The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants
© The Author(s) 2017
Received: 26 September 2016
Accepted: 23 January 2017
Published: 3 April 2017
KeywordsAbiotic stress Biostimulants Bioeffectors Microbial inoculants Humic acid Fulvic acid Protein hydrolysates Amino acids Seaweed extracts Bioprotection
Plant biostimulants, sometimes referred to as agricultural biostimulants, are a diverse classification of substances that can be added to the environment around a plant and have positive effects on plant growth and nutrition, but also on abiotic and biotic stress tolerance. Although most plant biostimulants are added to the rhizosphere to facilitate uptake of nutrients, many of these also have protective effects against environmental stress such as water deficit, soil salinization and exposure to sub-optimal growth temperatures . Biostimulants are not nutrients per se; instead they facilitate the uptake of nutrients or beneficially contribute to growth promotion or stress resistance . A newly emerged paradigm emphasizes that plants are not standalone entities within their environments; instead they are host and partner to microorganisms of bacteria and fungi; plants are a host to numerous microbiota and those associations, both outside and within its tissues, allow them to respond and adapt to abiotic and biotic stress . Reasonably, if we functionally optimize these associations, we may strengthen their role in plant stress protection.
The industry definition of biostimulants was originally proposed in 2012 and stated: “Plant biostimulants contain substance(s) and/or microorganisms whose function when applied to plants or the rhizosphere is to stimulate natural processes to enhance/benefit nutrient uptake, nutrient efficiency, tolerance to abiotic stress, and crop quality. Biostimulants have no direct action against pests, and therefore do not fall within the regulatory framework of pesticides”. Biostimulants were loosely defined for a long time and often regarded dubiously because of their aggregate nature and the inherent difficulty to determine which specific components were making beneficial contributions. The definition proposed by du Jardin  “A plant biostimulant is any substance or microorganism applied to plants with the aim to enhance nutrition efficiency, abiotic stress tolerance and/or crop quality traits, regardless of its nutrients content” represents the clearest and most concise way to define biostimulants.
Summary of species, biostimulant, and stress effect
Type of BE
Stress and effect
Salt and osmotic stress
A. brasilense/P. dispersa
Fulvic and humic acids
Fulvic and humic acids
Humic acid and phosporous
Salt tolerance and ion homeostasis
Oxidative and drought stress
Heavy metal tolerance
Salt tolerance, cold tolerance
D. kaki/D. lotus
Drought tolerance and ion homeostasis
While the growth-promoting effects of seaweed extracts have been documented in many species [8, 66], very little is actually known about the mechanisms behind these effects. The variable and complex nature of these substances makes it difficult to determine exactly which components are playing a key role. Commercial formulations of SWEs are often proprietary, and the composition is largely dependent on the method of extraction. Indeed, characterization of the actual composition of most common algal-based commercial products would be useful first step to better hypothesize and/or depict a cause–effect relationship of their mechanism of action. Mechanical disruption, pulverization, acid or alkali extractions are some of the more common methods employed . Most commercial products are derived from red (ex Lithothamnium calcareum) and brown (ex Ascophyllum nodosum, Durvillaea potatorum) macroalgae . The role of SWEs and cold tolerance is now emerging. Very recent work has focused on SWEs and their ability to enhance tolerance to chilling stress. When multiple extracts were tested for their ability to enhance cold tolerance in maize only extracts rich in Zn and Mn were able to enhance tolerance through enhanced ROS responses. In this case, the protective effects likely stem from supplying plants with micronutrients that play a role as co-factors in anti-oxidative enzymes . These results indicate that nutrient deficiency stress induced by cold can be overcome by supplying SWEs rich in micronutrients to improve oxidative stress tolerance. Previous studies with corn seedlings under root chilling stress supplemented with micronutrients demonstrated the utility of nutrient seed priming .
Some work has been done in model systems with the goal of determining the physiological and molecular responses induced by SWEs. In order to better understand the active components of A. nodosum, Rayirath et al.  separated the organic-sub-fractions of extracts and tested them with Arabidopsis thaliana and freezing experiments. Plants grown in vitro with sub-fractions added to the substrate or in “Peat pellet freezing assays” irrigated with sub-fractions were tested for freezing tolerance. The authors found that the ethyl acetate extracted fraction, rich in fatty acids and sterols enhanced freezing tolerance over water treated (controls) at temperatures from −2.5 to −5.5 °C. Treated plants maintained faster rates of recovery, greater membrane integrity, and had 70% less chlorophyll damage upon freezing recovery as well as increased expression of key freezing tolerance genes such as RD29A, COR15A, and CBF3 . Priming of key tolerance genes prior to exposure to stress greatly increases tolerance in many cases. The lipophilic components were found to be rich in fatty acids such as butyric acid, palmitic acid, oleic acid, linoleic acid the sterol fucosterol. These extracts increased proline content and total soluble sugars, contributing to freezing tolerance . A. nodosum extracts have even been used to reduce cold stress sensitivity in Kappaphycus alvarezii. Kappaphycus alvarezii is a red algae and the most important source of carrageenans; which are hydrophilic colloids largely used in foods and dairy products [29, 69]. Algal extracts have also been used on Kentucky bluegrass (Poa pratensis L. cv. Plush) to alleviate salinity stress from saline watering in turfgrass experiments . Similarly SWE-based cytokinins have been used on creeping bentgrass (Agrostis stolonifera L.) to improve tolerance to heat stress . SWEs from A. nodosum have also been used for ornamental plants, such as Spiraea nipponica “Snowmound” and Pittosporum eugenioides “Variegatum”, to enhance drought tolerance. Treated plants showed higher phenolic, proline, and flavonoid content while demonstrating improved physiology under mild drought stress conditions .
In horticultural crops and trees, SWE have been largely used for similar purposes. A. nodosum SWE increased RWC, Fresh Weight, and Dry Weight in spinach (Spinacia oleracea L.) plants under drought stress with some adverse effects on the nutritional value through reduced ferrous ion chelating ability . SWE applied to seedlings of lettuce (Lactuca sativa L.) enhanced cotyledon growth similar to fertilization with potassium .
Foliar application of marine bioactive substances (isopropanol extracts from microalgae) to grape plants (Vitis vinifera L) increased leaf water potential and stomatal conductance under drought stress . Consistent with an improved stomatal response, it was also observed that K+ and Ca2+ fluxes at the stomatal level were higher in treated plants. Commercial formulations of A. nodosum have been tested on almond plants (Prunus dulcis [Mill.] D. A. Webb), which demonstrated increased growth and accumulation of K+. In conditions with ample K+ both MegaFol and GroZyme (Valagro, Atessa, Chieti, ITALY) increased leaf area and number of leaves greater than controls treated with water or K+. In K+-deficiency conditions only MegaFol and a foliar application of K+ was able to stimulate growth, although at lower levels than observed with adequate K+ nutrition . Accumulation of K+ is an essential step in protecting against both ionic and osmotic stress and may contribute to tolerance. Orange trees, Citrus sinensis L., subjected to drought stress and treated with commercial extracts of A. nodosum had better water relations and increased water use efficiency (WUE) under irrigation at 50% restitution of evapotranspired water . The promise of biostimulants to increase drought tolerance and WUE holds great potential for drought prone regions where horticultural crops and fruit trees are agronomically important but water availability is becoming less reliable due to urbanization and climate change.
As earlier noted, almost all of the above-mentioned experiments with SWE use commercial formulations. This may be of some concern, due to the variable nature of these products and formulation methods. A recent transcriptomic study using A. thaliana plants treated with two different commercial A. nodosum extracts showed that not all extracts are alike. One commercial product resulted in dysregulation of 4.47% of the transcriptome while the other extract only affected 0.87% . Since transcriptional priming is likely a key component in enhancing abiotic stress tolerance using SWEs, these differences imply significant variability in responses elicited. Compositions of the extracts differed greatly, indicating that choice of commercial product may have a significant effect on plant responses. Commercial formulations are often proprietary and the exact composition and extraction methods, shifting the burden to the research community to analyse and isolate the active components in these products. In order to identify and characterize how these SWEs affect plants, some form of standardization is necessary.
Carbohydrates, proteins, amino acids, and lipids
Megafol (Valagro, Atessa, Chieti, ITALY) is a commercial biostimulant comprising vitamins, amino acids, proteins, and betaines from plant and algal extracts. Application of Megafol to tomato plants under drought stress enhanced induction of a number of drought responsive genes such as tomato orthologs of RAB18 and RD29B. Treated plants also had higher fresh weight and relative water content under drought stress, indicating a protective effect on water status and stress responsive genes [43, 71]. When hydrolysate-based biostimulants from alfalfa (Medicago sativa L.), containing triacontanol (TRIA) and indole-3-acetic acid (IAA), were applied to maize plants under salt stress, the protective effects were amplified. Treated plants had higher flavonoid, proline, and potassium content in salt stress conditions over untreated controls . Extracts that are rich in amino acids may play a role in increasing cold tolerance. When lettuce plants (Lactuca sativa) were treated with an amino acid mixture, derived from enzymatic hydrolysis of proteins, (Terra-Sorb) and subjected to cold, treated plants had higher fresh weights and improved stomatal conductance . Use of animal derived amino acid hydrolysates on strawberry plants after transplantation and cold stress did not improve survival though some growth promotions were observed in the absence of stress . Perennial Rye-grass (Lolium perenne L.) treated with hydrolyzed amino acids and high temperatures (36 °C) had improved photosynthetic efficiency over control plants .
Mutants of A. thaliana deficient in production of proline have stress sensitive phenotypes . These plants can have their phenotype rescued with exogenous application of l-proline, a common amino acid available in biostimulant formulations of various amino acids and hydrolysate mixtures . Hydrolysates from wheat germs show strong anti-oxidant and free radical scavenging properties as well as the ability to chelate some metals .
Lettuce (Lactuca sativa L.) is particularly salt sensitive and the addition of plant-derived protein hydrolysates improved fresh yield, dry biomass, and root dry weight as well as increased concentrations of osmoyltes, glucosinolates and the composition of sterols and terpenes . Hydrolysates have applications for trees, which require considerable investment costs and can be vulnerable to drought. Japanese persimmon trees, Diospyros kaki L. cv. “Rojo Brillante” grafted on Diospyros lotus L., are particularly sensitive to drought stress . Treatment of these trees with calcium protein hydrolysates decreased chloride uptake under saline irrigation, lowered water potentials as well as increased the concentration of compatible solutes , all of which would enhance plant growth under saline stress.
Recent reports indicate that melatonin, derived from l-tryptophan via the shikimate pathway, can prime seeds to tolerate adverse environmental conditions at imbibition and germination stages . Corn seeds pre-treated with melatonin show increased tolerance to chilling stress upon germination, indicating a priming effect by melatonin . Melatonin may prove to be an effective biostimulant for improving stress tolerance of seedlings.
Glycinebetaine is a compatible solute accumulated in many plants in response to salt stress . Exogenous application of glycinebetaine has increased tolerance for environmental stresses such as drought, chilling, freezing, salinity, and oxidative stress. Foliar application of glycinebetaine results in rapid uptake by leaves and concentration in meristematic tissues. Rapid uptake and localization of glycinebetaine in these most vulnerable tissues are particularly beneficial in chilling and freezing stress where glycinebetaine can exert a protective effect . Transgenic plants of various species expressing two biosynthetic genes, codA and betA, produce more glycinebetaine and had an increased tolerance to abiotic stress [38, 78]. Exogenous application of small amounts of compatible solutes such as proline and betaine to barley roots resulted in an immediate reduction of NaCl-induced efflux of K+, indicating that ion fluxes across the membrane can be affected by relatively low concentrations of compatible solutes . The cause–effect relationship between accumulation of compatible solutes and stress protection still remains to be fully understood . However, a better understanding of the specific mechanisms of action of these molecules is becoming increasingly important if we want to make predictions on which combination of biostimulants can be more effective.
Humic and fulvic acids
Treatment of bell pepper (Capsicum annuum L. cv. Demre) with humic acid and phosphorous resulted in plants with reduced Na content and elevated N, P, K, Ca, Fe, Mg, S, Mn, and Cu ion contents in roots and shoots, which were associated with a general protective effect under mild salinity stress . Application of humic acids to common bean (Phaseolus vulgaris L.) under high salinity (120 mM NaCl) increased endogenous proline levels and reduced membrane leakage , which are both indicators of better adaptation to saline envirnoments.
Humic acid extracts seem to be beneficial also for field crop monocots. Extracts from vermicompost applied to rice (Oryza sativa L.) played a role in activating anti-oxidative enzymatic function and increased ROS scavenging enzymes. These enzymes are required to inactivate toxic-free oxygen radicals produced in plants under drought and saline stress . One possible mode of action for vermicompost may be the differential regulation of proton ATPases located in the vacuolar and plasma membranes. When Micro-Tom tomato plants were treated with vermicompost, plasma membrane proton extrusion was increased by over 40% which facilitated acid growth and nutrient uptake potential. Interestingly, the auxin insensitive mutant diageotropica (dgt) showed no increase in proton extrusion, indicating that humic substance may increase root growth through mediating auxin signalling .
Microorganisms affecting stress tolerance
Tolerance to salt stress varies within these microorganisms and their tolerance can confer advantages to the host relationship under stress conditions. When two legumes, pea (Pisum sativum) and fava bean (Vicia faba), were inoculated with two different strains of Rhizobium leguminosarum, a salt-tolerant (GRA19) and salt-sensitive (GRL19) plants inoculated with the salt-tolerant strain performed better under moderate salt stress . The authors further found that pea plants had larger nodules and high levels of nitrogen fixation under salt stress when inoculated with GRA19, the salt-tolerant strain of R. leguminosarum. Similar results have been observed for non-symbiotic free-living soil bacteria that are capable of fixing nitrogen. Azospirillum brasilense is closely associated with the plant rhizosphere and can colonize the surface of roots. When chickpea (Cicer arietinum L.) and faba bean were inoculated with A. brasilense, they experienced enhanced nodulation by native rhizobia and greater tolerance to salt stress . Another free-living nitrogen-fixing species, Azotobacter chrococcum A2 demonstrated salt tolerance. Inoculation with A. chrococcum has been shown to increase yields of pea, potato, rice, wheat, and cotton in saline-arid soils. Increased root length and shoot growth was also observed with inoculation [26, 27] with significant positive yield effects for wheat (from 2.8 to 3.5 t ha−1 when grown in conjunction with A. chrococcum) [26, 27].
In barley, Hartmannibacter diazotrophicus E19 (T) is capable of colonizing roots in saline conditions. Inoculation of roots in saline soil increased root and shoot mass significantly, 308 and 189%, respectively. Inoculated roots also had increased relative water content over three and a half times that of control plants . High concentrations of salt can also be inhibitory to rhizobial bacteria. While certain strains of R. leguminosarum, such as viciae SAAN1, are very salt tolerant and able to withstand up to 0.34 M NaCl, they often show lower rates of nodulation in saline soils. These strains are often less competitive with natural rhizobial populations, however.
The stress protection of bacterial biostimulants to rainfed field crops can be of particular relevance under increasing temperatures foreseen by most climate change prediction models. Wheat inoculated with the thermo tolerant Pseudomonas putida strain AKMP7 significantly increased heat tolerance. Inoculated plants had increased biomass, shoot and root length, and seed size. ROS generation under stress treatment was also lessened, with lower levels of expression observed for ROS response genes such as superoxide dismutase, ascorbate peroxidase, and catalase . Similar results have been found with sorghum and other Pseudomonas putida AKMP strains . Psychrophilic (cold-adapted) microorganisms are capable of surviving in extreme conditions and their interactions with plants provide potential mechanisms for improving tolerance . While many strains of soil bacteria with growth-promoting properties have been isolated from low-temperature conditions, few have been tested in conjunction with plants subjected to cold stress.
Wheat inoculated with the cold-tolerant plant growth-promoting bacteria Pantoea dispersa showed improved growth and nutrient uptake, likely due to the solublization of phosphorous and production of IAA .
Inoculation of soil with psychrotolerant (cold tolerant) bacteria can play a role in chilling tolerance. The psychrotolerant soil bacterium, Burkholderia phytofirman, is a plant-growth-promoting rhizobacterium (PGPR) that is capable of colonizing multiple plant species. B. phytofirman was shown to play a role in enhancing chilling tolerance in Vitis vinifera L. by increasing ROS scavenging metabolites and stress-induced genes. Inoculated plants also recovered faster from chilling stress, returning to normal metabolic levels more quickly than controls . B. phytofirman inoculation also alters carbohydrate metabolism and accumulation while having a protective effect on net photosynthesis during cold acclimation and stress [32, 92].
Tomato plants (Solanum lycopersicum cv Mill) were inoculated with cold-tolerant strains of Pseudomonas vancouverensis, and frederiksbergensis as well as Flavobacterium glaciei that were isolated from agricultural fields during winter. Treated tomato seedlings were subjected to a week of chilling stress at 15C and inoculation three of these strains showed significantly reduced electrolyte leakage and ROS activity . Improved stress tolerance and growth-promoting effects of microorganism treatments have been seen in other species also. Inoculation of lettuce (Lactuca sativa L., cv Mantecosa) seeds with A. brasilense increased germination in the presence of salt and demonstrated tolerance through higher total fresh and dry weights of plants at harvest . Additional experiments studying these effects have shown increased biomass, chlorophyll, ascorbic acid content, antioxidant content, and post-harvest shelf life after being subjected to salt stress . Sweet pepper (Capsicum annuum L.) inoculated with A. brasilense and Pantoea dispersa was not affected by moderate levels of salinization, up to 80 mM NaCl, while uninoculated control plants demonstrated lower DW starting at 40 mM NaCl .
Triticum aestivum cv. Buck Ombú inoculated with A. brasilense sp. 245 and subjected to salt stress (320 mM NaCl) and osmotic stress (20 and 30% PEG 6000) had higher FW, DW, and RWC than non-inoculated controls . Analysis of phospholipids and fatty acid composition in inoculated wheat indicated that the distribution profiles of major root phospholipids are altered in inoculated plants, possibly contributing to the increased tolerance . Wheat inoculated with Azospirillum lipoferum and irrigated with 80 mM NaCl had significantly higher leaf and root dry weight than uninoculated controls .
While the mechanisms by which A. brasilense confer tolerance to osmotic stress are not clear, some evidence indicates that inoculation induces wider xylem vessels and greater hydraulic conductance . In inoculated tomato plants subjected to water stress similar changes have been observed, such as larger xylem vessel area, higher stem-specific hydraulic conductivity, thicker stems . Pepper plants co-inoculated with A. brasilense and Pantoea dispersa accumulated more dry matter under salt stress. Inoculated plants showed higher stomatal conductance and rates of photosynthesis under salt stress. The chlorophyll concentration and efficiency of photosystem II were not affected in inoculated plants under stress conditions .
Inhibition of root growth under salt stress conditions is well documented. One of the primary causes of this inhibition is the production and perception of ethylene in the roots . Plants and PGPR both have ACC-deaminases, which possess the ability to lower the concentration of ethylene in the roots and root zone. PGPR-derived ACC-deaminases can reduce ethylene induced inhibition by reducing root zone ethylene  and contribute to maintain relatively higher root-to-shoot ration, a trait that would result beneficial under water shortage.
Biostimulant treatments of agricultural crops have the potential to improve plant resilience to environmental perturbations. In order to fine-tune application rates, biostimulant-plant specificities and techniques is identified that may yield highest impact on stress protection; high priority should be given to better understanding of the causal/functional mechanism of biostimulants. Only once a good understanding of these mechanisms has been reached; we will be able to move to the next generation of biostimulants where synergies and complementary mechanisms can be functionally designed. Comprehension of the specific mechanisms that should be potentiated to overcame a specific stress can be based today on sound/reasonable hypotheses and be more fruitful than the try-and-see approach. A comprehensive and systematic approach has been proposed to discover and characterize novel biostimulants and understand the mode of action for those both known and new using a combined approach utilizing biology, chemistry, and ‘omics . Meta-analysis of the effects of biostimulants has been proposed and an extensive meta-level examination of humic substances on plant growth has been conducted. The analysis found that humic substances increased the dry weight of shoots and roots by at least 20% . However, it should be noted that the diverse conditions, compositions, and species tested do not lend to robust meta-level analysis when an excessive number of variables is present. Identification of synergistic/complementary properties of biostimulants can be pivotal to develop specific formulations targeted to enhance plant response to abiotic stress. For example, biostimulants for improving plant resilience in water limiting environments should stimulate root vs. shoot growth which would allow plants to explore deeper soil layer during the drought season and stimulate the synthesis of compatible solutes to re-establish favourable water potential gradients and water uptake at diminishing soil water. Similar positive effects can be given by those microbial biostimulants that create absorption surfaces around the root systems and sequester soil water in favour of the plants.
MJVA and AM wrote the first draft of the manuscript and took care of the revisions of the review; MJVA contributed to the section “Algal Extracts” and “Carbohydrates, proteins, amino acids and lipids”; OP contributed to the section “Microorganisms affecting stress tolerance”; SDP contributed to the section “Carbohydrates, proteins, amino acids and lipids”; SS contributed to the section “Humic and Fulvic Acids” and “Microorganisms affecting stress tolerance”. All authors read and approved the final manuscript.
All authors declare that they have no competing interests.
Consent for publication
All authors have given consent for publication.
Ethics approval and consent to participate
All authors have given consent to participate.
This work was supported by the EU Project BIOFECTOR Plant Growth–Promoting Bio-effectors (#FP7-KBBE-2012-6 Grant Agreement 312117) and MACSUR Modelling European Agriculture with Climate Change for Food Security—a knowledge hub within FACCE-JPI.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- du Jardin P. Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic. 2015;30(196):3–14.View ArticleGoogle Scholar
- Brown P, Saa S. Biostimulants in agriculture. Front Plant Sci [Internet]. 2015;6. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4550782/. Accessed 13 Oct 2015.
- Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. The importance of the microbiome of the plant holobiont. New Phytol. 2015;206(4):1196–206.View ArticlePubMedGoogle Scholar
- Colla G, Rouphael Y. Biostimulants in horticulture. Sci Hortic. 2015;30(196):1–2.View ArticleGoogle Scholar
- Du Jardin, P. The science of plant biostimulants—a bibliographic analysis. Ad hoc Study Report to the European Commission DG ENTR; 2012.Google Scholar
- Calvo P, Nelson L, Kloepper JW. Agricultural uses of plant biostimulants. Plant Soil. 2014;383(1–2):3–41.View ArticleGoogle Scholar
- Colla G, Nardi S, Cardarelli M, Ertani A, Lucini L, Canaguier R, et al. Protein hydrolysates as biostimulants in horticulture. Sci Hortic. 2015;30(196):28–38.View ArticleGoogle Scholar
- Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B. Seaweed extracts as biostimulants in horticulture. Sci Hortic. 2015;30(196):39–48.View ArticleGoogle Scholar
- Savvas D, Ntatsi G. Biostimulant activity of silicon in horticulture. Sci Hortic. 2015;30(196):66–81.View ArticleGoogle Scholar
- Pichyangkura R, Chadchawan S. Biostimulant activity of chitosan in horticulture. Sci Hortic. 2015;196:49–65.View ArticleGoogle Scholar
- Canellas LP, Olivares FL, Aguiar NO, Jones DL, Nebbioso A, Mazzei P, et al. Humic and fulvic acids as biostimulants in horticulture. Sci Hortic. 2015;30(196):15–27.View ArticleGoogle Scholar
- Gómez-Merino FC, Trejo-Téllez LI. Biostimulant activity of phosphite in horticulture. Sci Hortic. 2015;196:82–90.View ArticleGoogle Scholar
- Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, et al. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic. 2015;30(196):91–108.View ArticleGoogle Scholar
- López-Bucio J, Pelagio-Flores R, Herrera-Estrella A. Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic. 2015;30(196):109–23.View ArticleGoogle Scholar
- Ruzzi M, Aroca R. Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci Hortic. 2015;30(196):124–34.View ArticleGoogle Scholar
- Pereyra MA, Zalazar CA, Barassi CA. Root phospholipids in Azospirillum-inoculated wheat seedlings exposed to water stress. Plant Physiol Biochem. 2006;44(11–12):873–9.View ArticlePubMedGoogle Scholar
- Pereyra MA, García P, Colabelli MN, Barassi CA, Creus CM. A better water status in wheat seedlings induced by Azospirillum under osmotic stress is related to morphological changes in xylem vessels of the coleoptile. Appl Soil Ecol. 2012;53(1):94–7.View ArticleGoogle Scholar
- Hamaoui B, Abbadi J, Burdman S, Rashid A, Sarig S, Okon Y. Effects of inoculation with Azospirillum brasilense on chickpeas (Cicer arietinum) and faba beans (Vicia faba) under different growth conditions. Agronomie. 2001;21(6–7):553–60.View ArticleGoogle Scholar
- Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT. Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic. 2006;109(1):8–14.View ArticleGoogle Scholar
- Fasciglione G, Casanovas EM, Quillehauquy V, Yommi AK, Goñi MG, Roura SI, et al. Azospirillum inoculation effects on growth, product quality and storage life of lettuce plants grown under salt stress. Sci Hortic. 2015;195:154–62.View ArticleGoogle Scholar
- Creus CM, Sueldo RJ, Barassi CA. Shoot growth and water status in Azospirillum-inoculated wheat seedlings grown under osmotic and salt stresses. Plant Physiol Biochem. 1997;35(12):939–44.Google Scholar
- Romero AM, Vega D, Correa OS. Azospirillum brasilense mitigates water stress imposed by a vascular disease by increasing xylem vessel area and stem hydraulic conductivity in tomato. Appl Soil Ecol. 2014;82:38–43.View ArticleGoogle Scholar
- Del Amor FM, Cuadra-Crespo P. Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct Plant Biol. 2012;39(1):82–90.View ArticleGoogle Scholar
- Rojas-Tapias D, Moreno-Galván A, Pardo-Díaz S, Obando M, Rivera D, Bonilla R. Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Appl Soil Ecol. 2012;61:264–72.View ArticleGoogle Scholar
- Chaudhary D, Narula N, Sindhu SS, Behl RK. Plant growth stimulation of wheat (Triticum aestivum L.) by inoculation of salinity tolerant Azotobacter strains. Physiol Mol Biol Plants. 2013;19(4):515–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Egamberdiyeva D, Höflich G. Influence of growth-promoting bacteria on the growth of wheat in different soils and temperatures. Soil Biol Biochem. 2003;35(7):973–8.View ArticleGoogle Scholar
- Egamberdiyeva D, Höflich G. Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ. 2004;56(2):293–301.View ArticleGoogle Scholar
- Bacilio M, Rodriguez H, Moreno M, Hernandez J-P, Bashan Y. Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biol Fertil Soils. 2004;40(3):188–93.View ArticleGoogle Scholar
- Loureiro RR, Reis RP, Marroig RG. Effect of the commercial extract of the brown alga Ascophyllum nodosum Mont. on Kappaphycus alvarezii (Doty) Doty ex P.C. Silva in situ submitted to lethal temperatures. J Appl Phycol. 2014;26(1):629–34.View ArticleGoogle Scholar
- Saa S, Olivos-Del Rio A, Castro S, Brown PH. Foliar application of microbial and plant based biostimulants increases growth and potassium uptake in almond (Prunus dulcis [Mill.] D. A. Webb). Front. Plant Sci. 2015;6:87.Google Scholar
- Spann TM, Little HA. Applications of a commercial extract of the brown seaweed Ascophyllum nodosum increases drought tolerance in container-grown “hamlin” sweet orange nursery trees. Hort Science. 2011;46(4):577–82.Google Scholar
- Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clément C, et al. Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. MPMI. 2012;25(4):496–504.View ArticlePubMedGoogle Scholar
- Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, et al. Burkholderia phytofirmans PsJN Primes Vitis vinifera L. and Confers a better tolerance to low nonfreezing temperatures. MPMI. 2012;25(2):241–9.View ArticlePubMedGoogle Scholar
- Subramanian P, Kim K, Krishnamoorthy R, Mageswari A, Selvakumar G, Sa T. Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) under low temperatures. PLoS ONE. 2016;11(8):e0161592.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhang X, Schmidt RE, Ervin EH, Doak S. Creeping bentgrass physiological responses to natural plant growth regulators and iron under two regimes. HortScience. 2002;37(6):898–902.Google Scholar
- Zhang X, Schmidt RE. Hormone-containing products’; impact on antioxidant status of tall fescue and creeping bentgrass subjected to drought. Crop Sci. 2000;40(5):1344–9.View ArticleGoogle Scholar
- Zhang X, Ervin EH. Cytokinin-containing seaweed and humic acid extracts associated with creeping bentgrass leaf cytokinins and drought resistance. Crop Sci. 2004;44(5):1737.View ArticleGoogle Scholar
- Park E-J, Jeknić Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, et al. Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. Plant J. 2004;40(4):474–87.View ArticlePubMedGoogle Scholar
- Suarez C, Cardinale M, Ratering S, Steffens D, Jung S, Montoya AMZ, et al. Plant growth-promoting effects of Hartmannibacter diazotrophicus on summer barley (Hordeum vulgare L.) under salt stress. Appl Soil Ecol. 2015;95:23–30.View ArticleGoogle Scholar
- Çimrin KM, Türkmen Ö, Turan M, Tuncer B. Phosphorus and humic acid application alleviate salinity stress of pepper seedling. Afr J Biotechnol [Internet]. 2010;9(36). http://www.ajol.info/index.php/ajb/article/view/92903. Accessed 16 Nov 2015.
- García AC, Santos LA, Izquierdo FG, Sperandio MVL, Castro RN, Berbara RLL. Vermicompost humic acids as an ecological pathway to protect rice plant against oxidative stress. Ecol Eng. 2012;47:203–8.View ArticleGoogle Scholar
- Aydin A, Kant C, Turan M. Humic acid application alleviates salinity stress of bean (Phaseolus vulgaris L.) plants decreasing membrane leakage. Afr J Agric Res. 2012;7(7):1073–86.Google Scholar
- Petrozza A, Santaniello A, Summerer S, Di Tommaso G, Di Tommaso D, Paparelli E, et al. Physiological responses to Megafol® treatments in tomato plants under drought stress: a phenomic and molecular approach. Sci Hortic. 2014;22(174):185–92.View ArticleGoogle Scholar
- Kołodziejczyk I, Dzitko K, Szewczyk R, Posmyk MM. Exogenous melatonin improves corn (Zea mays L.) embryo proteome in seeds subjected to chilling stress. J Plant Physiol. 2016;1(193):47–56.View ArticleGoogle Scholar
- Ali SKZ, Sandhya V, Grover M, Linga VR, Bandi V. Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J Plant Interact. 2011;6(4):239–46.View ArticleGoogle Scholar
- Ali SKZ, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B. Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils. 2009;46:45–55.View ArticleGoogle Scholar
- Selvakumar G, Kundu S, Joshi P, Nazim S, Gupta AD, Mishra PK, et al. Characterization of a cold-tolerant plant growth-promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine soil in the North Western Indian Himalayas. World J Microbiol Biotechnol. 2008;24(7):955–60.View ArticleGoogle Scholar
- Cuin TA, Shabala S. Amino acids regulate salinity-induced potassium efflux in barley root epidermis. Planta. 2007;225(3):753–61.View ArticlePubMedGoogle Scholar
- Ertani A, Schiavon M, Muscolo A, Nardi S. Alfalfa plant-derived biostimulant stimulate short-term growth of salt stressed Zea mays L. plants. Plant Soil. 2012;364(1–2):145–58.Google Scholar
- Zhu K, Zhou H, Qian H. Antioxidant and free radical-scavenging activities of wheat germ protein hydrolysates (WGPH) prepared with alcalase. Process Biochem. 2006;41(6):1296–302.View ArticleGoogle Scholar
- Botta A. Enhancing plant tolerance to temperature stress with amino acids: an approach to their mode of action. Acta Horticulturae. 2013. doi:https://doi.org/10.17660/ActaHortic.2013.1009.1.Google Scholar
- Lucini L, Rouphael Y, Cardarelli M, Canaguier R, Kumar P, Colla G. The effect of a plant-derived biostimulant on metabolic profiling and crop performance of lettuce grown under saline conditions. Sci Hortic. 2015;23(182):124–33.View ArticleGoogle Scholar
- Visconti F, De Paz JM, Bonet L, Jordà M, Quiñones A, Intrigliolo DS. Effects of a commercial calcium protein hydrolysate on the salt tolerance of Diospyros kaki L. cv. “Rojo Brillante” grafted on Diospyros lotus L. Sci Hortic. 2015;185:129–38.View ArticleGoogle Scholar
- Del Pilar Cordovilla M, Berrido SI, Ligero F, Lluch C. Rhizobium strain effects on the growth and nitrogen assimilation in Pisum sativum and Vicia faba plant growth under salt stress. J Plant Physiol. 1999;154(1):127–31.View ArticleGoogle Scholar
- Rayirath P, Benkel B, Mark Hodges D, Allan-Wojtas P, MacKinnon S, Critchley AT, et al. Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta. 2009;230(1):135–47.View ArticlePubMedGoogle Scholar
- Nair P, Kandasamy S, Zhang J, Ji X, Kirby C, Benkel B, et al. Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana. BMC Genom. 2012;13(1):643.View ArticleGoogle Scholar
- Nabati DA, Schmidt RE, Parrish DJ. Alleviation of salinity stress in Kentucky bluegrass by plant growth regulators and iron. Crop Sci. 1994;34(1):198–202.View ArticleGoogle Scholar
- Zhang X, Ervin EH. Impact of seaweed extract-based cytokinins and zeatin riboside on creeping bentgrass heat tolerance. Crop Sci. 2008;48(1):364–70.View ArticleGoogle Scholar
- Xu C, Leskovar DI. Effects of A. nodosum seaweed extracts on spinach growth, physiology and nutrition value under drought stress. Sci Hortic. 2015;12(183):39–47.View ArticleGoogle Scholar
- Möller M, Smith ML. The significance of the mineral component of seaweed suspensions on lettuce (Lactuca sativa L.) seedling growth. J Plant Physiol. 1998;153(5–6):658–63.View ArticleGoogle Scholar
- Mancuso S, Azzarello E, Mugnai S, Briand X. Marine bioactive substances (IPA extract) improve foliar ion uptake and water stress tolerance in potted Vitis vinifera plants. Adv Hortic Sci. 2006;20(2):156–61.Google Scholar
- Elansary HO, Skalicka-Woźniak K, King IW. Enhancing stress growth traits as well as phytochemical and antioxidant contents of Spiraea and Pittosporum under seaweed extract treatments. Plant Physiol Biochem. 2016;105:310–20.View ArticlePubMedGoogle Scholar
- Bradáčová K, Weber NF, Morad-Talab N, Asim M, Imran M, Weinmann M, et al. Micronutrients (Zn/Mn), seaweed extracts, and plant growth-promoting bacteria as cold-stress protectants in maize. Chem Biol Technol Agric. 2016;3(1):19.View ArticleGoogle Scholar
- Craigie JS. Seaweed extract stimuli in plant science and agriculture. J Appl Phycol. 2011;23:371–93.View ArticleGoogle Scholar
- Sharma HS, Fleming C, Selby C, Rao JR, Martin T. Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. J Appl Phycol. 2014;26:465–90.View ArticleGoogle Scholar
- Verkleij FN. Seaweed extracts in agriculture and horticulture: a review. Biol Agric Hortic. 1992;8:309–24.View ArticleGoogle Scholar
- Khan W, Rayirath UP, Subramanian S, et al. Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul. 2009;28:386–99. doi:https://doi.org/10.1007/s00344-009-9103-x.View ArticleGoogle Scholar
- Imran M, Mahmood A, Römheld V, Neumann G. Nutrient seed priming improves seedling development of maize exposed to low root zone temperatures during early growth. Eur J Agron. 2013;49:141–8.View ArticleGoogle Scholar
- Guiseley K, Stanley N, Whitehouse P. Carrageenan. Handbook of water-soluble gums and resins. 1980. pp. 5–11.Google Scholar
- Goñi O, Fort A, Quille P, McKeown PC, Spillane C, O’Connell S. Comparative transcriptome analysis of two Ascophyllum nodosum extract biostimulants: same seaweed but different. J Agric Food Chem. 2016;64(14):2980–9.View ArticlePubMedGoogle Scholar
- de Vasconcelos ACF, Zhang X, Ervin EH, de Kiehl J. C. Enzymatic antioxidant responses to biostimulants in maize and soybean subjected to drought. Scientia Agricola. 2009;66(3):395–402.View ArticleGoogle Scholar
- Marfà O, Cáceres R, Polo J, Ródena J. Animal protein hydrolysate as a biostimulant for transplanted strawberry plants subjected to cold stress. Acta Horticulturae. 2009. doi:https://doi.org/10.17660/ActaHortic.2009.842.57.Google Scholar
- Szabados L, Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci. 2010;15(2):89–97.View ArticlePubMedGoogle Scholar
- Nanjo T, Kobayashi M, Yoshiba Y, Sanada Y, Wada K, Tsukaya H, et al. Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J. 1999;18(2):185–93.View ArticlePubMedGoogle Scholar
- Posmyk MM, Szafrańska K. Biostimulators: a new trend towards solving an old problem. Front Plant Sci. 2016;7:48.View ArticleGoogle Scholar
- Peel GJ, Mickelbart MV, Rhodes D. Choline metabolism in glycinebetaine accumulating and non-accumulating near-isogenic lines of Zea mays and Sorghum bicolor. Phytochemistry. 2010;71(4):404–14.View ArticlePubMedGoogle Scholar
- Park E-J, Jeknic Z, Chen THH. Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol. 2006;47(6):706–14.View ArticlePubMedGoogle Scholar
- Chen THH, Murata N. Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci. 2008;13(9):499–505.View ArticlePubMedGoogle Scholar
- Cuin TA, Shabala S. Exogenously supplied compatible solutes rapidly ameliorate NaCl-induced potassium efflux from barley roots. Plant Cell Physiol. 2005;46(12):1924–33.View ArticlePubMedGoogle Scholar
- Blum A. Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ. 2016.Google Scholar
- Bulgari R, Cocetta G, Trivellini A, Vernieri P, Ferrante A. Biostimulants and crop responses: a review. Biol Agric Hortic. 2015;31(1):1–17.View ArticleGoogle Scholar
- Zandonadi DB, Santos MP, Caixeta LS, Marinho EB, Peres LEP, Façanha AR, et al. Plant proton pumps as markers of biostimulant action. Scientia Agricola. 2016;73(1):24–8.View ArticleGoogle Scholar
- Selvakumar G, Joshi P, Mishra PK, Bisht JP, Gupta HS. Mountain aspects influence the genetic clustering of psychrotolerant phosphate solubilizing Pseudomonads in the Uttarkhand Himalayas. Curr Microbiol. 2009;59:432–8.View ArticlePubMedGoogle Scholar
- Upadhyay SK, Singh DP. Saikia R Genetic diversity of plant growth promoting rhizobacteria from rhizospheric soil of wheat under saline conditions. Curr Microbiol. 2009;59(5):489–96.View ArticlePubMedGoogle Scholar
- Sandhya V, Ali AS, Grover M, Reddy G, Venkateswarlu B. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils. 2009;46(1):17–26.View ArticleGoogle Scholar
- Zahran HH. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev. 1999;63(4):968–89.PubMedPubMed CentralGoogle Scholar
- Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L. Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech. 2015;5(4):355–77.View ArticleGoogle Scholar
- Egamberdiyeva D. Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant. 2009;31(4):861–4.View ArticleGoogle Scholar
- Paul D, Lade H. Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev. 2014;34(4):737–52.View ArticleGoogle Scholar
- Kaushal M, Wani SP. Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol. 2015;66(1):35–42.View ArticleGoogle Scholar
- Siddiqui KS, Williams TJ, Wilkins D, et al. Psychrophiles. Ann Rev Earth Planet Sci. 2013;41:87–115. doi:https://doi.org/10.1146/annurev-earth-040610-133514.View ArticleGoogle Scholar
- Thao HTB, Yamakawa T. Phosphite (phosphorous acid): fungicide, fertilizer or bio-stimulator? Soil Sci Plant Nutr. 2009;55(2):228–34.View ArticleGoogle Scholar
- Jiang C, Belfield EJ, Cao Y, Smith JAC, Harberd NP. An arabidopsis soil-salinity–tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. Plant Cell. 2013;25(9):3535–52.View ArticlePubMedPubMed CentralGoogle Scholar
- Nadeem SM, Zahir ZA, Naveed M, Ashraf M. Microbial ACC-deaminase: prospects and applications for inducing salt tolerance in plants. Crit Rev Plant Sci. 2010;29(6):360–93.View ArticleGoogle Scholar
- Povero G, Mejia JF, Di Tommaso D, Piaggesi A, Warrior P. A systematic approach to discover and characterize natural plant biostimulants. Front Plant Sci [Internet]. 2016;7. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4820456/. Accessed 31 Aug 2016.
- Rose M, Patti A, Little K, Brown A, Jackson W, Cavagnaro T. A meta-analysis and review of plant-growth response to humic substances: practical implications for agriculture. Adv Agron. 2014;124:37–89.View ArticleGoogle Scholar