Enhancing Sustainability by Improving Plant Salt Tolerance through Macro- and Micro-Algal Biostimulants
Abstract
:1. Introduction
2. Extraction Techniques, Chemical Characteristics of Macroalgae and Microalgae
3. Main Bioactive Compounds of Macroalgae and Microalgae that Affect Growth and Salt Tolerance
4. Mechanisms of Salinity Stress Tolerance in Macro and Microalgae-Treated Plants
4.1. Biochemical and Physiological Mechanisms in AE-Treated Plants
4.2. Molecular Response in Plants to AEs Treatment
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Class | Metabolite | Algae | Discussed Effects on Plants | Ref. |
---|---|---|---|---|
Amino acids | D-homocysteic acid, GABA, ornithine, citrulline, hydroxyproline | Chlorophyceae, Phaeophyceae, Rhodophyceae | Nitrogen storage, stress response, osmolytes, pH buffering, antioxidants | [79,80] |
Amino acids | Mycosporine-like amino acids | Rhodophyceae | Protection from UV radiation and oxidative damage, osmolytes | [90,91] |
Amino acids | Phosphoserine | Phaeophyceae | Phosphoserine-containing peptides lower lipid peroxidation, increase intracellular glutathione and expression of antioxidant enzymes | [82,83] |
Amino acid | Proline | Trebouxiophyceae (Stichococcus) | Osmolyte, antioxidant, cellular protectant against saline stress | [84] |
Amino acid | Taurine | Rhodophyceae (Porphyra) | Antioxidant activity | [81,92] |
Betains | Glycine betaine, γ-aminobutyric acid betaine and proline betaine | Entire algal kingdom | Osmolytes, ROS scavengers, macromolecules protectans | [28,32,33,89] |
Brassinosteroids | Brassinolide, castasterone, typhasterol | Chlorophyceae, Trebouxiophyceae | Promote plant growth, increase crop yield and resistance to biotic and abiotic stresses | [62,93] |
Carbohydrate | Trehalose | Chlamydomonas, Chlorella, Scytonema | Osmolyte, carbon reserve, and salt stress protectant | [88] |
Carotenoids | E-fucoxanthin | Nannochloris, Tetraselmis, Nannochloropsis, Phaedactylium | Radical scavenger and iron chelator | [70,94] |
Flavonoids | Catechin and epicatechin | Ankistrodesmus, Spirogyra, Euglena, Caespitella | ROS scavengers, metal ion chelators, induction of antioxidant enzymes, inhibition of pro-oxidant enzymes | [69] |
Phenolic acids | Gallic, syringic, protocatechuic, and chlorogenic acids | Ankistrodesmus, Spirogyra, Euglena, Caespitella | High antioxidant capacity, inhibition of generation as well as scavenging of free radicals, upregulation of antioxidant enzymes | [69] |
Phenolic acids | Protocatechuic acid | Nannochloris, Tetraselmis, Nannochloropsis, Phaedactylium | Superoxide anion radical and hydroxyl radical scavenger, metal ion chelator | [70,95] |
Phytohormones | Abscissic acid | Entire algal kingdom | Involvement in stress response | [73,74] |
Phytohormones | Auxins and cytochinins | Chlorophyceae, Trebouxiophyceae, Ulvophyceae, Charophyceae | Increase of plant growth, yield and defense response against abiotic stress | [63] |
Phytohormones | Auxins (IAA, IAM, IBA) | Rhodophyceae, Phaeophyceae, Ulvophyceae | Stimulation of rooting and root growth, increase of resources use efficiency, stress resistance | [34,72] |
Phytohormones | Isopentenyladenine, cis-zeatin | Chlorophyceae, Phaeophyceae, Rhodophyceae | Stimulation of seed germination, transition between vegetative to generative phases, inhibition of senescence, response to abiotic stresses | [38,96,97] |
Phytohormones | Gibberellins | Chlorophyceae, Trebouxiophyceae, Ulvophyceae, Charophyceae | Promote plant growth and resistance to salinity by inducing the degradation of the nuclear family of DELLA TFs and the increase of salicylic acid | [62,98] |
Polyamines | Putrescine and spermidine | Chlorophyceae, Charophyceae, Rhodophyceae | Regulation of the cell cycle and increased cell proliferation, stress tolerance | [85,86] |
Polyols | Sorbitol and mannitol | Platymonas, Stichococcus | Osmoprotectans | [88] |
Polyphenols | Phloroglucinol, eckol, and dieckol | Phaeophyceae (Ascophyllum, Fucus) | More efficient ROS detoxification due to the higher number of phenolic rings. | [65,67,68] |
Polyphenols | Phlorotannins | Phaeophyceae | Response to both biotic and abiotic stresses, ROS scavenging | [66] |
Polysaccharides | Agars, alginates, carrageenans, and fucans | Chlorophyceae, Phaeophyceae, Rhodophyceae | Elicitors of hormonal stress signals (i.e., SA, JA, ethylene) and inductor of resistance to biotic stresses | [77,78] |
Tertiary sulphonium compound | 3-dimethylsulfoniopropionate | Entire algal kingdom | Osmoprotectant | [32] |
Algae Species | Plant Species | Described Tolerance Mechanisms | Ref. |
---|---|---|---|
Ascophyllum nodosum | Agrostis stolonifera | Increase of SOD activity and resistance to Sclerotinia homoeocarpa. | [110] |
Ascophyllum nodosum | Amarantus tricolor | Increased growth parameters (stem length and diameter, root length, number of leaves, fresh and dry weight of leaves, stems and roots). | [111] |
Ascophyllum nodosum | Arabidopsis thaliana | Increase of biomass and polyphenols content. | [112] |
Ascophyllum nodosum | Asparagus aethiopicus | Increase of phenolics, chlorophylls, sugars, proline, anti-oxidant activities, gas exchanges. | [113] |
Ascophyllum nodosum | Lactuca sativa | Increase of weight. | [114] |
Ascophyllum nodosum | Paspalum vaginatum | Increase of ability of plants to maintain higher potassium to sodium ratios. | [115] |
Ascophyllum nodosum | Passiflora edulis | Increase of the initial growth of the seedlings. | [116] |
Ascophyllum nodosum | Persea americana | Increase of plant growth, potassium, and calcium in leaves. | [117] |
Ascophyllum nodosum | Solanum lycopersicum | Increase of beneficial minerals, antioxidants, and essential amino acids. | [108] |
Ascophyllum nodosum | Solanum melongena | Increase of phenols, tannins, total soluble sugars, activity of SOD and APX, and potassium to sodium ratio. | [118] |
Codium taylorii or Pterocladia capillacea | Raphanus sativus | Seed priming induces the synthesis of stress proteins in seedlings under salinity. | [119] |
Dunaliella salina | Solanum lycopersicum | Positive effects on length, dry weight, potassium, potassium to sodium ratio, increase of proline, phenolics, CAT, POD, and SOD activities. | [120] |
Dunaliella salina | Triticum aestivum | Increase of seed germination and seedling growth. | [121] |
Dunaliella spp. | Capsicum annuum | Increase of germination rate, root growth, and reduction of superoxide radical production and lipid peroxidation. | [122] |
Ecklonia maxima | Cucurbita pepo | Increase of yield, shoot biomass, fruit dry matter, total soluble solid contents, chlorophyll content, and photosynthetic rate | [123] |
Fucus spiralis | Triticum durum | Increase of seed germination, growth, and anti-oxidant enzyme activities. | [124] |
Galaxaura obtusata | Triticum vulgare | Increase of SOD activity and shoot length. | [125] |
Grateloupia filicina | Oriza sativa | Increase of proline, SOD, and POD activities, and alleviating salt stress during the seed germination stage. | [126] |
Kappaphycus alverezii | Triticum durum | Increase of tolerance to salt and drought stress. | [36] |
Laurencia obtusa | Triticum vulgare | Decrease of sodium uptake, increase of CAT and SOD activities, carbohydrates, shoot and root length. | [125] |
Lessonia nigrescens | Triticum aestivum | Increase of growth, chlorophyll, and antioxidant activities, decrease of membrane lipid peroxidation, efflux and compartmentation of intracellular ion. | [109] |
Padina pavonica | Triticum vulgare | Increase of CAT and SOD activities, carbohydrates, shoot, and root length. | [125] |
Phaeodactylum spp. | Capsicum annuum | Increase of germination rate, root growth, and reduction of superoxide radical production and lipid peroxidation. | [122] |
Sargassum muticum | Triticum vulgare | Increase of CAT and SOD activities, carbohydrates, shoot and root length. | [125] |
Sargassum muticum Jania rubens | Cicer aretinum | Increase of photosynthetic pigments, soluble sugars, amino acids, phenolics, Na+ extrusion SOD, CAT, APX, and POD activity. | [127] |
Scenedesmus obliquus Spirulina platensis | Triticum aestivum | Increase of activities of SOD, APX, CAT, and POD and chlorophyll and carotenoid content. | [128] |
Spirulina maxima Chlorella ellipsoida | Triticum aestivum | Increase of carotenoids, tocopherol, phenolics, proteins, and antioxidant activity | [129] |
Ulva lactuca | Triticum aestivum | Increase of plant growth and yield and antioxidant enzymes activity (SOD, CAT, APX and GR). | [35] |
Ulva rigida | Triticum durum | Increase of leaf pigments, total phenolics, and antioxidant enzymatic activities. | [130] |
Algae Species | Plant Species | Described Tolerance Mechanisms | Ref. |
---|---|---|---|
Ascophyllum nodosum | Arabidopsis thaliana | Downregulation of a putative pectin methylesterase inhibitor, acting as a negative regulator of salt tolerance | [142] |
Ascophyllum nodosum | Arabidopsis thaliana | Upregulation of genes involved in the ABA pathway (SnRK2), modification of expression of miRNA and their target genes involved in phosphate homeostasis | [134] |
Ascophyllum nodosum | Arabidopsis thaliana | Response to stress mediated by LEA proteins and dehydrins | [112,131] |
Ascophyllum nodosum | Arabidopsis thaliana | Post-transcriptional and post-translational regulation of Zinc Finger, MYB, and AP2 transcription factors | [131] |
Ascophyllum nodosum | Arabidopsis thaliana | Upregulation of CK and ABA biosynthetic genes | [29] |
Ascophyllum nodosum | Asparagus aethiopicus | Upregulation of stress-related genes involved in the synthesis of proline and chalcones | [113] |
Ascophyllum nodosum | Glycine max | Overexpression of genes involved in ABA catabolism and response to stress | [115] |
Dunaliella salina | Solanum lycopersicum | Upregulation of antioxidant defense and metabolic mechanisms related to jasmonic acid pathway | [120] |
Grateloupia filicina | Oriza sativa | Upregulation of SOS1 antiporter | [126] |
Kappaphycus alverezii | Triticum durum | Upregulation of stress-responsive genes (e.g., MAP kinase, WRKY transcription factor) | [36] |
Laminaria digitata | Arabidopsis thaliana | Upregulation of genes involved in terpenoid pathway, plastidial-derived secondary metabolite, and DEFL202, increasing chloroplast stability | [143] |
Lessonia nigrescens | Triticum aestivum | Upregulation of SOS1 and NHX Na+/K+ antiporters | [109] |
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Carillo, P.; Ciarmiello, L.F.; Woodrow, P.; Corrado, G.; Chiaiese, P.; Rouphael, Y. Enhancing Sustainability by Improving Plant Salt Tolerance through Macro- and Micro-Algal Biostimulants. Biology 2020, 9, 253. https://doi.org/10.3390/biology9090253
Carillo P, Ciarmiello LF, Woodrow P, Corrado G, Chiaiese P, Rouphael Y. Enhancing Sustainability by Improving Plant Salt Tolerance through Macro- and Micro-Algal Biostimulants. Biology. 2020; 9(9):253. https://doi.org/10.3390/biology9090253
Chicago/Turabian StyleCarillo, Petronia, Loredana F. Ciarmiello, Pasqualina Woodrow, Giandomenico Corrado, Pasquale Chiaiese, and Youssef Rouphael. 2020. "Enhancing Sustainability by Improving Plant Salt Tolerance through Macro- and Micro-Algal Biostimulants" Biology 9, no. 9: 253. https://doi.org/10.3390/biology9090253