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Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development

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Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development. / Djordjevic, Jelisaveta; Tran Van, Patrick; Toubiana, William et al.
In: PLOS Genetics, Vol. 21, No. 3, 10.03.2025, p. e1011615.

Research output: Contribution to journal › Article › peer-review

HarvardHarvard

Djordjevic, J, Tran Van, P, Toubiana, W, Labédan, M, Dumas, Z, Aury, J-M, Cruaud, C, Istace, B, Labadie, K, Noel, B, Parker, DJ & Schwander, T 2025, 'Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development', PLOS Genetics, vol. 21, no. 3, pp. e1011615. https://doi.org/10.1371/journal.pgen.1011615

APA

Djordjevic, J., Tran Van, P., Toubiana, W., Labédan, M., Dumas, Z., Aury, J.-M., Cruaud, C., Istace, B., Labadie, K., Noel, B., Parker, D. J., & Schwander, T. (2025). Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development. PLOS Genetics, 21(3), e1011615. https://doi.org/10.1371/journal.pgen.1011615

CBE

Djordjevic J, Tran Van P, Toubiana W, Labédan M, Dumas Z, Aury J-M, Cruaud C, Istace B, Labadie K, Noel B, et al. 2025. Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development. PLOS Genetics. 21(3):e1011615. https://doi.org/10.1371/journal.pgen.1011615

MLA

Djordjevic, Jelisaveta et al. "Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development". PLOS Genetics. 2025, 21(3). e1011615. https://doi.org/10.1371/journal.pgen.1011615

VancouverVancouver

Djordjevic J, Tran Van P, Toubiana W, Labédan M, Dumas Z, Aury JM et al. Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development. PLOS Genetics. 2025 Mar 10;21(3):e1011615. doi: 10.1371/journal.pgen.1011615

Author

Djordjevic, Jelisaveta ; Tran Van, Patrick ; Toubiana, William et al. / Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development. In: PLOS Genetics. 2025 ; Vol. 21, No. 3. pp. e1011615.

RIS

TY - JOUR

T1 - Dynamics of X chromosome hyper-expression and inactivation in male tissues during stick insect development

AU - Djordjevic, Jelisaveta

AU - Tran Van, Patrick

AU - Toubiana, William

AU - Labédan, Marjorie

AU - Dumas, Zoé

AU - Aury, Jean-Marc

AU - Cruaud, Corinne

AU - Istace, Benjamin

AU - Labadie, Karine

AU - Noel, Benjamin

AU - Parker, Darren J

AU - Schwander, Tanja

N1 - Copyright: © 2025 Djordjevic et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2025/3/10

Y1 - 2025/3/10

N2 - Differentiated sex chromosomes are frequently associated with major transcriptional changes: the evolution of dosage compensation (DC) to equalize gene expression between the sexes and the establishment of meiotic sex chromosome inactivation (MSCI). Our study investigates the mechanisms and developmental dynamics of dosage compensation and meiotic sex chromosome inactivation in the stick insect species T. poppense. Stick insects are characterized by XX/X0 sex determination, with an X chromosome that likely evolved prior to the diversification of insects over 450 Mya. We generated a chromosome-level genome assembly and analyzed gene expression from various tissues (brain, gut, antennae, leg, and reproductive tract) across developmental stages in both sexes. Our results show that complete dosage compensation is maintained in male somatic tissues throughout development, mediated by upregulation of the single X chromosome. Contrarily, in male reproductive tissues, dosage compensation is present only in the early nymphal stages. As males reach the 4th nymphal stage and adulthood, X-linked gene expression diminishes, coinciding with the onset of meiosis and MSCI, which involves classical silencing histone modifications. These findings reveal the dynamic regulation of X-linked gene expression in T. poppense, and suggest that reduced X-expression in insect testes is generally driven by MSCI rather than an absence of dosage compensation mechanisms. Our work provides critical insights into sex chromosome evolution and the complex interplay of dosage compensation and MSCI across tissues and developmental stages.

AB - Differentiated sex chromosomes are frequently associated with major transcriptional changes: the evolution of dosage compensation (DC) to equalize gene expression between the sexes and the establishment of meiotic sex chromosome inactivation (MSCI). Our study investigates the mechanisms and developmental dynamics of dosage compensation and meiotic sex chromosome inactivation in the stick insect species T. poppense. Stick insects are characterized by XX/X0 sex determination, with an X chromosome that likely evolved prior to the diversification of insects over 450 Mya. We generated a chromosome-level genome assembly and analyzed gene expression from various tissues (brain, gut, antennae, leg, and reproductive tract) across developmental stages in both sexes. Our results show that complete dosage compensation is maintained in male somatic tissues throughout development, mediated by upregulation of the single X chromosome. Contrarily, in male reproductive tissues, dosage compensation is present only in the early nymphal stages. As males reach the 4th nymphal stage and adulthood, X-linked gene expression diminishes, coinciding with the onset of meiosis and MSCI, which involves classical silencing histone modifications. These findings reveal the dynamic regulation of X-linked gene expression in T. poppense, and suggest that reduced X-expression in insect testes is generally driven by MSCI rather than an absence of dosage compensation mechanisms. Our work provides critical insights into sex chromosome evolution and the complex interplay of dosage compensation and MSCI across tissues and developmental stages.

U2 - 10.1371/journal.pgen.1011615

DO - 10.1371/journal.pgen.1011615

M3 - Article

C2 - 40063618

VL - 21

SP - e1011615

JO - PLOS Genetics

JF - PLOS Genetics

SN - 1553-7390

IS - 3

ER -