Regulation of shoot meristem shape by photoperiodic signaling and phytohormones during floral induction of Arabidopsis

  1. Atsuko Kinoshita
  2. Alice Vayssières
  3. René Richter
  4. Qing Sang
  5. Adrian Roggen
  6. Annabel D van Driel
  7. Richard S Smith
  8. George Coupland  Is a corresponding author
  1. Tokyo Metropolitan University, Japan
  2. Max Planck Institute for Plant Breeding Research, Germany

Abstract

Floral transition, the onset of plant reproduction, involves changes in shape and identity of the shoot apical meristem (SAM). The change in shape, termed doming, occurs early during floral transition when it is induced by environmental cues such as changes in day-length, but how it is regulated at the cellular level is unknown. We defined the morphological and cellular features of the SAM during floral transition of Arabidopsis thaliana. Both cell number and size increased during doming, and these changes were partially controlled by the gene regulatory network (GRN) that triggers flowering. Furthermore, dynamic modulation of expression of gibberellin biosynthesis and catabolism enzymes at the SAM contributed to doming. Expression of these enzymes was regulated by two MADS-domain transcription factors implicated in flowering. We provide a temporal and spatial framework for integrating the flowering GRN with cellular changes at the SAM, and highlight the role of local regulation of gibberellin.

Data availability

All data generated this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 3, 6 and 7 and 8

Article and author information

Author details

  1. Atsuko Kinoshita

    Biological Sciences, Tokyo Metropolitan University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9095-389X
  2. Alice Vayssières

    Plant developmental biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. René Richter

    Plant developmental biology, 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:" 0000-0001-9833-2211
  4. Qing Sang

    Plant developmental biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Adrian Roggen

    Plant developmental biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Annabel D van Driel

    Plant developmental biology, 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:" 0000-0002-1629-5961
  7. Richard S Smith

    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
  8. George Coupland

    Plant developmental biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany
    For correspondence
    coupland@mpipz.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6988-4172

Funding

Alexander von Humboldt-Stiftung

  • Atsuko Kinoshita

Japanese Society for the promotion of Science

  • Atsuko Kinoshita

Deutsche Forschungsgemeinschaft (390686111)

  • George Coupland

Max-Planck-Gesellschaft (Open-access funding)

  • George Coupland

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

Reviewing Editor

  1. Hao Yu, National University of Singapore & Temasek Life Sciences Laboratory, Singapore

Version history

  1. Received: July 2, 2020
  2. Accepted: December 12, 2020
  3. Accepted Manuscript published: December 14, 2020 (version 1)
  4. Version of Record published: December 29, 2020 (version 2)

Copyright

© 2020, Kinoshita 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

  • 7,592
    Page views
  • 1,370
    Downloads
  • 27
    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)

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. Atsuko Kinoshita
  2. Alice Vayssières
  3. René Richter
  4. Qing Sang
  5. Adrian Roggen
  6. Annabel D van Driel
  7. Richard S Smith
  8. George Coupland
(2020)
Regulation of shoot meristem shape by photoperiodic signaling and phytohormones during floral induction of Arabidopsis
eLife 9:e60661.
https://doi.org/10.7554/eLife.60661

Share this article

https://doi.org/10.7554/eLife.60661

Further reading

    1. Plant Biology
    Daniel S Yu, Megan A Outram ... Simon J Williams
    Research Article

    Plant pathogens secrete proteins, known as effectors, that function in the apoplast or inside plant cells to promote virulence. Effector recognition by cell-surface or cytosolic receptors results in the activation of defence pathways and plant immunity. Despite their importance, our general understanding of fungal effector function and recognition by immunity receptors remains poor. One complication often associated with effectors is their high sequence diversity and lack of identifiable sequence motifs precluding prediction of structure or function. In recent years, several studies have demonstrated that fungal effectors can be grouped into structural classes, despite significant sequence variation and existence across taxonomic groups. Using protein X-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors Avr1 (SIX4) and Avr3 (SIX1) represent the founding members of the Fol dual-domain (FOLD) effector class, with members containing two distinct domains. Using AlphaFold2, we predicted the full SIX effector repertoire of Fol and show that SIX6 and SIX13 are also FOLD effectors, which we validated experimentally for SIX6. Based on structural prediction and comparisons, we show that FOLD effectors are present within three divisions of fungi and are expanded in pathogens and symbionts. Further structural comparisons demonstrate that Fol secretes effectors that adopt a limited number of structural folds during infection of tomato. This analysis also revealed a structural relationship between transcriptionally co-regulated effector pairs. We make use of the Avr1 structure to understand its recognition by the I receptor, which leads to disease resistance in tomato. This study represents an important advance in our understanding of Fol-tomato, and by extension plant–fungal interactions, which will assist in the development of novel control and engineering strategies to combat plant pathogens.

    1. Ecology
    2. Plant Biology
    Jamie Mitchel Waterman, Tristan Michael Cofer ... Matthias Erb
    Research Article

    Volatiles emitted by herbivore-attacked plants (senders) can enhance defenses in neighboring plants (receivers), however, the temporal dynamics of this phenomenon remain poorly studied. Using a custom-built, high-throughput proton transfer reaction time-of-flight mass spectrometry (PTR-ToF-MS) system, we explored temporal patterns of volatile transfer and responses between herbivore-attacked and undamaged maize plants. We found that continuous exposure to natural blends of herbivore-induced volatiles results in clocked temporal response patterns in neighboring plants, characterized by an induced terpene burst at the onset of the second day of exposure. This delayed burst is not explained by terpene accumulation during the night, but coincides with delayed jasmonate accumulation in receiver plants. The delayed burst occurs independent of day:night light transitions and cannot be fully explained by sender volatile dynamics. Instead, it is the result of a stress memory from volatile exposure during the first day and secondary exposure to bioactive volatiles on the second day. Our study reveals that prolonged exposure to natural blends of stress-induced volatiles results in a response that integrates priming and direct induction into a distinct and predictable temporal response pattern. This provides an answer to the long-standing question of whether stress volatiles predominantly induce or prime plant defenses in neighboring plants, by revealing that they can do both in sequence.