The role of APETALA1 in petal number robustness

  1. Marie Monniaux
  2. Bjorn Pieper
  3. Sarah M McKim
  4. Anne-Lise Routier-Kierzkowska
  5. Daniel Kierzkowski
  6. Richard S Smith
  7. Angela Hay  Is a corresponding author
  1. Max Planck Institute for Plant Breeding Research, Germany
  2. University of Oxford, United Kingdom

Abstract

Invariant floral forms are important for reproductive success and robust to natural perturbations. Petal number, for example, is invariant in Arabidopsis thaliana flowers. However, petal number varies in the closely related species Cardamine hirsuta, and the genetic basis for this difference between species is unknown. Here we show that divergence in the pleiotropic floral regulator APETALA1 (AP1) can account for the species-specific difference in petal number robustness. This large effect of AP1 is explained by epistatic interactions: A. thaliana AP1 confers robustness by masking the phenotypic expression of quantitative trait loci controlling petal number in C. hirsuta. We show that C. hirsuta AP1 fails to complement this function of A. thaliana AP1, conferring variable petal number, and that upstream regulatory regions of AP1 contribute to this divergence. Moreover, variable petal number is maintained in C. hirsuta despite sufficient standing genetic variation in natural accessions to produce plants with four-petalled flowers.

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. Marie Monniaux

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Bjorn Pieper

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Sarah M McKim

    Plant Sciences Department, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Anne-Lise Routier-Kierzkowska

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Daniel Kierzkowski

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Richard S Smith

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9220-0787
  7. Angela Hay

    Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    For correspondence
    hay@mpipz.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4609-5490

Funding

Biotechnology and Biological Sciences Research Council (BB/H01313X/1)

  • Angela Hay

Human Frontier Science Program (RGP0008/2013)

  • Richard S Smith

Royal Society (University Research Fellowship)

  • Angela Hay

Max Planck Society (W2 Minerva Fellowship)

  • Angela Hay

European Molecular Biology Organization (Long Term Fellowship)

  • Marie Monniaux

National Science and Engineering Research Council of Canada (Post-Doctoral Fellowship)

  • Sarah M McKim

European Molecular Biology Organization (Long Term Fellowship)

  • Sarah M McKim

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

Reviewing Editor

  1. Sheila McCormick, University of California-Berkeley, United States

Publication history

  1. Received: June 23, 2018
  2. Accepted: October 11, 2018
  3. Accepted Manuscript published: October 18, 2018 (version 1)
  4. Version of Record published: October 29, 2018 (version 2)

Copyright

© 2018, Monniaux 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

  • 3,060
    Page views
  • 514
    Downloads
  • 17
    Citations

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

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. Marie Monniaux
  2. Bjorn Pieper
  3. Sarah M McKim
  4. Anne-Lise Routier-Kierzkowska
  5. Daniel Kierzkowski
  6. Richard S Smith
  7. Angela Hay
(2018)
The role of APETALA1 in petal number robustness
eLife 7:e39399.
https://doi.org/10.7554/eLife.39399

Further reading

    1. Plant Biology
    Jack Rhodes et al.
    Short Report Updated

    Plant genomes encode hundreds of secreted peptides; however, relatively few have been characterised. We report here an uncharacterised, stress-induced family of plant signalling peptides, which we call CTNIPs. Based on the role of the common co-receptor BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) in CTNIP-induced responses, we identified in Arabidopsis thaliana the orphan receptor kinase HAESA-LIKE 3 (HSL3) as the CTNIP receptor via a proteomics approach. CTNIP-binding, ligand-triggered complex formation with BAK1, and induced downstream responses all involve HSL3. Notably, the HSL3-CTNIP signalling module is evolutionarily conserved amongst most extant angiosperms. The identification of this novel signalling module will further shed light on the diverse functions played by plant signalling peptides and will provide insights into receptor-ligand co-evolution.

    1. Developmental Biology
    2. Plant Biology
    Sören Strauss et al.
    Tools and Resources Updated

    Positional information is a central concept in developmental biology. In developing organs, positional information can be idealized as a local coordinate system that arises from morphogen gradients controlled by organizers at key locations. This offers a plausible mechanism for the integration of the molecular networks operating in individual cells into the spatially coordinated multicellular responses necessary for the organization of emergent forms. Understanding how positional cues guide morphogenesis requires the quantification of gene expression and growth dynamics in the context of their underlying coordinate systems. Here, we present recent advances in the MorphoGraphX software (Barbier de Reuille et al., 2015⁠) that implement a generalized framework to annotate developing organs with local coordinate systems. These coordinate systems introduce an organ-centric spatial context to microscopy data, allowing gene expression and growth to be quantified and compared in the context of the positional information thought to control them.