The circadian clock controls temporal and spatial patterns of floral development in sunflower

  1. Carine M Marshall
  2. Veronica L Thompson
  3. Nicky M Creux
  4. Stacey L Harmer  Is a corresponding author
  1. University of California, Davis, United States
  2. University of Pretoria, South Africa

Abstract

Biological rhythms are ubiquitous. They can be generated by circadian oscillators, which produce daily rhythms in physiology and behavior, as well as by developmental oscillators such as the segmentation clock, which periodically produces modular developmental units. Here, we show that the circadian clock controls the timing of late-stage floret development, or anthesis, in domesticated sunflowers. In these plants, up to thousands of individual florets are tightly packed onto a capitulum disk. While early floret development occurs continuously across capitula to generate iconic spiral phyllotaxy, during anthesis floret development occurs in discrete ring-like pseudowhorls with up to hundreds of florets undergoing simultaneous maturation. We demonstrate circadian regulation of floral organ growth and show that the effects of light on this process are time-of-day dependent. Delays in the phase of floral anthesis delay morning visits by pollinators, while disruption of circadian rhythms in floral organ development causes loss of pseudowhorl formation and large reductions in pollinator visits. We therefore show that the sunflower circadian clock acts in concert with environmental response pathways to tightly synchronize the anthesis of hundreds of florets each day, generating spatial patterns on the developing capitulum disk. This coordinated mass release of floral rewards at predictable times of day likely promotes pollinator visits and plant reproductive success.

Data availability

All source data have been uploaded to Dryad under the following accession codes: 10.25338/B8865X (timelapse scoring), 10.25338/B86358 (pollinator visits), 10.25338/B8963G (consensus scoring), 10.25338/B8CW5R (ovary measurements), and 10.25338/B8HP9F (organ growth kinetics).

The following data sets were generated
    1. Marshall C
    2. Creux N
    (2023) Sunflower timelapse scoring
    Dryad Digital Repository, doi:10.25338/B8865X.
    1. Marshall C
    2. Thompson V
    (2022) Sunflower pollinator visit scoring
    Dryad Digital Repository, doi:10.25338/B86358.
    1. Marshall C
    (2023) Sunflower consensus scoring
    Dryad Digital Repository, doi:10.25338/B8963G.
    1. Marshall C
    (2023) Sunflower ovary measurements
    Dryad Digital Repository, doi:10.25338/B8CW5R.
    1. Marshall C
    2. Thompson V
    (2022) Organ kinetics measurements
    Dryad Digital Repository, doi:10.25338/B8HP9F.

Article and author information

Author details

  1. Carine M Marshall

    Department of Plant Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Veronica L Thompson

    Department of Plant Biology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0500-5639
  3. Nicky M Creux

    Department of Plant and Soil Sciences, University of Pretoria, Pretoria, South Africa
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4179-6995
  4. Stacey L Harmer

    Department of Plant Biology, University of California, Davis, Davis, United States
    For correspondence
    slharmer@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6813-6682

Funding

National Science Foundation (IOS 1238040)

  • Stacey L Harmer

U.S. Department of Agriculture (CA-D-PLB-2259-H)

  • Stacey L Harmer

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

Reviewing Editor

  1. Pil Joon Seo, Seoul National University, Korea (South), Republic of

Publication history

  1. Received: June 11, 2022
  2. Accepted: January 12, 2023
  3. Accepted Manuscript published: January 13, 2023 (version 1)

Copyright

© 2023, Marshall 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

  • 519
    Page views
  • 124
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Carine M Marshall
  2. Veronica L Thompson
  3. Nicky M Creux
  4. Stacey L Harmer
(2023)
The circadian clock controls temporal and spatial patterns of floral development in sunflower
eLife 12:e80984.
https://doi.org/10.7554/eLife.80984

Further reading

    1. Developmental Biology
    Marianne E Emmert, Parul Aggarwal ... Roger Cornwall
    Research Article Updated

    Neonatal brachial plexus injury (NBPI) causes disabling and incurable muscle contractures that result from impaired longitudinal growth of denervated muscles. This deficit in muscle growth is driven by increased proteasome-mediated protein degradation, suggesting a dysregulation of muscle proteostasis. The myostatin (MSTN) pathway, a prominent muscle-specific regulator of proteostasis, is a putative signaling mechanism by which neonatal denervation could impair longitudinal muscle growth, and thus a potential target to prevent NBPI-induced contractures. Through a mouse model of NBPI, our present study revealed that pharmacologic inhibition of MSTN signaling induces hypertrophy, restores longitudinal growth, and prevents contractures in denervated muscles of female but not male mice, despite inducing hypertrophy of normally innervated muscles in both sexes. Additionally, the MSTN-dependent impairment of longitudinal muscle growth after NBPI in female mice is associated with perturbation of 20S proteasome activity, but not through alterations in canonical MSTN signaling pathways. These findings reveal a sex dimorphism in the regulation of neonatal longitudinal muscle growth and contractures, thereby providing insights into contracture pathophysiology, identifying a potential muscle-specific therapeutic target for contracture prevention, and underscoring the importance of sex as a biological variable in the pathophysiology of neuromuscular disorders.

    1. Developmental Biology
    2. Genetics and Genomics
    Ankit Sabharwal, Mark D Wishman ... Stephen C Ekker
    Research Advance Updated

    The clinical and largely unpredictable heterogeneity of phenotypes in patients with mitochondrial disorders demonstrates the ongoing challenges in the understanding of this semi-autonomous organelle in biology and disease. Previously, we used the gene-breaking transposon to create 1200 transgenic zebrafish strains tagging protein-coding genes (Ichino et al., 2020), including the lrpprc locus. Here, we present and characterize a new genetic revertible animal model that recapitulates components of Leigh Syndrome French Canadian Type (LSFC), a mitochondrial disorder that includes diagnostic liver dysfunction. LSFC is caused by allelic variations in the LRPPRC gene, involved in mitochondrial mRNA polyadenylation and translation. lrpprc zebrafish homozygous mutants displayed biochemical and mitochondrial phenotypes similar to clinical manifestations observed in patients, including dysfunction in lipid homeostasis. We were able to rescue these phenotypes in the disease model using a liver-specific genetic model therapy, functionally demonstrating a previously under-recognized critical role for the liver in the pathophysiology of this disease.