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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.

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.

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.

The present study examines for the first time the effects of increased salinity on water relations and osmolyte (carbohydrates and amino acids) concentrations in two Mediterranean seagrass species, Posidonia oceanica and Cymodocea nodosa , which are adapted to growth in environments with contrasting salinity and have a known differential sensitivity to alterations in ambient salinity. The specific aim was to obtain insights into their respective capacities to cope with natural or anthropogenically induced (e.g. desalination plants) hypersaline stress and its ecological implications. To this end, large plant fragments of both seagrass species were maintained for 47 days in a laboratory mesocosm system under ambient salinity (37 psu; control) and three chronic hypersaline conditions (39, 41 and 43 psu). Analyses of leaf-tissue osmolality indicated that both species followed a dehydration avoidance strategy, decreasing their leaf water potential (Ψ w ) as the external salinity increased, but using different physiological mechanisms: whereas P. oceanica leaves exhibited a reduction in osmotic potential (Ψ π ), C. nodosa leaves maintained osmotic stability through a decrease in turgor pressure (Ψ p ) probably mediated through cell-hardening processes. Accordingly, the concentrations of soluble sugars and some amino acids (mainly Pro and Gly) suggested the activation of osmoregulatory processes in P. oceanica leaves, but not in C. nodosa leaves. Osmotic adjustments probably interfered with leaf growth and shoot survival of P. oceanica under hypersaline stress, whereas C. nodosa showed a more efficient physiological capacity to maintain plant performance under the same experimental conditions. These results are consistent with the more euryhaline ecological behaviour of C. nodosa and contribute to understanding the high vulnerability shown by P. oceanica to even mild increments in seawater salinity.

The knowledge of how molecular functions vary in relation to developmental and environmental cues within and among seagrass leaves is scarce in comparison with terrestrial angiosperms. This strongly limits the mechanistic understanding of photosynthetic development and light acclimation processes in seagrasses, besides having fundamental methodological implications when small leaf sections are utilized as a proxy for assessing the photosynthetic performance and molecular responses to environmental changes for the whole plant. Here, the expression gradients of genes associated with key plant metabolic processes (i.e. photosynthesis, energy dissipation mechanisms, stress response and programmed cell death) were determined, for the first time, in three segments (i.e. basal, medium and high) along the longitudinal axis of three ranked leaves (i.e. leaf 1, 2 and 3) in the large-sized seagrass Posidonia oceanica. The evaluation of major shifts in gene expression paralleled the analysis of photo-physiological properties and global DNA methylation level of the different leaf sections. Photo-physiological and molecular results converged in suggesting that the within-leaf (vertical) gradient was stronger than the leaf-rank (horizontal) gradient, likely reflecting the sharp irradiance attenuation occurring inside the complex canopy formed by this species. Specific correlations between target gene expression and photo-physiological measurements were found, providing a first description of molecular rearrangements underlying the differential photosynthetic performance and light acclimation capacity of seagrass leaves. DNA methylation varied with tissue age, being higher in the youngest and oldest leaf sections, while decreasing in intermediate tissues. We interpreted such changes as a consequence of the interplay between developmental and light cues.

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.

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.

Marine Heat Waves (MHWs) occurrence has been increasing in the Mediterranean Sea. The effects of field simulated MHWs of different intensity (medium and high temperature) on the transcriptome expression of the endemic seagrass Posidonia oceanica were evaluated considering different origins of the plant. The aim of the study was reached through a common garden transplant experiment in the North-west of Sardinia (Italy), where two P. oceanica meadows characterized by different thermal regimes (cold and warm) were chosen. MHWs were simulated in front of a power plant, that creates a natural laboratory by releasing warm water in the sea. Differential gene expression and GO enrichment analyses highlighted differences in the transcriptomic profiles of plants from cold and warm environments suggesting that the MHWs induced different levels of stress due to different tolerance to the heat event. Plants from both origins activated processes to achieve protein homeostasis, but only cold plants activated an antioxidant defense and altered sugar metabolism, both indicators of heat stress. Within plants of the same origin, a different response to MHW intensity was also detected: while warm plants showed the most complex response at high temperature rather than at medium temperature, cold plants seemed to better cope with the medium temperature intensity rather than with high temperature.

Seagrasses are key marine foundation species, currently declining due to the compounded action of global and regional anthropogenic stressors. Eutrophication has been associated with seagrass decline, while grazing has been traditionally considered to be a natural disturbance with a relatively low impact on seagrasses. In the recent years, this assumption has been revisited. Here, by means of a 16-month field-experiment, we investigated the molecular mechanisms driving the long-term response of Posidonia oceanica to the combination of nutrient enrichment, either as a chronic (press) or pulse disturbance, and herbivory. Changes in expression levels of 19 target genes involved in key steps of photosynthesis, nutrient assimilation, chlorophyll metabolism, oxidative-stress response and plant defense were evaluated through reverse transcription–quantitative polymerase chain reaction (RT-qPCR). High herbivore pressure affected the molecular response of P. oceanica more dramatically than did enhanced nutrient levels, altering the expression of genes involved in plant tolerance and resistance traits, such as photosynthesis and defense mechanisms. Genes involved in carbon fixation and N assimilation modulated the response of plants to high nutrient levels. Availability of resources seems to modify P. oceanica response to herbivory, where the upregulation of a nitrate transporter gene was accompanied by the decline in the expression of nitrate reductase in the leaves, suggesting a change in plant-nutrient allocation strategy. Finally, press and pulse fertilizations altered nitrate uptake and reduction-related genes in opposite ways, suggesting that taking into account the temporal regime of nutrient loading is important to assess the physiological response of seagrasses to eutrophication.

This study was funded by the project Marine habitats restoration in a climate change-impaired Mediterranean Sea (MAHRES), funded by the Italian Ministry of Research under the PRIN 2017 Program (Project N. 2017MHHWBN; CUP: 74I19001320001); by PON—National Operational Programme Research and Innovation 2014–2020 - PhDs and research contracts on innovation-related topics; and by the European Union Next-Generation EU (PIANO NAZIONALE DI RIPRESA E RESILIENZA (PNRR) – MISSIONE 4 COMPONENTE 2, “Dalla ricerca all’impresa” INVESTIMENTO 1.4 – D.D. 1034 17/06/2022, CN00000033). We acknowledge the European Union’s Horizon Europe Research and Innovation Programme ACTNOW, grant agreement N. 101060072. This manuscript reflects only the authors’ views and opinions, neither the European Union nor the European Commission can be considered responsible for them.