IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45771-5.html
   My bibliography  Save this article

Epiallelic variation of non-coding RNA genes and their phenotypic consequences

Author

Listed:
  • Jie Liu

    (Washington University in St. Louis)

  • Xuehua Zhong

    (Washington University in St. Louis)

Abstract

Epigenetic variations contribute greatly to the phenotypic plasticity and diversity. Current functional studies on epialleles have predominantly focused on protein-coding genes, leaving the epialleles of non-coding RNA (ncRNA) genes largely understudied. Here, we uncover abundant DNA methylation variations of ncRNA genes and their significant correlations with plant adaptation among 1001 natural Arabidopsis accessions. Through genome-wide association study (GWAS), we identify large numbers of methylation QTL (methylQTL) that are independent of known DNA methyltransferases and enriched in specific chromatin states. Proximal methylQTL closely located to ncRNA genes have a larger effect on DNA methylation than distal methylQTL. We ectopically tether a DNA methyltransferase MQ1v to miR157a by CRISPR-dCas9 and show de novo establishment of DNA methylation accompanied with decreased miR157a abundance and early flowering. These findings provide important insights into the genetic basis of epigenetic variations and highlight the contribution of epigenetic variations of ncRNA genes to plant phenotypes and diversity.

Suggested Citation

  • Jie Liu & Xuehua Zhong, 2024. "Epiallelic variation of non-coding RNA genes and their phenotypic consequences," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45771-5
    DOI: 10.1038/s41467-024-45771-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45771-5
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45771-5?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yong Lei & Xiaotian Zhang & Jianzhong Su & Mira Jeong & Michael C. Gundry & Yung-Hsin Huang & Yubin Zhou & Wei Li & Margaret A. Goodell, 2017. "Targeted DNA methylation in vivo using an engineered dCas9-MQ1 fusion protein," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    2. Musaddeque Ahmed & Fraser Soares & Ji-Han Xia & Yue Yang & Jing Li & Haiyang Guo & Peiran Su & Yijun Tian & Hyung Joo Lee & Miranda Wang & Nayeema Akhtar & Kathleen E. Houlahan & Almudena Bosch & Stan, 2021. "CRISPRi screens reveal a DNA methylation-mediated 3D genome dependent causal mechanism in prostate cancer," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    3. Pilar Cubas & Coral Vincent & Enrico Coen, 1999. "An epigenetic mutation responsible for natural variation in floral symmetry," Nature, Nature, vol. 401(6749), pages 157-161, September.
    4. Meilina Ong-Abdullah & Jared M. Ordway & Nan Jiang & Siew-Eng Ooi & Sau-Yee Kok & Norashikin Sarpan & Nuraziyan Azimi & Ahmad Tarmizi Hashim & Zamzuri Ishak & Samsul Kamal Rosli & Fadila Ahmad Malike , 2015. "Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm," Nature, Nature, vol. 525(7570), pages 533-537, September.
    5. Jian Fang & Jianjun Jiang & Sarah M. Leichter & Jie Liu & Mahamaya Biswal & Nelli Khudaverdyan & Xuehua Zhong & Jikui Song, 2022. "Mechanistic basis for maintenance of CHG DNA methylation in plants," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    6. Ian R. Henderson & Steven E. Jacobsen, 2007. "Epigenetic inheritance in plants," Nature, Nature, vol. 447(7143), pages 418-424, May.
    7. Szymon Swiezewski & Fuquan Liu & Andreas Magusin & Caroline Dean, 2009. "Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target," Nature, Nature, vol. 462(7274), pages 799-802, December.
    8. Cuijun Zhang & Xuan Du & Kai Tang & Zhenlin Yang & Li Pan & Peipei Zhu & Jinyan Luo & Yuwei Jiang & Hui Zhang & Huafang Wan & Xingang Wang & Fengkai Wu & W. Andy Tao & Xin-Jian He & Heng Zhang & Ray A, 2018. "Arabidopsis AGDP1 links H3K9me2 to DNA methylation in heterochromatin," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    9. Robert J. Schmitz & Matthew D. Schultz & Mark A. Urich & Joseph R. Nery & Mattia Pelizzola & Ondrej Libiger & Andrew Alix & Richard B. McCosh & Huaming Chen & Nicholas J. Schork & Joseph R. Ecker, 2013. "Patterns of population epigenomic diversity," Nature, Nature, vol. 495(7440), pages 193-198, March.
    10. Diana Buitrago & Mireia Labrador & Juan Pablo Arcon & Rafael Lema & Oscar Flores & Anna Esteve-Codina & Julie Blanc & Nuria Villegas & David Bellido & Marta Gut & Pablo D. Dans & Simon C. Heath & Ivo , 2021. "Impact of DNA methylation on 3D genome structure," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    11. Andrew P. Feinberg, 2007. "Phenotypic plasticity and the epigenetics of human disease," Nature, Nature, vol. 447(7143), pages 433-440, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Zengyu Shao & Jiuwei Lu & Nelli Khudaverdyan & Jikui Song, 2024. "Multi-layered heterochromatin interaction as a switch for DIM2-mediated DNA methylation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Yinwen Zhang & Hosung Jang & Rui Xiao & Ioanna Kakoulidou & Robert S. Piecyk & Frank Johannes & Robert J. Schmitz, 2021. "Heterochromatin is a quantitative trait associated with spontaneous epiallele formation," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Akihisa Osakabe & Yoshimasa Takizawa & Naoki Horikoshi & Suguru Hatazawa & Lumi Negishi & Shoko Sato & Frédéric Berger & Tetsuji Kakutani & Hitoshi Kurumizaka, 2024. "Molecular and structural basis of the chromatin remodeling activity by Arabidopsis DDM1," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Toyokawa, Satoshi & Uddin, Monica & Koenen, Karestan C. & Galea, Sandro, 2012. "How does the social environment ‘get into the mind’? Epigenetics at the intersection of social and psychiatric epidemiology," Social Science & Medicine, Elsevier, vol. 74(1), pages 67-74.
    5. Najihah Ahmad Latif & Fatini Nadhirah Mohd Nain & Nurul Hashimah Ahamed Hassain Malim & Rosni Abdullah & Muhammad Farid Abdul Rahim & Mohd Nasruddin Mohamad & Nurul Syafika Mohamad Fauzi, 2021. "Predicting Heritability of Oil Palm Breeding Using Phenotypic Traits and Machine Learning," Sustainability, MDPI, vol. 13(22), pages 1-24, November.
    6. Michelle Kelly-Irving & Laurence Mabile & Pascale Grosclaude & Thierry Lang & Cyrille Delpierre, 2013. "The embodiment of adverse childhood experiences and cancer development: potential biological mechanisms and pathways across the life course," International Journal of Public Health, Springer;Swiss School of Public Health (SSPH+), vol. 58(1), pages 3-11, February.
    7. Carja, Oana & Liberman, Uri & Feldman, Marcus W., 2013. "Evolution with stochastic fitnesses: A role for recombination," Theoretical Population Biology, Elsevier, vol. 86(C), pages 29-42.
    8. Sun Shuying & Yu Xiaoqing, 2016. "HMM-Fisher: identifying differential methylation using a hidden Markov model and Fisher’s exact test," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 15(1), pages 55-67, March.
    9. Qing Xie & Qi Liu & Fengbiao Mao & Wanshi Cai & Honghu Wu & Mingcong You & Zhen Wang & Bingyu Chen & Zhong Sheng Sun & Jinyu Wu, 2014. "A Bayesian Framework to Identify Methylcytosines from High-Throughput Bisulfite Sequencing Data," PLOS Computational Biology, Public Library of Science, vol. 10(9), pages 1-8, September.
    10. Zsolt Karányi & Ágnes Mosolygó-L & Orsolya Feró & Adrienn Horváth & Beáta Boros-Oláh & Éva Nagy & Szabolcs Hetey & Imre Holb & Henrik Mihály Szaker & Márton Miskei & Tibor Csorba & Lóránt Székvölgyi, 2022. "NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    11. Tamer Aldwairi & David J. Chevalier & Andy D. Perkins, 2021. "Exploring the Effect of Climate Factors on SNPs within FHA Domain Genes in Eurasian Arabidopsis Ecotypes," Agriculture, MDPI, vol. 11(2), pages 1-10, February.
    12. Peter Sarkies & Jennifer Westoby & Rebecca Mary Kilner & Rahia Mashoodh, 2024. "Gene body methylation evolves during the sustained loss of parental care in the burying beetle," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    13. Yi-Wen Lim & Ben N. Mansfeld & Pascal Schläpfer & Kerrigan B. Gilbert & Narayanan N. Narayanan & Weihong Qi & Qi Wang & Zhenhui Zhong & Adam Boyher & Jackson Gehan & Getu Beyene & Zuh-Jyh Daniel Lin &, 2022. "Mutations in DNA polymerase δ subunit 1 co-segregate with CMD2-type resistance to Cassava Mosaic Geminiviruses," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Xiaohe Lin & Junjie Yin & Yifan Wang & Jing Yao & Qingshun Q. Li & Vit Latzel & Oliver Bossdorf & Yuan-Ye Zhang, 2024. "Environment-induced heritable variations are common in Arabidopsis thaliana," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    15. William Senapedis & Kayleigh M. Gallagher & Elmer Figueroa & Jeremiah D. Farelli & Robert Lyng & J. Graeme Hodgson & Charles W. O’Donnell & Joseph V. Newman & Madison Pacaro & Stephen K. Siecinski & J, 2024. "Targeted transcriptional downregulation of MYC using epigenomic controllers demonstrates antitumor activity in hepatocellular carcinoma models," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Fengchao Lang & Karambir Kaur & Haiqing Fu & Javeria Zaheer & Diego Luis Ribeiro & Mirit I. Aladjem & Chunzhang Yang, 2025. "D-2-hydroxyglutarate impairs DNA repair through epigenetic reprogramming," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    17. Jian Fang & Jianjun Jiang & Sarah M. Leichter & Jie Liu & Mahamaya Biswal & Nelli Khudaverdyan & Xuehua Zhong & Jikui Song, 2022. "Mechanistic basis for maintenance of CHG DNA methylation in plants," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    18. Theodore Sakellaropoulos & Catherine Do & Guimei Jiang & Giulia Cova & Peter Meyn & Dacia Dimartino & Sitharam Ramaswami & Adriana Heguy & Aristotelis Tsirigos & Jane A. Skok, 2024. "MethNet: a robust approach to identify regulatory hubs and their distal targets from cancer data," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Li He & Huan Huang & Mariem Bradai & Cheng Zhao & Yin You & Jun Ma & Lun Zhao & Rosa Lozano-Durán & Jian-Kang Zhu, 2022. "DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Chih-Hung Hsieh & Ya-Ting Sabrina Chang & Ming-Ren Yen & Jo-Wei Allison Hsieh & Pao-Yang Chen, 2024. "Predicting protein synergistic effect in Arabidopsis using epigenome profiling," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45771-5. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.