Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. 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 genes, 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 macroalgae 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, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop 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 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.
Plant populations distributed along broad latitudinal gradients often show patterns of clinal variation in genotype and phenotype. Differences in photoperiod and temperature cues across latitudes ...influence major phenological events, such as timing of flowering or seed dormancy. Here, we used an array of 4,941 SNPs derived from 2b-RAD genotyping to characterize population differentiation and levels of genetic and genotypic diversity of three populations of the seagrass
along a latitudinal gradient extending across the Atlantic-Mediterranean boundary (i.e., Gran Canaria-Canary Islands, Faro-Portugal, and Ebro Delta-Spain). Our main goal was to search for potential outlier loci that could underlie adaptive differentiation of populations across the latitudinal distribution of the species. We hypothesized that such polymorphisms could be related to variation in photoperiod-temperature regime occurring across latitudes. The three populations were clearly differentiated and exhibited diverse levels of clonality and genetic diversity.
from the Mediterranean displayed the highest genotypic richness, while the Portuguese population had the highest clonality values. Gran Canaria exhibited the lowest genetic diversity (as observed heterozygosity). Nine SNPs were reliably identified as outliers across the three sites by two different methods (i.e., BayeScan and pcadapt), and three SNPs could be associated to specific protein-coding genes by screening available
transcriptomes. Two SNPs-carrying contigs encoded for transcription factors, while the other one encoded for an enzyme specifically involved in the regulation of flowering time, namely
. When analyzing biological processes enriched within the whole dataset of outlier SNPs identified by at least one method, "regulation of transcription" and "signalling" were among the most represented. Our results highlight the fundamental importance signal integration and gene-regulatory networks, as well as epigenetic regulation
DNA (de)methylation, could have for enabling adaptation of seagrass populations along environmental gradients.
Seagrass meadows provide important ecosystem services and are critical for the survival of the associated invertebrate community. However, they are threatened worldwide by human-driven environmental ...change. Understanding the seagrasses' potential for adaptation is critical to assess not only their ability to persist under future global change scenarios, but also to assess the persistence of the associated communities. Here we screened a wild population of Posidonia oceanica, an endemic long-lived seagrass in the Mediterranean Sea, for genes that may be target of environmental selection, using an outlier and a genome-wide transcriptome analysis. We identified loci where polymorphism or differential expression was associated with either a latitudinal or a bathymetric gradient, as well as with both gradients in an effort to identify loci associated with temperature and light. We found the candidate genes underlying growth and immunity to be divergent between populations adapted to different latitudes and/or depths, providing evidence for local adaptation. Furthermore, we found evidence of reduced gene flow among populations including adjacent populations. Reduced gene flow, combined with low sexual recombination, small effective population size, and long generation time of P. oceanica raises concerns for the long-term persistence of this species, especially in the face of rapid environmental change driven by human activities.
The endemic Mediterranean seagrass
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
plants from above and below the mean depth of the summer thermocline have differential resilience to heat.
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.
Circadian regulations are essential for enabling organisms to synchronize physiology with environmental light-dark cycles. Post-transcriptional RNA modifications still represent an understudied level ...of gene expression regulation in plants, although they could play crucial roles in environmental adaptation. N6-methyl-adenosine (m6A) is the most prevalent mRNA modification, established by “writer” and “eraser” proteins. It influences the clockwork in several taxa, but only few studies have been conducted in plants and none in marine plants. Here, we provided a first inventory of m6A-related genes in seagrasses and investigated daily changes in the global RNA methylation and transcript levels of writers and erasers in Cymodocea nodosa and Zostera marina. Both species showed methylation peaks during the dark period under the same photoperiod, despite exhibiting asynchronous changes in the m6A profile and related gene expression during a 24-h cycle. At contrasting latitudes, Z. marina populations displayed overlapping daily patterns of the m6A level and related gene expression. The observed rhythms are characteristic for each species and similar in populations of the same species with different photoperiods, suggesting the existence of an endogenous circadian control. Globally, our results indicate that m6A RNA methylation could widely contribute to circadian regulation in seagrasses, potentially affecting the photo-biological behaviour of these plants.
In the last three decades, quantitative approaches that rely on organism traits instead of taxonomy have advanced different fields of ecological research through establishing the mechanistic links ...between environmental drivers, functional traits, and ecosystem functions. A research subfield where trait-based approaches have been frequently used but poorly synthesized is the ecology of seagrasses; marine angiosperms that colonized the ocean 100M YA and today make up productive yet threatened coastal ecosystems globally. Here, we compiled a comprehensive trait-based response-effect framework (TBF) which builds on previous concepts and ideas, including the use of traits for the study of community assembly processes, from dispersal and response to abiotic and biotic factors, to ecosystem function and service provision. We then apply this framework to the global seagrass literature, using a systematic review to identify the strengths, gaps, and opportunities of the field. Seagrass trait research has mostly focused on the effect of environmental drivers on traits, i.e., "environmental filtering" (72%), whereas links between traits and functions are less common (26.9%). Despite the richness of trait-based data available, concepts related to TBFs are rare in the seagrass literature (15% of studies), including the relative importance of neutral and niche assembly processes, or the influence of trait dominance or complementarity in ecosystem function provision. These knowledge gaps indicate ample potential for further research, highlighting the need to understand the links between the unique traits of seagrasses and the ecosystem services they provide.
The circadian clock is an endogenous time-keeping mechanism that enables organisms to adapt to external environmental cycles. It produces rhythms of plant metabolism and physiology, and interacts ...with signaling pathways controlling daily and seasonal environmental responses through gene expression regulation. Downstream metabolic outputs, such as photosynthesis and sugar metabolism, besides being affected by the clock, can also contribute to the circadian timing itself. In marine plants, studies of circadian rhythms are still way behind in respect to terrestrial species, which strongly limits the understanding of how they coordinate their physiology and energetic metabolism with environmental signals at sea. Here, we provided a first description of daily timing of key core clock components and clock output pathways in two seagrass species,
Cymodocea nodosa
and
Zostera marina
(order
Alismatales
), co-occurring at the same geographic location, thus exposed to identical natural variations in photoperiod. Large differences were observed between species in the daily timing of accumulation of transcripts related to key metabolic pathways, such as photosynthesis and sucrose synthesis/transport, highlighting the importance of intrinsic biological, and likely ecological attributes of the species in determining the periodicity of functions. The two species exhibited a differential sensitivity to light-to-dark and dark-to-light transition times and could adopt different growth timing based on a differential strategy of resource allocation and mobilization throughout the day, possibly coordinated by the circadian clock. This behavior could potentially derive from divergent evolutionary adaptations of the species to their bio-geographical range of distributions.
Under unfavourable conditions, clonal plants benefit from physiological integration among ramets, sharing resources and information. Clonal integration can buffer against environmental changes and ...lets the plant clone work as a ‘macro’ organism. Molecular signals that regulate this phenomenon are completely unknown in marine plants.
Here we present a first comprehensive study providing insights into the metabolic role of different types of ramets (i.e. apical vs. vertical) in the foundation species Posidonia oceanica. Plants were exposed to 80% diminishing irradiance level (LL) in a controlled mesocosm system. Subsequent multiscale variations in whole transcriptome expression, global DNA methylation level, photo‐physiology, morphology and fitness‐related traits, were explored at different exposure times. We tested the hypothesis that vertical shoots (the ‘vassals’) can provide vital resources to apical shoots (the ‘kings’) under energy shortage, thus safeguarding the whole clone survival.
Whole transcriptome analysis of leaves and shoot‐apical meristems (SAMs) emphasized signatures of molecular integration among ramets, which strongly correlated with higher organization‐level responses. In both shoots types, the exposure to LL resulted in a growth slowdown throughout the experiment, which started from immediate signals in SAMs. In apical shoots, this was linked to an acclimative response, where they were suffering a mild stress condition, while in vertical ones it fell in a more severe stress response. Yet, they suffered from sugar starvation and showed a clear cellular stress response in terms of protein refolding and DNA repair mechanisms. Several epigenetic mechanisms modulated the observed gene‐expression patterns and the cross‐talk between DNA methylation and the cellular energetic status appeared to regulate shoot metabolism under LL.
Synthesis. Our results demonstrate a high level of specialization of integrated ramets within seagrass clones and a ‘division of labour’ under adverse conditions. Vertical shoots appear to do ‘most of the job’ especially in terms of resource providing, whereas activated functions in apical shoots were restricted to few important processes, according to an ‘energy‐saving’ strategy. The response of vertical shoots could be seen as a ‘sacrificing response’ allowing the survival of ‘the king’ that is key for ensuring propagation and population maintenance, and for the colonization of new environments.
Our results demonstrate a high level of specialization of integrated ramets within seagrass clones and a ‘division of labour’ under adverse conditions. Vertical shoots appear to do ‘most of the job’ especially in terms of resource providing, whereas activated functions in apical shoots were restricted to few important processes, according to an ‘energy‐saving’ strategy. The response of vertical shoots could be seen as a ‘sacrificing response’ allowing the survival of ‘the king’ that is key for ensuring propagation and population maintenance, and for the colonization of new environments.
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