ABSTRACT
Heat-priming improves plants' tolerance to a recurring heat stress event. The underlying molecular mechanisms of heat-priming are largely unknown in seagrasses. Here, ad hoc mesocosm experiments were conducted with two Mediterranean seagrass species, Posidonia oceanica and Cymodocea nodosa. Plants were first exposed to heat-priming, followed by a heat-triggering event. A comprehensive assessment of plant stress response across different levels of biological organization was performed at the end of the triggering event. Morphological and physiological results showed an improved response of heat-primed P. oceanica plants while in C. nodosa both heat- and non-primed plants enhanced their growth rates at the end of the triggering event. As resulting from whole transcriptome sequencing, molecular functions related to several cellular compartments and processes were involved in the response to warming of non-primed plants, while the response of heat-primed plants involved a limited group of processes. Our results suggest that seagrasses acquire a primed state during the priming event, that eventually gives plants the ability to induce a more energy-effective response when the thermal stress event recurs. Different species may differ in their ability to perform an improved heat stress response after priming. This study provides pioneer molecular insights into the emerging topic of seagrass stress priming and may benefit future studies in the field.
Subject(s)
Alismatales , Transcriptome , Alismatales/genetics , Alismatales/metabolism , Transcriptome/genetics , Species Specificity , Heat-Shock Response/genetics , Heat-Shock Response/physiology , Gene Expression Regulation, Plant , Mediterranean Sea , Hot TemperatureABSTRACT
The surfgrass Phyllospadix scouleri grows in highly productive meadows along the Pacific coast of North America. This region has experienced increasingly severe marine heatwaves (MHWs) in recent years. Our study evaluated the impact of consecutive MHWs, simulated in mesocosms, on essential ecophysiological features of P. scouleri. Overall, our findings show that the plants' overall physiological status has been progressively declining. Interestingly, the indicators of physiological stress in photosynthesis only showed up once the initial heat exposure stopped (i.e., during the recovery period). The warming caused increased oxidative damage and a decrease in nitrate uptake rates. However, the levels of non-structural carbohydrates and relative growth rates were not affected. Our findings emphasize the significance of incorporating recovery periods in this type of study as they expose delayed stress responses. Furthermore, experiencing consecutive intense MHWs can harm surfgrasses over time, compromising the health of their meadows and the services they offer to the ecosystem.
Subject(s)
Ecosystem , Zosteraceae , Stress, Physiological , Photosynthesis , CarbohydratesABSTRACT
We present chromosome-level genome assemblies from representative species of three independently evolved seagrass lineages: Posidonia oceanica, Cymodocea nodosa, Thalassia testudinum and Zostera marina. We also include a draft genome of Potamogeton acutifolius, belonging to a freshwater sister lineage to Zosteraceae. All seagrass species share an ancient whole-genome triplication, while additional whole-genome duplications were uncovered for C. nodosa, Z. marina and P. acutifolius. Comparative analysis of selected gene families suggests that the transition from submerged-freshwater to submerged-marine environments mainly involved fine-tuning of multiple processes (such as osmoregulation, salinity, light capture, carbon acquisition and temperature) that all had to happen in parallel, probably explaining why adaptation to a marine lifestyle has been exceedingly rare. Major gene losses related to stomata, volatiles, defence and lignification are probably a consequence of the return to the sea rather than the cause of it. These new genomes will accelerate functional studies and solutions, as continuing losses of the 'savannahs of the sea' are of major concern in times of climate change and loss of biodiversity.
Subject(s)
Alismatales , Zosteraceae , Alismatales/genetics , Zosteraceae/genetics , EcosystemABSTRACT
Desalination has been proposed as a global strategy for tackling freshwater shortage in the climate change era. However, there is a concern regarding the environmental effects of high salinity brines discharged from desalination plants on benthic communities. In this context, seagrasses such as the Mediterranean endemic and ecologically important Posidonia oceanica have shown high vulnerability to elevated salinities. Most ecotoxicological studies regarding desalination effects are based on salinity increments using artificial sea salts, although it has been postulated that certain additives within the industrial process of desalination may exacerbate a negative impact beyond just the increased salinities of the brine. To assess the potential effect of whole effluent brines on P. oceanica, mesocosm experiments were conducted within 10 days, simulating salinity increment with either artificial sea salts or brines from a desalination plant (at 43 psµ, 6 psµ over the natural 37 psµ). Morphometrical (growth and necrosis), photochemical (PSII chlorophyll a fluorometry), metabolic, such as hydrogen peroxide (H2O2), thiobarbituric reactive substances (TBARS) and ascorbate/dehydroascorbate (ASC/DHA), and molecular (expression of key tolerance genes) responses were analyzed in each different treatment. Although with a still positive leaf growth, associated parameters decreased similarly for both artificial sea salt and brine treatments. Photochemical parameters did not show general patterns, although only P. oceanica under brines demonstrated greater energy release through heat (NPQ). Lipid peroxidation and upregulation of genes related to oxidative stress (GR, MnSOD, and FeSOD) or ion exclusion (SOS3 and AKT2/3) were similarly incremented on both hypersalinity treatments. Conversely, the ASC/DHA ratio was significantly lower, and the expression of SOS1, CAT, and STRK1 was increased under brine influence. This study revealed that although metabolic and photochemical differences occurred under both hypersalinity treatments, growth (the last sign of physiological detriment) was similarly compromised, suggesting that the potential effects of desalination are mainly caused by brine-associated salinities and are not particularly related to other industrial additives.
Subject(s)
Alismatales , Salts , Chlorophyll A , Hydrogen Peroxide , Salinity , Ascorbic AcidABSTRACT
Introduction: Light gradients are ubiquitous in marine systems as light reduces exponentially with depth. Seagrasses have a set of mechanisms that help them to cope with light stress gradients. Physiological photoacclimation and clonal integration help to maximize light capture and minimize carbon losses. These mechanisms can shape plants minimum light requirements (MLR), which establish critical thresholds for seagrass survival and help us predict ecosystem responses to the alarming reduction in light availability. Methods: Using the seagrass Cymodocea nodosa as a case study, we compare the MLR under different carbon model scenarios, which include photoacclimation and/or self-facilitation (based on clonal integration) and that where parameterized with values from field experiments. Results: Physiological photoacclimation conferred plants with increased tolerance to reducing light, approximately halving their MLR from 5-6% surface irradiance (SI) to ≈ 3% SI. In oligotrophic waters, this change in MLR could translate to an increase of several meters in their depth colonization limit. In addition, we show that reduced mortality rates derived from self-facilitation mechanisms (promoted by high biomass) induce bistability of seagrass meadows along the light stress gradient, leading to abrupt shifts and hysteretic behaviors at their deep limit. Discussion: The results from our models point to (i) the critical role of physiological photoacclimation in conferring greater resistance and ability to recover (i.e., resilience), to seagrasses facing light deprivation and (ii) the importance of self-facilitating reinforcing mechanisms in driving the resilience and recovery of seagrass systems exposed to severe light reduction events.
ABSTRACT
Adaptation to local conditions is known to occur in seagrasses; however, knowledge of the genetic basis underlying this phenomenon remains scarce. Here, we analysed Posidonia oceanica from six sites within and around the Stagnone di Marsala, a semi-enclosed coastal lagoon where salinity and temperature exceed the generally described tolerance thresholds of the species. Sea surface temperatures (SSTs) were measured and plant samples were collected for the assessment of morphology, flowering rate and for screening genome-wide polymorphisms using double digest restriction-site-associated DNA sequencing. Results demonstrated more extreme SSTs and salinity levels inside the lagoon than the outer lagoon regions. Morphological results showed significantly fewer and shorter leaves and reduced rhizome growth of P. oceanica from the inner lagoon and past flowering events were recorded only for a meadow farthest away from the lagoon. Using an array of 51,329 single nucleotide polymorphisms, we revealed a clear genetic structure among the study sites and confirmed the genetic isolation and high clonality of the innermost site. In all, 14 outlier loci were identified and annotated with several proteins including those relate to plant stress response, protein transport and regulators of plant-specific developmental events. Especially, five outlier loci showed maximum allele frequency at the innermost site, likely reflecting adaptation to the extreme temperature and salinity regimes, possibly due to the selection of more resistant genotypes and the progressive restriction of gene flow. Overall, this study helps us to disentangle the genetic basis of seagrass adaptation to local environmental conditions and may support future works on assisted evolution in seagrasses.
Subject(s)
Alismatales , Salinity , Temperature , Oceans and Seas , Alismatales/genetics , Selection, Genetic , Mediterranean SeaABSTRACT
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.
ABSTRACT
The continuous worldwide seagrasses decline calls for immediate actions in order to preserve this precious marine ecosystem. The main stressors that have been linked with decline in seagrasses are 1) the increasing ocean temperature due to climate change and 2) the continuous inputs of nutrients (eutrophication) associated with coastal human activities. To avoid the loss of seagrass populations, an "early warning" system is needed. We used Weighed Gene Co-expression Network Analysis (WGCNA), a systems biology approach, to identify potential candidate genes that can provide an early warning signal of stress in the Mediterranean iconic seagrass Posidonia oceanica, anticipating plant mortality. Plants were collected from both eutrophic (EU) and oligotrophic (OL) environments and were exposed to thermal and nutrient stress in a dedicated mesocosm. By correlating the whole-genome gene expression after 2-weeks exposure with the shoot survival percentage after 5-weeks exposure to stressors, we were able to identify several transcripts that indicated an early activation of several biological processes (BP) including: protein metabolic process, RNA metabolic process, organonitrogen compound biosynthetic process, catabolic process and response to stimulus, which were shared among OL and EU plants and among leaf and shoot apical meristem (SAM), in response to excessive heat and nutrients. Our results suggest a more dynamic and specific response of the SAM compared to the leaf, especially the SAM from plants coming from a stressful environment appeared more dynamic than the SAM from a pristine environment. A vast list of potential molecular markers is also provided that can be used as targets to assess field samples.
Subject(s)
Alismatales , Hot Temperature , Humans , Ecosystem , Climate Change , Nutrients , Alismatales/physiology , Mediterranean SeaABSTRACT
In the Mediterranean, anthropogenic pressures (specifically those involving nutrient loads) have been progressively moved to deeper off-shore areas to meet current policies dealing with the protection of marine biodiversity (e.g., European Directives). However, conservation efforts devoted to protecting Posidonia oceanica and other vulnerable marine habitats against anthropogenic pressures have dedicated very little attention to the deepest areas of these habitats. We studied the remote influence of off-shore nutrient discharge on the physiology and structure of deep P. oceanica meadows located nearest to an urban sewage outfall (WW; 1 km) and an aquaculture facility (FF; 2.5 km). Light reduction and elevated external nutrient availability (as indicated by high δ15N, total N and P content and N uptake rates of seagrass tissues) were consistent with physiological responses to light and nutrient stress. This was particularly evident in the sites located up to 2.5 km from the WW source, where carbon budget imbalances and structural alterations were more evident. These results provide evidence that anthropogenic nutrient inputs can surpass critical thresholds for the species, even in off-shore waters at distances within the km scale. Therefore, the critical distances between this priority habitat and nutrient discharge points have been underestimated and should be corrected to achieve a good conservation status.
ABSTRACT
DNA methylation (DNAm) has been intensively studied in terrestrial plants in response to environmental changes, but its dynamic changes in a temporal scale remain unexplored in marine plants. The seagrass Posidonia oceanica ranks among the slowest-growing and longest-living plants on Earth, and is particularly vulnerable to sea warming and local anthropogenic pressures. Here, we analysed the dynamics of DNAm changes in plants collected from coastal areas differentially impacted by eutrophication (i.e. oligotrophic, Ol; eutrophic, Eu) and exposed to abiotic stressors (nutrients, temperature increase and their combination). Levels of global DNAm (% 5-mC) and the expression of key genes involved in DNAm were assessed after one, two and five weeks of exposure. Results revealed a clear differentiation between plants, depending on environmental stimuli, time of exposure and plants' origin. % 5-mC levels were higher during the initial stress exposure especially in Ol plants, which upregulated almost all genes involved in DNAm. Contrarily, Eu plants showed lower expression levels, which increased under chronic exposure to stressors, particularly to temperature. These findings show that DNAm is dynamic in P. oceanica during stress exposure and underlined that environmental epigenetic variations could be implicated in the regulation of acclimation and phenotypic differences depending on local conditions.
Subject(s)
Alismatales , DNA Methylation , Acclimatization/genetics , Temperature , Nutrients , Alismatales/geneticsABSTRACT
Human- and nature-induced hypersaline conditions in coastal systems can lead to profound alterations of the structure and vitality of seagrass meadows and their socio-ecological benefits. In the last two decades, recent research efforts (>50 publications) have contributed significantly to unravel the physiological basis underlying the seagrass-hypersalinity interactions, although most (â¼70%) are limited to few species (e.g. Posidonia oceanica, Zostera marina, Thalassia testudinum, Cymodocea nodosa). Variables related to photosynthesis and carbon metabolism are among the most prevalent in the literature, although other key metabolic processes such as plant water relations and responses at molecular (i.e. gene expression) and ultrastructure level are attracting attention. This review emphasises all these latest insights, offering an integrative perspective on the interplay among biological responses across different functional levels (from molecular to clonal structure), and their interaction with biotic/abiotic factors including those related to climate change. Other issues such as the role of salinity in driving the evolutionary trajectory of seagrasses, their acclimation mechanisms to withstand salinity increases or even the adaptive properties of populations that have historically lived under hypersaline conditions are also included. The pivotal role of the costs and limits of phenotypic plasticity in the successful acclimation of marine plants to hypersalinity is also discussed. Finally, some lines of research are proposed to fill the remaining knowledge gaps.
Subject(s)
Alismatales , Zosteraceae , Humans , Stress, Physiological/physiology , Alismatales/physiology , Photosynthesis/physiology , AcclimatizationABSTRACT
In seagrass sediments, lucinid bivalves and their chemoautotrophic bacterial symbionts consume H2S, relying indirectly on the plant productivity for the presence of the reduced chemical. Additionally, the role of lucinid bivalves in N provisioning to the plant (through N2 fixation by the symbionts) was hypothesized. Thus, lucinids may contribute to sediment detoxification and plant fitness. Seagrasses are subject to ever-increasing human pressure in coastal environments. Here, disentangling nested interactions between chemosynthetic lucinid bivalves and seagrass exposed to pollution may help to understand seagrass ecosystem dynamics and to develop successful seagrass restoration programs that consider the roles of animal-microbe symbioses. We evaluated the capacity of lucinid bivalves (Loripes orbiculatus) to promote nutrient cycling and seagrass (Cymodocea nodosa) growth during a 6-week mesocosm experiment. A fully crossed design was used to test for the effect of sediment contamination (metals, nutrients, and hydrocarbons) on plant and bivalve (alone or interacting) fitness, assessed by mortality, growth, and photosynthetic efficiency, and for the effect of their nested interaction on sediment biogeochemistry. Plants performed better in the contaminated sediment, where a larger pool of dissolved nitrogen combined with the presence of other trace elements allowed for an improved photosynthetic efficiency. In fact, pore water nitrogen accumulated during the experiment in the controls, while it was consumed in the contaminated sediment. This trend was accentuated when lucinids were present. Concurrently, the interaction between clams and plants benefitted both organisms and promoted plant growth irrespective of the sediment type. In particular, the interaction with lucinid clams resulted in higher aboveground biomass of C. nodosa in terms of leaf growth, leaf surface, and leaf biomass. Our results consolidate the notion that nested interactions involving animal-microbe associations promote ecosystem functioning, and potentially help designing unconventional seagrass restoration strategies that exploit chemosynthetic symbioses.
ABSTRACT
The intensification of anomalous events of seawater warming and the co-occurrence with local anthropogenic stressors are threatening coastal marine habitats, including seagrasses, which form extensive underwater meadows. Eutrophication highly affects coastal environments, potentially summing up to the widespread effects of global climate changes. In the present study, we investigated for the first time in seagrasses, the transcriptional response of different plant organs (i.e., leaf and shoot apical meristem, SAM) of the Mediterranean seagrass Posidonia oceanica growing in environments with a different history of nutrient enrichment. To this end, a mesocosm experiment exposing plants to single (nutrient enrichment or temperature increase) and multiple stressors (nutrient enrichment plus temperature increase), was performed. Results revealed a differential transcriptome regulation of plants under single and multiple stressors, showing an organ-specific sensitivity depending on plants' origin. While leaf tissues were more responsive to nutrient stress, SAM revealed a higher sensitivity to temperature treatments, especially in plants already impacted in their native environment. The exposure to stress conditions induced the modulation of different biological processes. Plants living in an oligotrophic environment were more responsive to nutrients compared to plants from a eutrophic environment. Evidences that epigenetic mechanisms were involved in the regulation of transcriptional reprogramming were also observed in both plants' organs. These results represent a further step in the comprehension of seagrass response to abiotic stressors pointing out the importance of local pressures in a global warming scenario.
Subject(s)
Alismatales , Transcriptome , Alismatales/physiology , Ecosystem , Global Warming , Mediterranean Sea , Nutrients , SeawaterABSTRACT
Seawater warming and increased incidence of marine heatwaves (MHW) are threatening the integrity of coastal marine habitats including seagrasses, which are particularly vulnerable to climate changes. Novel stress tolerance-enhancing strategies, including thermo-priming, have been extensively applied in terrestrial plants for enhancing resilience capacity under the re-occurrence of a stress event. We applied, for the first time in seedlings of the Mediterranean seagrass Posidonia oceanica, a thermo-priming treatment through the exposure to a simulated warming event. We analyzed the photo-physiological and growth performance of primed and non-primed seedlings, and the gene expression responses of selected genes (i.e. stress-, photosynthesis- and epigenetic-related genes). Results revealed that during the re-occurring stress event, primed seedlings performed better than unprimed showing unaltered photo-physiology supported by high expression levels of genes related to stress response, photosynthesis, and epigenetic modifications. These findings offer new opportunities to improve conservation and restoration efforts in a future scenario of environmental changes.
Subject(s)
Alismatales , Seedlings , Climate Change , Heat-Shock Response , Hot Temperature , Mediterranean SeaABSTRACT
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.
Subject(s)
Alismatales/genetics , DNA Methylation/genetics , Transcriptome/genetics , Epigenesis, Genetic/genetics , Heat-Shock Response/genetics , Heat-Shock Response/physiologyABSTRACT
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.
ABSTRACT
Seagrasses are valuable sources of food and habitat for marine life and are one of Earth's most efficient carbon sinks. However, they are facing a global decline due to ocean warming and eutrophication. In the last decade, with the advent of new technology and molecular advances, there has been a dramatic increase in the number of studies focusing on the effects of ocean warming on seagrasses. Here, we provide a comprehensive review of the future of seagrasses in an era of ocean warming. We have gathered information from published studies to identify potential commonalities in the effects of warming and the responses of seagrasses across four distinct levels: molecular, biochemical/physiological, morphological/population, and ecosystem/planetary. To date, we know that although warming strongly affects seagrasses at all four levels, seagrass responses diverge amongst species, populations, and over depths. Furthermore, warming alters seagrass distribution causing massive die-offs in some seagrass populations, whilst also causing tropicalization and migration of temperate species. In this review, we evaluate the combined effects of ocean warming with other environmental stressors and emphasize the need for multiple-stressor studies to provide a deeper understanding of seagrass resilience. We conclude by discussing the most significant knowledge gaps and future directions for seagrass research.
Subject(s)
Ecosystem , Eutrophication , Oceans and SeasABSTRACT
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 Posidonia australis and pioneer species Zostera muelleri, 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 a 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.
ABSTRACT
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.
ABSTRACT
The Mediterranean Sea is particularly vulnerable to warming and the abrupt declines experienced by the endemic Posidonia oceanica populations after recent heatwaves have forecasted severe consequences for the ecological functions and socio-economical services this habitat forming species provides. Nevertheless, this highly clonal and long-lived species could be more resilient to warming than commonly thought since heat-sensitive plants massively bloomed after a simulated heatwave, which provides the species with an opportunity to adapt to climate change. Taking advantage of this unexpected plant response, we investigated for the first time the molecular and physiological mechanisms involved in seagrass flowering through the transcriptomic analysis of bloomed plants. We also aimed to identify if flowering is a stress-induced response as suggested from the fact that heat-sensitive but not heat-tolerant plants flowered. The transcriptomic profiles of flowered plants showed a strong metabolic activation of sugars and hormones and indications of an active transport of these solutes within the plant, most likely to induce flower initiation in the apical meristem. Preflowered plants also activated numerous epigenetic-related genes commonly used by plants to regulate the expression of key floral genes and stress-tolerance genes, which could be interpreted as a mechanism to survive and optimize reproductive success under stress conditions. Furthermore, these plants provided numerous molecular clues suggesting that the factor responsible for the massive flowering of plants from cold environments (heat-sensitive) can be considered as a stress. Heat-stress induced flowering may thus be regarded as an ultimate response to survive extreme warming events with potential adaptive consequences for the species. Fitness implications of this unexpected stress-response and the potential consequences on the phenotypic plasticity (acclimation) and evolutionary (adaptation) opportunity of the species to ocean warming are finally discussed.