Environmental morphing enables informed dispersal of the dandelion diaspore

  1. Madeleine Seale
  2. Oleksandr Zhdanov
  3. Merel Barbara Soons
  4. Cathal Cummins
  5. Erika Kroll
  6. Michael R Blatt
  7. Hossein Zare-Behtash
  8. Angela Busse
  9. Enrico Mastropaolo
  10. James M Bullock
  11. Ignazio Maria Viola
  12. Naomi Nakayama  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. University of Glasgow, United Kingdom
  3. Utrecht University, Netherlands
  4. Heriot-Watt University, United Kingdom
  5. University of Edinburgh, United Kingdom
  6. UK Centre for Ecology & Hydrology, United Kingdom
  7. Imperial College London, United Kingdom

Abstract

Animal migration is highly sensitised to environmental cues, but plant dispersal is considered largely passive. The common dandelion, Taraxacum officinale, bears an intricate haired pappus facilitating flight. The pappus enables the formation of a separated vortex ring during flight; however, the pappus structure is not static but reversibly changes shape by closing in response to moisture. We hypothesised that this leads to changed dispersal properties in response to environmental conditions. Using wind tunnel experiments for flow visualisation, particle image velocimetry, and flight tests we characterised the fluid mechanics effects of the pappus morphing. We also modelled dispersal to understand the impact of pappus morphing on diaspore distribution. Pappus morphing dramatically alters the fluid mechanics of diaspore flight. We found that when the pappus closes in moist conditions, the drag coefficient decreases and thus the falling velocity is greatly increased. Detachment of diaspores from the parent plant also substantially decreases. The change in detachment when the pappus closes increases dispersal distances by reducing diaspore release when wind speeds are low. We propose that moisture-dependent pappus-morphing is a form of informed dispersal allowing rapid responses to changing conditions.

Data availability

The Source data for all figures has been deposited to Zenodo, doi: 10.5281/zenodo.7038366

The following data sets were generated

Article and author information

Author details

  1. Madeleine Seale

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Oleksandr Zhdanov

    James Watt School of Engineering, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1742-9765
  3. Merel Barbara Soons

    Ecology and Biodiversity group, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Cathal Cummins

    School of Energy, Geosciences, Infrastructure and Environment, Heriot-Watt University, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Erika Kroll

    School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8832-7208
  6. Michael R Blatt

    Laboratory of Plant Physiology and Biophysics, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Hossein Zare-Behtash

    James Watt School of Engineering, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Angela Busse

    James Watt School of Engineering, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Enrico Mastropaolo

    School of Engineering, Institute for Integrated Micro and Nano Systems, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. James M Bullock

    UK Centre for Ecology & Hydrology, Wallingford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Ignazio Maria Viola

    School of Engineering, Institute for Energy Systems, University of Edinburgh, Edinburgh, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3831-8423
  12. Naomi Nakayama

    Department of Bioengineering, Imperial College London, London, United Kingdom
    For correspondence
    n.nakayama@imperial.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9390-3545

Funding

Leverhulme Trust (RPG-2016-255)

  • Enrico Mastropaolo
  • Ignazio Maria Viola
  • Naomi Nakayama

Leverhulme Trust (ECF-2019-424)

  • Madeleine Seale

Biotechnology and Biological Sciences Research Council (P011586/1 and T006153/1)

  • Michael R Blatt

European Commission (ERC-2020-COG 101001499)

  • Ignazio Maria Viola

Royal Society (UF140640 and URF-R-201035)

  • Naomi Nakayama

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

Copyright

© 2022, Seale 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

  • 1,973
    views
  • 235
    downloads
  • 6
    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. Madeleine Seale
  2. Oleksandr Zhdanov
  3. Merel Barbara Soons
  4. Cathal Cummins
  5. Erika Kroll
  6. Michael R Blatt
  7. Hossein Zare-Behtash
  8. Angela Busse
  9. Enrico Mastropaolo
  10. James M Bullock
  11. Ignazio Maria Viola
  12. Naomi Nakayama
(2022)
Environmental morphing enables informed dispersal of the dandelion diaspore
eLife 11:e81962.
https://doi.org/10.7554/eLife.81962

Share this article

https://doi.org/10.7554/eLife.81962

Further reading

    1. Biochemistry and Chemical Biology
    2. Physics of Living Systems
    Debabrata Dey, Shir Marciano ... Gideon Schreiber
    Research Article

    For drugs to be active they have to reach their targets. Within cells this requires crossing the cell membrane, and then free diffusion, distribution, and availability. Here, we explored the in-cell diffusion rates and distribution of a series of small molecular fluorescent drugs, in comparison to proteins, by microscopy and fluorescence recovery after photobleaching (FRAP). While all proteins diffused freely, we found a strong correlation between pKa and the intracellular diffusion and distribution of small molecule drugs. Weakly basic, small-molecule drugs displayed lower fractional recovery after photobleaching and 10- to-20-fold slower diffusion rates in cells than in aqueous solutions. As, more than half of pharmaceutical drugs are weakly basic, they, are protonated in the cell cytoplasm. Protonation, facilitates the formation of membrane impermeable ionic form of the weak base small molecules. This results in ion trapping, further reducing diffusion rates of weakly basic small molecule drugs under macromolecular crowding conditions where other nonspecific interactions become more relevant and dominant. Our imaging studies showed that acidic organelles, particularly the lysosome, captured these molecules. Surprisingly, blocking lysosomal import only slightly increased diffusion rates and fractional recovery. Conversely, blocking protonation by N-acetylated analogues, greatly enhanced their diffusion and fractional recovery after FRAP. Based on these results, N-acetylation of small molecule drugs may improve the intracellular availability and distribution of weakly basic, small molecule drugs within cells.

    1. Computational and Systems Biology
    2. Physics of Living Systems
    Divyoj Singh, Sriram Ramaswamy ... Mohd Suhail Rizvi
    Research Article Updated

    Planar cell polarity (PCP) – tissue-scale alignment of the direction of asymmetric localization of proteins at the cell-cell interface – is essential for embryonic development and physiological functions. Abnormalities in PCP can result in developmental imperfections, including neural tube closure defects and misaligned hair follicles. Decoding the mechanisms responsible for PCP establishment and maintenance remains a fundamental open question. While the roles of various molecules – broadly classified into ‘global’ and ‘local’ modules – have been well-studied, their necessity and sufficiency in explaining PCP and connecting their perturbations to experimentally observed patterns have not been examined. Here, we develop a minimal model that captures the proposed features of PCP establishment – a global tissue-level gradient and local asymmetric distribution of protein complexes. The proposed model suggests that while polarity can emerge without a gradient, the gradient not only acts as a global cue but also increases the robustness of PCP against stochastic perturbations. We also recapitulated and quantified the experimentally observed features of swirling patterns and domineering non-autonomy, using only three free model parameters - rate of protein binding to membrane, the concentration of PCP proteins, and the gradient steepness. We explain how self-stabilizing asymmetric protein localizations in the presence of tissue-level gradient can lead to robust PCP patterns and reveal minimal design principles for a polarized system.