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  • Effect of salinity and nitrogen fertilization levels on growth parameters of Sarcocornia fruticosa, Salicornia brachiata, and Arthrocnemum macrostachyum
    Publication . Sisay, Tesfaye Asmare; Nurbekova, Zhadyrassyn; Oshanova, Dinara; Dubey, Arvind Kumar; Khatri, Kusum; Mudgal, Varsha; Mudgal, Anurag; Neori, Amir; Shpigel, Muki; Srivastava, Rajeev Kumar; Custódio, Luísa; Standing, Dominic; Sagi, Moshe
    Salinity negatively influences crop growth, but several salt-tolerant plant species (halophytes) are viable crops. Sarcocornia fruticosa (ecotypes EL and VM) is currently cultivated, but there is demand for new crop candidates and higher biomass production. Salicornia brachiata Roxb. and Arthrocneum macrostachyum L. are considered novel crops, and to realize their potential, their response to salinity and nitrogen nutrition was compared to S. fruticosa ecotypes. Experiments revealed that higher N supplemented with lower NaCl significantly increased fresh and dry shoot biomass. Lower biomass was obtained at lower nitrogen supplemented with elevated NaCl, whereas total soluble solids content positively correlated with NaCl fertigation in both Sarcocornia ecotypes. Protein content increased with a lower nitrogen supply. Anthocyanins and oxygen radical absorbance capacity were highest in S. fruticosa EL and A. macrostachyum at higher NaCl supply. The results show that halophytes have a variety of strategies to cope with high NaCl, even between ecotypes of the same species. Notably, repetitive harvesting of S. brachiata delayed flowering enabling year-round biomass production. Additionally, S. brachiata accumulated higher biomass than Sarcocornia VM when grown in a greenhouse at higher radiation than in a growth room and strongly supports its inclusion as a cash-crop halophyte.
  • A review on sarcocornia species: Ethnopharmacology, nutritional properties, phytochemistry, biological activities and propagation
    Publication . Custódio, Luísa; Rodrigues, Maria João; Pereira, Catarina Guerreiro; Castañeda-Loaiza, Viana; Fernandes, Eliana; Standing, Dominic; Neori, Amir; Shpigel, Muki; Sagi, Moshe
    Sarcocornia A. J. Scott is a halophytic edible succulent plant belonging to the Amaranthaceae family. To date, the genus includes 28 species distributed worldwide in saline environments, usually salt marshes. Sarcocornia (Scott) is similar to Salicornia (L.), which has a recognized commercial value in morphological and taxonomical traits. Species of both genera are commonly named samphire or glassworts in Europe, and their fleshy shoots are commercialized under their traditional names. Due to their nutritional, organoleptic and medicinal properties, Sarcocornia species have a high economic potential in various biotechnology sectors. Being highly tolerant to salt, they can be cultivated in saline conditions, and dissimilar to Salicornia, they are perennial, i.e., they can be harvested year-round. Therefore, Sarcocornia species are considered promising gourmet vegetables to be explored in the context of climate change, soil and water salinization and eco-sustainability. We hereby put together and reviewed the most relevant information on Sarcocornia taxonomy, morphology, nutritional and pharmacological properties, uses in ethnomedicine, potential applications in biotechnology, and propagation strategies.
  • A characterization of biological activities and bioactive phenolics from the non-volatile fraction of the edible and medicinal Halophyte Sea Fennel (Crithmum maritimum L.)
    Publication . Lemoine, Clément; Rodrigues, Maria João; Dauvergne, Xavier; Cérantola, Stéphane; Custódio, Luísa; Magné, Christian
    Although the biochemical composition and biological properties of the volatile fraction of the halophyte sea fennel (Crithmum maritimum L.) have been largely described, little is known about its polar constituents and bioactivities. Here, a hydromethanolic extract of Crithmum maritimum (L.) leaves was fractionated, and the fractions were evaluated in vitro for antioxidant (using DPPH, ABTS, and FRAP bioassays), anti-inflammatory (inhibition of NO production in RAW 264.7 macrophages), antidiabetic (alpha-glucosidase inhibition), neuroprotective (inhibition of acetylcholinesterase), and skin-protective (tyrosinase and melanogenesis inhibitions) activities. Polar fractions of the extract were rich in phenolics and, correlatively, displayed a strong antioxidant power. Moreover, fractions eluted with MeOH20 and MeOH80 exhibited a marked inhibition of alpha-glucosidase (IC50 = 0.02 and 0.04 mg/mL, respectively), MeOH60 fractions showed a strong capacity to reduce NO production in macrophages (IC50 = 6.4 µg/mL), and MeOH80 and MeOH100 fractions had strong anti-tyrosinase activities (630 mgKAE/gDW). NMR analyses revealed the predominance of chlorogenic acid in MeOH20 fractions, 3,5-dicaffeoylquinic acid in MeOH40 fractions, and 3-O-rutinoside, 3-O-glucoside, 3-O-galactoside, and 3-O-robinobioside derivatives of quercetin in MeOH60 fractions. These compounds likely account for the strong antidiabetic, antioxidant, and anti-inflammatory properties of sea-fennel polar extract, respectively. Overall, our results make sea fennel a valuable source of medicinal or nutraceutical agents to prevent diabetes, inflammation processes, and oxidative damage.
  • Bioactive extracts from Salicornia ramosissima J. woods biorefinery as a source of ingredients for high-value industries
    Publication . Hulkko, Laura Sini Sofia; Rocha, Rui Miranda; Trentin, Riccardo; Fredsgaard, Malthe; Chaturvedi, Tanmay; L, Custódio; Thomsen, Mette Hedegaard
    Salt-tolerant plants, also known as halophytes, could provide a novel source of feedstock for biorefineries. After harvesting fresh shoots for food, the lignified fraction of Salicornia ramosissima J. Woods could be used to produce bioactive botanical extracts for high-value industries such as nutraceuticals, cosmetics, and biopharmaceuticals. The residual fraction after extraction can be further used for bioenergy or lignocellulose-derived platform chemicals. This work analysed S. ramosissima from different sources and growth stages. After pre-processing and extractions, the obtained fractions were analysed for their contents of fatty acids, pigments, and total phenolics. Extracts were also evaluated for their in vitro antioxidant properties and inhibitory effect towards enzymes related to diabetes, hyperpigmentation, obesity, and neurogenerative diseases. The ethanol extract from the fibre residue and the water extract from completely lignified plants showed the highest concentration of phenolic compounds along with the highest antioxidant potential and enzyme-inhibitory properties. Hence, they should be further explored in the context of biorefinery.
  • In vitro and in silico approaches to appraise Polygonum maritimum L. as a source of innovative products with anti-ageing potential
    Publication . Rodrigues, Maria Joao; Slusarczyk, Sylwester; Pecio, Łukasz; Matkowski, Adam; Salmas, Ramin Ekhteiari; Durdagi, Serdar; Pereira, Catarina; Varela, J.; Barreira, Luísa; Custódio, Luísa
    Different Polygonum species have in vitro neuroprotective properties and are traditionally used for their anti-ageing benefits. In this context this work explored for the first time P. maritimum (sea knotgrass) as a potential source of natural products with industrial application as cognitive enhancers with anti-ageing potential. For that purpose methanol and dichloromethane extracts were prepared from leaves and roots of that species and evaluated for in vitro neuroprotective effects through the inhibition on acetyl- (AChE) and butyrylcholinesterase (BuChE), protection against hydrogen peroxide (H2O2)-induced cytoxicity on neuroblastoma cells and lipopolysaccharide (LPS)-induced neuroinflammation on microglia cells. The extracts were chemically characterized by ultra-high-pressure liquid chromatography (UHPLC) coupled to tandem mass spectrometry (MS/MS) and docking studies were performed on the identified compounds. Methanol extracts had the highest activity in AChE (leaves: IC50 = 0.27 mg/mL; roots: IC50 = 0.17 mg/mL) and BuChE (leaves: IC50 = 0.62 mg/mL; roots: IC50 = 0.61 mg/mL) inhibition, as well as reduction of nitric oxide (NO) production in LPS-treated microglia (leaves: IC50 = 4.17 μg/mL; roots: IC50 = 9.95 μg/mL). Methanol extracts prevented oxidative stress-induced cytotoxicity in SH-SY5Y cells when applied simultaneously with H2O2, whereas cells pre-treated with the dichloromethane extracts had increased viability. Fifteen flavonoids were identified and showed favorable binding energies to AChE and BuChE binding pockets. These data suggests P. maritimum as a promising source of natural products and/or molecules with cognitive enhancement and anti-ageing properties.
  • Impact of seasonal and Organ-Related Fluctuations on the anthelmintic properties and chemical profile of Cladium mariscus (L.) Pohl Extracts
    Publication . Oliveira, Marta; Lima, Caroline Sprengel; Llorent-Martínez, Eulogio J.; Hoste, Hervé; Custódio, Luísa
    The use of plants and their metabolites stands as a promising option to tackle parasitic infections by gastrointestinal nematodes (GIN) in integrated control strategies. Still, the influence of environmental and phenological factors, and their interactions, in the wild on the metabolomics and biological properties of target plant species, is often disregarded. In this work, we hypothesized that variations in the anthelmintic (AH) properties and chemical composition of extracts from the salt tolerant species Cladium mariscus L. Pohl (sawgrass) may be influenced by seasonal factors and organ-parts. To test this hypothesis, acetone/water extracts were prepared from dried biomass obtained from aerial organs collected from sawgrass in consecutive seasons and tested against Haemonchus contortus and Trichostrongylus colubriformis by the larval exsheathment inhibition assay (LEIA) and egg hatching inhibition assay (EHIA). To ascertain the role of plant organ, the activity of leaves and inflorescences extracts from summer samples was compared. The role of polyphenols in the anthelmintic activity depending on GINs and fluctuations across seasons and plant organs was assessed using polyvinylpolypyrrolidone (PVPP), coupled with an in-depth chemical profiling analysis using high-performance liquid chromatography completed with electrospray ionization mass spectrometric detection (HPLC-ESI-MSn). Main differences in anthelmintic activities were observed for summer and autumn samples, for both assays. Moreover, inflorescences' extracts were significantly more active than those from leaves against both parasite species on EHIA and against H. contortus on LEIA. Application of PVPP totally inhibit the AH effects based on EHIA and only partly for LEIA. Non-treated PVPP extracts were predominantly composed of flavan-3-ols, proanthocyanidins, luteolin and glycosylated flavonoids, while two flavonoid glycosides were quantified in all PVPP-treated samples. Thus, the activity of such compounds should be further explored, although some unknown metabolites remain to be identified. This study reinforces the hypothesis of the AH potential of sawgrass and of its polyphenolic metabolites uses as nutraceutical and/or phytotherapeutic drugs.
  • Natural products from extreme marine environments: searching for potential industrial uses within extremophile plants
    Publication . Lopes, Andreia; Rodrigues, Maria João; Pereira, Catarina; Oliveira, Marta; Barreira, Luísa; Varela, J.; Trampetti, Francesca; Custódio, Luísa
    Extremophile plants, halophytes in particular, still remain largely unexplored and underutilized despite their high potential as source of industrial raw materials like natural antioxidants in industries related to pharmaceutical, cosmetics and functional ingredients. The goal of this study was to explore the phenolic content and the in vitro antioxidant and tyrosine inhibition properties of polyphenol-rich extracts of twenty-one extremophile plant species collected in saline habitats of the South of Portugal (Algarve). Aqueous acetone extracts of Lithrum salicaria, Cladium mariscus, Frankenia laevis, F. pulverulenta, Limoniastrum monopetalum, Aster tripolium and Typha domigensis had remarkable levels of total phenolics (>= 230 mg GAE/g DW); Halopeplis amplexicaulis, Cladium mariscus,F. puiverulenta and Salsola vermiculata contained high levels of flavonoids (>= 10 mg RE/g DW); tannins peaked in T. domingensis and C. mariscus (>= 35 mg CE/g DW) and L. salicaria and A. tripolium had the upmost hydrocinamic acids content (>= 60 mg CAE/g DW). Overall L. salicaria had the highest antioxidant activity and only P. lentiscus had the capacity to inhibit tyrosinase. As the most bioactive extracts were not cytotoxic towards mammalian cell lines, our results suggest that several halophytes present in Southern Portugal could be used in the food and/or cosmetic industries.
  • Greener is better: first approach for the use of natural deep eutectic solvents (NADES) to extract antioxidants from the medicinal halophyte Ppolygonum maritimum L.
    Publication . Rukavina, Iva; Rodrigues, Maria João; Pereira, Catarina; Mansinhos, Inês; Romano, Anabela; Ślusarczyk, Sylwester; Matkowski, Adam; Custódio, Luísa
    In this study, natural deep eutectic solvents (NADES) formed by choline chloride (ChCl), su crose, fructose, glucose, and xylose, were used to extract antioxidants from the halophyte Polygonum maritimum L. (sea knotgrass) and compared with conventional solvents (ethanol and acetone). NADES and conventional extracts were made by an ultrasound-assisted procedure and evaluated for in vitro antioxidant properties by the radical scavenging activity (RSA) on the 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical, oxygen radical absorbance capacity (ORAC), and cop per chelating activity (CCA). Samples were profiled by liquid chromatography (LC)-electrospray ionization (ESI)-QTOF-MS analysis. ChCl:fructose was more efficient in the DPPH assay, than the acetone extract. ChCl:sucrose and ChCl:fructose extracts had the highest ORAC when compared with the acetone extract. NADES extracts had higher CCA, than the acetone extract. The phenolic composition of the NADES extracts was less complex than the conventional extracts, but the pro portions of major antioxidants, such as flavonols and flavan-3-ols, were similar in all the solvents. Myricitrin was the major flavonoid in all of the samples, while gallic acid was the main phenolic acid in the conventional extracts and present in a greater amount in ChCl:fructose. Results suggest that NADES containing ChCl and sucrose/fructose can replace conventional solvents, especially acetone, in the extraction of antioxidants from sea knotgrass.
  • A systematic review on the ethnoveterinary uses of mediterranean salt-tolerant plants: Exploring its potential use as fodder, nutraceuticals or phytotherapeutics in ruminant production
    Publication . Oliveira, Marta; Hoste, Herve; Custódio, Luísa
    Ethnopharmacological relevance: Salt-tolerant plants are well adapted to the harsh conditions of the Mediterranean region, where have been used traditionally as food and medicines for human and animals. In addition, various species are currently recognized as sources of metabolites with pharmacological, cosmetical and nutraceutical interest. Nevertheless, ethnoveterinary data on salt-tolerant plants are dispersed in the literature and there are few discussions on its veterinary potential. Having in mind the rising interest on organic farming, alternatives to chemical substances in livestock production and concern for animal health and welfare practices, these plants may represent an untapped resource for animal management and veterinary purposes. In this sense, the purpose of this work is to summarize the ethnoveterinary knowledge on salt-tolerant plants described in the Mediterranean region, raising awareness to the potential of this group of plants to be used in veterinary science, targeting especially ruminants. Material and methods: Literature search (2000-2020) was conducted using Web of Science and Science Direct databases. Ethnoveterinary reports (EVR) concerning salt-tolerant plants were summarized and filtered for ruminants. From the final 29 publications, EVR concerning therapeutic uses were categorized according to its ATCvet code and results analyzed. Results: A total of 221 EVR were identified from 39 plants, belonging to 21 plant families, targetting ruminants. Ten EVR (4.5%) concerned uses of salt-tolerant species as animal feed, while around 75% of therapeutic uses was represented by three categories: alimentary tract and metabolism (QA; n = 75), dermatologicals (QD; n = 53) and genitourinary system and sex hormones (QG; n = 41). Pistacia lentiscus L., Foeniculum vulgare Mill., Dittrichia viscosa (L.) Greuter, Plantago major L. and Hordeum vulgare L. were the most cited species in the latter categories. Conclusions: The ethnoveterinary knowledge on salt-tolerant species hints some plants of veterinary pharmacological potential, but other species deserve further notice. This information should serve as a basis and, coupled with the currently available scientific data on bioactive properties and chemical composition of salt-tolerant species, inspire additional research on the exploitation of this botanical group, as sources of novel products for ruminant nutrition, health and quality of its products.
  • Metabolomic profile and biological properties of sea lavender (Limonium algarvense Erben) plants cultivated with aquaculture wastewaters: implications for its use in herbal formulations and food additives
    Publication . Rodrigues, Maria João; Castañeda-Loaiza, Viana; Monteiro, Ivo; Pinela, José; Barros, Lillian; Abreu, Rui M. V.; Oliveira, Maria Conceição; Reis, Catarina; Soares, Florbela; Pousão-Ferreira, Pedro; Pereira, Catarina; Custódio, Luísa
    Water extracts from sea lavender (Limonium algarvense Erben) plants cultivated in greenhouse conditions and irrigated with freshwater and saline aquaculture effluents were evaluated for metabolomics by liquid chromatography-tandem high-resolution mass spectrometry (LC-HRMS/MS), and functional properties by in vitro and ex vivo methods. In vitro antioxidant methods included radical scavenging of 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid (ABTS), ferric-reducing antioxidant power (FRAP), and copper and iron chelating assets. Flowers’ extracts had the highest compounds’ diversity (flavonoids and its derivatives) and strongest in vitro antioxidant activity. These extracts were further tested for ex vivo antioxidant properties by oxidative haemolysis inhibition (OxHLIA), lipid peroxidation inhibition by thiobarbituric acid reactive substances (TBARS) formation, and anti-melanogenic, anti-tyrosinase, anti-inflammation, and cytotoxicity. Extract from plants irrigated with 300 mM NaCl was the most active towards TBARS (IC50 = 81 µg/mL) and tyrosinase (IC50 = 873 µg/mL). In OxHLIA, the activity was similar for fresh- and saltwater-irrigated plants (300 mM NaCl; IC50 = 136 and 140 µg/mL, respectively). Samples had no anti-inflammatory and anti-melanogenic abilities and were not toxic. Our results suggest that sea lavender cultivated under saline conditions could provide a flavonoid-rich water extract with antioxidant and anti-tyrosinase properties with potential use as a food preservative or as a functional ingredient in herbal supplements.