Negative regulation of conserved RSL class I bHLH transcription factors evolved independently among land plants

  1. Suvi Honkanen
  2. Anna Thamm
  3. Mario A Arteaga-Vazquez
  4. Liam Dolan  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. Universidad Veracruzana, Mexico

Abstract

Basic helix-loop-helix transcription factors encoded by RSL class I genes control a gene regulatory network that positively regulates the development of filamentous rooting cells - root hairs and rhizoids - in land plants. The GLABRA2 transcription factor negatively regulates these genes in the angiosperm Arabidopsis thaliana. To find negative regulators of RSL class I genes in early diverging land plants we conducted a mutant screen in the liverwort Marchantia polymorpha. This identified FEW RHIZOIDS1 (MpFRH1) microRNA (miRNA) that negatively regulates the RSL class I gene MpRSL1. The miRNA and its mRNA target constitute a feedback mechanism that controls epidermal cell differentiation. MpFRH1 miRNA target sites are conserved among liverwort RSL class I mRNAs but are not present in RSL class I mRNAs of other land plants. These findings indicate that while RSL class I genes are ancient and conserved, independent negative regulatory mechanisms evolved in different lineages during land plant evolution.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

The following previously published data sets were used

Article and author information

Author details

  1. Suvi Honkanen

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3923-3365
  2. Anna Thamm

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Mario A Arteaga-Vazquez

    Instituto de Biotecnología y Ecología Aplicada, Universidad Veracruzana, Veracruz, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Liam Dolan

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    For correspondence
    liam.dolan@plants.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1206-7096

Funding

European Commission (EVO-500 25028)

  • Suvi Honkanen
  • Liam Dolan

Biotechnology and Biological Sciences Research Council (BB/F016093/1)

  • Suvi Honkanen
  • Anna Thamm

University of Oxford EPA Cephalosporin scholarship

  • Anna Thamm

University of California Institute for Mexico and the United States (UCMEXUS-19941-44-OAC7)

  • Mario A Arteaga-Vazquez

The Royal Society Newton Advanced Fellowship (NA150181 RG79985)

  • Mario A Arteaga-Vazquez

Biotechnology and Biological Sciences Research Council (J0144271/1)

  • Suvi Honkanen
  • Anna Thamm

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

Copyright

© 2018, Honkanen 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

  • 3,541
    views
  • 525
    downloads
  • 32
    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. Suvi Honkanen
  2. Anna Thamm
  3. Mario A Arteaga-Vazquez
  4. Liam Dolan
(2018)
Negative regulation of conserved RSL class I bHLH transcription factors evolved independently among land plants
eLife 7:e38529.
https://doi.org/10.7554/eLife.38529

Share this article

https://doi.org/10.7554/eLife.38529

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    Torsten Günther, Jacob Chisausky ... Cristina Valdiosera
    Research Article

    Cattle (Bos taurus) play an important role in the life of humans in the Iberian Peninsula not just as a food source but also in cultural events. When domestic cattle were first introduced to Iberia, wild aurochs (Bos primigenius) were still present, leaving ample opportunity for mating (whether intended by farmers or not). Using a temporal bioarchaeological dataset covering eight millennia, we trace gene flow between the two groups. Our results show frequent hybridisation during the Neolithic and Chalcolithic, likely reflecting a mix of hunting and herding or relatively unmanaged herds, with mostly male aurochs and female domestic cattle involved. This is supported by isotopic evidence consistent with ecological niche sharing, with only a few domestic cattle possibly being managed. The proportion of aurochs ancestry in domestic cattle remains relatively constant from about 4000 years ago, probably due to herd management and selection against first generation hybrids, coinciding with other cultural transitions. The constant level of wild ancestry (~20%) continues into modern Western European breeds including Iberian cattle selected for aggressiveness and fighting ability. This study illuminates the genomic impact of human actions and wild introgression in the establishment of cattle as one of the most important domestic species today.

    1. Evolutionary Biology
    2. Genetics and Genomics
    James Boocock, Noah Alexander ... Leonid Kruglyak
    Research Article

    Expression quantitative trait loci (eQTLs) provide a key bridge between noncoding DNA sequence variants and organismal traits. The effects of eQTLs can differ among tissues, cell types, and cellular states, but these differences are obscured by gene expression measurements in bulk populations. We developed a one-pot approach to map eQTLs in Saccharomyces cerevisiae by single-cell RNA sequencing (scRNA-seq) and applied it to over 100,000 single cells from three crosses. We used scRNA-seq data to genotype each cell, measure gene expression, and classify the cells by cell-cycle stage. We mapped thousands of local and distant eQTLs and identified interactions between eQTL effects and cell-cycle stages. We took advantage of single-cell expression information to identify hundreds of genes with allele-specific effects on expression noise. We used cell-cycle stage classification to map 20 loci that influence cell-cycle progression. One of these loci influenced the expression of genes involved in the mating response. We showed that the effects of this locus arise from a common variant (W82R) in the gene GPA1, which encodes a signaling protein that negatively regulates the mating pathway. The 82R allele increases mating efficiency at the cost of slower cell-cycle progression and is associated with a higher rate of outcrossing in nature. Our results provide a more granular picture of the effects of genetic variants on gene expression and downstream traits.