Seagrass meadows are disappearing at rates comparable to those reported for mangroves, coral reefs, and tropical rainforests. One of the main causes of their decline is the so-called cultural eutrophication, i.e., the input of abnormal amounts of nutrients derived from human activities. Besides the impact of eutrophication at a local scale, the occurrence of additional stress factors such as global sea warming may create synergisms in detriment of seagrass meadows’ health. In the present study, we aimed to evaluate if plants undergoing chronic cultural eutrophication and plants growing in relatively pristine waters are more (or less) sensitive to heat stress, nutrient load and the combination of both stressors. To address this question, a mesocosm experiment was conducted using Posidonia oceanica collected from two environments with different nutrients load history. Plants were exposed in controlled conditions to high nutrient concentrations, increased temperature and their combination for 5 weeks, to assess the effect of the single stressors and their interaction. Our results revealed that plants experiencing chronic cultural eutrophication (EU) are more sensitive to further exposure to multiple stressors than plants growing in oligotrophic habitats (OL). OL and EU plants showed different morphological traits and physiological performances, which corroborates the role of local pressures in activating different strategies in response to global environmental changes. EU-plants appeared to be weaker during the treatments, showing the greatest percentage of mortality, particularly under increased temperature. Temperature and nutrient treatments showed opposite effects when tested individually and an offset response when combined. The activation of physiological strategies with high energetic expenses to cope with excess of nutrients and other stressors, could affect plants present and future persistence, particularly under eutrophic conditions. Our results represent a step forward in understanding the complex interactions that occur in natural environments. Moreover, unraveling intraspecific strategies and the role of local acclimation/adaptation in response to multiple stressors could be crucial for seagrass conservation strategies under a climate change scenario.

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.

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Introduction: Gene-expression patterns and their upstream regulatory mechanisms (e.g. epigenetic) are known to modulate plant acclimatability and thus tolerance to heat stress. Within species, thermal plasticity (i.e. temperature-sensitive phenotypic plasticity) and differential thermo-tolerance are recognized among different genotypes, development stages, organs or tissues. Leaf age and lifespan have been demonstrated to strongly affect photosynthetic thermo-tolerance in terrestrial species, whereas there is no information available for marine plants. Materials and Methods: Here, we investigated how an intense warming event affects molecular and photo-physiological functions in the large-sized seagrass Posidonia oceanica, at fine spatial resolution. Plants were exposed for one week at 34°C in a controlled-mesocosm system. Subsequent variations in the expression of 12 target genes and global DNA methylation level were evaluated in three leaf-age sections (i.e. basal, medium and high) established along the longitudinal axis of youngest, young and fully mature leaves of the shoot. Targeted genes were involved in photosynthesis, chlorophyll biosynthesis, energy dissipation mechanisms, stress response and programmed cell death. Molecular analyses paralleled the assessment of pigment content and photosynthetic performance of the same leaf segments, as well as of plant growth inhibition under acute warming. Results: Our data revealed, for the first time, the presence of variable leaf age-dependent stress-induced epigenetic and gene-expression changes in seagrasses, underlying photo-physiological and growth responses to heat stress. An investment in protective responses and growth arrest was observed in immature tissues; while mature leaf sections displayed a higher ability to offset gene down-regulation, possibly through the involvement of DNA methylation changes, although heat-induced damages were visible at photo-physiological level. Discussion: Overall, mature and young leaf tissues exhibited different strategies to withstand heat stress and thus a variable thermal plasticity. This should be taken in consideration when addressing seagrass response to warming and other stressors, especially in large-sized species, where sharp age differences are present within and among leaves, and other gradients of environmental factors (e.g. light) could be at play. Molecular and physiological evaluations conducted only on adult leaf tissues, as common practice in seagrass research, could give inadequate estimates of the overall plant state, and should not be considered as a proxy for the whole shoot.

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