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The conserved molting/circadian rhythm regulator NHR-23/NR1F1 serves as an essential co-regulator of C. elegans spermatogenesis

View ORCID ProfileJames Matthew Ragle, View ORCID ProfileAbigail L. Aita, View ORCID ProfileKayleigh N. Morrison, View ORCID ProfileRaquel Martinez-Mendez, View ORCID ProfileHannah N. Saeger, View ORCID ProfileGuinevere A. Ashley, View ORCID ProfileLonden C. Johnson, View ORCID ProfileKatherine A. Schubert, View ORCID ProfileDiane C. Shakes, View ORCID ProfileJordan D. Ward
doi: https://doi.org/10.1101/2020.06.11.147298
James Matthew Ragle
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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  • ORCID record for James Matthew Ragle
Abigail L. Aita
2Department of Biology, William & Mary, Williamsburg, VA 23187, USA
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Kayleigh N. Morrison
2Department of Biology, William & Mary, Williamsburg, VA 23187, USA
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Raquel Martinez-Mendez
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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Hannah N. Saeger
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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Guinevere A. Ashley
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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  • ORCID record for Guinevere A. Ashley
Londen C. Johnson
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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Katherine A. Schubert
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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Diane C. Shakes
2Department of Biology, William & Mary, Williamsburg, VA 23187, USA
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Jordan D. Ward
1Department of Molecular, Cell, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, CA 95064, USA
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  • For correspondence: jward2@ucsc.edu
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Abstract

In sexually reproducing metazoans, spermatogenesis is the process by which uncommitted germ cells give rise to haploid sperm. Work in model systems has revealed mechanisms controlling commitment to the sperm fate, but how this fate is subsequently executed remains less clear. While studying the well-established role of the conserved nuclear hormone receptor transcription factor, NHR-23/NR1F1, in regulation of C. elegans molting, we discovered NHR-23/NR1F1 is also constitutively expressed in developing 1° spermatocytes and is a critical regulator of spermatogenesis. In this novel role, NHR-23/NR1F1 functions downstream of the canonical sex determination pathway. Degron-mediated depletion of NHR-23/NR1F1 within hermaphrodite or male germlines causes sterility due to an absence of functional sperm as depleted animals produce arrested primary spermatocytes rather than haploid sperm. These spermatocytes arrest in prometaphase I and fail to either progress to anaphase or attempt spermatid-residual body partitioning. They make sperm-specific membranous organelles (MOs) but fail to assemble their major sperm protein into fibrous bodies. NHR-23/NR1F1 appears to function independently of the known SPE-44 gene regulatory network, revealing the existence of an NHR-23/NR1F1-mediated module that regulates the spermatogenesis program.

Summary Statement A well-characterized regulator of C. elegans molting also unexpectedly controls the spermatogenesis program; our work provides insights into the gene regulatory networks controlling spermatogenesis.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted June 12, 2020.
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The conserved molting/circadian rhythm regulator NHR-23/NR1F1 serves as an essential co-regulator of C. elegans spermatogenesis
James Matthew Ragle, Abigail L. Aita, Kayleigh N. Morrison, Raquel Martinez-Mendez, Hannah N. Saeger, Guinevere A. Ashley, Londen C. Johnson, Katherine A. Schubert, Diane C. Shakes, Jordan D. Ward
bioRxiv 2020.06.11.147298; doi: https://doi.org/10.1101/2020.06.11.147298
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The conserved molting/circadian rhythm regulator NHR-23/NR1F1 serves as an essential co-regulator of C. elegans spermatogenesis
James Matthew Ragle, Abigail L. Aita, Kayleigh N. Morrison, Raquel Martinez-Mendez, Hannah N. Saeger, Guinevere A. Ashley, Londen C. Johnson, Katherine A. Schubert, Diane C. Shakes, Jordan D. Ward
bioRxiv 2020.06.11.147298; doi: https://doi.org/10.1101/2020.06.11.147298

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