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A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa

BACKGROUND: Plants can transmit somatic mutations and epimutations to offspring, which in turn can affect fitness. Knowledge of the rate at which these variations arise is necessary to understand how plant development contributes to local adaption in an ecoevolutionary context, particularly in long-...

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Autores principales: Hofmeister, Brigitte T., Denkena, Johanna, Colomé-Tatché, Maria, Shahryary, Yadollah, Hazarika, Rashmi, Grimwood, Jane, Mamidi, Sujan, Jenkins, Jerry, Grabowski, Paul P., Sreedasyam, Avinash, Shu, Shengqiang, Barry, Kerrie, Lail, Kathleen, Adam, Catherine, Lipzen, Anna, Sorek, Rotem, Kudrna, Dave, Talag, Jayson, Wing, Rod, Hall, David W., Jacobsen, Daniel, Tuskan, Gerald A., Schmutz, Jeremy, Johannes, Frank, Schmitz, Robert J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7539514/
https://www.ncbi.nlm.nih.gov/pubmed/33023654
http://dx.doi.org/10.1186/s13059-020-02162-5
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author Hofmeister, Brigitte T.
Denkena, Johanna
Colomé-Tatché, Maria
Shahryary, Yadollah
Hazarika, Rashmi
Grimwood, Jane
Mamidi, Sujan
Jenkins, Jerry
Grabowski, Paul P.
Sreedasyam, Avinash
Shu, Shengqiang
Barry, Kerrie
Lail, Kathleen
Adam, Catherine
Lipzen, Anna
Sorek, Rotem
Kudrna, Dave
Talag, Jayson
Wing, Rod
Hall, David W.
Jacobsen, Daniel
Tuskan, Gerald A.
Schmutz, Jeremy
Johannes, Frank
Schmitz, Robert J.
author_facet Hofmeister, Brigitte T.
Denkena, Johanna
Colomé-Tatché, Maria
Shahryary, Yadollah
Hazarika, Rashmi
Grimwood, Jane
Mamidi, Sujan
Jenkins, Jerry
Grabowski, Paul P.
Sreedasyam, Avinash
Shu, Shengqiang
Barry, Kerrie
Lail, Kathleen
Adam, Catherine
Lipzen, Anna
Sorek, Rotem
Kudrna, Dave
Talag, Jayson
Wing, Rod
Hall, David W.
Jacobsen, Daniel
Tuskan, Gerald A.
Schmutz, Jeremy
Johannes, Frank
Schmitz, Robert J.
author_sort Hofmeister, Brigitte T.
collection PubMed
description BACKGROUND: Plants can transmit somatic mutations and epimutations to offspring, which in turn can affect fitness. Knowledge of the rate at which these variations arise is necessary to understand how plant development contributes to local adaption in an ecoevolutionary context, particularly in long-lived perennials. RESULTS: Here, we generate a new high-quality reference genome from the oldest branch of a wild Populus trichocarpa tree with two dominant stems which have been evolving independently for 330 years. By sampling multiple, age-estimated branches of this tree, we use a multi-omics approach to quantify age-related somatic changes at the genetic, epigenetic, and transcriptional level. We show that the per-year somatic mutation and epimutation rates are lower than in annuals and that transcriptional variation is mainly independent of age divergence and cytosine methylation. Furthermore, a detailed analysis of the somatic epimutation spectrum indicates that transgenerationally heritable epimutations originate mainly from DNA methylation maintenance errors during mitotic rather than during meiotic cell divisions. CONCLUSION: Taken together, our study provides unprecedented insights into the origin of nucleotide and functional variation in a long-lived perennial plant.
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spelling pubmed-75395142020-10-08 A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa Hofmeister, Brigitte T. Denkena, Johanna Colomé-Tatché, Maria Shahryary, Yadollah Hazarika, Rashmi Grimwood, Jane Mamidi, Sujan Jenkins, Jerry Grabowski, Paul P. Sreedasyam, Avinash Shu, Shengqiang Barry, Kerrie Lail, Kathleen Adam, Catherine Lipzen, Anna Sorek, Rotem Kudrna, Dave Talag, Jayson Wing, Rod Hall, David W. Jacobsen, Daniel Tuskan, Gerald A. Schmutz, Jeremy Johannes, Frank Schmitz, Robert J. Genome Biol Research BACKGROUND: Plants can transmit somatic mutations and epimutations to offspring, which in turn can affect fitness. Knowledge of the rate at which these variations arise is necessary to understand how plant development contributes to local adaption in an ecoevolutionary context, particularly in long-lived perennials. RESULTS: Here, we generate a new high-quality reference genome from the oldest branch of a wild Populus trichocarpa tree with two dominant stems which have been evolving independently for 330 years. By sampling multiple, age-estimated branches of this tree, we use a multi-omics approach to quantify age-related somatic changes at the genetic, epigenetic, and transcriptional level. We show that the per-year somatic mutation and epimutation rates are lower than in annuals and that transcriptional variation is mainly independent of age divergence and cytosine methylation. Furthermore, a detailed analysis of the somatic epimutation spectrum indicates that transgenerationally heritable epimutations originate mainly from DNA methylation maintenance errors during mitotic rather than during meiotic cell divisions. CONCLUSION: Taken together, our study provides unprecedented insights into the origin of nucleotide and functional variation in a long-lived perennial plant. BioMed Central 2020-10-06 /pmc/articles/PMC7539514/ /pubmed/33023654 http://dx.doi.org/10.1186/s13059-020-02162-5 Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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
Hofmeister, Brigitte T.
Denkena, Johanna
Colomé-Tatché, Maria
Shahryary, Yadollah
Hazarika, Rashmi
Grimwood, Jane
Mamidi, Sujan
Jenkins, Jerry
Grabowski, Paul P.
Sreedasyam, Avinash
Shu, Shengqiang
Barry, Kerrie
Lail, Kathleen
Adam, Catherine
Lipzen, Anna
Sorek, Rotem
Kudrna, Dave
Talag, Jayson
Wing, Rod
Hall, David W.
Jacobsen, Daniel
Tuskan, Gerald A.
Schmutz, Jeremy
Johannes, Frank
Schmitz, Robert J.
A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa
title A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa
title_full A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa
title_fullStr A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa
title_full_unstemmed A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa
title_short A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa
title_sort genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial populus trichocarpa
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7539514/
https://www.ncbi.nlm.nih.gov/pubmed/33023654
http://dx.doi.org/10.1186/s13059-020-02162-5
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