A supernumerary “B-sex” chromosome drives male sex determination in the Pachón cavefish, Astyanax mexicanus

• Published in: Current biology Vol. 31; no. 21; pp. 4800 - 4809.e9
• Main Authors: Imarazene, Boudjema, Du, Kang, Beille, Séverine, Jouanno, Elodie, Feron, Romain, Pan, Qiaowei, Torres-Paz, Jorge, Lopez-Roques, Céline, Castinel, Adrien, Gil, Lisa, Kuchly, Claire, Donnadieu, Cécile, Parrinello, Hugues, Journot, Laurent, Cabau, Cédric, Zahm, Margot, Klopp, Christophe, Pavlica, Tomáš, Al-Rikabi, Ahmed, Liehr, Thomas, Simanovsky, Sergey A., Bohlen, Joerg, Sember, Alexandr, Perez, Julie, Veyrunes, Frédéric, Mueller, Thomas D., Postlethwait, John H., Schartl, Manfred, Herpin, Amaury, Rétaux, Sylvie, Guiguen, Yann
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 08.11.2021; Elsevier
• Subjects: Animals; B chromosome; Biological Evolution; cavefish; Caves; Characidae - genetics; Female; gdf6; genome; Life Sciences; Male; sex chromosomes; Sex Chromosomes - genetics; sex determination; sex differentiation, gonads; sex differentiation, gonads; genome; B chromosome; sex chromosomes; gdf6; sex determination; cavefish; sex differentiation; gonads
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2021.08.030

Sex chromosomes are generally derived from a pair of classical type-A chromosomes, and relatively few alternative models have been proposed up to now.1,2 B chromosomes (Bs) are supernumerary and dispensable chromosomes with non-Mendelian inheritance found in many plant and animal species3,4 that have often been considered as selfish genetic elements that behave as genome parasites.5,6 The observation that in some species Bs can be either restricted or predominant in one sex7–14 raised the interesting hypothesis that Bs could play a role in sex determination.15 The characterization of putative B master sex-determining (MSD) genes, however, has not yet been provided to support this hypothesis. Here, in Astyanax mexicanus cavefish originating from Pachón cave, we show that Bs are strongly male predominant. Based on a high-quality genome assembly of a B-carrying male, we characterized the Pachón cavefish B sequence and found that it contains two duplicated loci of the putative MSD gene growth differentiation factor 6b (gdf6b). Supporting its role as an MSD gene, we found that the Pachón cavefish gdf6b gene is expressed specifically in differentiating male gonads, and that its knockout induces male-to-female sex reversal in B-carrying males. This demonstrates that gdf6b is necessary for triggering male sex determination in Pachón cavefish. Altogether these results bring multiple and independent lines of evidence supporting the conclusion that the Pachón cavefish B is a “B-sex” chromosome that contains duplicated copies of the gdf6b gene, which can promote male sex determination in this species. [Display omitted] •Pachón cavefish have supernumerary male-predominant B chromosomes (Bs)•This Pachón B contain two loci of the putative gdf6b master sex-determining gene•gdf6b is only expressed in Pachón male gonads and its knockout induces sex reversal•Pachón B is a “B-sex” chromosome containing a putative male sex determination gene B chromosomes (Bs) are supernumerary chromosomes. Their implication in sex determination has been often suggested, but expressional and functional proofs are scarce. Imarazene et al. show that Pachón cavefish, Astyanax mexicanus, males have a predominant B-sex chromosome that contains a gene that can promote male sex determination in this species.