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

Abstract
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Article and author information
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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

Carine M Marshall

Department of Plant Biology, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.
Veronica L Thompson

Department of Plant Biology, University of California, Davis, Davis, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-0500-5639
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.

"This ORCID iD identifies the author of this article:" 0000-0002-4179-6995
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.

"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

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.