

Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.

 



List by Sergio Menchero et al.

EMBL Seeing is Believing – Imaging the Molecular Processes of Life

Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019

 



List by Dey Lab

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

Young Embryologist Network Conference 2019

Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar