A quantitative hypermorphic CNGC allele confers ectopic calcium flux and impairs cellular development

  1. David M Chiasson
  2. Kristina Haage
  3. Katharina Sollweck
  4. Andreas Brachmann
  5. Petra Dietrich
  6. Martin Parniske  Is a corresponding author
  1. Ludwig Maximilian University of Munich, Germany
  2. Friedrich-Alexander Universität Erlangen-Nürnberg, Germany

Abstract

The coordinated control of Ca2+ signaling is essential for development in eukaryotes. Cyclic nucleotide-gated channel (CNGC) family members mediate Ca2+ influx from cellular stores in plants1-4. Here we report the unusual genetic behavior of a quantitative gain-of-function CNGC mutation (brush) in Lotus japonicus resulting in a leaky tetrameric channel. brush resides in a cluster of redundant CNGCs encoding subunits which resemble metazoan voltage-gated potassium (Kv1-Kv4) channels in assembly and gating properties. Plants homozygous for brush are impaired in root development and infection by nitrogen-fixing rhizobia which segregated as a recessive monogenic trait. The brush allele exhibited quantitative behavior since overexpression of the cluster subunits was required to suppress the brush phenotype. The results reveal a mechanism by which quantitative competition between channel subunits for tetramer assembly can impact the phenotype of the mutation carrier.

Article and author information

Author details

  1. David M Chiasson

    Faculty of Biology, Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0770-2684
  2. Kristina Haage

    Faculty of Biology, Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Katharina Sollweck

    Faculty of Biology, Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Andreas Brachmann

    Faculty of Biology, Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Petra Dietrich

    Division of Molecular Plant Physiology, Department of Biology, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Martin Parniske

    Faculty of Biology, Genetics, Ludwig Maximilian University of Munich, Martinsried, Germany
    For correspondence
    parniske@lmu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8561-747X

Funding

Deutsche Forschungsgemeinschaft (FOR964 (Calcium))

  • Kristina Haage
  • Petra Dietrich
  • Martin Parniske

H2020 European Research Council (340904 (EvolvingNodules))

  • Martin Parniske

Alexander von Humboldt-Stiftung

  • David M Chiasson

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

Copyright

© 2017, Chiasson 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

  • 3,019
    views
  • 643
    downloads
  • 29
    citations

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

Download links

Share this article

https://doi.org/10.7554/eLife.25012

Further reading

    1. Chromosomes and Gene Expression
    Shihui Chen, Carolyn Marie Phillips
    Research Article

    RNA interference (RNAi) is a conserved pathway that utilizes Argonaute proteins and their associated small RNAs to exert gene regulatory function on complementary transcripts. While the majority of germline-expressed RNAi proteins reside in perinuclear germ granules, it is unknown whether and how RNAi pathways are spatially organized in other cell types. Here, we find that the small RNA biogenesis machinery is spatially and temporally organized during Caenorhabditis elegans embryogenesis. Specifically, the RNAi factor, SIMR-1, forms visible concentrates during mid-embryogenesis that contain an RNA-dependent RNA polymerase, a poly-UG polymerase, and the unloaded nuclear Argonaute protein, NRDE-3. Curiously, coincident with the appearance of the SIMR granules, the small RNAs bound to NRDE-3 switch from predominantly CSR-class 22G-RNAs to ERGO-dependent 22G-RNAs. NRDE-3 binds ERGO-dependent 22G-RNAs in the somatic cells of larvae and adults to silence ERGO-target genes; here we further demonstrate that NRDE-3-bound, CSR-class 22G-RNAs repress transcription in oocytes. Thus, our study defines two separable roles for NRDE-3, targeting germline-expressed genes during oogenesis to promote global transcriptional repression, and switching during embryogenesis to repress recently duplicated genes and retrotransposons in somatic cells, highlighting the plasticity of Argonaute proteins and the need for more precise temporal characterization of Argonaute-small RNA interactions.

    1. Chromosomes and Gene Expression
    2. Genetics and Genomics
    Steven Henikoff, David L Levens
    Insight

    A new method for mapping torsion provides insights into the ways that the genome responds to the torsion generated by RNA polymerase II.