Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions

  1. Michael J Prigge
  2. Matthieu Platre
  3. Nikita Kadakia
  4. Yi Zhang
  5. Kathleen Greenham
  6. Whitnie Szutu
  7. Bipin Kumar Pandey
  8. Rahul Arvind Bhosale
  9. Malcolm J Bennett
  10. Wolfgang Busch
  11. Mark Estelle  Is a corresponding author
  1. University of California, San Diego, United States
  2. Salk Institute for Biological Sciences, United States
  3. University of Nottingham, United Kingdom
  4. Salk Institute for Biological Studies, United States

Abstract

The TIR1/AFB auxin co-receptors mediate diverse responses to the plant hormone auxin. The Arabidopsis genome encodes six TIR1/AFB proteins representing three of the four clades that were established prior to angiosperm radiation. To determine the role of these proteins in plant development we performed an extensive genetic analysis involving the generation and characterization of all possible multiply-mutant lines. We find that loss of all six TIR1/AFB proteins results in early embryo defects and eventually seed abortion, and yet a single wild-type allele of TIR1 or AFB2 is sufficient to support growth throughout development. Our analysis reveals extensive functional overlap between even the most distantly related TIR1/AFB genes except for AFB1. Surprisingly, AFB1 has a specialized function in rapid auxin-dependent inhibition of root growth and early phase of root gravitropism. This activity may be related to a difference in subcellular localization compared to the other members of the family.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 1-figure supplement 2B, Figure 1-figure supplement 4, Figure 1-figure supplement 5. Figure 5-figure supplement 1, Figure 6, Figure 6-figure supplement 2 , Figure 7, Figure 7-figure supplement 1

The following previously published data sets were used
    1. Eric J Carpenter et al
    (2019) One 1000 plant transciptomics
    https://datacommons.cyverse.org/browse/iplant/home/shared/commons_repo/curated/oneKP_capstone_2019.

Article and author information

Author details

  1. Michael J Prigge

    Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0671-2538
  2. Matthieu Platre

    Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Sciences, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Nikita Kadakia

    Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yi Zhang

    Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Kathleen Greenham

    Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7681-5263
  6. Whitnie Szutu

    Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Bipin Kumar Pandey

    School of Biosciences, University of Nottingham, Loughborough, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9614-1347
  8. Rahul Arvind Bhosale

    School of Biosciences, Plant Sciences, University of Nottingham, Loughborough, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6515-4922
  9. Malcolm J Bennett

    Plant Sciences Division, University of Nottingham, Loughborough, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  10. Wolfgang Busch

    Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Mark Estelle

    Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, United States
    For correspondence
    mestelle@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2613-8652

Funding

National Institutes of Health (GM43644)

  • Mark Estelle

Human Frontier Science Program (LT000340/2019-L)

  • Matthieu Platre

Biotechnology and Biological Sciences Research Council (research fellowship)

  • Rahul Arvind Bhosale

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

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Version history

  1. Received: December 27, 2019
  2. Accepted: February 4, 2020
  3. Accepted Manuscript published: February 18, 2020 (version 1)
  4. Version of Record published: February 28, 2020 (version 2)

Copyright

© 2020, Prigge 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. Michael J Prigge
  2. Matthieu Platre
  3. Nikita Kadakia
  4. Yi Zhang
  5. Kathleen Greenham
  6. Whitnie Szutu
  7. Bipin Kumar Pandey
  8. Rahul Arvind Bhosale
  9. Malcolm J Bennett
  10. Wolfgang Busch
  11. Mark Estelle
(2020)
Genetic analysis of the Arabidopsis TIR1/AFB auxin receptors reveals both overlapping and specialized functions
eLife 9:e54740.
https://doi.org/10.7554/eLife.54740

Share this article

https://doi.org/10.7554/eLife.54740

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