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Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci

BACKGROUND: Genomic organization and gene expression regulation in trypanosomes are remarkable because protein-coding genes are organized into codirectional gene clusters with unrelated functions. Moreover, there is no dedicated promoter for each gene, resulting in polycistronic gene transcription,...

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Autores principales: Lima, Alex Ranieri Jerônimo, Silva, Herbert Guimarães de Sousa, Poubel, Saloe, Rosón, Juliana Nunes, de Lima, Loyze Paola Oliveira, Costa-Silva, Héllida Marina, Gonçalves, Camila Silva, Galante, Pedro A. F., Holetz, Fabiola, Motta, Maria Cristina Machado M., Silber, Ariel M., Elias, M. Carolina, da Cunha, Julia Pinheiro Chagas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9158160/
https://www.ncbi.nlm.nih.gov/pubmed/35650626
http://dx.doi.org/10.1186/s13072-022-00450-x
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author Lima, Alex Ranieri Jerônimo
Silva, Herbert Guimarães de Sousa
Poubel, Saloe
Rosón, Juliana Nunes
de Lima, Loyze Paola Oliveira
Costa-Silva, Héllida Marina
Gonçalves, Camila Silva
Galante, Pedro A. F.
Holetz, Fabiola
Motta, Maria Cristina Machado M.
Silber, Ariel M.
Elias, M. Carolina
da Cunha, Julia Pinheiro Chagas
author_facet Lima, Alex Ranieri Jerônimo
Silva, Herbert Guimarães de Sousa
Poubel, Saloe
Rosón, Juliana Nunes
de Lima, Loyze Paola Oliveira
Costa-Silva, Héllida Marina
Gonçalves, Camila Silva
Galante, Pedro A. F.
Holetz, Fabiola
Motta, Maria Cristina Machado M.
Silber, Ariel M.
Elias, M. Carolina
da Cunha, Julia Pinheiro Chagas
author_sort Lima, Alex Ranieri Jerônimo
collection PubMed
description BACKGROUND: Genomic organization and gene expression regulation in trypanosomes are remarkable because protein-coding genes are organized into codirectional gene clusters with unrelated functions. Moreover, there is no dedicated promoter for each gene, resulting in polycistronic gene transcription, with posttranscriptional control playing a major role. Nonetheless, these parasites harbor epigenetic modifications at critical regulatory genome features that dynamically change among parasite stages, which are not fully understood. RESULTS: Here, we investigated the impact of chromatin changes in a scenario commanded by posttranscriptional control exploring the parasite Trypanosoma cruzi and its differentiation program using FAIRE-seq approach supported by transmission electron microscopy. We identified differences in T. cruzi genome compartments, putative transcriptional start regions, and virulence factors. In addition, we also detected a developmental chromatin regulation at tRNA loci (tDNA), which could be linked to the intense chromatin remodeling and/or the translation regulatory mechanism required for parasite differentiation. We further integrated the open chromatin profile with public transcriptomic and MNase-seq datasets. Strikingly, a positive correlation was observed between active chromatin and steady-state transcription levels. CONCLUSION: Taken together, our results indicate that chromatin changes reflect the unusual gene expression regulation of trypanosomes and the differences among parasite developmental stages, even in the context of a lack of canonical transcriptional control of protein-coding genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13072-022-00450-x.
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spelling pubmed-91581602022-06-02 Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci Lima, Alex Ranieri Jerônimo Silva, Herbert Guimarães de Sousa Poubel, Saloe Rosón, Juliana Nunes de Lima, Loyze Paola Oliveira Costa-Silva, Héllida Marina Gonçalves, Camila Silva Galante, Pedro A. F. Holetz, Fabiola Motta, Maria Cristina Machado M. Silber, Ariel M. Elias, M. Carolina da Cunha, Julia Pinheiro Chagas Epigenetics Chromatin Research BACKGROUND: Genomic organization and gene expression regulation in trypanosomes are remarkable because protein-coding genes are organized into codirectional gene clusters with unrelated functions. Moreover, there is no dedicated promoter for each gene, resulting in polycistronic gene transcription, with posttranscriptional control playing a major role. Nonetheless, these parasites harbor epigenetic modifications at critical regulatory genome features that dynamically change among parasite stages, which are not fully understood. RESULTS: Here, we investigated the impact of chromatin changes in a scenario commanded by posttranscriptional control exploring the parasite Trypanosoma cruzi and its differentiation program using FAIRE-seq approach supported by transmission electron microscopy. We identified differences in T. cruzi genome compartments, putative transcriptional start regions, and virulence factors. In addition, we also detected a developmental chromatin regulation at tRNA loci (tDNA), which could be linked to the intense chromatin remodeling and/or the translation regulatory mechanism required for parasite differentiation. We further integrated the open chromatin profile with public transcriptomic and MNase-seq datasets. Strikingly, a positive correlation was observed between active chromatin and steady-state transcription levels. CONCLUSION: Taken together, our results indicate that chromatin changes reflect the unusual gene expression regulation of trypanosomes and the differences among parasite developmental stages, even in the context of a lack of canonical transcriptional control of protein-coding genes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13072-022-00450-x. BioMed Central 2022-06-01 /pmc/articles/PMC9158160/ /pubmed/35650626 http://dx.doi.org/10.1186/s13072-022-00450-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Lima, Alex Ranieri Jerônimo
Silva, Herbert Guimarães de Sousa
Poubel, Saloe
Rosón, Juliana Nunes
de Lima, Loyze Paola Oliveira
Costa-Silva, Héllida Marina
Gonçalves, Camila Silva
Galante, Pedro A. F.
Holetz, Fabiola
Motta, Maria Cristina Machado M.
Silber, Ariel M.
Elias, M. Carolina
da Cunha, Julia Pinheiro Chagas
Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci
title Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci
title_full Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci
title_fullStr Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci
title_full_unstemmed Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci
title_short Open chromatin analysis in Trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tDNA loci
title_sort open chromatin analysis in trypanosoma cruzi life forms highlights critical differences in genomic compartments and developmental regulation at tdna loci
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9158160/
https://www.ncbi.nlm.nih.gov/pubmed/35650626
http://dx.doi.org/10.1186/s13072-022-00450-x
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