Depth-specific fluctuations of gene expression and protein abundance modulate the photophysiology in the seagrass Posidonia oceanica

Gabriele Procaccini,Mats Björk,Martin Gullström,Irene Olivé,João Silva,Lázaro Marín-Guirao,Daniela D’Esposito,Sven Beer,Chiara Lauritano,Letizia Bernardo,Christophe Brunet,Silvia Mazzuca,Pimchanok Buapet,Sylvie Gobert,Miriam Ruocco,Monya M Costa,Paulo Felisberto,John W Runcie,Emanuela Dattolo,Amalia Piro,Lina M Rasmusson,Isabel Barrote,Ilia Anna Serra,Rui Santos

doi:10.1038/srep42890

Abstract

Here we present the results of a multiple organizational level analysis conceived to identify acclimative/adaptive strategies exhibited by the seagrass Posidonia oceanica to the daily fluctuations in the light environment, at contrasting depths. We assessed changes in photophysiological parameters, leaf respiration, pigments, and protein and mRNA expression levels. The results show that the diel oscillations of P. oceanica photophysiological and respiratory responses were related to transcripts and proteins expression of the genes involved in those processes and that there was a response asynchrony between shallow and deep plants probably caused by the strong differences in the light environment. The photochemical pathway of energy use was more effective in shallow plants due to higher light availability, but these plants needed more investment in photoprotection and photorepair, requiring higher translation and protein synthesis than deep plants. The genetic differentiation between deep and shallow stands suggests the existence of locally adapted genotypes to contrasting light environments. The depth-specific diel rhythms of photosynthetic and respiratory processes, from molecular to physiological levels, must be considered in the management and conservation of these key coastal ecosystems.

Highlights

Functional groups of proteins have been reported, including down-regulation of the Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (RuBisCO) large subunit and modification of the PSI/PSII ratio[12]
Our results revealed for the first time that diel oscillation of P. oceanica photophysiological and respiratory responses were related to transcriptional responses and protein expression of the genes involved in those processes, and that there was a response asynchrony between shallow and deep plants, probably due to strong differences in the light environment
The non-photochemical quenching (NPQ) induction, the decrease in photochemical efficiency and the upregulation of the photoprotective genes observed both in shallow and deep plants of P. oceanica during high-light hours suggest the triggering of energy dissipation mechanisms such as the xanthophyll cycle[29]

Summary

Introduction

Functional groups of proteins have been reported, including down-regulation of the Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (RuBisCO) large subunit and modification of the PSI/PSII ratio[12]. According to daily variation in irradiance levels, seagrasses, like their terrestrial counterparts, maintain a permanent and dynamic trade-off between photosynthetic efficiency and photoprotection through so-called dynamic photoinhibition[27] It is not known whether and how this reversible regulation of photosynthesis is driven by internal circadian cycles, allowing the species to anticipate upcoming light patterns (i.e. seasonally or daily), or is regulated by environmental cues. Together with a companion study (in preparation), performed at the same time, which focuses on how plant photosynthetic production is conveyed to higher organizational levels of community and ecosystem production, we provide the first comprehensive, multilevel approach of the functional responses of a seagrass ecosystem to the daily irradiance cycle at different depths. Our results represent an important source of information on the adaptive strategies used by this species, in response to variations in light, and provide a better understanding of the overall functioning of P. oceanica meadows

Methods

Results

Conclusion