Daily Regulation of Key Metabolic Pathways in Two Seagrasses Under Natural Light Conditions

Miriam Ruocco,Katia Pes,Isabel Barrote,Emanuela Dattolo,Jan Dirk Hofman,Gabriele Procaccini,Monya M Costa,João Silva

doi:10.3389/fevo.2021.757187

Abstract

The circadian clock is an endogenous time-keeping mechanism that enables organisms to adapt to external environmental cycles. It produces rhythms of plant metabolism and physiology, and interacts with signaling pathways controlling daily and seasonal environmental responses through gene expression regulation. Downstream metabolic outputs, such as photosynthesis and sugar metabolism, besides being affected by the clock, can also contribute to the circadian timing itself. In marine plants, studies of circadian rhythms are still way behind in respect to terrestrial species, which strongly limits the understanding of how they coordinate their physiology and energetic metabolism with environmental signals at sea. Here, we provided a first description of daily timing of key core clock components and clock output pathways in two seagrass species, Cymodocea nodosa and Zostera marina (order Alismatales), co-occurring at the same geographic location, thus exposed to identical natural variations in photoperiod. Large differences were observed between species in the daily timing of accumulation of transcripts related to key metabolic pathways, such as photosynthesis and sucrose synthesis/transport, highlighting the importance of intrinsic biological, and likely ecological attributes of the species in determining the periodicity of functions. The two species exhibited a differential sensitivity to light-to-dark and dark-to-light transition times and could adopt different growth timing based on a differential strategy of resource allocation and mobilization throughout the day, possibly coordinated by the circadian clock. This behavior could potentially derive from divergent evolutionary adaptations of the species to their bio-geographical range of distributions.

Highlights

Earth’s rotation causes repetitive changes of day and night that are reflected in diurnal cycles of light and temperature
In C. nodosa, both approaches identified two main groups: a first including dawn, sunrise and solar noon samples and a second comprising sunset, dusk, and midnight samples (Figure 1A). Transcripts responsible for such separation are highlighted in the principal component analysis (PCA) biplot and their weightings are outlined in Supplementary Table 4
General Overview of Daily Timing in Cymodocea nodosa and Zostera marina Here, we provided a first description of daily regulation of key pathways in two seagrass species, C. nodosa and Z. marina, co-occurring at the same geographic location, exposed to identical natural variations in light and temperature

Summary

Introduction

Earth’s rotation causes repetitive changes of day and night that are reflected in diurnal cycles of light and temperature. Most living organisms experience these changes and face the challenge of coordinating their lives with such rhythms. This was the primary driver for the emergence and evolution of endogenous clocks that can be set by the rising or the setting of the sun (McWatters and Devlin, 2011). Circadian clocks regulate many aspects of physiology, growth, development and reproduction (Harmer et al, 2000; Harmer, 2009). These produce daily rhythms of metabolism, Daily Timing in Marine Plants and interact with signaling pathways controlling daily environmental responses (Dodd et al, 2015; Kim et al, 2017). Circadian clocks allow plants to anticipate daily and seasonal changes in the environment, conferring them an adaptive advantage (Ouyang et al, 1998)

Methods

Results

Conclusion