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High-quality genome and methylomes illustrate features underlying evolutionary success of oaks

Author

Listed:
  • Victoria L. Sork

    (University of California
    University of California)

  • Shawn J. Cokus

    (University of California)

  • Sorel T. Fitz-Gibbon

    (University of California)

  • Aleksey V. Zimin

    (Johns Hopkins University
    Johns Hopkins University)

  • Daniela Puiu

    (Johns Hopkins University)

  • Jesse A. Garcia

    (University of California)

  • Paul F. Gugger

    (University of Maryland Center for Environmental Science)

  • Claudia L. Henriquez

    (University of California)

  • Ying Zhen

    (University of California)

  • Kirk E. Lohmueller

    (University of California
    University of California)

  • Matteo Pellegrini

    (University of California)

  • Steven L. Salzberg

    (Johns Hopkins University
    Johns Hopkins University)

Abstract

The genus Quercus, which emerged ∼55 million years ago during globally warm temperatures, diversified into ∼450 extant species. We present a high-quality de novo genome assembly of a California endemic oak, Quercus lobata, revealing features consistent with oak evolutionary success. Effective population size remained large throughout history despite declining since early Miocene. Analysis of 39,373 mapped protein-coding genes outlined copious duplications consistent with genetic and phenotypic diversity, both by retention of genes created during the ancient γ whole genome hexaploid duplication event and by tandem duplication within families, including numerous resistance genes and a very large block of duplicated DUF247 genes, which have been found to be associated with self-incompatibility in grasses. An additional surprising finding is that subcontext-specific patterns of DNA methylation associated with transposable elements reveal broadly-distributed heterochromatin in intergenic regions, similar to grasses. Collectively, these features promote genetic and phenotypic variation that would facilitate adaptability to changing environments.

Suggested Citation

  • Victoria L. Sork & Shawn J. Cokus & Sorel T. Fitz-Gibbon & Aleksey V. Zimin & Daniela Puiu & Jesse A. Garcia & Paul F. Gugger & Claudia L. Henriquez & Ying Zhen & Kirk E. Lohmueller & Matteo Pellegrin, 2022. "High-quality genome and methylomes illustrate features underlying evolutionary success of oaks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29584-y
    DOI: 10.1038/s41467-022-29584-y
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    1. Asuka Higo & Noriko Saihara & Fumihito Miura & Yoko Higashi & Megumi Yamada & Shojiro Tamaki & Tasuku Ito & Yoshiaki Tarutani & Tomoaki Sakamoto & Masayuki Fujiwara & Tetsuya Kurata & Yoichiro Fukao &, 2020. "DNA methylation is reconfigured at the onset of reproduction in rice shoot apical meristem," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. Marie-Christine Carpentier & Ernandes Manfroi & Fu-Jin Wei & Hshin-Ping Wu & Eric Lasserre & Christel Llauro & Emilie Debladis & Roland Akakpo & Yue-Ie Hsing & Olivier Panaud, 2019. "Retrotranspositional landscape of Asian rice revealed by 3000 genomes," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Alex Harkess & Jinsong Zhou & Chunyan Xu & John E. Bowers & Ron Hulst & Saravanaraj Ayyampalayam & Francesco Mercati & Paolo Riccardi & Michael R. McKain & Atul Kakrana & Haibao Tang & Jeremy Ray & Jo, 2017. "The asparagus genome sheds light on the origin and evolution of a young Y chromosome," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    4. Alexander A. Myburg & Dario Grattapaglia & Gerald A. Tuskan & Uffe Hellsten & Richard D. Hayes & Jane Grimwood & Jerry Jenkins & Erika Lindquist & Hope Tice & Diane Bauer & David M. Goodstein & Inna D, 2014. "The genome of Eucalyptus grandis," Nature, Nature, vol. 510(7505), pages 356-362, June.
    5. Pierre Baduel & Leandro Quadrana & Ben Hunter & Kirsten Bomblies & Vincent Colot, 2019. "Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    6. Lun Zhao & Shuangqi Wang & Zhilin Cao & Weizhi Ouyang & Qing Zhang & Liang Xie & Ruiqin Zheng & Minrong Guo & Meng Ma & Zhe Hu & Wing-Kin Sung & Qifa Zhang & Guoliang Li & Xingwang Li, 2019. "Chromatin loops associated with active genes and heterochromatin shape rice genome architecture for transcriptional regulation," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    7. Matthew D. Schultz & Yupeng He & John W. Whitaker & Manoj Hariharan & Eran A. Mukamel & Danny Leung & Nisha Rajagopal & Joseph R. Nery & Mark A. Urich & Huaming Chen & Shin Lin & Yiing Lin & Inkyung J, 2015. "Human body epigenome maps reveal noncanonical DNA methylation variation," Nature, Nature, vol. 523(7559), pages 212-216, July.
    8. En Li & Han Liu & Liangliang Huang & Xiangbo Zhang & Xiaomei Dong & Weibin Song & Haiming Zhao & Jinsheng Lai, 2019. "Long-range interactions between proximal and distal regulatory regions in maize," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    9. Jerome Kelleher & Alison M Etheridge & Gilean McVean, 2016. "Efficient Coalescent Simulation and Genealogical Analysis for Large Sample Sizes," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-22, May.
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