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

Abstract

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.

Authors:
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Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE); USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1670495
Alternate Identifier(s):
OSTI ID: 1684685; OSTI ID: 1765576
Grant/Contract Number:  
AC02-05CH11231; AC05-00OR22725
Resource Type:
Published Article
Journal Name:
Genome Biology (Online)
Additional Journal Information:
Journal Name: Genome Biology (Online) Journal Volume: 21 Journal Issue: 1; Journal ID: ISSN 1474-760X
Publisher:
BioMed Central
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Mutation rate; Epimutation rate; Epigenetics; Poplar; DNA methylation

Citation Formats

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, and Schmitz, Robert J.. A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa. United Kingdom: N. p., 2020. Web. doi:10.1186/s13059-020-02162-5.
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. United Kingdom. https://doi.org/10.1186/s13059-020-02162-5
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, and Schmitz, Robert J.. Tue . "A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa". United Kingdom. https://doi.org/10.1186/s13059-020-02162-5.
@article{osti_1670495,
title = {A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa},
author = {Hofmeister, Brigitte T. and Denkena, Johanna and Colomé-Tatché, Maria and Shahryary, Yadollah and Hazarika, Rashmi and Grimwood, Jane and Mamidi, Sujan and Jenkins, Jerry and Grabowski, Paul P. and Sreedasyam, Avinash and Shu, Shengqiang and Barry, Kerrie and Lail, Kathleen and Adam, Catherine and Lipzen, Anna and Sorek, Rotem and Kudrna, Dave and Talag, Jayson and Wing, Rod and Hall, David W. and Jacobsen, Daniel and Tuskan, Gerald A. and Schmutz, Jeremy and Johannes, Frank and Schmitz, Robert J.},
abstractNote = {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.},
doi = {10.1186/s13059-020-02162-5},
journal = {Genome Biology (Online)},
number = 1,
volume = 21,
place = {United Kingdom},
year = {2020},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s13059-020-02162-5

Figures / Tables:

Fig. 1 Fig. 1: Photograph and schematic drawing of tree 13 and tree 14. This wild P. trichocarpa, located near Mt. Hood, Oregon, experienced a decapitation event ~ 300 years ago. Tree 14 re-sprouted from the stump and ~ 80–100 years later tree 13 re-sprouted. a Leaf samples were collected from themore » labeled terminal branches. b Age was estimated for both the end of the branch (black font) and where it meets the main stem (gray italics). Ages with * indicate age was estimated using diameter; all other estimates were from core samples. Leaf samples of each branch was used to create genomic sequencing libraries, PacBio libraries, whole-genome bisulfite sequencing libraries, and mRNA-sequencing libraries« less

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