The conserved sex regulator DMRT1 recruits SOX9 in sexual cell fate reprogramming
Open accessAbstract
Mammalian sexual development commences when fetal bipotential progenitor cells adopt male Sertoli (in XY) or female granulosa (in XX) gonadal cell fates. Differentiation of these cells involves extensive divergence in chromatin state and gene expression, reflecting distinct roles in sexual differentiation and gametogenesis. Surprisingly, differentiated gonadal cell fates require active maintenance through postnatal life to prevent sexual transdifferentiation and female cell fate can be reprogrammed by ectopic expression of the sex regulator DMRT1. Here we examine how DMRT1 reprograms granulosa cells to Sertoli-like cells in vivo and in culture. We define postnatal sex-biased gene expression programs and identify three-dimensional chromatin contacts and differentially accessible chromatin regions (DARs) associated with differentially expressed genes. Using a conditional transgene we find DMRT1 only partially reprograms the ovarian transcriptome in the absence of SOX9 and its paralog SOX8, indicating that these factors functionally cooperate with DMRT1. ATAC-seq and ChIP-seq show that DMRT1 induces formation of many DARs that it binds with SOX9, and DMRT1 is required for binding of SOX9 at most of these. We suggest that DMRT1 can act as a pioneer factor to open chromatin and allow binding of SOX9, which then cooperates with DMRT1 to reprogram sexual cell fate.
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In gonadal cell fate transition, DMRT1 opens chromatin to allow binding of SOX9, while SOX9 did not have strong pioneering abilities.
“In gonadal cell fate transition, DMRT1 was shown to open chromatin to allow binding of SOX9, while SOX9 did not have strong pioneering abilities (74).”
From SOX9 reprograms endothelial cells by altering the chromatin landscape (2022) · cites this paper as [74]
The Results section reports that SOX9 binding at many Sertoli-biased regions was strongly DMRT1-dependent, and the Discussion says SOX9 alone could not make many such regions accessible in cultured postnatal granulosa cells. But the paper presents DMRT1’s chromatin-opening pioneer mechanism as a favored interpretation requiring biochemical confirmation, not as established; it also notes that SOX9’s dependence on DMRT1 may differ in fetal gonads. (LLM, conf=0.86)
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Additional file 9 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647245
Additional file 8 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647242
Additional file 5 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647233
Additional file 6 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647236
Additional file 3 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647227
Additional file 2 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.24670374
Additional file 7 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647239
Additional file 10 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647248
Additional file 1 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2023) · Figshare · doi:10.6084/m9.figshare.24669908
Additional file 4 of Ovarian ERβ cistrome and transcriptome reveal chromatin interaction with LRH-1
Birgersson, M., Indukuri, R., Lindquist, L., Stepanauskaitė, L., Luo, Q., Deng, Q., Archer, A., & Williams, C. (2024) · Figshare · doi:10.6084/m9.figshare.26647230
Male fertility is independent of Enh13 control of Sox9 testicular expressionPreprint
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Post-translational modification of proteins in the human testis development pathway
Idris, F. P., Ferreira, L. G. A., Houston, B. J., Humphrey, S. J., Sinclair, A. H., & Ayers, K. L. (2026) · Human Reproduction Update · doi:10.1093/humupd/dmag016
TRIM28 PRESERVES OVARIAN IDENTITY BY STABILIZING LINEAGE-SPECIFIC TRANSCRIPTION FACTOR HUBSPreprint
Sitkiewicz, L., Chaleil, F., Granes, G., Rossitto, M., Déjardin, S., Cammas, F. M., Lefrançois‐Martinez, A., Stévant, I., & Poulat, F. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.21.739817
Testis Development and Descent
Mattioli, G., Maiorano, N. G., FIORENZA, V., Rotondi, G., Lazzeroni, P., Paraboschi, I., Iorgi, N. D., Napoli, F., & Maghnie, M. (2026) · Endocrinology · doi:10.1007/978-3-319-29456-8_8-2
DMRT1 is required at two steps of ovarian differentiation in rabbits
Dujardin, E., Poulat, F., Aura, I. B., Dewaele, A., André, M., Mckey, J., Gras, S. L., Frambourg, A., Jouneau, L., Lupiáñez, D. G., et al. (2026) · Science Advances · doi:10.1126/sciadv.aeh1087
- Authors
- Lindeman, R. E., Murphy, M. W., Agrimson, K. S., Gewiss, R. L., Bardwell, V. J., Gearhart, M. D., & Zarkower, D.
- Affiliations
- University of Minnesota (US)
- Corresponding author
- Gearhart, Micah D
- Zarkower, David
- ORCID
- Venue
- Nucleic Acids Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2021-06-07
- Volume
- 49
- Issue
- 11
- Pages
- 6144-6164
- ISSN
- 0305-1048 (ISSN-L)
- 1362-4962
- PMC
- PMC8216462
- OpenAlex
- W3168714668
- Cited by
- 66
- References
- 66
- Citations by year
- 2026: 9 · 2025: 15 · 2024: 13 · 2023: 16 · 2022: 8 · 2021: 5
- FWCI
- 7.07
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nucleic Acids Research (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5 R01 GM59152, 1 R01 GM127379, 1 F32GM106484, IRACDA K126M119955)
- Minnesota Medical Foundation
- University of Minnesota Medical School
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- DMRT1, SOX9, Sox8, sexual differentiation, Sertoli cells, granulosa cells, pioneer factors, chromatin accessibility, sex-biased gene expression, ovarian transcriptome, gonad development
- MeSH terms
- Animals, Cells, Cultured, Chromatin, DNA, Female, Granulosa Cells, Male, Sertoli Cells, Transcription Factors, Regulatory Elements, Transcriptional, Mice, SOXE Transcription Factors, SOX9 Transcription Factor, Transcriptome, Cellular Reprogramming
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