IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43024-5.html
   My bibliography  Save this article

The transcriptional legacy of developmental stochasticity

Author

Listed:
  • Sara Ballouz

    (Cold Spring Harbor Laboratory
    University of New South Wales Sydney)

  • Risa Karakida Kawaguchi

    (Cold Spring Harbor Laboratory
    Kyoto University)

  • Maria T. Pena

    (National Hansen’s Disease Program)

  • Stephan Fischer

    (Cold Spring Harbor Laboratory
    Université Paris Cité, Bioinformatics and Biostatistics Hub)

  • Megan Crow

    (Cold Spring Harbor Laboratory
    Genentech, Inc.)

  • Leon French

    (University of Toronto)

  • Frank M. Knight

    (University of the Ozarks)

  • Linda B. Adams

    (National Hansen’s Disease Program)

  • Jesse Gillis

    (Cold Spring Harbor Laboratory
    University of Toronto)

Abstract

Genetic and environmental variation are key contributors during organism development, but the influence of minor perturbations or noise is difficult to assess. This study focuses on the stochastic variation in allele-specific expression that persists through cell divisions in the nine-banded armadillo (Dasypus novemcinctus). We investigated the blood transcriptome of five wild monozygotic quadruplets over time to explore the influence of developmental stochasticity on gene expression. We identify an enduring signal of autosomal allelic variability that distinguishes individuals within a quadruplet despite their genetic similarity. This stochastic allelic variation, akin to X-inactivation but broader, provides insight into non-genetic influences on phenotype. The presence of stochastically canalized allelic signatures represents a novel axis for characterizing organismal variability, complementing traditional approaches based on genetic and environmental factors. We also developed a model to explain the inconsistent penetrance associated with these stochastically canalized allelic expressions. By elucidating mechanisms underlying the persistence of allele-specific expression, we enhance understanding of development’s role in shaping organismal diversity.

Suggested Citation

  • Sara Ballouz & Risa Karakida Kawaguchi & Maria T. Pena & Stephan Fischer & Megan Crow & Leon French & Frank M. Knight & Linda B. Adams & Jesse Gillis, 2023. "The transcriptional legacy of developmental stochasticity," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43024-5
    DOI: 10.1038/s41467-023-43024-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43024-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43024-5?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. Weike Pei & Thorsten B. Feyerabend & Jens Rössler & Xi Wang & Daniel Postrach & Katrin Busch & Immanuel Rode & Kay Klapproth & Nikolaus Dietlein & Claudia Quedenau & Wei Chen & Sascha Sauer & Stephan , 2017. "Polylox barcoding reveals haematopoietic stem cell fates realized in vivo," Nature, Nature, vol. 548(7668), pages 456-460, August.
    2. Lucie A. Bergeron & Søren Besenbacher & Jiao Zheng & Panyi Li & Mads Frost Bertelsen & Benoit Quintard & Joseph I. Hoffman & Zhipeng Li & Judy St. Leger & Changwei Shao & Josefin Stiller & M. Thomas P, 2023. "Evolution of the germline mutation rate across vertebrates," Nature, Nature, vol. 615(7951), pages 285-291, March.
    3. Alex T. Kalinka & Karolina M. Varga & Dave T. Gerrard & Stephan Preibisch & David L. Corcoran & Julia Jarrells & Uwe Ohler & Casey M. Bergman & Pavel Tomancak, 2010. "Gene expression divergence recapitulates the developmental hourglass model," Nature, Nature, vol. 468(7325), pages 811-814, December.
    4. Ivan Iossifov & Brian J. O’Roak & Stephan J. Sanders & Michael Ronemus & Niklas Krumm & Dan Levy & Holly A. Stessman & Kali T. Witherspoon & Laura Vives & Karynne E. Patterson & Joshua D. Smith & Brya, 2014. "The contribution of de novo coding mutations to autism spectrum disorder," Nature, Nature, vol. 515(7526), pages 216-221, November.
    5. Dan Frumkin & Adam Wasserstrom & Shai Kaplan & Uriel Feige & Ehud Shapiro, 2005. "Genomic Variability within an Organism Exposes Its Cell Lineage Tree," PLOS Computational Biology, Public Library of Science, vol. 1(5), pages 1-13, October.
    6. Federico Gaiti & Ronan Chaligne & Hongcang Gu & Ryan M. Brand & Steven Kothen-Hill & Rafael C. Schulman & Kirill Grigorev & Davide Risso & Kyu-Tae Kim & Alessandro Pastore & Kevin Y. Huang & Alicia Al, 2019. "Epigenetic evolution and lineage histories of chronic lymphocytic leukaemia," Nature, Nature, vol. 569(7757), pages 576-580, 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. Damien G Hicks & Terence P Speed & Mohammed Yassin & Sarah M Russell, 2019. "Maps of variability in cell lineage trees," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-32, February.
    2. Marine Lanfranchi & Sozerko Yandiev & Géraldine Meyer-Dilhet & Salma Ellouze & Martijn Kerkhofs & Raphael Dos Reis & Audrey Garcia & Camille Blondet & Alizée Amar & Anita Kneppers & Hélène Polvèche & , 2024. "The AMPK-related kinase NUAK1 controls cortical axons branching by locally modulating mitochondrial metabolic functions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Ada J. S. Chan & Worrawat Engchuan & Miriam S. Reuter & Zhuozhi Wang & Bhooma Thiruvahindrapuram & Brett Trost & Thomas Nalpathamkalam & Carol Negrijn & Sylvia Lamoureux & Giovanna Pellecchia & Rohan , 2022. "Genome-wide rare variant score associates with morphological subtypes of autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Hyosang Kim & Doyoun Kim & Yisul Cho & Kyungdeok Kim & Junyeop Daniel Roh & Yangsik Kim & Esther Yang & Seong Soon Kim & Sunjoo Ahn & Hyun Kim & Hyojin Kang & Yongchul Bae & Eunjoon Kim, 2022. "Early postnatal serotonin modulation prevents adult-stage deficits in Arid1b-deficient mice through synaptic transcriptional reprogramming," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. Luye Qin & Jamal B. Williams & Tao Tan & Tiaotiao Liu & Qing Cao & Kaijie Ma & Zhen Yan, 2021. "Deficiency of autism risk factor ASH1L in prefrontal cortex induces epigenetic aberrations and seizures," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Ken-ichi Dewa & Nariko Arimura & Wataru Kakegawa & Masayuki Itoh & Toma Adachi & Satoshi Miyashita & Yukiko U. Inoue & Kento Hizawa & Kei Hori & Natsumi Honjoya & Haruya Yagishita & Shinichiro Taya & , 2024. "Neuronal DSCAM regulates the peri-synaptic localization of GLAST in Bergmann glia for functional synapse formation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Mathilde Paris & Tommy Kaplan & Xiao Yong Li & Jacqueline E Villalta & Susan E Lott & Michael B Eisen, 2013. "Extensive Divergence of Transcription Factor Binding in Drosophila Embryos with Highly Conserved Gene Expression," PLOS Genetics, Public Library of Science, vol. 9(9), pages 1-18, September.
    8. Noa Chapal-Ilani & Yosef E Maruvka & Adam Spiro & Yitzhak Reizel & Rivka Adar & Liran I Shlush & Ehud Shapiro, 2013. "Comparing Algorithms That Reconstruct Cell Lineage Trees Utilizing Information on Microsatellite Mutations," PLOS Computational Biology, Public Library of Science, vol. 9(11), pages 1-17, November.
    9. Chang Hoon Cho & Ilana Vasilisa Deyneko & Dylann Cordova-Martinez & Juan Vazquez & Anne S. Maguire & Jenny R. Diaz & Abigail U. Carbonell & Jaafar O. Tindi & Min-Hui Cui & Roman Fleysher & Sophie Molh, 2023. "ANKS1B encoded AIDA-1 regulates social behaviors by controlling oligodendrocyte function," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    10. Juraj Bergman & Rasmus Ø. Pedersen & Erick J. Lundgren & Rhys T. Lemoine & Sophie Monsarrat & Elena A. Pearce & Mikkel H. Schierup & Jens-Christian Svenning, 2023. "Worldwide Late Pleistocene and Early Holocene population declines in extant megafauna are associated with Homo sapiens expansion rather than climate change," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    11. Mina N. F. Morcos & Congxin Li & Clara M. Munz & Alessandro Greco & Nicole Dressel & Susanne Reinhardt & Katrin Sameith & Andreas Dahl & Nils B. Becker & Axel Roers & Thomas Höfer & Alexander Gerbaule, 2022. "Fate mapping of hematopoietic stem cells reveals two pathways of native thrombopoiesis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    12. Ashley T. Sendell-Price & Frank J. Tulenko & Mats Pettersson & Du Kang & Margo Montandon & Sylke Winkler & Kathleen Kulb & Gavin P. Naylor & Adam Phillippy & Olivier Fedrigo & Jacquelyn Mountcastle & , 2023. "Low mutation rate in epaulette sharks is consistent with a slow rate of evolution in sharks," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Kellan P. Weston & Xiaoyi Gao & Jinghan Zhao & Kwang-Soo Kim & Susan E. Maloney & Jill Gotoff & Sumit Parikh & Yen-Chen Leu & Kuen-Phon Wu & Marwan Shinawi & Joshua P. Steimel & Joseph S. Harrison & J, 2021. "Identification of disease-linked hyperactivating mutations in UBE3A through large-scale functional variant analysis," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    14. C. Biben & T. S. Weber & K. S. Potts & J. Choi & D. C. Miles & A. Carmagnac & T. Sargeant & C. A. Graaf & K. A. Fennell & A. Farley & O. J. Stonehouse & M. A. Dawson & D. J. Hilton & S. H. Naik & S. T, 2023. "In vivo clonal tracking reveals evidence of haemangioblast and haematomesoblast contribution to yolk sac haematopoiesis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Sheng Wang & Belinda Wang & Vanessa Drury & Sam Drake & Nawei Sun & Hasan Alkhairo & Juan Arbelaez & Clif Duhn & Vanessa H. Bal & Kate Langley & Joanna Martin & Pieter J. Hoekstra & Andrea Dietrich & , 2023. "Rare X-linked variants carry predominantly male risk in autism, Tourette syndrome, and ADHD," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Avrin Ghanaeian & Sumita Majhi & Caitlyn L. McCafferty & Babak Nami & Corbin S. Black & Shun Kai Yang & Thibault Legal & Ophelia Papoulas & Martyna Janowska & Melissa Valente-Paterno & Edward M. Marco, 2023. "Integrated modeling of the Nexin-dynein regulatory complex reveals its regulatory mechanism," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Yiqin Wang & Xiaoxian Guo & Xiumei Hong & Guoying Wang & Colleen Pearson & Barry Zuckerman & Andrew G. Clark & Kimberly O. O’Brien & Xiaobin Wang & Zhenglong Gu, 2022. "Association of mitochondrial DNA content, heteroplasmies and inter-generational transmission with autism," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    18. Dang Ton Nguyen & Hai Ha Nguyen & Thuy Duong Nguyen & Thi Thanh Hoa Nguyen & Kaoru Nakano & Kazuhiro Maejima & Aya Sasaki-Oku & Van Ba Nguyen & Duy Bac Nguyen & Bach Quang Le & Jing Hao Wong & Tatsuhi, 2018. "Whole Genome Sequencing of a Vietnamese Family from a Dioxin Contamination Hotspot Reveals Novel Variants in the Son with Undiagnosed Intellectual Disability," IJERPH, MDPI, vol. 15(12), pages 1-11, November.
    19. Saeede Salehi & Abdolhossein Zare & Gianluca Prezza & Jakob Bader & Cornelius Schneider & Utz Fischer & Felix Meissner & Matthias Mann & Michael Briese & Michael Sendtner, 2023. "Cytosolic Ptbp2 modulates axon growth in motoneurons through axonal localization and translation of Hnrnpr," Nature Communications, Nature, vol. 14(1), pages 1-19, 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:14:y:2023:i:1:d:10.1038_s41467-023-43024-5. 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.