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Incomplete transcriptional dosage compensation of chicken and platypus sex chromosomes is balanced by post-transcriptional compensation

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posted on 2024-08-13, 01:24 authored by Nicholas C Lister, Ashley M Milton, Hardip R Patel, Shafagh A Waters, Benjamin J Hanrahan, Kim L McIntyre, Alexandra M Livernois, William B Horspool, Lee Kian Wee, Alessa R Ringel, Stefan Mundlos, Michael I Robson, Linda Shearwin-Whyatt, Frank Grützner, Jennifer GravesJennifer Graves, Aurora Ruiz-Herrera, Paul D Waters
Heteromorphic sex chromosomes (XY or ZW) present problems of gene dosage imbalance between sexes and with autosomes. A need for dosage compensation has long been thought to be critical in vertebrates. However, this was questioned by findings of unequal mRNA abundance measurements in monotreme mammals and birds. Here, we demonstrate unbalanced mRNA levels of X genes in platypus males and females and a correlation with differential loading of histone modifications. We also observed unbalanced transcripts of Z genes in chicken. Surprisingly, however, we found that protein abundance ratios were 1:1 between the sexes in both species, indicating a post-transcriptional layer of dosage compensation. We conclude that sex chromosome output is maintained in chicken and platypus (and perhaps many other non therian vertebrates) via a combination of transcriptional and post-transcriptional control, consistent with a critical importance of sex chromosome dosage compensation.

Funding

J.A.M.G. and P.D.W. are supported by Australian Research Council Discovery Projects (DP210103512 and DP220101429). P.D.W. is supported by National Health Medical and Research Council (NHMRC) Ideas Grants (2021172, 2027730). H.R.P. is supported by an NHMRC Ideas Grant (2021172). S.A.W. is supported by the University of New South Wales (UNSW) Scientia program and an NHMRC Ideas Grant (1188987). M.I.R is supported by Helmholz association core funding and a DFG project grant FOR2841. S.M. was supported by grant MU 880/27-1 from the Deutsche Forschungsgemeinschaft (DFG). A.R.-H. is supported by the Spanish Ministry of Science and Innovation (PID2020-112557GB-I00 founded by AEI/10.13039/501100011033) and the Agència de Gestió d’Ajuts Universitaris i de Recerca, AGAUR (2021SGR00122). F.G. and L.S.-W. is supported by an Australian Research Council Discovery Project (DP210103512).

History

Publication Date

2024-08-06

Journal

Proceedings of the National Academy of Sciences of the United States of America

Volume

121

Issue

32

Article Number

e2322360121

Pagination

7p.

Publisher

Proceedings of the National Academy of Sciences

ISSN

0027-8424

Rights Statement

Copyright © 2024 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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