IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-50169-4.html
   My bibliography  Save this article

Rapid meiotic prophase chromosome movements in Arabidopsis thaliana are linked to essential reorganization at the nuclear envelope

Author

Listed:
  • Laurence Cromer

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Mariana Tiscareno-Andrade

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Sandrine Lefranc

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Aurélie Chambon

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Aurélie Hurel

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Manon Brogniez

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Julie Guérin

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Ivan Masson

    (UMR Agronomie)

  • Gabriele Adam

    (Institute of Plant Sciences Paris-Saclay (IPS2)
    Institute of Plant Sciences Paris-Saclay (IPS2)
    Institute of Plant Sciences Paris-Saclay (IPS2))

  • Delphine Charif

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Philippe Andrey

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

  • Mathilde Grelon

    (Institute Jean-Pierre Bourgin for Plant Sciences (IJPB))

Abstract

Meiotic rapid prophase chromosome movements (RPMs) require connections between the chromosomes and the cytoskeleton, involving SUN (Sad1/UNC-84)-domain-containing proteins at the inner nuclear envelope (NE). RPMs remain significantly understudied in plants, with respect to their importance in the regulation of meiosis. Here, we demonstrate that Arabidopsis thaliana meiotic centromeres undergo rapid (up to 500 nm/s) and uncoordinated movements during the zygotene and pachytene stages. These centromere movements are not affected by altered chromosome organization and recombination but are abolished in the double mutant sun1 sun2. We also document the changes in chromosome dynamics and nucleus organization during the transition from leptotene to zygotene, including telomere attachment to SUN-enriched NE domains, bouquet formation, and nucleolus displacement, all of which were defective in sun1 sun2. These results establish A. thaliana as a model species for studying the functional implications of meiotic RPMs and demonstrate the mechanistic conservation of telomere-led RPMs in plants.

Suggested Citation

  • Laurence Cromer & Mariana Tiscareno-Andrade & Sandrine Lefranc & Aurélie Chambon & Aurélie Hurel & Manon Brogniez & Julie Guérin & Ivan Masson & Gabriele Adam & Delphine Charif & Philippe Andrey & Mat, 2024. "Rapid meiotic prophase chromosome movements in Arabidopsis thaliana are linked to essential reorganization at the nuclear envelope," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50169-4
    DOI: 10.1038/s41467-024-50169-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-50169-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-50169-4?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. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    2. Yuki Sakamoto & Mayuko Sato & Yoshikatsu Sato & Akihito Harada & Takamasa Suzuki & Chieko Goto & Kentaro Tamura & Kiminori Toyooka & Hiroshi Kimura & Yasuyuki Ohkawa & Ikuko Hara-Nishimura & Shingo Ta, 2020. "Subnuclear gene positioning through lamina association affects copper tolerance," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    3. Yan Wang & Yanyan Chen & Juan Chen & Lijun Wang & Leitong Nie & Juanjuan Long & Haishuang Chang & Jian Wu & Chenhui Huang & Ming Lei, 2019. "The meiotic TERB1-TERB2-MAJIN complex tethers telomeres to the nuclear envelope," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
    4. Maruthachalam Ravi & Simon W. L. Chan, 2010. "Haploid plants produced by centromere-mediated genome elimination," Nature, Nature, vol. 464(7288), pages 615-618, March.
    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. JANSSENS, Jochen & DE CORTE, Annelies & SÖRENSEN, Kenneth, 2016. "Water distribution network design optimisation with respect to reliability," Working Papers 2016007, University of Antwerp, Faculty of Business and Economics.
    2. Raymond Hernandez & Elizabeth A. Pyatak & Cheryl L. P. Vigen & Haomiao Jin & Stefan Schneider & Donna Spruijt-Metz & Shawn C. Roll, 2021. "Understanding Worker Well-Being Relative to High-Workload and Recovery Activities across a Whole Day: Pilot Testing an Ecological Momentary Assessment Technique," IJERPH, MDPI, vol. 18(19), pages 1-17, October.
    3. Christopher Hassall & Michael Nisbet & Evan Norcliffe & He Wang, 2024. "The Potential Health Benefits of Urban Tree Planting Suggested through Immersive Environments," Land, MDPI, vol. 13(3), pages 1-12, February.
    4. Jie Zhao & Ji Chen & Damien Beillouin & Hans Lambers & Yadong Yang & Pete Smith & Zhaohai Zeng & Jørgen E. Olesen & Huadong Zang, 2022. "Global systematic review with meta-analysis reveals yield advantage of legume-based rotations and its drivers," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    5. Elisabeth Beckmann & Lukas Olbrich & Joseph Sakshaug, 2024. "Multivariate assessment of interviewer-related errors in a cross-national economic survey (Lukas Olbrich, Elisabeth Beckmann, Joseph W. Sakshaug)," Working Papers 253, Oesterreichische Nationalbank (Austrian Central Bank).
    6. F J Heather & D Z Childs & A M Darnaude & J L Blanchard, 2018. "Using an integral projection model to assess the effect of temperature on the growth of gilthead seabream Sparus aurata," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-19, May.
    7. Valentina Krenz & Arjen Alink & Tobias Sommer & Benno Roozendaal & Lars Schwabe, 2023. "Time-dependent memory transformation in hippocampus and neocortex is semantic in nature," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Morán-Ordóñez, Alejandra & Ameztegui, Aitor & De Cáceres, Miquel & de-Miguel, Sergio & Lefèvre, François & Brotons, Lluís & Coll, Lluís, 2020. "Future trade-offs and synergies among ecosystem services in Mediterranean forests under global change scenarios," Ecosystem Services, Elsevier, vol. 45(C).
    9. Jack McDonnell & Thomas McKenna & Kathryn A. Yurkonis & Deirdre Hennessy & Rafael Andrade Moral & Caroline Brophy, 2023. "A Mixed Model for Assessing the Effect of Numerous Plant Species Interactions on Grassland Biodiversity and Ecosystem Function Relationships," Journal of Agricultural, Biological and Environmental Statistics, Springer;The International Biometric Society;American Statistical Association, vol. 28(1), pages 1-19, March.
    10. Ana Pinto & Tong Yin & Marion Reichenbach & Raghavendra Bhatta & Pradeep Kumar Malik & Eva Schlecht & Sven König, 2020. "Enteric Methane Emissions of Dairy Cattle Considering Breed Composition, Pasture Management, Housing Conditions and Feeding Characteristics along a Rural-Urban Gradient in a Rising Megacity," Agriculture, MDPI, vol. 10(12), pages 1-18, December.
    11. Damian M. Herz & Manuel Bange & Gabriel Gonzalez-Escamilla & Miriam Auer & Keyoumars Ashkan & Petra Fischer & Huiling Tan & Rafal Bogacz & Muthuraman Muthuraman & Sergiu Groppa & Peter Brown, 2022. "Dynamic control of decision and movement speed in the human basal ganglia," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Kathrin Stenchly & Marc Victor Hansen & Katharina Stein & Andreas Buerkert & Wilhelm Loewenstein, 2018. "Income Vulnerability of West African Farming Households to Losses in Pollination Services: A Case Study from Ouagadougou, Burkina Faso," Sustainability, MDPI, vol. 10(11), pages 1-12, November.
    13. Dongyan Liu & Chongran Zhou & John K. Keesing & Oscar Serrano & Axel Werner & Yin Fang & Yingjun Chen & Pere Masque & Janine Kinloch & Aleksey Sadekov & Yan Du, 2022. "Wildfires enhance phytoplankton production in tropical oceans," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    14. Zhaogeng Yang & Yanhui Li & Peijin Hu & Jun Ma & Yi Song, 2020. "Prevalence of Anemia and its Associated Factors among Chinese 9-, 12-, and 14-Year-Old Children: Results from 2014 Chinese National Survey on Students Constitution and Health," IJERPH, MDPI, vol. 17(5), pages 1-10, February.
    15. Marco Lopez-Cruz & Fernando M. Aguate & Jacob D. Washburn & Natalia Leon & Shawn M. Kaeppler & Dayane Cristina Lima & Ruijuan Tan & Addie Thompson & Laurence Willard Bretonne & Gustavo los Campos, 2023. "Leveraging data from the Genomes-to-Fields Initiative to investigate genotype-by-environment interactions in maize in North America," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Baumann, Elias & Kern, Jana & Lessmann, Stefan, 2019. "Usage Continuance in Software-as-a-Service," IRTG 1792 Discussion Papers 2019-005, Humboldt University of Berlin, International Research Training Group 1792 "High Dimensional Nonstationary Time Series".
    17. Alexandra M. Cheney & Stephanann M. Costello & Nicholas V. Pinkham & Annie Waldum & Susan C. Broadaway & Maria Cotrina-Vidal & Marc Mergy & Brian Tripet & Douglas J. Kominsky & Heather M. Grifka-Walk , 2023. "Gut microbiome dysbiosis drives metabolic dysfunction in Familial dysautonomia," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    18. repec:cup:judgdm:v:16:y:2021:i:1:p:201-237 is not listed on IDEAS
    19. C. Gabriel Hidalgo Pizango & Eurídice N. Honorio Coronado & Jhon del Águila-Pasquel & Gerardo Flores Llampazo & Johan de Jong & César J. Córdova Oroche & José M. Reyna Huaymacari & Steve J. Carver & D, 2022. "Sustainable palm fruit harvesting as a pathway to conserve Amazon peatland forests," Nature Sustainability, Nature, vol. 5(6), pages 479-487, June.
    20. Myrto Pantazi & Olivier Klein & Mikhail Kissine, 2020. "Is justice blind or myopic? An examination of the effects of meta-cognitive myopia and truth bias on mock jurors and judges," Judgment and Decision Making, Society for Judgment and Decision Making, vol. 15(2), pages 214-229, March.
    21. 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.

    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_s41467-024-50169-4. 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.