The circadian clock controls temporal and spatial patterns of floral development in sunflower
- University of California, Davis, United States
- 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).
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Sunflower timelapse scoringDryad Digital Repository, doi:10.25338/B8865X.
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Sunflower pollinator visit scoringDryad Digital Repository, doi:10.25338/B86358.
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Sunflower consensus scoringDryad Digital Repository, doi:10.25338/B8963G.
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Sunflower ovary measurementsDryad Digital Repository, doi:10.25338/B8CW5R.
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Organ kinetics measurementsDryad Digital Repository, doi:10.25338/B8HP9F.
Article and author information
Author details
Veronica L Thompson
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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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
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Sunflowers need to keep track of time to develop and reproduce
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- Developmental Biology
Numerous reports showed that the epididymis plays key roles in the acquisition of sperm fertilizing ability but its contribution to embryo development remains less understood. Female mice mated with males with simultaneous mutations in Crisp1 and Crisp3 genes exhibited normal in vivo fertilization but impaired embryo development. In this work, we found that this phenotype was not due to delayed fertilization, and it was observed in eggs fertilized by epididymal sperm either in vivo or in vitro. Of note, eggs fertilized in vitro by mutant sperm displayed impaired meiotic resumption unrelated to Ca2+ oscillations defects during egg activation, supporting potential sperm DNA defects. Interestingly, cauda but not caput epididymal mutant sperm exhibited increased DNA fragmentation, revealing that DNA integrity defects appear during epididymal transit. Moreover, exposing control sperm to mutant epididymal fluid or to Ca2+-supplemented control fluid significantly increased DNA fragmentation. This, together with the higher intracellular Ca2+ levels detected in mutant sperm, supports a dysregulation in Ca2+ homeostasis within the epididymis and sperm as the main factor responsible for embryo development failure. These findings highlight the contribution of the epididymis beyond fertilization and identify CRISP1 and CRISP3 as novel factors essential for sperm DNA integrity and early embryo development.
