Developmental conversion of the nucleolus into an RNA Polymerase II transcriptional platform in Drosophila spermatocytes
Posted on: 22 June 2026
Preprint posted on 23 May 2026
An organelle changes careers: in fly sperm cells, the cell's ribosome factory becomes a hub where fertility genes, silenced everywhere else, are switched on.
Selected by Panagiotis Giannios
Categories: cell biology, developmental biology
Background
The nucleolus is textbook shorthand for a single job, making ribosomes: RNA polymerase I transcribes the ribosomal RNA that gets folded and packaged into them. But cell biologists have long known about an awkward exception: “atypical nucleoli,” or nucleolus-like bodies (NLBs), seen in oocytes, spermatids, and early embryos. NLBs keep canonical nucleolar proteins such as Fibrillarin and Nucleolin and are wrapped in heterochromatin, yet they make no rRNA. Removing the maternal NLB doesn’t block rRNA reactivation in the embryo but is nonetheless lethal. So the NLBs must do something essential that has nothing to do with ribosomes. What that something is, has stayed a mystery for decades.
In this preprint, Fingerhut and colleagues go looking for that function in Drosophila spermatocytes. After their mitotic divisions, spermatocytes spend an unusually long (~80–90 h) meiotic G2 (Fig. 1A), running a large differentiation-specific transcription program controlled by two testis-specific regulators: the tTAFs (TFIID paralogs) and tMAC (a testis-specific MuvB/DREAM complex). Among the most striking outputs are the Y-linked fertility genes (kl-3, kl-5, ORY, kl-2, Ppr-Y); heterochromatic and silent in every other cell type, but transcribed robustly here, often as lampbrush loops. Many carry megabase-scale introns stuffed with satellite DNA (Fig. 1B). How a heterochromatic Y chromosome becomes a high-output transcription template has been unclear and, intriguingly, the tTAFs were already known to sit at the nucleolus, where they were thought to act indirectly by sequestering Polycomb. These threads converge on the question the authors set out to answer: what is the spermatocyte nucleolus actually doing, and does it play a direct part in transcribing these genes?
Figure 1. A prolonged spermatocyte growth phase transcribes giant, heterochromatic Y-linked genes. (A) Drosophila male germline development: germline stem cells and spermatogonia (blue) at the apical tip give rise to spermatocytes (green), which spend ~80–90 h growing before the meiotic divisions and sperm differentiation. (B) Spermatocytes enlarge as they mature, each with a prominent nucleolus (left); the Y-linked fertility gene kl-3 drawn to scale (right); a few exons (boxes) separated by introns packed with repetitive satellite DNA (dashes), so the locus spans at least 4.3 Mb of DNA to encode a ~13.9 kb transcript. Transcription begins in early spermatocytes and takes essentially the whole growth phase to complete. Adapted from Fingerhut et al. (2026), bioRxiv (doi: 10.64898/2026.05.20.726666), under CC BY 4.0.
Key findings
What they found is an organelle caught mid-transition: still present, but no longer doing the main thing it is known for. As spermatocytes matured, the nucleolus gradually lost the features that define its ribosome-producing identity. RNA polymerase I disappeared from the body, and both mature and unprocessed rRNAs were depleted, while canonical nucleolar proteins such as Fibrillarin and Modulo, the fly Nucleolin, remained. An organelle had kept its identity while letting go of its function. This did not leave the cell short of ribosomes: cytoplasmic rRNA stayed abundant through the rest of germ-cell development, pointing to a stored pool of ribosomes large enough to support sperm formation.
As the old programme shut down, a new one appeared around the same body. Pol II accumulated at the NLB (Fig. 2A), and it was not simply inactive polymerase parked there: both initiation- and elongation-associated CTD phosphorylation marks were detected, with the initiating form shown in Fig. 2B. The NLB was therefore no longer just a nucleolar remnant. It had become associated with active Pol II transcription.
So which genes were being transcribed there? RNA FISH showed nascent transcripts from the giant Y-linked fertility genes (kl-3, kl-2, Ppr-Y, kl-5 and ORY) positioned right next to the NLB (Fig. 2C). These are not ordinary genes: they are heterochromatic, silent in most cell types, and switched on specifically in spermatocytes, where they must be transcribed across enormous satellite-rich introns. One detail makes the story more nuanced: kl-3 transcription appeared to begin before Pol II clearly accumulated at the NLB, suggesting that the body may not simply switch these genes on, but may instead support the long, high-output, intron-spanning phase of their transcription.
Control of this switch traced back to known spermatocyte regulators. tMAC was required to recruit Pol II to the NLB, whereas the tTAFs were needed to activate it: in tTAF mutants, Pol II still reached the body but failed to acquire active phospho-marks. Both regulators were therefore needed for proper Y-linked gene expression, but they acted at different steps, as their effects on chromatin made clear. The satellite-rich introns normally decompacted during transcription; they remained compact in tMAC mutants but still opened in tTAF mutants. tMAC therefore appeared to make the heterochromatic DNA permissive for transcription, while the tTAFs enabled productive Pol II activity.
Together, these findings redefine the spermatocyte nucleolus as a developmentally repurposed organelle.
Figure 2. The spermatocyte nucleolus is repurposed as an active Pol II site for Y-linked gene transcription. (A) Early-to-mid spermatocytes stained for Pol I (Polr1B-GFP, magenta), Pol II (yellow) and DNA (DAPI, white); nuclei are outlined and the nucleolus/NLB arrowed. Early on, Pol I fills the nucleolus and Pol II is excluded from it; as cells mature, Pol I is lost and Pol II instead forms a ring around the nucleolus-like body (NLB) (schematic, top). (B) The NLB-associated Pol II carries the initiation-associated CTD mark phospho-Ser5 (magenta; with DNA, right), marking polymerase engaged in transcription rather than passively stored. (C) Nascent kl-3 transcript (intron 1–exon 2 junction, magenta) lies immediately against the NLB (Sa-GFP, green; DNA, white), placing transcription of this heterochromatic Y-linked gene at the repurposed organelle. Scale bars, 5 µm. Adapted from Fingerhut et al. (2026), bioRxiv (doi: 10.64898/2026.05.20.726666), under CC BY 4.0.
Why I think this is important
This is a clean shot at a decades-old open question. The work offers a concrete, active role for an NLB: not an inert storage depot but a Pol II workspace. In doing so, it rewrites the earlier view in which nucleolar tTAFs were merely a Polycomb sponge.
I also like the conceptual unification it hints at: rDNA and the Y-linked fertility genes share two hard problems: they are heterochromatic, and they need many polymerases loaded at once (the “Christmas tree”/lampbrush configuration). The idea that the nucleolus/NLB offers a permissive environment for that class of transcription, whichever polymerase happens to be involved, is a new way to think about what the organelle is for. And the case is built with care: the Pol I-to-Pol II handoff is caught with several independent markers, and the clean division of labour between tMAC (which opens the heterochromatin) and the tTAFs (which switch the polymerase on) gives the model real texture.
Future directions
The detail I keep returning to is the timing. Pol I leaves, Pol II arrives, the regulators come on, and the Y genes fire inside the same developmental window. That sequence is what makes the story feel like a principle rather than a quirk of one organelle. It also leaves an inviting question open. What we can see, for now, is that these genes are transcribed next to the NLB; what we can’t yet see is whether the NLB is driving that transcription, or simply sharing a neighbourhood with it. The observations here are solid enough that answering this question feels within reach rather than far off, which is part of why the preprint is worth reading now.
Questions for the authors
- The timing is striking: Pol I leaves, Pol II arrives, and the Y genes come on within the same window. Do you picture the NLB as driving that transcription, as an environment these genes settle into, or something in between?
- Beyond the Y-linked genes, do you see evidence that other highly expressed spermatocyte genes also gather at the NLB, or does the association look specific to the Y-linked set?
- Both rDNA and the Y-linked genes are heterochromatic and load many polymerases at once. Do you think the NLB is solving that problem the same way for both, or does it do something different once Pol II takes over?
- If NLBs in oocytes or early embryos turn out to play a similar Pol II role, what would be the first sign you’d look for? Say, active Pol II at the body, or transcripts coming from it that aren’t rRNA?
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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 |