Seagrasses colonized the sea¹ on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet². Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes³, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae⁴ and that is important for ion homoeostasis, nutrient uptake and O₂/CO₂ exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming^5,6, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants⁷.

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 heat-acclimation 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.

Seagrasses are marine flowering plants providing key ecological services and functions in coasts and estuaries across the globe. Increased environmental changes fueled by human activities are affecting their existence, compromising natural habitats and ecosystems’ biodiversity and functioning. In this context, restoration of disturbed seagrass environments has become a worldwide priority to reverse ecosystem degradation and to recover ecosystem functionality and associated services. Despite the proven importance of genetic research to perform successful restoration projects, this aspect has often been overlooked in seagrass restoration. Here, we aimed to provide a comprehensive perspective of genetic aspects related to seagrass restoration. To this end, we first reviewed the importance of studying the genetic diversity and population structure of target seagrass populations; then, we discussed the pros and cons of different approaches used to restore and/or reinforce degraded populations. In general, the collection of genetic information and the development of connectivity maps are critical steps for any seagrass restoration activity. Traditionally, the selection of donor population preferred the use of local gene pools, thought to be the best adapted to current conditions. However, in the face of rapid ocean changes, alternative approaches such as the use of climate-adjusted or admixture genotypes might provide more sustainable options to secure the survival of restored meadows. Also, we discussed different transplantation strategies applied in seagrasses and emphasized the importance of long-term seagrass monitoring in restoration. The newly developed information on epigenetics as well as the application of assisted evolution strategies were also explored. Finally, a view of legal and ethical issues related to national and international restoration management is included, highlighting improvements and potential new directions to integrate with the genetic assessment. We concluded that a good restoration effort should incorporate: (1) a good understanding of the genetic structure of both donors and populations being restored; (2) the analysis of local environmental conditions and disturbances that affect the site to be restored; (3) the analysis of local adaptation constraints influencing the performances of donor populations and native plants; (4) the integration of distribution/connectivity maps with genetic information and environmental factors relative to the target seagrass populations; (5) the planning of long-term monitoring programs to assess the performance of the restored populations. The inclusion of epigenetic knowledge and the development of assisted evolution programs are strongly hoped for the future.

The endemic Mediterranean seagrass Posidonia oceanica is highly threatened by the increased frequency and intensity of heatwaves. Meadows of the species offer a unique opportunity to unravel mechanisms marine plants activate to cope transient warming, since their wide depth distribution impose divergent heat-tolerance. Understanding these mechanisms is imperative for their conservation. Shallow and deep genotypes within the same population were exposed to a simulated heatwave in mesocosms, to analyze their transcriptomic and photo-physiological responses during and after the exposure. Shallow plants, living in a more unstable thermal environment, optimized phenotype variation in response to warming. These plants showed a pre-adaptation of genes in anticipation of stress. Shallow plants also showed a stronger activation of heat-responsive genes and the exclusive activation of genes involved in epigenetic mechanisms and in molecular mechanisms that are behind their higher photosynthetic stability and respiratory acclimation. Deep plants experienced higher heat-induced damage and activated metabolic processes for obtaining extra energy from sugars and amino acids, likely to support the higher protein turnover induced by heat. In this study we identify transcriptomic mechanisms that may facilitate persistence of seagrasses to anomalous warming events and we discovered that P. oceanica plants from above and below the mean depth of the summer thermocline have differential resilience to heat.

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.