1. Plant Biology
Download icon

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
Research Article
  • Cited 9
  • Views 2,504
  • Annotations
Cite this article as: eLife 2018;7:e39399 doi: 10.7554/eLife.39399

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.

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

  • 2,504
    Page views
  • 453
    Downloads
  • 9
    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)

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)

Categories and tags

Research organism

Further reading

    1. Plant Biology
    2. Structural Biology and Molecular Biophysics

    Identification of distinct pH-and zeaxanthin-dependent quenching in LHCSR3 from Chlamydomonas reinhardtii

    Julianne M Troiano et al.
    Research Article

    Under high light, oxygenic photosynthetic organisms avoid photodamage by thermally dissipating absorbed energy, which is called non-photochemical quenching. In green algae, a chlorophyll and carotenoid-binding protein, light-harvesting complex stress-related (LHCSR3), detects excess energy via a pH drop and serves as a quenching site. Using a combined in vivo and in vitro approach, we investigated quenching within LHCSR3 from Chlamydomonas reinhardtii. In vitro two distinct quenching processes, individually controlled by pH and zeaxanthin, were identified within LHCSR3. The pH-dependent quenching was removed within a mutant LHCSR3 that lacks the residues that are protonated to sense the pH drop. Observation of quenching in zeaxanthin-enriched LHCSR3 even at neutral pH demonstrated zeaxanthin-dependent quenching, which also occurs in other light-harvesting complexes. Either pH- or zeaxanthin-dependent quenching prevented the formation of damaging reactive oxygen species, and thus the two quenching processes may together provide different induction and recovery kinetics for photoprotection in a changing environment.

    1. Plant Biology

    Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis

    Kurataka Otsuka et al.
    Research Article

    Although mechanisms that activate organogenesis in plants are well established, much less is known about the subsequent fine-tuning of cell proliferation, which is crucial for creating properly structured and sized organs. Here we show, through analysis of temperature-dependent fasciation (TDF) mutants of Arabidopsis, root redifferentiation defective 1 (rrd1), rrd2, and root initiation defective 4 (rid4), that mitochondrial RNA processing is required for limiting cell division during early lateral root (LR) organogenesis. These mutants formed abnormally broadened (i.e., fasciated) LRs under high-temperature conditions due to extra cell division. All TDF proteins localized to mitochondria, where they were found to participate in RNA processing: RRD1 in mRNA deadenylation, and RRD2 and RID4 in mRNA editing. Further analysis suggested that LR fasciation in the TDF mutants is triggered by reactive oxygen species generation caused by defective mitochondrial respiration. Our findings provide novel clues for the physiological significance of mitochondrial activities in plant organogenesis.

    1. Plant Biology

    A fungal member of the Arabidopsis thaliana phyllosphere antagonizes Albugo laibachii via a GH25 lysozyme

    Katharina Eitzen et al.
    Research Article

    Plants are not only challenged by pathogenic organisms, but also colonized by commensal microbes. The network of interactions these microbes establish with their host and amongst each other is suggested to contribute to the immune responses of plants against pathogens. In wild Arabidopsis thaliana populations, the oomycete pathogen Albugo laibachii plays an influential role in structuring the leaf phyllosphere. We show that the epiphytic yeast Moesziomyces bullatus ex Albugo on Arabidopsis, a close relative of pathogenic smut fungi, is an antagonistic member of the A. thaliana phyllosphere, which reduces infection of A. thaliana by A. laibachii. Combination of transcriptomics, reverse genetics and protein characterization identified a GH25 hydrolase with lysozyme activity as a major effector of this microbial antagonism. Our findings broaden the understanding of microbial interactions within the phyllosphere, provide insights into the evolution of epiphytic basidiomycete yeasts and pave the way for novel biocontrol strategies.