The Arabidopsis SHORTROOT network coordinates shoot apical meristem development with auxin dependent lateral organ initiation

  1. Elmehdi Bahafid
  2. Imke Bradtmöller
  3. Ann M Thies
  4. Thi TON Nguyen
  5. Crisanto Gutierrez
  6. Bénédicte Desvoyes
  7. Yvonne Stahl
  8. Ikram Blilou
  9. Rüdiger GW Simon  Is a corresponding author
  1. Heinrich Heine University Düsseldorf, Germany
  2. Centro de Biologia Molecular Severo Ochoa, Spain
  3. King Abdullah University of Science and Technology, Saudi Arabia

Abstract

Plants produce new organs post-embryonically throughout their entire life cycle. This is due to stem cells present in the shoot and root apical meristems, the SAM and RAM, respectively. In the SAM, stem cells are located in the central zone where they divide slowly. Stem cell daughters are displaced laterally and enter the peripheral zone, where their mitotic activity increases and lateral organ primordia are formed. How the spatial arrangement of these different domains is initiated and controlled during SAM growth and development, and how sites of lateral organ primordia are determined in the peripheral zone is not yet completely understood. We found that the SHORTROOT (SHR) transcription factor together with its target transcription factors SCARECROW (SCR), SCARECROW-LIKE23 (SCL23) and JACKDAW (JKD), promotes formation of lateral organs and controls shoot meristem size. SHR, SCR, SCL23 and JKD are expressed in distinct, but partially overlapping patterns in the SAM. They can physically interact and activate expression of key cell cycle regulators such as CYCLIND6;1 (CYCD6;1) to promote the formation of new cell layers. In the peripheral zone, auxin accumulates at sites of lateral organ primordia initiation and activates SHR expression via the auxin response factor MONOPTEROS (MP) and auxin response elements in the SHR promoter. In the central zone, the SHR-target SCL23 physically interacts with the key stem cell regulator WUSCHEL (WUS) to promote stem cell fate. Both SCL23 and WUS expression are subject to negative feedback regulation from stem cells through the CLAVATA signaling pathway. Together, our findings illustrate how SHR-dependent transcription factor complexes act in different domains of the shoot meristem to mediate cell division and auxin dependent organ initiation in the peripheral zone, and coordinate this activity with stem cell maintenance in the central zone of the SAM.

Data availability

Original microscopy and image analysis data referenced in the manuscriptare accessible through BioStudies at the following link:https://www.ebi.ac.uk/biostudies/bioimages/studies/S-BIAD903

Article and author information

Author details

  1. Elmehdi Bahafid

    Institute for Developmental Genetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Imke Bradtmöller

    Institute for Developmental Genetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ann M Thies

    Institute for Developmental Genetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Thi TON Nguyen

    Institute for Developmental Genetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Crisanto Gutierrez

    Genome Dynamics and Function, Centro de Biologia Molecular Severo Ochoa, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8905-8222
  6. Bénédicte Desvoyes

    Genome Dynamics and Function, Centro de Biologia Molecular Severo Ochoa, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Yvonne Stahl

    Institute for Developmental Genetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Ikram Blilou

    Laboratory of Plant Cell and Developmental Biology, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
    Competing interests
    The authors declare that no competing interests exist.
  9. Rüdiger GW Simon

    Institute for Developmental Genetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany
    For correspondence
    ruediger.simon@hhu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1317-7716

Funding

Deutsche Forschungsgemeinschaft (CSCS)

  • Rüdiger GW Simon

Deutsche Forschungsgemeinschaft (EXC2048)

  • Elmehdi Bahafid
  • Imke Bradtmöller
  • Ann M Thies
  • Thi TON Nguyen
  • Yvonne Stahl
  • Rüdiger GW Simon

Deutsche Forschungsgemeinschaft (CRC1208)

  • Rüdiger GW Simon

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

Reviewing Editor

  1. Dominique C Bergmann, Stanford University, United States

Version history

  1. Received: September 8, 2022
  2. Preprint posted: September 29, 2022 (view preprint)
  3. Accepted: September 29, 2023
  4. Accepted Manuscript published: October 20, 2023 (version 1)
  5. Version of Record published: November 13, 2023 (version 2)

Copyright

© 2023, Bahafid 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.

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  1. Elmehdi Bahafid
  2. Imke Bradtmöller
  3. Ann M Thies
  4. Thi TON Nguyen
  5. Crisanto Gutierrez
  6. Bénédicte Desvoyes
  7. Yvonne Stahl
  8. Ikram Blilou
  9. Rüdiger GW Simon
(2023)
The Arabidopsis SHORTROOT network coordinates shoot apical meristem development with auxin dependent lateral organ initiation
eLife 12:e83334.
https://doi.org/10.7554/eLife.83334

Share this article

https://doi.org/10.7554/eLife.83334

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