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Most ferns, unlike all seed plants, are homosporous and produce sexually undifferentiated spores. Sex ratio in many homosporous species is environmentally established by the secretion of antheridiogen from female/hermaphrodite gametophytes. Nearby undetermined gametophytes perceive antheridiogen, which induces male development. In the fern Ceratopteris richardii (Ceratopteris), hermaphroditic (her) mutants develop as hermaphrodites even in the presence of antheridiogen. Modern sequencing and genomic tools make the molecular identification of mutants in the 11-Gbp genome of this fern possible. We mapped 2 linked mutants, her7-14 and her7-19, to the same 16-Mbp interval on chromosome 29 of the Ceratopteris genome. An ortholog of the receptor kinase gene BRASSINOSTEROID INSENSITIVE 1 (BRI1) within this interval encoded a deletion mutation in her7-14 and a missense mutation in her7-19. Three other linked her mutants encoded missense mutations in the same gene, which we name HER7. Consistent with a function as a receptor kinase, HER7-GFP fusion protein localized to the plasma membrane and cytoplasm. Analysis of gene expression showed that brassinosteroid biosynthesis was upregulated in hermaphrodites compared with male gametophytes. Our work demonstrates that HER7 is required for sex determination in Ceratopteris and opens avenues for studying the evolution of antheridiogen systems.
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This content will become publicly available on December 12, 2025
Robust sex determination in the Caenorhabditis nigoni germ line
Abstract Sexual characteristics and reproductive systems are dynamic traits in many taxa, but the developmental modifications that allow change and innovation are largely unknown. A leading model for this process is the evolution of self-fertile hermaphrodites from male/female ancestors. However, these studies require direct analysis of sex determination in male/female species, as well as in the hermaphroditic species that are related to them. In Caenorhabditis nematodes, this has only become possible recently, with the discovery of new species. Here, we use gene editing to characterize major sex determination genes in Caenorhabditis nigoni, a sister to the widely studied hermaphroditic species Caenorhabditis briggsae. These 2 species are close enough to mate and form partially fertile hybrids. First, we find that tra-1 functions as the master regulator of sex in C. nigoni, in both the soma and the germ line. Surprisingly, these mutants make only sperm, in contrast to tra-1 mutants in related hermaphroditic species. Moreover, the XX mutants display a unique defect in somatic gonad development that is not seen elsewhere in the genus. Second, the fem-3 gene acts upstream of tra-1 in C. nigoni, and the mutants are females, unlike in the sister species C. briggsae, where they develop as hermaphrodites. This result points to a divergence in the role of fem-3 in the germ line of these species. Third, tra-2 encodes a transmembrane receptor that acts upstream of fem-3 in C. nigoni. Outside of the germ line, tra-2 mutations in all species cause a similar pattern of partial masculinization. However, heterozygosity for tra-2 does not alter germ cell fates in C. nigoni, as it can in sensitized backgrounds of 2 hermaphroditic species of Caenorhabditis. Finally, the epistatic relationships point to a simple, linear germline pathway in which tra-2 regulates fem-3 which regulates tra-1, unlike the more complex relationships seen in hermaphrodite germ cell development. Taking these results together, the regulation of sex determination is more robust and streamlined in the male/female species C. nigoni than in related species that make self-fertile hermaphrodites, a conclusion supported by studies of interspecies hybrids using sex determination mutations. Thus, we infer that the origin of self-fertility not only required mutations that activated the spermatogenesis program in XX germ lines, but prior to these there must have been mutations that decanalized the sex determination process, allowing for subsequent changes to germ cell fates.
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- Award ID(s):
- 2308465
- PAR ID:
- 10611907
- Editor(s):
- Conradt, B
- Publisher / Repository:
- PubMed Central
- Date Published:
- Journal Name:
- GENETICS
- Volume:
- 229
- Issue:
- 4
- ISSN:
- 1943-2631
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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