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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

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:
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE)
OSTI Identifier:
1670495
Grant/Contract Number:  
AC02-05CH11231; Community sequencing project 1678
Resource Type:
Journal Article: 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:
Springer Science + Business Media
Country of Publication:
United Kingdom
Language:
English

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. 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, 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. doi: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 = {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.},
doi = {10.1186/s13059-020-02162-5},
journal = {Genome Biology (Online)},
issn = {1474-760X},
number = 1,
volume = 21,
place = {United Kingdom},
year = {2020},
month = {10}
}

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Works referenced in this record:

BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1.
journal, November 2015


Low number of fixed somatic mutations in a long-lived oak tree
journal, December 2017


Somatic deleterious mutation rate in a woody plant: estimation from phenotypic data
journal, June 2013

  • Bobiwash, K.; Schultz, S. T.; Schoen, D. J.
  • Heredity, Vol. 111, Issue 4
  • DOI: 10.1038/hdy.2013.57

Ab initio Gene Finding in Drosophila Genomic DNA
journal, April 2000

  • Salamov, Asaf A.; Solovyev, Victor V.
  • Genome Research, Vol. 10, Issue 4, p. 516-522
  • DOI: 10.1101/gr.10.4.516

SeqEM: an adaptive genotype-calling approach for next-generation sequencing studies
journal, September 2010


Comparing Fruit and Tree Characteristics of Two Peaches and Their Nectarine Mutants
journal, January 1995

  • Wen, Ien-Chi; Koch, K. E.; Sherman, W. B.
  • Journal of the American Society for Horticultural Science, Vol. 120, Issue 1
  • DOI: 10.21273/JASHS.120.1.101

Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

Dynamic DNA methylation reconfiguration during seed development and germination
journal, September 2017


Differences in gene expression within a striking phenotypic mosaic Eucalyptus tree that varies in susceptibility to herbivory
journal, January 2013

  • Padovan, Amanda; Keszei, Andras; Foley, William J.
  • BMC Plant Biology, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2229-13-29

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Reprogramming of DNA Methylation in Pollen Guides Epigenetic Inheritance via Small RNA
journal, September 2012


Detection of somatic epigenetic variation in Norway spruce via targeted bisulfite sequencing
journal, September 2018

  • Heer, Katrin; Ullrich, Kristian K.; Hiss, Manuel
  • Ecology and Evolution, Vol. 8, Issue 19
  • DOI: 10.1002/ece3.4374

On the origin and evolutionary consequences of gene body DNA methylation
journal, July 2016

  • Bewick, Adam J.; Ji, Lexiang; Niederhuth, Chad E.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 32
  • DOI: 10.1073/pnas.1604666113

Big old cottonwoods
journal, July 2003

  • Rood, Stewart B.; Polzin, Mary Louise
  • Canadian Journal of Botany, Vol. 81, Issue 7
  • DOI: 10.1139/b03-065

Technique to Improve Visualization of Elusive Tree-Ring Boundaries in Aspen (Populus tremuloides)
journal, January 2010

  • DeRose, Justin R.; Gardner, Richard S.
  • Tree-Ring Research, Vol. 66, Issue 1
  • DOI: 10.3959/2009-11.1

Human body epigenome maps reveal noncanonical DNA methylation variation
journal, June 2015

  • Schultz, Matthew D.; He, Yupeng; Whitaker, John W.
  • Nature, Vol. 523, Issue 7559
  • DOI: 10.1038/nature14465

Patterns of Stem Cell Divisions Contribute to Plant Longevity
journal, June 2016

  • Burian, Agata; Barbier de Reuille, Pierre; Kuhlemeier, Cris
  • Current Biology, Vol. 26, Issue 11
  • DOI: 10.1016/j.cub.2016.03.067

A Conflict Between Two Evolutionary Levels in Trees
journal, February 2001


Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm
journal, September 2015

  • Ong-Abdullah, Meilina; Ordway, Jared M.; Jiang, Nan
  • Nature, Vol. 525, Issue 7570
  • DOI: 10.1038/nature15365

Integrative genomics viewer
journal, January 2011

  • Robinson, James T.; Thorvaldsdóttir, Helga; Winckler, Wendy
  • Nature Biotechnology, Vol. 29, Issue 1
  • DOI: 10.1038/nbt.1754

A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening
journal, July 2006

  • Manning, Kenneth; Tör, Mahmut; Poole, Mervin
  • Nature Genetics, Vol. 38, Issue 8
  • DOI: 10.1038/ng1841

Systematic genome sequence differences among leaf cells within individual trees
journal, January 2014


The application of wood decay fungi to enhance annual ring detection in three diffuse-porous hardwoods
journal, May 2005


VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing
journal, February 2012


Similarity between soybean and Arabidopsis seed methylomes and loss of non-CG methylation does not affect seed development
journal, October 2017

  • Lin, Jer-Young; Le, Brandon H.; Chen, Min
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 45
  • DOI: 10.1073/pnas.1716758114

Genome-Wide Reinforcement of DNA Methylation Occurs during Somatic Embryogenesis in Soybean
journal, August 2019

  • Ji, Lexiang; Mathioni, Sandra M.; Johnson, Sarah
  • The Plant Cell, Vol. 31, Issue 10
  • DOI: 10.1105/tpc.19.00255

High throughput analysis of grape genetic diversity as a tool for germplasm collection management
journal, January 2011


Patterns of population epigenomic diversity
journal, March 2013

  • Schmitz, Robert J.; Schultz, Matthew D.; Urich, Mark A.
  • Nature, Vol. 495, Issue 7440
  • DOI: 10.1038/nature11968

Tandem repeats finder: a program to analyze DNA sequences
journal, January 1999


Oak genome reveals facets of long lifespan
journal, June 2018


The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana
journal, December 2009


MethylC-seq library preparation for base-resolution whole-genome bisulfite sequencing
journal, February 2015

  • Urich, Mark A.; Nery, Joseph R.; Lister, Ryan
  • Nature Protocols, Vol. 10, Issue 3
  • DOI: 10.1038/nprot.2014.114

Spontaneous epigenetic variation in the Arabidopsis thaliana methylome
journal, September 2011

  • Becker, Claude; Hagmann, Jörg; Müller, Jonas
  • Nature, Vol. 480, Issue 7376
  • DOI: 10.1038/nature10555

Establishing, maintaining and modifying DNA methylation patterns in plants and animals
journal, February 2010

  • Law, Julie A.; Jacobsen, Steven E.
  • Nature Reviews Genetics, Vol. 11, Issue 3
  • DOI: 10.1038/nrg2719

Ageing and mutation in plants
journal, August 1989

  • Klekowski, Edward J.; Godfrey, Paul J.
  • Nature, Vol. 340, Issue 6232
  • DOI: 10.1038/340389a0

DNA methylation dynamics during early plant life
journal, September 2017


Extensive transcriptomic and epigenomic remodelling occurs during Arabidopsis thaliana germination
journal, September 2017


MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads
journal, September 2017

  • Xiao, Chuan-Le; Chen, Ying; Xie, Shang-Qian
  • Nature Methods, Vol. 14, Issue 11
  • DOI: 10.1038/nmeth.4432

BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Extensive Natural Epigenetic Variation at a De Novo Originated Gene
journal, April 2013


The rate and potential relevance of new mutations in a colonizing plant lineage
journal, February 2018


Century-scale Methylome Stability in a Recently Diverged Arabidopsis thaliana Lineage
journal, January 2015


Winter-dormant shoot apical meristem in poplar trees shows environmental epigenetic memory
journal, August 2018

  • Le Gac, Anne-Laure; Lafon-Placette, Clément; Chauveau, Didier
  • Journal of Experimental Botany, Vol. 69, Issue 20
  • DOI: 10.1093/jxb/ery271

Ageing: How Do Long-Lived Plants Escape Mutational Meltdown?
journal, July 2016


Rate, spectrum, and evolutionary dynamics of spontaneous epimutations
journal, May 2015

  • van der Graaf, Adriaan; Wardenaar, René; Neumann, Drexel A.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 21
  • DOI: 10.1073/pnas.1424254112

‘Leveling’ the playing field for analyses of single-base resolution DNA methylomes
journal, December 2012

  • Schultz, Matthew D.; Schmitz, Robert J.; Ecker, Joseph R.
  • Trends in Genetics, Vol. 28, Issue 12
  • DOI: 10.1016/j.tig.2012.10.012

The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010


Hardwood Tree Genomics: Unlocking Woody Plant Biology
journal, December 2018

  • Tuskan, Gerald A.; Groover, Andrew T.; Schmutz, Jeremy
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.01799

The genomic landscape of molecular responses to natural drought stress in Panicum hallii
journal, December 2018


Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements
journal, July 2015


Natural variation in DNA methylation homeostasis and the emergence of epialleles
journal, February 2020

  • Zhang, Yinwen; Wendte, Jered M.; Ji, Lexiang
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 9
  • DOI: 10.1073/pnas.1918172117

The architecture of intra-organism mutation rate variation in plants
journal, April 2019


StringTie enables improved reconstruction of a transcriptome from RNA-seq reads
journal, February 2015

  • Pertea, Mihaela; Pertea, Geo M.; Antonescu, Corina M.
  • Nature Biotechnology, Vol. 33, Issue 3
  • DOI: 10.1038/nbt.3122

Spontaneous epimutations in plants
journal, September 2018

  • Johannes, Frank; Schmitz, Robert J.
  • New Phytologist, Vol. 221, Issue 3
  • DOI: 10.1111/nph.15434

Accurate detection of complex structural variations using single-molecule sequencing
journal, April 2018


An epigenetic mutation responsible for natural variation in floral symmetry
journal, September 1999

  • Cubas, Pilar; Vincent, Coral; Coen, Enrico
  • Nature, Vol. 401, Issue 6749
  • DOI: 10.1038/43657

Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies
journal, October 2003


On the life strategies of plants and animals
journal, January 1985


Genetic Mosaicism in Plants and Clonal Animals
journal, November 1995


Single-base-resolution methylomes of populus trichocarpa reveal the association between DNA methylation and drought stress
journal, January 2014


Single-base-resolution methylomes of Populus euphratica reveal the association between DNA methylation and salt stress
journal, November 2018


The Sequence Alignment/Map format and SAMtools
journal, June 2009


RAPD markers reveal diversity within and among clonal and seedling stands of aspen in Yellowstone National Park, U.S.A.
journal, December 1996

  • Tuskan, G. A.; Francis, K. E.; Russ, S. L.
  • Canadian Journal of Forest Research, Vol. 26, Issue 12
  • DOI: 10.1139/x26-237

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


HISAT: a fast spliced aligner with low memory requirements
journal, March 2015

  • Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3317

Transgenerational Epigenetic Instability Is a Source of Novel Methylation Variants
journal, September 2011