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Possible stochastic sex determination in Bursaphelenchus nematodes

Shinya, Ryoji and Sun, Simo and Dayi, Mehmet and Tsai, Isheng Jason and Miyama, Atsushi and Chen, Anthony Fu and Hasegawa, Koichi and Antoshechkin, Igor and Kikuchi, Taisei and Sternberg, Paul W. (2022) Possible stochastic sex determination in Bursaphelenchus nematodes. Nature Communications, 13 . Art. No. 2574. ISSN 2041-1723. doi:10.1038/s41467-022-30173-2. https://resolver.caltech.edu/CaltechAUTHORS:20220511-863713500

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Abstract

Sex determination mechanisms evolve surprisingly rapidly, yet little is known in the large nematode phylum other than for Caenorhabditis elegans, which relies on chromosomal XX-XO sex determination and a dosage compensation mechanism. Here we analyze by sex-specific genome sequencing and genetic analysis sex determination in two fungal feeding/plant-parasitic Bursaphelenchus nematodes and find that their sex differentiation is more likely triggered by random, epigenetic regulation than by more well-known mechanisms of chromosomal or environmental sex determination. There is no detectable difference in male and female chromosomes, nor any linkage to sexual phenotype. Moreover, the protein sets of these nematodes lack genes involved in X chromosome dosage counting or compensation. By contrast, our genetic screen for sex differentiation mutants identifies a Bursaphelenchus ortholog of tra-1, the major output of the C. elegans sex determination cascade. Nematode sex determination pathways might have evolved by “bottom-up” accretion from the most downstream regulator, tra-1.


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https://doi.org/10.1038/s41467-022-30173-2DOIArticle
https://identifiers.org/resolve?query=ena.embl:PRJEB40022Related ItemData
https://identifiers.org/resolve?query=ena.embl:PRJEB40023Related ItemData
https://identifiers.org/resolve?query=ena.embl:PRJDB10466Related ItemData
https://www.ncbi.nlm.nih.gov/data-hub/assembly/GCA_904066235.2/Related ItemData
https://www.ncbi.nlm.nih.gov/data-hub/assembly/GCA_904066225.2/Related ItemData
ORCID:
AuthorORCID
Shinya, Ryoji0000-0002-2450-3054
Dayi, Mehmet0000-0002-5367-918X
Tsai, Isheng Jason0000-0002-2123-5058
Hasegawa, Koichi0000-0002-9968-8129
Antoshechkin, Igor0000-0002-9934-3040
Kikuchi, Taisei0000-0003-2759-9167
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 24 August 2021; Accepted 19 April 2022; Published 11 May 2022. We sincerely thank Ms. Miwako Kobayashi, Meiji University, Dr. Sota Ozawa, FFPRI, and Akemi Yoshida, the University of Miyazaki for their technical assistance in maintaining mutant nematodes and sequencing. This study was funded by JSPS Grant-in-Aid for Early-Career Scientists JP19K15853 (to R.S.), JSPS Grants-in-Aid for Scientific Research (B) 19H03212 (to T.K.), JST PRESTO Grant Number JPMJPR17Q5 (to R.S.) and JST CREST Grant Number JPMJCR18S7 (to T.K.). P.W.S. was an Investigator with the Howard Hughes Medical Institute, which supported this work. Data availability: All sequence data generated during and/or analyzed during the current study have been deposited at DDBJ/ENA/GenBank under BioProject accession PRJEB40022, PRJEB40023, and PRJDB10466 The reference genomes, v5.1 for B. xylophilus and v2.0 for B. okinawaensis are available from GenBank assembly accessions GCA_904066235.2 and GCA_904066225.2, respectively. All other relevant data are available from the authors. Supplementary Data 1–6 detail the genes differentially expressed between males and hermaphrodites, between wild-type and tra mutant males, between wild-type and tra mutant hermaphrodites, and the Gene Ontology analysis for each. Supplementary Data 7–8 list the genes in two clusters that are commonly upregulated or commonly downregulated in tra mutants of both B. okinawaensis and C. elegans based on their orthology relationships. Source data are provided in this paper. Contributions: R.S., K.H., T.K., and P.W.S. designed the research; R.S., S.S., M.D., I.J.T., A.M., A.F.C., I.A., and T.K. performed the research; R.S., S.S., M.D., I.J.T., and T.K. analyzed the data; and R.S., K.H., T.K., and P.W.S. wrote the paper. The authors declare no competing interests. Peer review information: Nature Communications thanks Andre Pires da Silva and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Funders:
Funding AgencyGrant Number
Japan Society for the Promotion of Science (JSPS)JP19K15853
Japan Society for the Promotion of Science (JSPS)19H03212
Japan Society for the Promotion of Science (JSPS)JPMJPR17Q5
Japan Science and Technology AgencyJPMJCR18S7
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:Comparative genomics; Development; Evolutionary genetics
DOI:10.1038/s41467-022-30173-2
Record Number:CaltechAUTHORS:20220511-863713500
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220511-863713500
Official Citation:Shinya, R., Sun, S., Dayi, M. et al. Possible stochastic sex determination in Bursaphelenchus nematodes. Nat Commun 13, 2574 (2022). https://doi.org/10.1038/s41467-022-30173-2
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114690
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:11 May 2022 23:56
Last Modified:11 May 2022 23:56

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