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X-Chromosome Target Specificity Diverged Between Dosage Compensation Mechanisms of Two Closely Related Caenorhabditis Species

View ORCID ProfileQiming Yang, View ORCID ProfileTe-Wen Lo, View ORCID ProfileKatjuša Brejc, View ORCID ProfileCaitlin Schartner, Edward J. Ralston, Denise M. Lapidus, View ORCID ProfileBarbara J. Meyer
doi: https://doi.org/10.1101/2022.12.05.519163
Qiming Yang
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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  • ORCID record for Qiming Yang
Te-Wen Lo
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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Katjuša Brejc
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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Caitlin Schartner
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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Edward J. Ralston
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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Denise M. Lapidus
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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Barbara J. Meyer
1Howard Hughes Medical Institute, United States
2Department of Molecular and Cell Biology University of California at Berkeley Berkeley, United States
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  • For correspondence: bjmeyer@berkeley.edu
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Abstract

An evolutionary perspective enhances our understanding of biological mechanisms. Comparison of sex determination and X-chromosome dosage compensation mechanisms between the closely related nematode species C. briggsae (Cbr) and C. elegans (Cel) revealed that the genetic regulatory hierarchy controlling these processes is conserved, but both the X-chromosome target specificity and mode of binding for the specialized condensin dosage compensation complex (DCC) controlling X gene expression have diverged. We identified two motifs within Cbr DCC recruitment sites that are highly enriched on X: 13-bp MEX and 30-bp MEX II. Mutating either MEX or MEX II in an endogenous recruitment site with multiple copies of one or both motifs reduced binding, but only removing all motifs eliminated binding in vivo. Hence, DCC binding to Cbr recruitment sites appears additive. In contrast, DCC binding to Cel recruitment sites is synergistic: mutating even one motif in vivo eliminated binding. Although all X-chromosome motifs share the sequence CAGGG, they have otherwise diverged so that a motif from one species cannot function in the other. This functional divergence was demonstrated in vivo and in vitro. A single nucleotide position in Cbr MEX can act as a critical determinant for whether Cel DCC binds. The rapid divergence of DCC target specificity could have contributed to nematode speciation and contrasts dramatically with the conservation of target specificity for transcription factors that control developmental processes such as body-plan specification from fruit flies to mice.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 05, 2022.
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X-Chromosome Target Specificity Diverged Between Dosage Compensation Mechanisms of Two Closely Related Caenorhabditis Species
Qiming Yang, Te-Wen Lo, Katjuša Brejc, Caitlin Schartner, Edward J. Ralston, Denise M. Lapidus, Barbara J. Meyer
bioRxiv 2022.12.05.519163; doi: https://doi.org/10.1101/2022.12.05.519163
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X-Chromosome Target Specificity Diverged Between Dosage Compensation Mechanisms of Two Closely Related Caenorhabditis Species
Qiming Yang, Te-Wen Lo, Katjuša Brejc, Caitlin Schartner, Edward J. Ralston, Denise M. Lapidus, Barbara J. Meyer
bioRxiv 2022.12.05.519163; doi: https://doi.org/10.1101/2022.12.05.519163

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