Browsing by Author "Procaccini, Gabriele"
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- 2b-RAD genotyping of the seagrass Cymodocea nodosa along a latitudinal cline identifies candidate genes for environmental adaptationPublication . Ruocco, Miriam; Jahnke, Marlene; Silva, João; Procaccini, Gabriele; Dattolo, EmanuelaPlant 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 Cymodocea nodosa 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. Cymodocea nodosa 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 C. nodosa 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 Lysine-specific histone demethylase 1 homolog 2. 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 via DNA (de)methylation, could have for enabling adaptation of seagrass populations along environmental gradients.
- Daily regulation of key metabolic pathways in two seagrasses under natural light conditionsPublication . Ruocco, Miriam; Barrote, Isabel; Hofman, Jan Dirk; Pes, Katia; Costa, Monya; Procaccini, Gabriele; Silva, João; Dattolo, EmanuelaThe 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), cooccurring 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.
- Depth-specific fluctuations of gene expression and protein abundance modulate the photophysiology in the seagrass Posidonia oceanicaPublication . Procaccini, Gabriele; Ruocco, Miriam; Marin-Guirao, Lazaro; Dattolo, Emanuela; Brunet, Christophe; D'Esposito, Daniela; Lauritano, Chiara; Mazzuca, Silvia; Serra, Ilia Anna; Bernardo, Letizia; Piro, Amalia; Beer, Sven; Bjork, Mats; Gullström, Martin; Buapet, Pimchanok; Rasmusson, Lina M.; Felisberto, Paulo; Gobert, Sylvie; Runcie, John W.; Silva, João; Olive, Irene; Costa, Monya M.; Barrote, Isabel; Santos, RuiHere 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.
- Genomewide transcriptional reprogramming in the seagrass Cymodocea nodosa under experimental ocean acidificationPublication . Ruocco, Miriam; Musacchia, Francesco; Olivé, Irene; Costa, Monya; Barrote, Isabel; Santos, Rui; Sanges, Remo; Procaccini, Gabriele; Silva, JoãoHere, we report the first use of massive-scale RNA-sequencing to explore seagrass response to CO2-driven ocean acidification (OA). Large-scale gene expression changes in the seagrass Cymodocea nodosa occurred at CO2 levels projected by the end of the century. C. nodosa transcriptome was obtained using Illumina RNA-Seq technology and de novo assembly, and differential gene expression was explored in plants exposed to short-term high CO2/low pH conditions. At high pCO(2), there was a significant increased expression of transcripts associated with photosynthesis, including light reaction functions and CO2 fixation, and also to respiratory pathways, specifically for enzymes involved in glycolysis, in the tricarboxylic acid cycle and in the energy metabolism of the mitochondrial electron transport. The upregulation of respiratory metabolism is probably supported by the increased availability of photo-synthates and increased energy demand for biosynthesis and stress-related processes under elevated CO2 and low pH. The upregulation of several chaperones resembling heat stress-induced changes in gene expression highlighted the positive role these proteins play in tolerance to intracellular acid stress in seagrasses. OA further modifies C. nodosa secondary metabolism inducing the transcription of enzymes related to biosynthesis of carbon-based secondary compounds, in particular the synthesis of polyphenols and isoprenoid compounds that have a variety of biological functions including plant defence. By demonstrating which physiological processes are most sensitive to OA, this research provides a major advance in the understanding of seagrass metabolism in the context of altered seawater chemistry from global climate change.
- Harnessing positive species interactions as a tool against climate-driven loss of coastal biodiversityPublication . Bulleri, Fabio; Eriksson, Britas Klemens; Queiros, Ana; Airoldi, Laura; Arenas, Francisco; Arvanitidis, Christos; Bouma, Tjeerd J.; Crowe, Tasman P.; Davoult, Dominique; Guizien, Katell; Ivesa, Ljiljana; Jenkins, Stuart R.; Michalet, Richard; Olabarria, Celia; Procaccini, Gabriele; Serrao, Ester; Wahl, Martin; Benedetti-Cecchi, LisandroHabitat-forming species sustain biodiversity and ecosystem functioning in harsh environments through the amelioration of physical stress. Nonetheless, their role in shaping patterns of species distribution under future climate scenarios is generally overlooked. Focusing on coastal systems, we assess how habitat-forming species can influence the ability of stress-sensitive species to exhibit plastic responses, adapt to novel environmental conditions, or track suitable climates. Here, we argue that habitat-former populations could be managed as a nature-based solution against climate-driven loss of biodiversity. Drawing from different ecological and biological disciplines, we identify a series of actions to sustain the resilience of marine habitat-forming species to climate change, as well as their effectiveness and reliability in rescuing stress-sensitive species from increasingly adverse environmental conditions.
- Linking gene expression to productivity to unravel long-and short-term responses of seagrasses exposed to CO2 in volcanic ventsPublication . Olive, Irene; Silva, João; Lauritano, Chiara; Costa, Monya M.; Ruocco, Miriam; Procaccini, Gabriele; Santos, RuiOcean acidification is a major threat for marine life but seagrasses are expected to benefit from high CO2. In situ (long-term) and transplanted (short-term) plant incubations of the seagrass Cymodocea nodosa were performed near and away the influence of volcanic CO2 vents at Vulcano Island to test the hypothesis of beneficial effects of CO2 on plant productivity. We relate, for the first time, the expression of photosynthetic, antioxidant and metal detoxification-related genes to net plant productivity (NPP). Results revealed a consistent pattern between gene expression and productivity indicating water origin as the main source of variability. However, the hypothesised beneficial effect of high CO2 around vents was not supported. We observed a consistent long-and short-term pattern of gene downregulation and 2.5-fold NPP decrease in plants incubated in water from the vents and a generalized upregulation and NPP increase in plants from the vent site incubated with water from the Reference site. Contrastingly, NPP of specimens experimentally exposed to a CO2 range significantly correlated with CO2 availability. The down-regulation of metal-related genes in C. nodosa leaves exposed to water from the venting site suggests that other factors than heavy metals, may be at play at Vulcano confounding the CO2 effects.
- m6A RNA Methylation in marine plants: first insights and relevance for biological rhythmsPublication . Ruocco, Miriam; Ambrosino, Luca; Jahnke, Marlene; Chiusano, Maria; Barrote, Isabel; Procaccini, Gabriele; Silva, João; Dattolo, EmanuelaCircadian 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.
- Marine heatwaves recurrence aggravates thermal stress in the surfgrass Phyllospadix scouleriPublication . Vivanco-Bercovich, Manuel; Sandoval-Gil, Jose Miguel; Bonet-Meliá, Paula; Cabello-Pasini, Alejandro; Muñiz-Salazar, Raquel; Montoya, Leonardo Ruiz; Schubert, Nadine; Marín-Guirao, Lázaro; Procaccini, Gabriele; Ferreira-Arrieta, AlejandraThe surfgrass Phyllospadix scouleri constitutes highly productive meadows along the Pacific coast of North America – a region that has been increasingly affected by severe marine heatwaves (MHWs) in recent years. Our study assessed the effects of consecutive MHWs simulated in mesocosms on critical ecophysiological descriptors of P. scouleri. Generally, our results revealed a progressive deterioration of the plant overall physiological status. Surprisingly, photosynthetic parameters only indicated physiological stress once the first heat exposure ceased (i.e., recovery period). Warming induced elevated oxidative damage and a decline in nitrate uptake rates. By contrast, non-structural carbohydrates and growth rates remained unaffected. Our results highlight the importance of including recovery periods in this sort of experiments, as they reveal delayed stress responses. Further, the accumulative detrimental effects due to the exposure to consecutive intense MHWs indicate that these events can compromise the vitality of surfgrasses and the ecosystem services provided by their meadows.
- The genome of the seagrass Zostera marina reveals angiosperm adaptation to the seaPublication . Olsen, Jeanine L.; Rouze, Pierre; Verhelst, Brain; Lin, Yao-Cheng; Bayer, Till; Collen, Jonas; Dattolo, Emanuela; De Paoli, Emanuele; Dittami, Simon; Maumus, Florian; Michel, Gurvan; Kersting, Anna; Lauritano, Chiara; Lohaus, Rolf; Topel, Mats; Tonon, Thierry; Vanneste, Kevin; Amirebrahimi, Mojgan; Brakel, Janina; Bostrom, Christoffer; Chovatia, Mansi; Grimwood, Jane; Jenkins, Jerry W.; Jueterbock, Alexander; Mraz, Amy; Stam, Wytze T.; Tice, Hope; Bornberg-Bauer, Erich; Green, Pamela J.; Pearson, Gareth; Procaccini, Gabriele; Duarte, Carlos M.; Schmutz, Jeremy; Reusch, Thorsten B. H.; Van de Peer, YvesSeagrasses colonized the sea(1) on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet(2). 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(3), 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(4) and that is important for ion homoeostasis, nutrient uptake and O-2/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 plants(7).
- The tropical seagrass halophila stipulacea: reviewing what we know from its native and invasive habitats, alongside identifying knowledge gapsPublication . Winters, Gidon; Beer, Sven; Willette, Demian A.; Viana, Inés G.; Chiquillo, Kelcie L.; Beca-Carretero, Pedro; Villamayor, Betty; Azcárate-García, Tomás; Shem-Tov, Rachamim; Mwabvu, Bridget; Migliore, Luciana; Rotini, Alice; Oscar, Michelle A.; Belmaker, Jonathan; Gamliel, Inbal; Alexandre, Ana; Engelen, Aschwin; Procaccini, Gabriele; Rilov, GilHalophila stipulacea is a small tropical seagrass, native to the Red Sea, Persian Gulf, and the Indian Ocean. It invaded the Mediterranean Sea 150 years ago as a Lessepsian migrant, but so far has remained in insulated, small populations across this basin. Surprisingly, in 2002 it was reported in the Caribbean Sea, where within less than two decades it spread to most of the Caribbean Island nations and reaching the South American continent. Unlike its invasion of Mediterranean, in the Caribbean H. stipulacea creates large, continuous populations in many areas. Reports from the Caribbean demonstrated the invasiveness of H. stipulacea by showing that it displaces local Caribbean seagrass species. The motivation for this review comes from the necessity to unify the existing knowledge on several aspects of this species in its native and invasive habitats, identify knowledge gaps and develop a critical strategy to understand its invasive capacity and implement an effective monitoring and conservation plan to mitigate its potential spread outside its native ranges. We systematically reviewed 164 studies related to H. stipulacea to create the "Halophila stipulacea database." This allowed us to evaluate the current biological, ecological, physiological, biochemical, and molecular knowledge of H. stipulacea in its native and invasive ranges. Here we (i) discuss the possible environmental conditions and plant mechanisms involved in its invasiveness, (ii) assess the impact of H. stipulacea on native seagrasses and ecosystem functions in the invaded regions, (iii) predict the ability of this species to invade European and transoceanic coastal waters, (iv) identify knowledge gaps that should be addressed to better understand the biology and ecology of this species both in its native and non-native habitats, which would improve our ability to predict H. stipulacea's potential to expand into new areas in the future. Considering the predicted climate change scenarios and exponential human pressures on coastal areas, we stress the need for coordinated global monitoring and mapping efforts that will record changes in H. stipulacea and its associated communities over time, across its native, invasive and prospective distributional ranges. This will require the involvement of biologists, ecologists, economists, modelers, managers, and local stakeholders.