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X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species

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 Caenorhabditis briggsae (Cbr) and Caenorhabditis elegans (Cel) revealed that the genetic regul...

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Autores principales: Yang, Qiming, Lo, Te-Wen, Brejc, Katjuša, Schartner, Caitlin, Ralston, Edward J, Lapidus, Denise M, Meyer, Barbara J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10076027/
https://www.ncbi.nlm.nih.gov/pubmed/36951246
http://dx.doi.org/10.7554/eLife.85413
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author Yang, Qiming
Lo, Te-Wen
Brejc, Katjuša
Schartner, Caitlin
Ralston, Edward J
Lapidus, Denise M
Meyer, Barbara J
author_facet Yang, Qiming
Lo, Te-Wen
Brejc, Katjuša
Schartner, Caitlin
Ralston, Edward J
Lapidus, Denise M
Meyer, Barbara J
author_sort Yang, Qiming
collection PubMed
description 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 Caenorhabditis briggsae (Cbr) and Caenorhabditis elegans (Cel) revealed that the genetic regulatory hierarchy controlling both processes is conserved, but the X-chromosome target specificity and mode of binding for the specialized condensin dosage compensation complex (DCC) controlling X 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. Functional divergence was demonstrated in vivo and in vitro. A single nucleotide position in Cbr MEX can determine whether Cel DCC binds. This rapid divergence of DCC target specificity could have been an important factor in establishing reproductive isolation between nematode species and contrasts dramatically with the conservation of target specificity for X-chromosome dosage compensation across Drosophila species and for transcription factors controlling developmental processes such as body-plan specification from fruit flies to mice.
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spelling pubmed-100760272023-04-06 X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species Yang, Qiming Lo, Te-Wen Brejc, Katjuša Schartner, Caitlin Ralston, Edward J Lapidus, Denise M Meyer, Barbara J eLife Chromosomes and Gene Expression 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 Caenorhabditis briggsae (Cbr) and Caenorhabditis elegans (Cel) revealed that the genetic regulatory hierarchy controlling both processes is conserved, but the X-chromosome target specificity and mode of binding for the specialized condensin dosage compensation complex (DCC) controlling X 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. Functional divergence was demonstrated in vivo and in vitro. A single nucleotide position in Cbr MEX can determine whether Cel DCC binds. This rapid divergence of DCC target specificity could have been an important factor in establishing reproductive isolation between nematode species and contrasts dramatically with the conservation of target specificity for X-chromosome dosage compensation across Drosophila species and for transcription factors controlling developmental processes such as body-plan specification from fruit flies to mice. eLife Sciences Publications, Ltd 2023-03-23 /pmc/articles/PMC10076027/ /pubmed/36951246 http://dx.doi.org/10.7554/eLife.85413 Text en © 2023, Yang, Lo et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Chromosomes and Gene Expression
Yang, Qiming
Lo, Te-Wen
Brejc, Katjuša
Schartner, Caitlin
Ralston, Edward J
Lapidus, Denise M
Meyer, Barbara J
X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species
title X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species
title_full X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species
title_fullStr X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species
title_full_unstemmed X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species
title_short X-chromosome target specificity diverged between dosage compensation mechanisms of two closely related Caenorhabditis species
title_sort x-chromosome target specificity diverged between dosage compensation mechanisms of two closely related caenorhabditis species
topic Chromosomes and Gene Expression
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10076027/
https://www.ncbi.nlm.nih.gov/pubmed/36951246
http://dx.doi.org/10.7554/eLife.85413
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