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Transcriptional interferences ensure one olfactory receptor per ant neuron

Nature volume 648, pages 418–426 (2025)Cite this article

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Abstract

To ensure specificity, sensory neurons must select and express a single receptor from often vast gene families, adhering to the rule of ‘one receptor per neuron’. For example, each olfactory sensory neuron in mammals expresses only one odorant receptor (Or) gene1,2. In Drosophila, which has about 60 Or genes, this selection is deterministic3. By contrast, mice face the challenge of choosing one Or gene from over 1,000 options4. They solve this through a complex system of stochastic choices5,6,7,8,9. Ants also possess many Or genes, most of which are organized into tandem arrays similar to those in mammals, but their regulatory mechanisms have evolved independently. Here we show that, in the ant Harpegnathos saltator, each olfactory sensory neuron activates a single promoter within an Or gene array, producing a mature capped and polyadenylated mRNA. While the promoters of downstream genes in the array are inactive, all downstream genes are nonetheless transcribed due to transcriptional readthrough from the active promoter, probably caused by inefficient RNA polymerase II termination. This readthrough appears to suppress downstream promoters through transcriptional interference, resulting in aberrant non-capped transcripts that are not translated, ensuring that only the active gene is expressed. Simultaneously, long antisense transcription originating from the chosen Or promoter covers upstream genes, presumably silencing them. Ants therefore appear to have evolved a unique transcriptional-interference-based mechanism to express a single OR protein from an array of Or genes with functionally similar promoters.

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Fig. 1: Genomic arrangement and expression pattern of Or genes in H. saltator.
Fig. 2: Transcriptional readthrough at Or loci.
Fig. 3: Antisense transcription at Or loci.
Fig. 4: The chromatin environment of Or loci.

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Data availability

Sequencing data generated in this study have been deposited at the Gene Expression Omnibus (GSE280477 and GSE280492) and SRA (PRJNA1178663, PRJNA1178688 and PRJNA1261453).

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Acknowledgements

We thank the members of Desplan and Yan laboratories for discussions and Y.-C. Lin for maintaining ant colonies. We acknowledge the library preparation and DNA sequencing support provided by the ICBR NGS Shared Resource at the University of Florida and the Genomics Core at New York University. This work was funded by the National Institutes of Health grants K99DC021991 to B.S.; R01AG058762 to C.D. and D.R.; R01EY13010 and Tamkeen under the NYUAD Center for Genomics and Systems Biology (ADHPG-CGSB) to C.D.; R01DC020203 to H.Y.; and the Human Frontier Science Program grant LT000010/2020-L to B.S.

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Authors and Affiliations

  1. Department of Biology, New York University, New York, NY, USA

    Bogdan Sieriebriennikov, Olena Kolumba, Aurore de Beaurepaire, Jennifer Wu, Valentina Fambri, Eva Bardol, Yuwei Zhong, Ildar Gainetdinov & Claude Desplan

  2. Department of Biology, University of Florida, Gainesville, FL, USA

    Bogdan Sieriebriennikov & Hua Yan

  3. Program in Biology and Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates

    Olena Kolumba, Valentina Fambri & Claude Desplan

  4. Howard Hughes Medical Institute, Sylvester Comprehensive Cancer Center, Miller School of Medicine, University of Miami, Miami, FL, USA

    Danny Reinberg

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Contributions

Conceptualization: B.S. and C.D. Methodology: B.S., O.K., A.d.B., J.W., V.F. and I.G. Software: B.S., O.K., A.d.B. and V.F. Validation: O.K., J.W. and E.B. Formal analysis: B.S., O.K., A.d.B. and V.F. Investigation: B.S., O.K., A.d.B., J.W., V.F. and E.B. Resources: Y.Z. Data curation: B.S. Writing—original draft: B.S., J.W. and C.D. Writing—review and editing: B.S., O.K., A.d.B., J.W., V.F., Y.Z., I.G., D.R., H.Y. and C.D. Visualization: B.S. and Y.Z. Supervision: D.R., H.Y. and C.D. Project administration: B.S. and C.D. Funding acquisition: B.S., D.R., H.Y. and C.D.; B.S. conceived the study with C.D. and performed most of the experiments and analyses. O.K. developed a protocol for snRNA-seq, prepared libraries, performed analyses that uncovered the stair-step expression pattern indicating co-expression within arrays, and conceptualized the next steps with B.S. and C.D.; A.d.B. performed RNA-seq analyses that identified antisense transcripts, quantified the expression of different genes in sets of co-expressed genes, developed a protocol for multiome sequencing and prepared multiome libraries. J.W. developed a protocol for CUT&RUN, prepared CUT&RUN libraries and performed sequencing of 5′-capped and 5′-phosphorylated RNA ends. V.F. analysed TF expression and identified that different arrays tend to express different sets of TFs. Y.Z. assisted with the majority of experiments and participated in conceptual discussions. I.G. supervised the study and suggested methods of sequencing of 5′-capped and 5′-phosphorylated RNA ends. D.R. supervised the study and provided conceptual feedback. H.Y. initiated snRNA-seq experiments on ant antennae and supervised the study. C.D. conceived the study with B.S. and supervised every stage of the research.

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Correspondence to Danny Reinberg, Hua Yan or Claude Desplan.

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Extended data figures and tables

Extended Data Fig. 1 Additional plots.

(A) Long-read RNA-seq coverage profile in bulk and combined single-nucleus data. One representative biological replicate out of two is shown. (B) CUT&RUN for H3K36me3 in Or locus 3, alongside the ATAC-seq and CUT&RUN tracks shown in Fig. 4a. (C) Expression of putative transcription factors in OSN types defined by the expressed Or locus. These genes were identified by searching for protein domains often present in transcription factors, and they may include genes that are not bona fide transcription factors.

Extended Data Fig. 2 Subclustering of OSNs expressing locus 5 Or genes.

The plots show expression level of individual Or genes in the locus (HsOr273 is the most 5’ gene). (A) Subclustering where Or genes were permitted to remain in the list of highly variable genes. Nuclei are separated by the Or genes they express. (B) Subclustering where Or genes were removed from the list of highly variable genes. Nuclei expressing different Or genes are intermixed, showing that non-Or genes (including any TFs) do not separate OSNs expressing different Or genes from the same array.

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Sieriebriennikov, B., Kolumba, O., de Beaurepaire, A. et al. Transcriptional interferences ensure one olfactory receptor per ant neuron. Nature 648, 418–426 (2025). https://doi.org/10.1038/s41586-025-09664-x

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