Abstract

To follow the dynamics of meiosis in the model plant Arabidopsis, we have established a live cell imaging setup to observe male meiocytes. Our method is based on the concomitant visualization of microtubules (MTs) and a meiotic cohesin subunit that allows following five cellular parameters: cell shape, MT array, nucleus position, nucleolus position, and chromatin condensation. We find that the states of these parameters are not randomly associated and identify 11 cellular states, referred to as landmarks, which occur much more frequently than closely related ones, indicating that they are convergence points during meiotic progression. As a first application of our system, we revisited a previously identified mutant in the meiotic A-type cyclin TARDY ASYNCHRONOUS MEIOSIS (TAM). Our imaging system enabled us to reveal both qualitatively and quantitatively altered landmarks in tam, foremost the formation of previously not recognized ectopic spindle- or phragmoplast-like structures that arise without attachment to chromosomes.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Maria A Prusicki

    Department of Developmental Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3755-3402
  2. Emma M Keizer

    Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen, Netherlands
    Competing interests
    No competing interests declared.
  3. Rik Peter van Rosmalen

    Department of Agrotechnology and Food Sciences; Laboratory of Systems and Synthetic Biology, Wageningen University, Wageningen, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6911-3298
  4. Shinichiro Komaki

    Department of Developmental Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1189-288X
  5. Felix Seifert

    Department of Developmental Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    Felix Seifert, is affiliated with CropSeq bioinformatics. The author has no other competing interests to declare.
  6. Katja Müller

    Department of Developmental Biology, University of Hamburg, Hamburg, Germany
    Competing interests
    No competing interests declared.
  7. Erik Wijnker

    Department of Plant Science, Wageningen University, Wageningen, Netherlands
    Competing interests
    No competing interests declared.
  8. Christian Fleck

    Department of Agrotechnology and Food Sciences, Wageningen University, Wageningen, Netherlands
    Competing interests
    No competing interests declared.
  9. Arp Schnittger

    Department of Developmental Biology, University of Hamburg, Hamburg, Germany
    For correspondence
    arp.schnittger@uni-hamburg.de
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7067-0091

Funding

European Union (ITN-606956)

  • Maria A Prusicki
  • Erik Wijnker
  • Arp Schnittger

University of Hamburg (Core funding)

  • Maria A Prusicki
  • Shinichiro Komaki
  • Felix Seifert
  • Katja Müller
  • Erik Wijnker
  • Arp Schnittger

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Dominique C Bergmann, Stanford University/HHMI, United States

Version history

  1. Received: October 14, 2018
  2. Accepted: May 17, 2019
  3. Accepted Manuscript published: May 20, 2019 (version 1)
  4. Version of Record published: June 11, 2019 (version 2)

Copyright

© 2019, Prusicki et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 8,123
    views
  • 1,074
    downloads
  • 61
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Maria A Prusicki
  2. Emma M Keizer
  3. Rik Peter van Rosmalen
  4. Shinichiro Komaki
  5. Felix Seifert
  6. Katja Müller
  7. Erik Wijnker
  8. Christian Fleck
  9. Arp Schnittger
(2019)
Live cell imaging of meiosis in Arabidopsis thaliana
eLife 8:e42834.
https://doi.org/10.7554/eLife.42834

Share this article

https://doi.org/10.7554/eLife.42834

Further reading

    1. Cell Biology
    2. Computational and Systems Biology
    N Suhas Jagannathan, Javier Yu Peng Koh ... Lisa Tucker-Kellogg
    Research Article

    Bats have unique characteristics compared to other mammals, including increased longevity and higher resistance to cancer and infectious disease. While previous studies have analyzed the metabolic requirements for flight, it is still unclear how bat metabolism supports these unique features, and no study has integrated metabolomics, transcriptomics, and proteomics to characterize bat metabolism. In this work, we performed a multi-omics data analysis using a computational model of metabolic fluxes to identify fundamental differences in central metabolism between primary lung fibroblast cell lines from the black flying fox fruit bat (Pteropus alecto) and human. Bat cells showed higher expression levels of Complex I components of electron transport chain (ETC), but, remarkably, a lower rate of oxygen consumption. Computational modeling interpreted these results as indicating that Complex II activity may be low or reversed, similar to an ischemic state. An ischemic-like state of bats was also supported by decreased levels of central metabolites and increased ratios of succinate to fumarate in bat cells. Ischemic states tend to produce reactive oxygen species (ROS), which would be incompatible with the longevity of bats. However, bat cells had higher antioxidant reservoirs (higher total glutathione and higher ratio of NADPH to NADP) despite higher mitochondrial ROS levels. In addition, bat cells were more resistant to glucose deprivation and had increased resistance to ferroptosis, one of the characteristics of which is oxidative stress. Thus, our studies revealed distinct differences in the ETC regulation and metabolic stress responses between human and bat cells.

    1. Cell Biology
    2. Developmental Biology
    Filip Knop, Apolena Zounarova ... Marie Macůrková
    Research Article

    During Caenorhabditis elegans development, multiple cells migrate long distances or extend processes to reach their final position and/or attain proper shape. The Wnt signalling pathway stands out as one of the major coordinators of cell migration or cell outgrowth along the anterior-posterior body axis. The outcome of Wnt signalling is fine-tuned by various mechanisms including endocytosis. In this study, we show that SEL-5, the C. elegans orthologue of mammalian AP2-associated kinase AAK1, acts together with the retromer complex as a positive regulator of EGL-20/Wnt signalling during the migration of QL neuroblast daughter cells. At the same time, SEL-5 in cooperation with the retromer complex is also required during excretory canal cell outgrowth. Importantly, SEL-5 kinase activity is not required for its role in neuronal migration or excretory cell outgrowth, and neither of these processes is dependent on DPY-23/AP2M1 phosphorylation. We further establish that the Wnt proteins CWN-1 and CWN-2 together with the Frizzled receptor CFZ-2 positively regulate excretory cell outgrowth, while LIN-44/Wnt and LIN-17/Frizzled together generate a stop signal inhibiting its extension.