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Coastal oceans are particularly affected by rapid and extreme environmental changes with dramatic consequences for the entire ecosystem. Seagrasses are key ecosystem engineering or foundation species supporting diverse and productive ecosystems along the coastline that are particularly susceptible to fast environmental changes. In this context, the analysis of phenotypic plasticity could reveal important insights into seagrasses persistence, as it represents an individual property that allows species’ phenotypes to accommodate and react to fast environmental changes and stress. Many studies have provided different definitions of plasticity and related processes (acclimation and adaptation) resulting in a variety of associated terminology. Here, we review different ways to define phenotypic plasticity with particular reference to seagrass responses to single and multiple stressors. We relate plasticity to the shape of reaction norms, resulting from genotype by environment interactions, and examine its role in the presence of environmental shifts. The potential role of genetic and epigenetic changes in underlying seagrasses plasticity in face of environmental changes is also discussed. Different approaches aimed to assess local acclimation and adaptation in seagrasses are explored, explaining strengths and weaknesses based on the main results obtained from the most recent literature. We conclude that the implemented experimental approaches, whether performed with controlled or field experiments, provide new insights to explore the basis of plasticity in seagrasses. However, an improvement of molecular analysis and the application of multi‐factorial experiments are required to better explore genetic and epigenetic adjustments to rapid environmental shifts. These considerations revealed the potential for selecting the best phenotypes to promote assisted evolution with fundamental implications on restoration and preservation efforts.

The role of DNA methylation and its interaction with gene expression and transcriptome plasticity is poorly understood, and current insight comes mainly from studies in very few model plant species. Here, we study gene body DNA methylation (gbM) and gene expression patterns in ecotypes from contrasting thermal environments of two marine plants with contrasting life history strategies in order to explore the potential role epigenetic mechanisms could play in gene plasticity and responsiveness to heat stress. In silico transcriptome analysis of CpGO/E ratios suggested that the bulk of Posidonia oceanica and Cymodocea nodosa genes possess high levels of intragenic methylation. We also observed a correlation between gbM and gene expression flexibility: genes with low DNA methylation tend to show flexible gene expression and plasticity under changing conditions. Furthermore, the empirical determination of global DNA methylation (5-mC) showed patterns of intra and inter-specific divergence that suggests a link between methylation level and the plants’ latitude of origin and life history. Although we cannot discern whether gbM regulates gene expression or vice versa, or if other molecular mechanisms play a role in facilitating transcriptome responsiveness, our findings point to the existence of a relationship between gene responsiveness and gbM patterns in marine plants.

While thermal priming and the relative role of epigenetic modifications have been widely studied in terrestrial plants, their roles remain unexplored in seagrasses so far. Here, we experimentally compared the ability of two different functional types of seagrass species, dominant in the Southern hemisphere, climax species and pioneer species , to acquire thermal-stress memory to better survive successive stressful thermal events. To this end, a two-heatwave experimental design was conducted in a mesocosm setup. Findings across levels of biological organization including the molecular (gene expression), physiological (photosynthetic performances and pigments content) and organismal (growth) levels provided the first evidence of thermal priming in seagrasses. Non-preheated plants suffered a significant reduction in photosynthetic capacity, leaf growth and chlorophyll content, while preheated plants were able to cope better with the recurrent stressful event. Gene expression results demonstrated significant regulation of methylation-related genes in response to thermal stress, suggesting that epigenetic modifications could play a central role in seagrass thermal stress memory. In addition, we revealed some interspecific differences in thermal responses between the two different functional types of seagrass species. These results provide the first insights into thermal priming and relative epigenetic modifications in seagrasses paving the way for more comprehensive forecasting and management of thermal stress in these marine foundation species in an era of rapid environmental change.

During the last 150 years, the tropical seagrass species Halophila stipulacea has established itself in the southern and eastern parts of the Mediterranean Sea. More recently (2018), Halophila decipiens was observed for the first time in the eastern Mediterranean, and was described as the second non-native seagrass species in the Mediterranean Sea. We implemented a species distribution model (SDM) approach to (1) hindcast the habitat suitability of H. stipulacea over the last 100 years in the Mediterranean basin, and (2) to model the increase in the potential habitat suitability of H. stipulacea and H. decipiens during the current century under two very different climate scenarios, RCP 2.6 (lowest carbon emission scenario) and RCP 8.5 (highest carbon emission scenario). In addition, a principal component analysis (PCA) and k -means cluster based on temperature and salinity drivers were applied to visualize the distance and relatedness between the native and invasive H. stipulacea and H. decipiens populations. Results from this PCA suggest that the H. stipulacea populations of the Mediterranean and Red Sea are likely to be similar. In contrast, H. decipiens from the Mediterranean is more related to the Atlantic populations rather than to the Red Sea populations. The hindcast model suggests that the expansion of H. stipulacea was related to the increases in seawater temperatures in the Mediterranean over the last 100 years. The SDMs predict that more suitable habitat will become available for both tropical species during this century. The habitat suitability for H. stipulacea will keep expanding westward and northward as the Mediterranean continues to become saltier and warmer. In comparison, the SDMs built for H. decipiens forecast a restricted habitat suitability in the south-eastern Mediterranean Sea at the present environmental conditions and predicts a progressive expansion with a potential increase in habitat suitability along 85% of the Mediterranean coastline. The predicted rapid expansion of non-native seagrass species could alter the Mediterranean’s seagrass community and may entail massive impacts on associated ecosystem functions and services, impacts that have severe socio-economic consequences.

The increase in extreme heat events associated to global warming threatens seagrass ecosystems, likely by affecting key plant physiological processes such as photosynthesis and respiration. Understanding species’ ability to acclimate to warming is crucial to better predict their future trends. Here, we study tolerance to warming in two key Mediterranean seagrasses, Posidonia oceanica and Cymodocea nodosa. Stress responses of shallow and deep plants were followed during and after short-term heat exposure in mesocosms by coupling photo-physiological measures with analysis of expression of photosynthesis and stress-related genes. Contrasting tolerance and capacity to heat acclimation were shown by shallow and deep P. oceanica ecotypes. While shallow plants acclimated through respiratory homeostasis and activation of photo-protective mechanisms, deep ones experienced photosynthetic injury and impaired carbon balance. This suggests that P. oceanica ecotypes are thermally adapted to local conditions and that Mediterranean warming will likely diversely affect deep and shallow meadow stands. On the other hand, contrasting mechanisms of heatacclimation were adopted by the two species. P. oceanica regulates photosynthesis and respiration at the level of control plants while C. nodosa balances both processes at enhanced rates. These acclimation discrepancies are discussed in relation to inherent attributes of the two species.

The common octopus, Octopus vulgaris Cuvier 1797, is a largely exploited cephalopod species in the Mediterranean Sea and the Atlantic Ocean, as well as along the coasts of Africa, Brazil and Japan, where its taxonomic identity is still debated. The assessment of its genetic structure is a pressing need to correctly manage the resource and to avoid overfishing and collapsing of local stocks. Here we analysed genetic variation and population structure of O. vulgaris using thirteen microsatellite loci in seven sampling localities from the Mediterranean Sea and one from the Atlantic Ocean. We also used a DNA barcoding approach by COI gene fragment to understand the phylogenetic relationships among the specimens here investigated and the ones whose sequences are available in literature. Our results reveal high levels of allelic richness and moderate heterozygosity in all samples investigated, and a pronounced differentiation of the Atlantic and Sicilian specimens. This latter aspect seems to support the isolation of the biota within the Strait of Messina. A certain degree of differentiation was detected among the other geographic samples within the Mediterranean Sea, which is more compatible with an island model than isolation by distance. The occurrence of null alleles affected more genetic diversity indices than population structure estimations. This study provides new insights about the genetic diversity and structure of O. vulgaris in the area of interest, which can be used as guidelines for a fisheries management perspective.

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. Here, we investigated how an intense warming event affects molecular and photo-physiological functions in the large-sized seagrass , 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. 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. 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.

Diatoms are key phytoplankton organisms and one of the main primary producers in aquatic ecosystems. However, many diatom species produce a series of secondary metabolites, collectively termed oxylipins, that disrupt development in the offspring of grazers, such as copepods, that feed on these unicellular algae. We hypothesized that different populations of copepods may deal differently with the same oxylipin-producing diatom diet. Here we provide comparative studies of expression level analyses of selected genes of interest for three Calanus helgolandicus populations (North Sea, Atlantic Ocean and Mediterranean Sea) exposed to the same strain of the oxylipin-producing diatom Skeletonema marinoi using as control algae the flagellate Rhodomonas baltica. Expression levels of detoxification enzymes and stress proteins (e.g. glutathione S-transferase, glutathione synthase, superoxide dismutase, catalase, aldehyde dehydrogenases and heat shock proteins) and proteins involved in apoptosis regulation and cell cycle progression were analyzed in copepods after both 24 and 48 hours of feeding on the diatom or on a control diet. Strong differences occurred among copepod populations, with the Mediterranean population of C. helgolandicus being more susceptible to the toxic diet compared to the others. This study opens new perspectives for understanding copepod population-specific responses to diatom toxins and may help in underpinning the cellular mechanisms underlying copepod toxicity during diatom blooms.

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.

A better understanding of species and population responses to thermal stress is critical to predict changes in their distribution under warming scenarios. Seagrasses are a unique group of marine plants that play fundamental roles in marine environments and provide vital ecosystem services. Nevertheless, previous studies on seagrass thermal tolerance have focused exclusively on a handful of species, with the majority of these remaining virtually unexplored. Moreover, to date, no study has compared the response to thermal stress between northern and southern hemisphere seagrasses. Here, we conducted comparative mesocosm experiments using four seagrass species from the northern (i.e. Mediterranean: Posidonia oceanica, Cymodocea nodosa) and southern (i.e. Australia: Posidonia australis and Zostera muelleri) hemisphere as representative of two different life strategies, i.e. climax (P. oceanica, P. australis) and pioneer (C. nodosa, Z. muelleri). Plants acclimatized to the mesocosm conditions at ambient temperature (i.e. 26 °C) during a 5-week period, were exposed to a simulated marine heatwave (i.e. 32 °C) for 2 weeks. Measurements of plant responses, including photo-physiology, morphology, and pigment content, were performed at the end of the warming exposure. Results showed that warming had no significant effects on photosynthetic performances of northern hemisphere seagrasses while negatively impacted their southern hemisphere counterparts. Similarly, warming favored the growth of northern hemisphere plants, but strongly inhibited the development of southern hemisphere species. Furthermore, photo-physiological and pigment content results suggested pioneer seagrasses better dealt with warming than climax species. Our study provides more insights into the field of seagrass ecology and yields potential implication for future seagrass conservation and restoration activities.