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

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.

Development and evolution of the Asteraceae capitulum

“…Interestingly, while the initiation of florets in a capitulum occurs in Fibonacci spirals, the final stages of their maturation, that is the timing of anthesis, occur in discrete, ring-like pseudowhorls (Marshall et al, 2023). The recent study by Marshall et al (2023) in sunflower shows how the timing of floret opening is controlled by the circadian clock with each whorl of florets undergoing anthesis on successive days.…”

“…Interestingly, while the initiation of florets in a capitulum occurs in Fibonacci spirals, the final stages of their maturation, that is the timing of anthesis, occur in discrete, ring-like pseudowhorls (Marshall et al, 2023). The recent study by Marshall et al (2023) in sunflower shows how the timing of floret opening is controlled by the circadian clock with each whorl of florets undergoing anthesis on successive days. When the circadian oscillator was disrupted under constant light conditions or distinct temperature cycles, the coordination of floret maturation in pseudowhorls was lost, and in fact, the florets aged continuously along the spirals (Marshall et al, 2023).…”

“…The recent study by Marshall et al (2023) in sunflower shows how the timing of floret opening is controlled by the circadian clock with each whorl of florets undergoing anthesis on successive days. When the circadian oscillator was disrupted under constant light conditions or distinct temperature cycles, the coordination of floret maturation in pseudowhorls was lost, and in fact, the florets aged continuously along the spirals (Marshall et al, 2023). Fast and synchronous maturation in pseudowhorls, rather than spirals, was shown to increase pollinator visits, showing the importance of the phenomenon for efficient reproduction (Marshall et al, 2023).…”

“…In Asteraceae, efficient reproduction relies on secondary pollen presentation that is a characteristic and ancestral feature of the whole family (Jeffrey, 2009), and strictly coordinated by the daily rhythm to prevent selfing (Baroncelli et al ., 1990; Marshall et al ., 2023). Pollen presentation occurs through a plunger‐style mechanism that separates pollen release and stigma presentation temporally and spatially.…”

“…Interestingly, while the initiation of florets in a capitulum occurs in Fibonacci spirals, the final stages of their maturation, that is the timing of anthesis, occur in discrete, ring‐like pseudowhorls (Marshall et al ., 2023). The recent study by Marshall et al .…”