1. Plant Biology
Download icon

Pollen Tube Guidance: Growing straight through walls

  1. Subramanian Sankaranarayanan  Is a corresponding author
  2. Sharon A Kessler  Is a corresponding author
  1. Department of Botany and Plant Pathology, Purdue University, United States
  2. Purdue Center for Plant Biology, Purdue University, United States
Insight
  • Cited 0
  • Views 466
  • Annotations
Cite this article as: eLife 2020;9:e61647 doi: 10.7554/eLife.61647

Abstract

The pollen tube in a flowering plant grows in a direction that is influenced by the mechanical properties of the stigma papillae and the organization of structures called cortical microtubules inside these cells.

Main text

In a flowering plant, reproduction begins when grains of pollen stick to cells called stigma papillae that are located at the top of the pistil, which is the female part of the flower. A cell called a pollen tube then delivers the sperm cells contained in the pollen grains to the female gametes for fertilization. This is a long journey that involves the pollen tube travelling from the stigma papillae at the top of the pistil to the ovules that contain the female gametes, which are at the bottom of the pistil.

So how does the plant ensure that the pollen tube – which is a single cell that grows longer over time – finds the ovules and does not get lost en route? Several molecules and nutrients secreted by the pistil direct the growth of the pollen tube (Higashiyama and Takeuchi, 2015). However, the identity of the cues that guide the pollen tube in the first stages of its journey have remained a mystery.

Most plant cells grow by increasing their surface area while remaining attached to neighboring cells: pollen tubes are different in that they are tip-growing cells that can grow through the walls of other cells to reach their target. When the pollen tube first enters the pistil, it remains within the cell wall of the stigma papillae (Figure 1; left): could the components of this cell wall, or the mechanical properties of these cells, influence the growth of the pollen tube?

Pollen tube growth in stigma papillae.

When a grain of pollen (shown in mustard) lands on a papilla in the stigma (green) of a flowering plant, a pollen tube (PT; also shown in mustard) begins to grow through the cell wall (CW) of the papilla so that the sperm cells (S; red) in the pollen can be delivered to the female gametes, which are located in ovules deep inside the plant. In stage 12 flowers (left), the organization of the cortical microtubules (CMTs; blue lines) inside the papilla is highly anisotropic and the pollen tube grows in a straight line. In older stage 15 flowers (right), the organization of the microtubules is isotropic and the pollen tube forms a coil around the papilla as it grows. The vegetative cell (V) makes up the body of the pollen tube and encloses the sperm cells.

A number of studies have demonstrated how mechanical properties can influence a variety of cellular processes – including proliferation, differentiation, migration and cell signaling – in animal cells (Discher et al., 2005; Fu et al., 2010; Provenzano and Keely, 2011), and there is evidence that mechanical properties can also shape plant growth and development (Eng and Sampathkumar, 2018; Sampathkumar et al., 2019). For example, it is known that when a pollen tube penetrates the cell wall of a stigma papilla, it causes changes in the mechanical properties of the cell wall by exerting pressure (Zerzour et al., 2009; Sanati Nezhad and Geitmann, 2013).

However, the role of these mechanical properties in regulating the growth of pollen tube has not been explored in detail. Moreover, although the pollen tube is a good model for understanding the behavior of plant cells, and has been used in numerous in vitro studies of tip growth, it has proved challenging to study the directed growth of pollen tubes through the cell walls of stigma papillae in vivo. Now, in eLife, Thierry Gaude and co-workers at the Université de Lyon – including Lucie Riglet as first author – report the results of experiments on the model plant Arabidopsis thaliana that combine the power of microscopy, genetics, and chemical biology to provide new insights into the regulation of pollen tube growth (Riglet et al., 2020).

As stigmas age, they become less receptive to pollen (Gao et al., 2018), and the observation that pollen tubes tend to coil around papillae in aging stigmas forms the basis of this study. Riglet et al. found that aging was associated with changes in the organization of the cortical microtubules in the cytoskeleton: the orientations of these microtubules were more isotopic in older stigmas than in younger stigmas (Figure 1). To test the hypothesis that the organization of these microtubules has a role in directing pollen tube growth, the researchers examined plants that had a loss of function mutation in an enzyme called KATANIN (KTN1): this enzyme can sever microtubules, and thus allows microtubules to be re-oriented following mechanical stimulation (Sampathkumar et al., 2014). Riglet et al. found that pollen tubes coiled around the papillae in both young and old mutant plants: this indicates that the arrangement of the microtubules affects the ability of pollen tubes to grow straight through the cell walls and into the rest of the pistil.

Cortical microtubules are associated with cellulose synthesis, so the researchers tested whether the stiffness and composition of the cell wall in mutant and aging papillae was associated with pollen tube coiling. They found that softer cell walls and isotropic arrangements of cellulose microfibrils in mutant and aging papillae were associated with faster pollen tube growth and loss of directionality. Overall, the latest work supports the thesis that the mechanical properties and cell wall composition of the stigma papillae have an influence on pollen tube growth and help to guide it through the stigma. Moreover, by providing fundamental insights into the process of sexual reproduction in plants, the work is also relevant in the context of global food security as pollen-stigma interactions are critical for successful pollination and seed production in flowering plants.

Apart from pollen tubes, several types of plant, animal and fungal cells grow invasively, including root hairs, fibroblasts, cancer cells and fungal hyphae. In the future, it will be important to determine the contribution of mechanical forces to invasive growth. New technological advances such as lab-on-a-chip, MEMS (micro-electro-mechanical systems), deep-tissue imaging and computational tools will help researchers to measure the mechanical forces operating on and in cells (Nezhad et al., 2013). The pollen tube/pistil system will also make it possible to explore how chemical guidance cues work together with mechanical forces to regulate directional cell growth.

References

  1. 1
  2. 2
  3. 3
  4. 4
  5. 5
  6. 6
  7. 7
  8. 8
  9. 9
  10. 10
  11. 11
  12. 12

Article and author information

Author details

  1. Subramanian Sankaranarayanan

    Subramanian Sankaranarayanan is in the Department of Botany and Plant Pathology and the Purdue Center for Plant Biology, Purdue University, West Lafayette, United States

    For correspondence
    sankara3@purdue.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0398-2113
  2. Sharon A Kessler

    Sharon A Kessler is in the Department of Botany and Plant Pathology and the Purdue Center for Plant Biology, Purdue University, West Lafayette, United States

    For correspondence
    sakessler@purdue.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7964-0451

Publication history

  1. Version of Record published: September 1, 2020 (version 1)

Copyright

© 2020, Sankaranarayanan and Kessler

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

Metrics

  • 466
    Page views
  • 57
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

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

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

Further reading

    1. Chromosomes and Gene Expression
    2. Plant Biology
    Jo Hepworth et al.
    Research Article Updated

    In Arabidopsis thaliana, winter is registered during vernalization through the temperature-dependent repression and epigenetic silencing of floral repressor FLOWERING LOCUS C (FLC). Natural Arabidopsis accessions show considerable variation in vernalization. However, which aspect of the FLC repression mechanism is most important for adaptation to different environments is unclear. By analysing FLC dynamics in natural variants and mutants throughout winter in three field sites, we find that autumnal FLC expression, rather than epigenetic silencing, is the major variable conferred by the distinct Arabidopsis FLChaplotypes. This variation influences flowering responses of Arabidopsis accessions resulting in an interplay between promotion and delay of flowering in different climates to balance survival and, through a post-vernalization effect, reproductive output. These data reveal how expression variation through non-coding cis variation at FLC has enabled Arabidopsis accessions to adapt to different climatic conditions and year-on-year fluctuations.

    1. Plant Biology
    Pengqi Xu et al.
    Research Article

    Carotenoids are essential in oxygenic photosynthesis: they stabilize the pigment-protein complexes, are active in harvesting sunlight and in photoprotection. In plants, they are present as carotenes and their oxygenated derivatives, xanthophylls. While mutant plants lacking xanthophylls are capable of photoautotrophic growth, no plants without carotenes in their photosystems have been reported so far, which has led to the common opinion that carotenes are essential for photosynthesis. Here, we report the first plant that grows photoautotrophically in the absence of carotenes: a tobacco plant containing only the xanthophyll astaxanthin. Surprisingly, both photosystems are fully functional despite their carotenoid-binding sites being occupied by astaxanthin instead of β-carotene or remaining empty (i.e., are not occupied by carotenoids). These plants display non-photochemical quenching, despite the absence of both zeaxanthin and lutein and show that tobacco can regulate the ratio between the two photosystems in a very large dynamic range to optimize electron transport.