1. Developmental Biology
  2. Plant Biology

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
https://doi.org/10.7554/eLife.54740
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.
    https://sites.google.com/a/ualberta.ca/onekp/

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.

Metrics

  • 8,285
    views
  • 1,118
    downloads
  • 90
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. 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

Categories and tags

Research organism

Further reading

    1. Developmental Biology

    Inhibitory G proteins play multiple roles to polarize sensory hair cell morphogenesis

    Amandine Jarysta, Abigail LD Tadenev ... Basile Tarchini
    Research Article

    Inhibitory G alpha (GNAI or Gαi) proteins are critical for the polarized morphogenesis of sensory hair cells and for hearing. The extent and nature of their actual contributions remains unclear, however, as previous studies did not investigate all GNAI proteins and included non-physiological approaches. Pertussis toxin can downregulate functionally redundant GNAI1, GNAI2, GNAI3, and GNAO proteins, but may also induce unrelated defects. Here, we directly and systematically determine the role(s) of each individual GNAI protein in mouse auditory hair cells. GNAI2 and GNAI3 are similarly polarized at the hair cell apex with their binding partner G protein signaling modulator 2 (GPSM2), whereas GNAI1 and GNAO are not detected. In Gnai3 mutants, GNAI2 progressively fails to fully occupy the sub-cellular compartments where GNAI3 is missing. In contrast, GNAI3 can fully compensate for the loss of GNAI2 and is essential for hair bundle morphogenesis and auditory function. Simultaneous inactivation of Gnai2 and Gnai3 recapitulates for the first time two distinct types of defects only observed so far with pertussis toxin: (1) a delay or failure of the basal body to migrate off-center in prospective hair cells, and (2) a reversal in the orientation of some hair cell types. We conclude that GNAI proteins are critical for hair cells to break planar symmetry and to orient properly before GNAI2/3 regulate hair bundle morphogenesis with GPSM2.

    1. Computational and Systems Biology
    2. Developmental Biology

    A logic-incorporated gene regulatory network deciphers principles in cell fate decisions

    Gang Xue, Xiaoyi Zhang ... Zhiyuan Li
    Research Article

    Organisms utilize gene regulatory networks (GRN) to make fate decisions, but the regulatory mechanisms of transcription factors (TF) in GRNs are exceedingly intricate. A longstanding question in this field is how these tangled interactions synergistically contribute to decision-making procedures. To comprehensively understand the role of regulatory logic in cell fate decisions, we constructed a logic-incorporated GRN model and examined its behavior under two distinct driving forces (noise-driven and signal-driven). Under the noise-driven mode, we distilled the relationship among fate bias, regulatory logic, and noise profile. Under the signal-driven mode, we bridged regulatory logic and progression-accuracy trade-off, and uncovered distinctive trajectories of reprogramming influenced by logic motifs. In differentiation, we characterized a special logic-dependent priming stage by the solution landscape. Finally, we applied our findings to decipher three biological instances: hematopoiesis, embryogenesis, and trans-differentiation. Orthogonal to the classical analysis of expression profile, we harnessed noise patterns to construct the GRN corresponding to fate transition. Our work presents a generalizable framework for top-down fate-decision studies and a practical approach to the taxonomy of cell fate decisions.

    1. Developmental Biology
    2. Evolutionary Biology

    The rapidly evolving X-linked MIR-506 family fine-tunes spermatogenesis to enhance sperm competition

    Zhuqing Wang, Yue Wang ... Wei Yan
    Research Article

    Despite rapid evolution across eutherian mammals, the X-linked MIR-506 family miRNAs are located in a region flanked by two highly conserved protein-coding genes (SLITRK2 and FMR1) on the X chromosome. Intriguingly, these miRNAs are predominantly expressed in the testis, suggesting a potential role in spermatogenesis and male fertility. Here, we report that the X-linked MIR-506 family miRNAs were derived from the MER91C DNA transposons. Selective inactivation of individual miRNAs or clusters caused no discernible defects, but simultaneous ablation of five clusters containing 19 members of the MIR-506 family led to reduced male fertility in mice. Despite normal sperm counts, motility, and morphology, the KO sperm were less competitive than wild-type sperm when subjected to a polyandrous mating scheme. Transcriptomic and bioinformatic analyses revealed that these X-linked MIR-506 family miRNAs, in addition to targeting a set of conserved genes, have more targets that are critical for spermatogenesis and embryonic development during evolution. Our data suggest that the MIR-506 family miRNAs function to enhance sperm competitiveness and reproductive fitness of the male by finetuning gene expression during spermatogenesis.