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

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...

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Autores principales: Marshall, Carine M, Thompson, Veronica L, Creux, Nicky M, Harmer, Stacey L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9977281/
https://www.ncbi.nlm.nih.gov/pubmed/36637156
http://dx.doi.org/10.7554/eLife.80984
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author Marshall, Carine M
Thompson, Veronica L
Creux, Nicky M
Harmer, Stacey L
author_facet Marshall, Carine M
Thompson, Veronica L
Creux, Nicky M
Harmer, Stacey L
author_sort Marshall, Carine M
collection PubMed
description 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.
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spelling pubmed-99772812023-03-02 The circadian clock controls temporal and spatial patterns of floral development in sunflower Marshall, Carine M Thompson, Veronica L Creux, Nicky M Harmer, Stacey L eLife Developmental Biology 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. eLife Sciences Publications, Ltd 2023-01-13 /pmc/articles/PMC9977281/ /pubmed/36637156 http://dx.doi.org/10.7554/eLife.80984 Text en © 2023, Marshall et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Marshall, Carine M
Thompson, Veronica L
Creux, Nicky M
Harmer, Stacey L
The circadian clock controls temporal and spatial patterns of floral development in sunflower
title The circadian clock controls temporal and spatial patterns of floral development in sunflower
title_full The circadian clock controls temporal and spatial patterns of floral development in sunflower
title_fullStr The circadian clock controls temporal and spatial patterns of floral development in sunflower
title_full_unstemmed The circadian clock controls temporal and spatial patterns of floral development in sunflower
title_short The circadian clock controls temporal and spatial patterns of floral development in sunflower
title_sort circadian clock controls temporal and spatial patterns of floral development in sunflower
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9977281/
https://www.ncbi.nlm.nih.gov/pubmed/36637156
http://dx.doi.org/10.7554/eLife.80984
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