1. Developmental Biology
  2. Plant Biology

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
https://doi.org/10.7554/eLife.80984
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  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
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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.
    https://doi.org/10.25338/B8865X
    1. Marshall C
    2. Thompson V
    (2022) Sunflower pollinator visit scoring
    Dryad Digital Repository, doi:10.25338/B86358.
    https://doi.org/10.25338/B86358
    1. Marshall C
    (2023) Sunflower consensus scoring
    Dryad Digital Repository, doi:10.25338/B8963G.
    https://doi.org/10.25338/B8963G
    1. Marshall C
    (2023) Sunflower ovary measurements
    Dryad Digital Repository, doi:10.25338/B8CW5R.
    https://doi.org/10.25338/B8CW5R
    1. Marshall C
    2. Thompson V
    (2022) Organ kinetics measurements
    Dryad Digital Repository, doi:10.25338/B8HP9F.
    https://doi.org/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.

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.

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  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

Share this article

https://doi.org/10.7554/eLife.80984

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Further reading

    1. Developmental Biology
    2. Plant Biology

    Floral Maturation: How the sunflower gets its rings

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  2. Listen to Stacey Harmer explain how sunflowers coordinate their flowering patterns.

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    Mouse oocytes undergo drastic changes in organellar composition and their activities during maturation from the germinal vesicle (GV) to metaphase II (MII) stage. After fertilization, the embryo degrades parts of the maternal components via lysosomal degradation systems, including autophagy and endocytosis, as zygotic gene expression begins during embryogenesis. Here, we demonstrate that endosomal-lysosomal organelles form large spherical assembly structures, termed endosomal-lysosomal organellar assemblies (ELYSAs), in mouse oocytes. ELYSAs are observed in GV oocytes, attaining sizes up to 7–8 μm in diameter in MII oocytes. ELYSAs comprise tubular-vesicular structures containing endosomes and lysosomes along with cytosolic components. Most ELYSAs are also positive for an autophagy regulator, LC3. These characteristics of ELYSA resemble those of ELVA (endolysosomal vesicular assemblies) identified independently. The signals of V1-subunit of vacuolar ATPase tends to be detected on the periphery of ELYSAs in MII oocytes. After fertilization, the localization of the V1-subunit on endosomes and lysosomes increase as ELYSAs gradually disassemble at the 2-cell stage, leading to further acidification of endosomal-lysosomal organelles. These findings suggest that the ELYSA/ELVA maintain endosomal-lysosomal activity in a static state in oocytes for timely activation during early development.