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- Population level variation in reproductive development and output in the golden kelp Laminaria ochroleuca under marine heat wave scenariosPublication . Strasser, Fiona-Elaine; Barreto, Luis M.; Kaidi, Soukaina; Sabour, Brahim; A, Serrão; Pearson, Gareth; Martins, NeusaThermal tolerance is often interpreted as a species-wide thermal niche in the absence of studies focusing on the adaptive potential of populations to exhibit differential thermal tolerance. Thus, considering intraspecific thermal plasticity, local adaptation or both between populations along distributional gradients when interpreting and predicting species responses to warming is imperative. Removing the effect of environmental histories by raising kelp gametophyte generations in vitro under common garden conditions allows unbiased comparison between population-specific adaptive variation under different environmental conditions. Following this approach, this study aims to detect (potentially) adaptive differentiation in microscopic life-stages (gametophytes) between populations of a temperate forest forming kelp, Laminaria ochroleuca from locations with distinct thermal conditions. Gametophytes from four geographically distinct populations were subjected to different temperature treatments (17, marine heat waves of 23, 25 and 27 degrees C) and gametophyte survival during thermal stress as well as reproductive success and photosynthetic responses during recovery were investigated. Intraspecific variation in resilience and reproductive output to thermal stress was found in L. ochroleuca; gametophytes from the most northern population (Brittany, France) were the most thermally sensitive, with mortality onset at 23 degrees C, whereas mortality in the remaining populations was only apparent at 27 degrees C. Gametophytes from northern Spain and Morocco exhibited very low reproductive success during recovery from 23 and 25 degrees C. However, when recovering from the highest thermal treatment (27 degrees C) the reproductive development and sporophyte output was higher than in the gametophytes from France and Italy (Mediterranean). The population-specific responses of gametophyte resilience and reproductive success to temperature stress suggest genetic differentiation in response to variation in local thermal regimes.
- Aluminum bioaccumulation and tolerance in Plantago algarbiensis Samp. and Plantago almogravensis Franco, assessed by using in vitro cultures and micropropagated plantsPublication . Martins, Neusa; Romano, AnabelaThis thesis aims to understand the aluminum (Al) bioaccumulation capacity, toxicity effects and tolerance mechanisms in two rare species endemic from Portugal, Plantago algarbiensis Samp. and Plantago almogravensis Franco. Firstly, two protocols were developed to propagate in vitro these species (Chapter 2). Afterwards it was investigated the influence of low pH on in vitro growth (Chapter 3). The seed germination requirements and the effects of Al on the germination and early development of seedlings were then evaluated in Chapters 4 and 5, respectively. The impact of low pH and Al on physiological responses, oxidative stress status and capacity for Al accumulation in micropropagated shoots and plantlets was investigated in the subsequent chapters (Chapters 6, 7 and 8). Finally, in Chapter 9 the possible implications of organic acids in Al detoxification were evaluated. Both species were successfully micropropagated showing high shoot multiplication rates and rooting frequencies and the micropropagated shoots of both species were able to tolerate and grow in low pH conditions. The seeds of both species germinate readily at 15 ºC and Al showed no impact on the germination percentage in either species but oxidative stress during early seedling development was detected. Although, both species accumulated considerable Al amounts and showed to be moderately tolerant to low pH and Al, P. almogravensis appeared to be more able to manage the oxidative stress and, therefore, adapted to maintain cellular physiology and growth under these stress conditions. Results suggested that Al detoxification in P. almogravensis implies both secretion of organic acids from roots and Al intracellular chelation by organic acids, while in P. algarbiensis only the internal mechanism seems to be involved. This research contributes to the understanding of the mechanisms underlying P. algarbiensis and P. almogravensis adaptation to acidic Al-rich conditions.
- Physiological traits and oxidative stress markers during acclimatization of micropropagated plants from two endangered Plantago species: P-algarbiensis Samp. and P-almogravensis FrancoPublication . Gonçalves, Sandra; Martins, Neusa; Romano, A.Plantago algarbiensis Samp. and Plantago almogravensis Franco are species endemic to Portugal at risk of global extinction. The aim of this study was to investigate the ex vitro performance of micropropagated P. algarbiensis and P. almogravensis plants in terms of survival, relative water content (RWC), photosynthetic pigment contents, H2O2 accumulation, activities of superoxide dismutase (SOD) and catalase (CAT), lipid peroxidation, and soluble protein content, in comparison with wild-grown plants. Relatively high survival rates and RWC values during the acclimatization process were observed for both species. In P. algarbiensis, the pigment content increased when plantlets were transferred to ex vitro conditions, indicating enhanced light absorption capacity. No significant alterations in H2O2 content, CAT activity, or lipid peroxidation level were observed during acclimatization, but the protein content decreased in plants at the end of the growth chamber and greenhouse stages. When P. almogravensis plantlets were transferred to the ex vitro environment, decreases in the H2O2 content were observed that correlated to increased CAT activity and SOD maintenance, which lead to decreased lipid peroxidation and protein content. It was concluded that micropropagated P. algarbiensis and P. almogravensis plants were able to manage the oxidative stress induced by the in vitro environment and to perform well under ex vitro conditions.
- Increased evolutionary rates and conserved transcriptional response following allopolyploidization in brown algaePublication . Sousa, Filipe; Neiva, J.; Martins, Neusa; Jacinto, Rita; Anderson, Laura; Raimondi, Peter T.; Serrao, Ester; Pearson, GarethGenome mergers between independently evolving lineages, via allopolyploidy, can potentially lead to instantaneous sympatric speciation. However, little is known about the consequences of allopolyploidy and the resultant "genome shock" on genome evolution and expression beyond the plant and fungal branches of the Tree of Life. The aim of this study was to compare substitution rates and gene expression patterns in two allopolyploid brown algae (Phaeophyceae and Heterokonta) and their progenitors in the genus Pelvetiopsis N. L. Gardner in the north-east Pacific, and to date their relationships. We used RNA-seq data, all potential orthologues, and putative single-copy loci for phylogenomic, divergence, and gene expression analyses. The multispecies coalescent placed the origin of allopolyploids in the late Pleistocene (0.35-0.05 Ma). Homoeologues displayed increased nonsynonymous divergence compared with parental orthologues, consistent with relaxed selective constraint following allopolyploidization, including for genes with no evidence of pseudogenization or neofunctionalization. Patterns of homoeologue-orthologue expression conservation and expression level dominance were largely shared with both natural plant and fungal allopolyploids. Our results provide further support for common cross-Kingdom patterns of allopolyploid genome evolution and transcriptional responses, here in the evolutionarily distinct marine heterokont brown algae.
- A novel sexual system in male gametophytes of Laminaria pallida (Phaeophyceae)Publication . Liboureau, Pierre; Pearson, Gareth; Serrao, Ester; Kreiner, Anja; Martins, NeusaBrown algae (Phaeophyceae) exhibit a wide diversity of sexual systems, reproductive modes and life histories. The evolution of this diversity has often involved transitions between sexual systems, which may influence genetic diversity and diversification, and phenotypic evolution. This study reports a novel sexual system in kelp. We identified male gametophyte strains of Laminaria pallida that, despite presenting morphological features typical of a male, developed both antheridia and egg-like structures, which suggest an incomplete suppression of femaleness during sexual determination of gametophytes. The sperm released by these variant male gametophytes successfully fertilize eggs produced by female gametophytes, developing into sporophytes with normal morphologies. However, morphologically abnormal sporophytic offspring were formed in isolated variant male gametophytes, indicating that the egg-like structures were not successfully self-fertilized by sperm. The causes of the unsuccessful intragametophytic selfing are unknown, but absence of pheromone production by the egg-like structures is a hypothesis suggested by available evidence. Partial co-sexuality is clearly inherited, as all male gametophyte strains descended from the same sporophyte developed egg-like structures. Further investigation into the genetics and maturation of male partheno-sporophytes will help to estimate the potential effects of this mechanism on natural populations.
- Editorial: Opening the black box of kelps: Response of early life stages to anthropogenic stressorsPublication . Martins, Neusa; Coleman, Melinda A.; Wernberg, Thomas; Roleda, Michael Y.Kelps form marine forests along world’s coastlines, providing valuable ecosystem goods and services, either directly as a source offood or medicinal products, or indirectly as biogenic habitats or carbon sink agents (Teagle et al., 2017; Wernberg et al., 2019). However, kelp forests are currently under threat due to anthropogenic climate change with latitudinal range shifts and large-scale declines at a global scale (Smale et al., 2019; Wernberg et al., 2019). Most studies on the impact of anthropogenic stressors on kelps have focused on the macroscopic sporophyte stage of the haploid-diploid life cycle (Schiel and Foster, 2006; Veenhof et al., 2022). However, the microscopic stages considered as the “black box” of kelps due to the complexity of studying them in situ, have been suggested to play a crucial role in the persistence of populations that experience sporophyte mortality after large-scale disturbances (McConnico and Foster, 2005; Barradas et al., 2011) as they can persist as “seed bank” analogues under adverse conditions (Hoffmann and Santelices, 1991; Veenhof et al., 2022). This Research Topic is a collection of 8 articles contributing to opening the “black box” of kelps by providing greater insight into how microscopic life stages of kelps are affected by anthropogenic climate change, helping to predict the persistence of these foundation species and therefore the fate of ecosystems and coastal communities. These studies highlight that the response of kelp early life stages to stressors can be strongly dependent on the population and thermal history.
- Thermal traits for reproduction and recruitment differ between Arctic and Atlantic kelp Laminaria digitataPublication . Martins, Neusa; Pearson, Gareth; Bernard, Julien; Serrao, Ester; Bartsch, InkaThe plasticity of different kelp populations to heat stress has seldom been investigated excluding environmental effects due to thermal histories, by raising a generation under common garden conditions. Comparisons of populations in the absence of environmental effects allow unbiased quantification of the meta-population adaptive potential and resolution of population-specific differentiation. Following this approach, we tested the hypothesis that genetically distinct arctic and temperate kelp exhibit different thermal phenotypes, by comparing the capacity of their microscopic life stages to recover from elevated temperatures. Gametophytes of Laminaria digitata (Arctic and North Sea) grown at 15°C for 3 years were subjected to common garden conditions with static or dynamic (i.e., gradual) thermal treatments ranging between 15 and 25°C and also to darkness. Gametophyte growth and survival during thermal stress conditions, and subsequent sporophyte recruitment at two recovery temperatures (5 and 15°C), were investigated. Population-specific responses were apparent; North Sea gametophytes exhibited higher growth rates and greater sporophyte recruitment than those from the Arctic when recovering from high temperatures, revealing differential thermal adaptation. All gametophytes performed poorly after recovery from a static 8-day exposure at 22.5°C compared to the response under a dynamic thermal treatment with a peak temperature of 25°C, demonstrating the importance of gradual warming and/or acclimation time in modifying thermal limits. Recovery temperature markedly affected the capacity of gametophytes to reproduce following high temperatures, regardless of the population. Recovery at 5°C resulted in higher sporophyte production following a 15°C and 20°C static exposure, whereas recovery at 15°C was better for gametophyte exposures to static 22.5°C or dynamic heat stress to 25°C. The subtle performance differences between populations originating from sites with contrasting local in situ temperatures support our hypothesis that their thermal plasticity has diverged over evolutionary time scales.
- The influence of low pH on in vitro growth and biochemical parameters of Plantago almogravensis and P. algarbiensisPublication . Martins, Neusa; Gonçalves, Sandra; Romano, AnabelaThe effects of low medium pH (4.50, 5.00 and 5.75) on in vitro growth and on several biochemical parameters (lipid peroxidation, proline and carbohydrate content, antioxidant enzymes activities and total soluble protein) of Plantago almogravensis and P. algarbiensis micropropagated shoots were investigated. Overall, it was observed that medium pH did not affect in vitro proliferation and rooting. Interestingly, cultures of both species modify the initial pH value to the same final value. Results have shown that the lowest pH tested induced an increase in the level of lipid peroxidation in roots of both species and in shoots of P. algarbiensis, indicating plasma membrane damage. An accumulation of carbohydrates was observed in roots of P. almogravensis cultured in pH 4.50 and 5.00. It was observed a slight response of the enzymatic system to medium pH, particularly in P. almogravensis. Based on the results obtained we can conclude that Plantago species are apt to grow in vitro in medium with pH values much lower than the usually used in tissue culture, which is in agreement with the fact that both species colonize acid soils.
- Hybrid vigour for thermal tolerance in hybrids between the allopatric kelps Laminaria digitata and L. pallida (Laminariales, Phaeophyceae) with contrasting thermal affinitiesPublication . Martins, Neusa; Pearson, Gareth; Gouveia, Licínia; Tavares, Ana I; Serrao, Ester; Bartsch, InkaKelps are globally important bioengineering species with high ecological and economic value, but are increasingly threatened by climate-driven geographic range shifts. The inheritance of economically important traits from parents to offspring is poorly understood in kelps but it is of utmost interest to seaweed farmers wishing to select strains with superior performance and resilience to environmental change. For two allopatric kelp species (N-Atlantic Laminaria digitata and S-Atlantic L. pallida), we compared the speed of gametogenesis and reproductive success in parental gametophytes, and produced intraspecific and reciprocal interspecific crosses of female × male gametophyte parents isolated from the two species. We then compared the upper thermal resilience of microscopic and macroscopic sibling sporophytes in an exposure experiment over two weeks. The upper thermal limit of the sporophytes resulting from intraspecific crosses of the two species deviated by 1°C. In contrast, sporophytes from both interspecific hybrid crosses had a 2–3°C higher upper thermal tolerance than single species sporophytes, indicating heterosis for thermal tolerance. This phenotypic response appears partially sex-dependent in our study, with female parents being more important in determining the thermal-response phenotype than male parents. The presence of male gametophytes generally enhanced female reproductive success. Both gametogenesis rate and reproductive success differed among the types of reciprocal crosses. Although the interspecific crosses were artificial in an ecological sense, they may provide a tool for understanding the molecular basis of heterosis and thermal tolerance in kelps (e.g. by investigating species-specific gene expression), or for aquaculture breeding programmes against a background of rapid environmental change.
- Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissimaPublication . Pearson, Gareth; Martins, Neusa; Madeira, Pedro M.; Serrao, Ester; Bartsch, InkaIn haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.
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