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Review

Sustainable Olive Culture under Climate Change: The Potential of Biostimulants

1
Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal
2
LAQV-REQUIMTE, Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal
3
Integrated Biology and Biotechnology Laboratory, Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal
4
Center for the Research and Technology of Agro-Environmental and Biological Sciences, University of Trás-os-Montes and Alto Douro, 5001-801 Vila Real, Portugal
5
LAQV-REQUIMTE, Department of Biology, Faculty of Sciences, University of Porto, Rua Campo Alegre, 4169-007 Porto, Portugal
*
Author to whom correspondence should be addressed.
Horticulturae 2022, 8(11), 1048; https://doi.org/10.3390/horticulturae8111048
Submission received: 22 September 2022 / Revised: 31 October 2022 / Accepted: 31 October 2022 / Published: 8 November 2022
(This article belongs to the Special Issue Sustainable Oliviculture Facing Emerging Challenges)

Abstract

:
Climatic extreme events, like droughts, heatwaves, and floods are becoming recurrent and represent a threat to agriculture, lowering plant growth and productivity. The Mediterranean region is a climate-change hotspot, where traditional agricultural systems, like olive groves, are particularly challenged. Both the traditional and intensive systems of olive culture coexist in the Mediterranean. Both systems differ in their demands for water and agrochemicals, but nowadays, the global inputs of agrochemicals and irrigation have increased to achieve high productivity and profitability. Finding sustainable alternatives to maintain high productivity under the ongoing climate change is urgent to meet the EU-Farm to Fork strategy and climate neutrality. Candidate eco-friendly alternatives include biostimulants. These are substances or microorganisms, that activate signaling cascades and metabolic processes, increasing plant yield, quality, and tolerance to stressors. These benefits include a better growth, nutritional status and water availability, leading to a decreased demand for irrigation and agrochemicals. In this review, we aim to present different types of biostimulants (e.g., seaweed, protein hydrolysates, humic substances, microorganisms and nanomaterials), their mode of action and benefits in agriculture. We also explore the current state-of-the-art regarding the use of biostimulants in olive culture, and their potential benefits to increase tolerance to (a)biotic challenges.

Graphical Abstract

1. Introduction

Agriculture is facing unprecedented challenges due to the high food demand for the increasing world population, high competition over the scarce natural resources, and climate change threats [1]. The increasing global population exerts high pressure on the arable land to increase productivity but at the expense of high uses of agrochemicals (e.g., fertilizers and pesticides) [1]. In addition, climate change, particularly drought and heat waves are threats to food security and production all over the world [2,3] and are predicted to become more frequent and intense leading to vast socioeconomic and biodiversity losses [2,3]. Under this scenario, several changes must be implemented, starting with developing more sustainable agricultural practices without increasing resource deterioration. Within the Farm to Fork strategy of the European Union (EU), several targets to adapt to climate change and to increase crops’ resilience were established [4]. The Farm to Fork strategy aims to reduce the use of fertilizers by 20% and pesticides by 50%, by implementing sustainable agricultural practices [4]. To achieve these goals, new strategies evolved in the last decades to improve agriculture’s sustainable production. Biostimulants are a promising strategy to reach sustainable agricultural practices, since are based on the use of (preferably) natural compounds or microorganisms whose function in low levels promote plant growth-related processes, improve plant nutrient uptake and use efficiency, increase resistance or tolerance to abiotic stress, improve the quality of crop-derived products, and/or improve soil quality and health [5,6].
Biostimulants differ from the synthetic substances widely used in agriculture to enhance crop productivity, like inorganic nitrogen and phosphorous fertilizers, pesticides and others agrochemical [7]. Biostimulants act in several molecular and physiological processes of the plant boosting its performance. Fertilizers supply the plants with nutrients required for cells to sustain growth and metabolism, and pesticides help in the control (extermination) of pests and weeds, but their imbalanced use impact negatively various components of water, air and soil ecosystem as well as human health [7]. In the case of biostimulants, since most of the components are from natural origin, their impact in the environment is reduced [5,6]. Biostimulants are reported to be biodegradable, non-polluting and non-hazardous/non-toxic to several organisms, particularly at the recommended application rates [8]. This aspect is important from an environmental point of view. Therefore, the use of biostimulants in agriculture is in line with the demand for more sustainability in the agri-food sector, and these substances or microorganisms are suitable for organic and/or conventional farming [8].
Several categories of biostimulants have been described, but some of them still need a more comprehensive assessment in agriculture to answer all the requirements necessary for their wider use. The most used biostimulants are the seaweeds, protein hydrolysates, humic substances and microorganisms, and recently a new type of biostimulant have been described, the nanoparticles or nanomaterials [5,6]. Various studies are available on the advantages (e.g., growth promotion and stress tolerance) of using these biostimulants on crop species, such as rice, soybean, maize, tomato, grapevine, orange, and lemon trees [9]. However, their potential benefits in olive culture, one of the most important economic sectors in the Mediterranean basin, is less known.

2. Olive Tree and Culture Systems

The olive tree (Olea europaea L.) belongs to the genus Olea within the Oleaceae family, which comprises 600 species within 25 genera [10]. The O. europaea L. species is an evergreen tree presenting a medium size that can grow up to 10 m [11]. It is a xerophyte species, well adapted to the harsh environment conditions of the Mediterranean region. Olea europaea, subspecies europaea, includes the wild (Olea europaea subsp. europaea var. sylvestris) and the cultivated olive form (Olea europaea subsp. europaea var. europaea) [11].
This species is grown in the Mediterranean basin many years ago. The olive tree’s existence goes back to the 12th millennium BC, and the cultivated olive has appeared in Asia Minor [11]. Archaeological findings from Ebla, Syria, mention oil production dating back to the 3rd millennium BC [11]. Over the years, the olive tree plantations increased mainly in Syria, Palestine, and Egypt, where oil was used in the lamps, and also for health purposes (used of oil to protect the skin against cracks and sunburns) [11]. The expansion of cultivated olive in the Mediterranean basin occurred mostly during the Roman Empire [11].
Nowadays, the olive culture comprises several socioeconomic benefits for the Mediterranean region. For instance, their products (table olives and olive oil) are increasingly recognized for their health benefits, which increased the demand by consumers, increase the producers’ income, and the generation of employment [11,12,13]. Also, oliviculture and olive oil integrate the landscape and socio-cultural heritage of many Mediterranean countries, including in gastronomy [14]. The importance of this chain of value has thus raised the research and innovation dedicated to olive culture.
Europe dominates the Olive production and market. According to the EU agricultural outlook 2021-31, EU produces roughly 68% of the world’s olive oil, with ~4 million ha mostly in the EU Mediterranean countries, with Spain and Italy, Greece and Portugal being top producers [11]. The EU also holds a major share of global consumption (47%), being Spain, Italy, Greece, and France in the top consuming countries (EC 2021) [11]. Table 1 shows the production of olive oil in the last years and their consumption in the Mediterranean countries. Beside olive oil, also table olives market has been increasing in the last years and the Mediterranean countries, particularly Spain and Egypt, are the main producers (Table 1) [11]. Olive fruits and oil are well known for their nutritional value. They are rich in lipids (particularly a high content of unsaturated, monounsaturated and polyunsaturated fatty acids), on other minor compounds like phenols, sterols, squalene, tocopherol, proteins and pigments [15].
In the Mediterranean region, there are two major models of olive cultivation, the traditional and the intensive and/or high-density olive groves model, although with different cultivated area (much more for the traditional olive culture). In the traditional model, where olive trees are dryland farming or irrigated, with 40 to 240 trees/ha, the use of phytopharmaceuticals and fertilizers is reduced [16]. In some way, the grove is managed less industrially, farmers often only cut the weeds to facilitate access to the olive trees. Also, biodiversity is higher in this model of production [17,18]. In the intensive and/or high-density olive groves model the density of the trees per hectare varies between 200 to 2500/ha [12]. In these orchards, trees can be planted in hedgerows, the trees are irrigated [e.g., olive water requirement in intensive culture: around 800 mm ha −1 year−1 (source: International Olive Oil Council)], and phytopharmaceuticals and fertilizers are applied under control measures. This model of culture is oriented to be super productive and with high income [16]. The biodiversity in this model of production is usually poorer than compared in the traditional model [17,18].
Besides requiring different cultivation practices, the intensive and/or high-density olive groves model and the traditional model of olive cultivation also require cultivars with different characteristics. Regarding the olive cultivars, more than 2600 cultivars are estimated to exist worldwide [19]. Of these, over 600 cultivars are certified and registered in the World Bank of Olive Germplasm established in Spain [20]. Few are the cultivars that proved to be suitable for intensive and/or super-intensive culture systems (e.g., ‘Oliana’, ‘Sikitita’, ‘Lecciana’, ‘Arbequina’, ‘Arbosana’ and ‘Koroneiki’) [21], while interest is boosting regarding an integrative characterization of the genetic resources provided by ancient cultivars (e.g., ‘Cobrançosa’, ‘Negrinha’, ‘Manzanilla’, ‘Hojiblanca’, ‘Cornicabra’, ‘Castellana’) to improve tolerance to (a)biotic stressors.
Table 1. Olive oil production (×1000 t) and consumption (% of world), and table olives production (×1000 t) in the Mediterranean countries in the last years (source: International Olive Oil Council) and main cultivars [19,22]. Na–data not available at the International Olive Oil Council.
Table 1. Olive oil production (×1000 t) and consumption (% of world), and table olives production (×1000 t) in the Mediterranean countries in the last years (source: International Olive Oil Council) and main cultivars [19,22]. Na–data not available at the International Olive Oil Council.
CountryOlive Oil ProductionOlive Oil
Consumption
Table Olives ProductionCultivars
2020/20212021/20222020/20212021/2022
Spain1389130017547645Arbequina, Arbosana, Aloreña, Alfafara, Blanqueta, Cornicabra, Empeltre, Farga, Hojiblanca, Lechín, Manzanilla, Morisca, Negral, Nevadillo, Picual, Picudo, Redondilla, Royal, Sevillenca, Verdeal de Vélez-Málaga and Villalonga
Greece2752254230165Anphissis, Chalkidiki, Conservolia, Kalamon, Koroneiki, Kolybada, Liano-lia, Mastoidis, Megaritiki, Ntopia Atsicholou, Ntopia Pierias, Petrolia Serron, Smertolia and Chrysophylli
Italy274315158059Ascolana, Bella di Cerignola, Biancolilla, Bosana, Canino, Carolea, Casaliva, Casasene, Cellina di Nardò, Cima di Melfi, Coratina, Frantoio, Giarraffa, Leccino, Maurino, Mele, Moraiolo, Nocellara del Belice, Nocellara etnea, Ogliarola, Olivastra Seggianese, Pendolino, Peranzana, Razzola, Taggiasca and Termite di Bitetto.
Portugal10012021621Azeiteira, Blanqueta, Cobrançosa, Cordovil, Carrasquenha, Galega, Lentisca, Madural, Verdeal and Redondil
Tunisia1402401NaNaBaroni, Chétoui, Chemlali, Oueslati, Chemlali Tataouine, Esraadki, Gerboui, Meski, Neb Jmel, Rkhami, Roumi, Rajou and Zalmati
Turkey2102285360402Ayvalik, Balıkesir, Domat, Erkence, Çakir, Halhali, Memecik, Memeli, Uslu, Izmir Sofralik, Gemlik, Kilis, Kiraz and Otur
Morocco1602004130130Picholine Marocaine, Picholine Languedoc, Dahbia, Haouzia, Menara and Meslala
Algeria70983278326Aaroun, Albani, Aedli, Azeradj, ‘Ballouti amzel, Blanquette, Bouchouk, Chemlal, Djbaili, Ferkani, Ferdel, Khadraya, Hamra, Limli, Mekki, Sigoise, Roulette and Zeboudj
Egypt30201500500Wateken, Maraki, Wardan, Meloky, Sebhawy, Sinawy, Bez El Anza, Kosiem, Abou Monkar and Siwy

3. Impact of Climate Changes on Olive Trees Performance and Quality

Olive trees are known to tolerate a broad range of environmental stresses, including heat, drought, salinity and high levels of UVB [13,23,24]. For drought stress tolerance, olive trees developed several morphological adaptations and physiological and biochemical mechanisms, including some xerophytic morpho-anatomic characteristics [25,26]. Salt tolerance in olives is mostly related to efficient mechanisms of ion exclusion and retention of Na+ and Cl- in the root [27]. These stress adaptation strategies are already activated at the expense of plant energy, reducing plant development and growth.
The persistence and frequency of weather climate events due to climate change represent a threat to this culture, decreasing photosynthesis, yield, and changing fruit and oil quality [12,13,15]. Changes in temperature and precipitation patterns in spring and summer coincide with one of the most sensitive phases of the olive life cycle, the reproductive phases of fruit set and fruit development, leading to negative consequences for olive crop yields [28]. Drought and salinity may decrease the olive leaf water status and influence stomatal closure [29,30]. Water deficit may also compromise photosynthetic rates and photochemical efficiency [23,29,31]. Moreover, photosynthetic pigments are very sensitive to drought, decreasing their content [23]. Also, excessive heat decreases the net CO2 assimilation rate, stomatal conductance, transpiration, and intercellular CO2 concentration, and increases pigment contents in olives [32,33]. Moderate and high levels of UV-B rays increase the production of reactive oxygen species (ROS) in olives, leading to oxidative stress and consequent reductions in photosynthesis (light-dependent reactions and C assimilation), including decreases in RuBisCO activity, and in photosynthetic pigments [32,34,35,36]. Salt stress in olive reduce photosynthesis, chlorophyll levels, stomatal conductance and increase the production of ROS leading to lipid peroxidation [24,27,30]. These alterations in olive performance also affect productivity and quality [13]. Drought decreases fruit yield and oil accumulation and accelerates maturation [13]. Fruit metabolite content (phenolic and lipid compounds), as well as oil total phenols and sensory quality, can be increased by drought conditions [15]. However, mild effects of drought conditions on oil free acidity, peroxide value, and specific absorption coefficients (K232, K270, and ΔK) were reported [13,37]. High temperatures also change oil quality, reducing oil concentration in fruits, oleic acid, and total polyphenol contents [38,39]. Salinity may lead to increased phenolic compounds levels, such as tyrosol, hydroxyltyrosol, and acids vanillic, coumaric, and ferulic [30]. Some reports pinpoint that salinity induced some effects on oil composition, but no major adverse effect on fatty acid composition were found [30].

4. Sustainable Strategies to Improve Olive Culture under Climate Change Conditions: Biostimulants

The intensive and/or high-density systems of olive culture have been increasing in the last years, as this model offers a better cost/benefit for the producers. However, the cost for the environment is often neglected. As this model of olive production uses more fertilizers and pesticides, increase soil erosion and the rates of soil fertility loss, degradation of habitats and landscapes, and over-exploitation of vulnerable and scarce water resources [40]. Thus, it is primordial to establish a commitment in terms of the socioeconomic benefits without neglecting the ecosystem crucial for the generations to come.
Sustainable olive culture practices must address the challenges posed by climate change, and the intensive and high-density systems has to be replaced by less water-demanding practices like dry farming or the emerging partial root-zone drying [12,41] or even integrate the olive cultivation in agroforestry models. Also, other strategies to enhance olive culture under climate change conditions have been proposed, such as improvement of soil management, cover crop and pruning, use of alternative sources of irrigation water [42], and application of spray compounds to protect against extreme weather conditions (e.g., kaolin, salicylic acid and copper) [12]. Within the cover crop management practices, the use of seed-mix cover crops have been proposed, but it should be taken in to account that some types of cover crops can compete with the main crop for nutrients and/or water, particularly during the growing season [12]. However, in areas suffering from, for example, severe drought it may even turn out to be unsustainable the olive production as it demands irrigation [43,44,45]. Therefore, several changes in the olive culture practices must be implemented to produce safe and enough food without depletion of resources. Among the several emerging strategies to increase plant tolerance to biotic and abiotic stresses, biostimulants are a promising agronomic tool to achieve a sustainable agriculture [46]. Biostimulants are natural compounds or microorganisms that stimulate plant processes leading to improved nutrient use efficiency, growth and yield, and increased tolerance to biotic and abiotic stresses [47,48]. The positive effects of using biostimulants on plant growth and yield under biotic and abiotic stresses are described for several important horticultural crops (e.g., rice, soybean, maize, tomato, maize, grapevine, and spinach), fruit trees (e.g., orange and lemon trees) and ornamentals plants [9]. Biostimulants have also been proposed as candidates to enhance the phytoremediation of polluted environments [49]. Recent studies showed that plants treated with biostimulants (e.g., arbuscular mycorrhizal fungi, plant growth promoting rhizobacteria, silymarin-based biostimulant, and commercial biostimulants like Fertiactyl Pós ® and Megafol®) and growing in polluted sites with heavy metals or pesticides, showed higher capacity to growth and promoted phytoremediation [49].
In the last years, the market for biostimulants has been increasing at a rate of around 12% per year, and it is expected to achieve in 2026 a market value of around 6 billion dollars [50]. The success of these products is mostly related to the actual changes in agricultural and environmental policies that drive the use of sustainable alternatives to synthetic chemicals allied to the increase in climate change scenarios [50].
Mediterranean olive producers’ countries have been implementing strategies to be more sustainable. Aligned with the Farm to Fork (F2F) Strategy, the EU aimed that the food systems become fair, healthy, and environmentally friendly. To be able to achieve these goals, agriculture must be neutral and have a positive impact on the environment, promote climate change mitigation and adapt to its impacts, promote biodiversity, ensure food security, nutrition, and public health, make sufficient, safe, nutritious and sustainable food access to everyone promoting fair trade and a fairer economic return [51]. EU countries when implementing those measures need to reduce, or even eliminate, the use of agrochemicals and pollutants, replacing them with natural alternatives. The biostimulants are alternatives able to maintain or even improve the nutritional value of soil (and consequently food) and promote and/or improve water management [5]. Moreover, the use of these compounds meets the F2F-EU goals, valorizing the native biodiversity, promoting strategies to reduce or eliminate alien species, and educating people to achieve those goals and improve food security [4].
The beneficial impacts of biostimulants led researchers to hypothesize that they may help the plant to better resist environmental stresses [5,52], namely heat and drought. The advantage of using these substances relay on their effectiveness in improving crop productivity and quality [52]. In line with the F2F strategy and to face the challenges of climate change, biostimulants thus emerge as promising alternatives to hazardous agrochemicals, putatively suitable for more sustainable agriculture. Additionally, these biostimulants are often considered to be of low cost [53], and may have multiple natural origins, including algae [52].

4.1. Types of Biostimulants and Mode of Action

Several types of biostimulants are available in the market, and they can be found in liquid, powder, or granular form applied in leaves (foliar spray) or/and around the root zone. Biostimulants can be classified according to the source of raw material into several groups, such as seaweed, protein hydrolysates, humic acids, nanoparticle and microorganisms (e.g., bacteria and fungi) [48]. More recently, nanomaterials were also integrated into the class of biostimulant as they can stimulate plant metabolic and physiological responses [54]. Despite the great interest and the several studies available on biostimulants, the natural complexity of these compounds makes it difficult to unveil their mode of action. Previous studies indicate that biostimulants act as priming agents, triggering molecular and physiological mechanisms that improve the plant’s ability to defend faster and stronger against subsequent stresses [55].

4.1.1. Seaweeds

Seaweeds have been used as a fertilizer in agriculture for many years and provide a source of organic matter and nutrients [9]. Seaweed extracts represent around 1/3 of biostimulants’ market worldwide [56]. Seaweeds include macroalgae comprising around 10,000 species, of which brown seaweeds with Ascophyllum, Fucus, Laminaria are the dominant groups [57]. Several seaweed species were already analyzed as plant biostimulants, belonging to the red algae (Jania rubens, Gracilaria edulis, and Kappaphycus alvarezii), green algae (Ulva lactuca) and brown algae (Ascophyllum nodosum, Ecklonia maxima, and Laminaria) [58,59,60,61]. The species, algae production and localization, and extraction methods of seaweed extracts influences their characteristics (color of the extract as well as the viscosity, solid content, particulate matter content and chemical composition) and hence its efficacy/bioactivity [62].
Seaweed extracts benefit plant growth and yield, root development, plant water status and water use efficiency, promote nutrient assimilation and increase resistance to abiotic (drought, salinity and heat), and biotic (pests and diseases) stressors [63,64]. These algae contain several compounds, such as polyphenols (e.g., phloroglucinol and eckol), hormones (e.g., auxins and cytokinins), polysaccharides (e.g., fucoidan, laminaran, carrageenan, and alginates) and vitamin K1 derivatives (e.g., kahydrin), that act in several central metabolic processes, like photosynthesis and antioxidant defence system. In particular, these biostimulants modulate the photosynthesis (adjusting the expression of genes related to RuBisCO activation, RbCS1A and RCA), control stomata aperture and induce protection against dehydration (through the overexpression of several genes, like PIP1;2, bCA1, MYB60 and RK2, RAB18 and LEA group 2), and activate the expression of genes related to antioxidants (e.g., ascorbate) and antioxidant enzymes (e.g., SOD, CAT and APX) that help to control the levels of reactive oxygen species (ROS), reducing lipid peroxidation [9,45,57,59,65]. These biostimulants also stimulate the phenylpropanoid pathway as well as flavonoids biosynthesis, contributing to oxidative stress alleviation [9,45].

4.1.2. Protein Hydrolysates

Another type of biostimulant very used in agriculture includes animal- or plant-based hydrolysed proteins. Protein hydrolysates are usually derived from by-products of agro-industrial activities and are a combination of amino acids, polypeptides, and oligopeptides obtained by chemical, thermal, microbial, or enzymatic hydrolysis [66]. Protein hydrolysate biostimulants derived from collagen are rich in proline and glycine, whereas glutamic acid is more abundant in those derived from plant sources [67]. Protein hydrolysates derived from animal sources are richer in nitrogen (9–16% total dry matter) and have a lower release rate [61].
The action mechanism of PH involves stimulation of the plant antioxidant defense system and the photosynthesis. Concerning the antioxidant protection, PH upregulate the expression of phenylalanine ammonia lyase (PAL), heat shock proteins (e.g., HSP16.9, HSP22 and HSP116.9) and dehydrins (e.g., DHN2, DHN2, DHN4, DHN13 and DHNCCor410) genes, increase the antioxidant enzyme activities (SOD and APX), and the production of stress defence metabolites like terpenes, carbohydrates, amino acids and flavonoids, that control ROS overaccumulation, protect proteins and increase membrane stabilization [68]. Moreover, PH promote the photosynthesis and growth by stimulating pigment synthesis and protein production [69].
Beside plant performance, PH are also described to promote fruit productivity, growth, and quality in several crops, like tomato, papaya, passionfruit, corn, kiwifruit and pepper [70,71]. PH improve fruits nutritional level, increasing glucose, ascorbate, carotenoids, and stimulate secondary metabolism enzymes and consequently secondary metabolites production, like thymidine and flavonoids levels [70,71]. These beneficial effects of PH are particularly notorious under limited water availability (drought conditions), which is very relevant under the actual scenario of climate change.

4.1.3. Humic Substances

Biostimulants based on humic substances (HS) contain fulvic and/or humic acids, which are the major components of soil organic matter [58,72]. Humic substances biostimulants result from the decomposition processes of animals and plants, or the activity of soil microbes [48,73]. Humic substances are mostly composed of small amphitatic molecules that can form (supra)molecular aggregates in solution. In plants, the application of HS (e.g., extracted from leonardites or derived from vermicompost) activate several antioxidant defences like, antioxidant enzymes (e.g., increase the activity of SOD, CAT, APX and Gr), antioxidants (e.g., tocopherols, phenolic compounds, ascorbate and proline) and heat shock proteins (e.g., upregulate the expression of HSP101, HSP81.8 and HSP17.6A genes) [74,75,76]. HS modulate the production of chlorophyll, regulate the expression of aquaporins leading to higher plant water status, and activate the nitrate metabolism which increase protein production and biomass accumulation [74,76]. Moreover, this king of biostimulants enhance root growth, nutrient uptake (e.g., can act as Fe-HS complexes), crop tolerance to environmental stresses [77], and even reduce the mutagenic activities of chemical compounds used in agriculture [78,79]. Current evidence suggests that the biostimulant effects of HS are characterized by both structural and physiological changes in roots and shoots related to nutrient uptake, assimilation and distribution (nutrient use efficiency traits). In addition, they can induce shifts in plant primary and secondary metabolism related to abiotic stress tolerance which collectively modulate plant growth and promote plant fitness [80]. When combined with other biostimulants, like microalgae, HS have synergic activity [66,67].
Concerning HS effects on fruit and vegetable productivity and quality, several studies demonstrated positive effects, even under stress conditions. In strawberry and muskmelon, HS application enhanced fruit yield, fresh weight, sugar content, firmness and diameter [80]. Moreover, HS increased aubergine, pineapple, potato and peach growth, tomato productivity, yield and sugar content, and enhanced grape berry and pepper size (width and weight) [80]. Vegetable crop growth and biomass production (e.g., in broccoli and chicory) are also stimulated by HS, mainly due to the enhancement of the nutrient use efficiency [80,81,82].

4.1.4. Microorganisms

Biostimulants based on microorganisms contain bacteria (e.g., plant growth-promoting bacteria-PGPB), yeast, and fungi (arbuscular mycorrhizal fungi-AMF) isolated from soils, plants, water, and/or organic materials [59,83] that interact with the plant roots, establishing mutual symbiotic associations or enhancing nutrient availability [48]. Within the PGPB biostimulants, those based on several rhizobacteria genera, like Azotobacter, Azospirillum, Bacillus, Pseudomonas, Rhodococcus, Rhizobium, Streptomyces, and Ochrobactrum, and within the AMF biostimulants, those derived from Rhizophagus spp., Septoglycus viscosum, Claroideoglomus etunicatum, and Claroideoglo mus claroideum are very used in agriculture [84]. Moreover, other fungal-based biostimulants derived from endophytic fungi, like the Trichoderma spp. (Ascomycota) and Sebacinales (Basidiomycota), are also well known and used in sustainable agriculture production [5].
PGPB action mechanism includes the activation of the antioxidant battery (e.g., antioxidant enzymes and metabolites), upregulation of stress protective genes (sHSP, ERD15, CaPR-10, VA and Cadhn), increase of the synthesis of 1-aminocyclopropane-1-carboxylate deaminase that promote growth, improvement of nutrient availability, osmoregulation, production of volatile organic compounds, and stomata control regulation [85,86,87]. Considering the AMF biostimulants action mode, they also involve the activation of the antioxidant enzymes (SOD and CAT) and metabolites (glutathione), and the downregulation of lipoxygenase [88]. Moreover, AMF also promote nutrient uptake, increase chlorophyll synthesis, osmoregulation and modulated the stomatal aperture by controlling ABA metabolism [88,89,90]. This kind of biostimulant regulate the expression of genes related to cellulose biosynthesis and cell growth (XM_020312442.1 and XM_020331230.1) strengthening cell wall [91].

4.1.5. Nanoparticles or Nanomaterials

A new type of biostimulant includes nanoparticles/nanomaterials (with a size between 1 nm and 100 nm) [54]. These can be of metals (e.g., metal-oxides), metalloids (e.g., silicon), and non-metals, or of carbon (e.g., carbon nanotubes), organic (e.g., chitosan-based) or made of other materials (e.g., nanoclays). The nanoparticles (NPs) have a superior surface area to volume ratio compared to the non-nano-scale counterparts, improving their properties and significantly increasing their activity. NPs are often applied by foliar spray or in nutrient solutions, and can modify the plants growth and yield, and increase the nutraceutical quality of food crops, as well as their tolerance to stress [54]. Some NPs acting as biostimulants may be metallic such as TiO2, ZnO2, and Cu [54,92], of Si [93], and chitosan-based NPs [94]. For example, Regni et al. [95] showed that ZnO-NPs were beneficial to the olive tree in in vitro culture, while Cu-NPs showed activity against F. oleagineum and Colletotrichum spp., thus being beneficial to olive plants disease control [96]. Also, Si-NPs show potential for abiotic stress management, once alleviated drought effects on olive trees and modulated their response to the stress [93], besides of improving photosynthesis in drought stressed rice plants [97], and increasing the tolerance against salinity stress in cucumber by regulating proline and cytokinins [98].
The biostimulant properties of these compounds are associated with the type on NP, structure and nature of the materials [92]. For instance, due to the catalytic properties of TiO2, they increased the content and expression of LHCII b genes in the thylakoid membrane, thus improving light absorption in chloroplasts, and accelerated RuBisCO activase, overall improving photosynthesis [92]. Moreover, this kind of NPs, can act as pro-oxidants and antioxidants modulating ROS signaling, can enhance nitrate reductase activity and nitrogen assimilation, leading to higher amino acids and protein production, and can promote growth [92]. In the case of ZnO2NPs, they increase Zn availability in plants, enhancing chlorophyll and photosynthesis, and modulate the expression of genes and transcription factors (e.g., ARP, MPK4, MKK2, SKRD2, MYC, bHLH, EREB, HsfA1a, R2R3MYB, and WRKY1) associated with multiple responses, like physiological, hormonal, and abiotic stress tolerance [54,92].
Metal-NPs may slowly release, at controlled levels, nutrients (e.g., Fe, Mn, Zn, and Cu), thus providing a balanced transfer to the soils and food chain, in comparison with bulk fertilizer [99]. Besides the interest as plant stimulants, an increasing interest for nanomaterials in agriculture is related with their capability of controlled delivery of chemicals, pesticides or plant growth regulators [100].

4.2. Biostimulants Use in Olive Culture and Their Impact on Stress Tolerance

The use of biostimulants in olive culture is very limited, and few information is available about the advantages of the application of these compounds to alleviate the negative effects of biotic and abiotic stresses (Figure 1). Most of these studies were performed with microbial based biostimulants to control some pathogens responsible for disease that causes enormous productivity losses.

4.2.1. Biotic Stress Tolerance

The fungal disease, verticillium wilt of olive (VWO), caused by the fungal pathogen Verticillium dahliae Kleb is considered one of the most destructive diseases in olive groves causing enormous economic losses [101,102]. Verticillium wilt disease is very difficult to control, since the microsclerotia (the infective propagules of V. dahliae) can persist in the soil or in plant debris for several years and they can be spread by rain, irrigation and/or agricultural practices [102]. V. dahliae can penetrate the plant cell wall and infect the xylem vessels causing callose accumulation and obstruction of these vessels. This reduce the water transport and causes the wilt syndrome which symptoms are chlorosis, necrosis, defoliation, stunting, and in the worst case scenario plant death [102].
In the last decades, innovative approach based on natural products and microorganism (e.g., fungus, bacteria, seaweed and plant extracts) have been studied to control VWO [76,77]. Regarding the group of microbial biostimulants, several fungi and bacteria are described to be effective on the biocontrol of VWO (Table 2). The fungal-based biostimulants derived from the endophytic fungi Trichoderma spp. have been studied and the mechanisms of action are mostly based on the synthesis of antibiotics, production of hydrolytic enzymes that degrade the cell walls of the pathogen, competition for nutrients and space, and stimulation of plant defence system [103,104]. In the high susceptible olive cultivar ‘Picual’ (4 to 5-months-old plants), the treatment with Trichoderma asperellum (strains Bt3 and T25), or Trichoderma harzianum (strain GFP22) or T. asperellum combined with Trichoderma gamsii reduced the severity of VWO symptoms and V. dahliae growth [105,106,107]. Also, the fungus Fusarium oxysporum (strain FO12) showed a high effectiveness in the control of VWO disease in several olive cultivars, ‘Picual’, ‘Arbequina’, and ‘Frantoio’ (a susceptible, moderately susceptible, and moderately resistant to V. dahliae, respectively) by reducing the inoculum density of V. dahliae and VWO progress in the field [108]. Other fungus like Phoma spp. (PH01 and PH02) also showed potential to control VWO [107].
The bacteria Paenibacillus alvei (strain K165) is also effective in the control VWO on the susceptible cultivar ‘Amfissis’, by reducing the relative area under disease progress curve and the final disease severity index [109]. Other bacteria, like Pseudomonas fluorescens (PICF7) and Pseudomonas putida (PICP2 and PICP5) are also effective in the delay of VWO symptoms in the cultivars ‘Picual’ and ‘Arbequina’, decreasing the final disease incidence and severity, and in some case they also promote olive growth [110,111,112]. Moreover, P. fluorescens PICF7 induces systemic defence responses in stems and leaves of the cultivar ‘Arbequina’, upregulating several genes related to biotic and abiotic stress response (e.g., genes involved in plant hormones and phenylpropanoids biosynthesis such as PAL, ACL, LOX-2, and oxidative stress, like catalase) and inducing different transcription factors (e.g., bHLH, WRKYs and GRAS1) [113,114].
Concerning the use of biostimulants based on seaweeds and plant extracts in VWO control, few studies were conducted (Table 2). Salah et al. [101] reported that several polysaccharides extracted from the algae Ulva lactuca, such as ulvan, carrageenan, alginate and laminarin, stimulate natural defences in olive trees (cultivar ‘Picholine Marocaine’) against the VWO and limit V. dahliae spread. These polysaccharides seem to induce signalling processes through the modulation of secondary metabolic pathways [115]. The algal polysaccharides stimulate the activity of PAL and induce the accumulation of phenolics and lignin. Cell wall lignification increase plant resistant to the fungus mechanical penetration and membrane enzymatic degradation (caused by enzymes present in this fungus) [101]. Moreover, U. lactuca polysaccharides delayed the symptoms of senescence in olive, decreasing around 50% of vascular browning and reducing defoliation after elicitation. The use of biostimulants based on plant extract have been shown a low efficiency on the control of VWO. Varo et al. [107] reported that within the 44 plant extracts, only few induced some inhibitory effects on V. dahliae micellar growth. Future research on plant derived biostimulants is necessary, possibly exploring other plant extracts.
The biological control of other relevant olive diseases with microbial biostimulants have been less investigated (Table 2). For instance, several strands of Bacillus (B. cereus NB-4 and NB-5, B. megaterium NB-3, B. mojavensis A-BC-7, B. subtilis NB HNEB-1 and NB-6) showed positive effects on the control of the agents that cause the olive leaf spot (Spilocea oleaginea), anthracnose (Colletotrichum acutatum) and knot disease (Pseudomonas savastanoi pv. Savastanoi) [116,117,118,119,120]. The B. mojavensis is able to control P. savastanoi pv. Savastanoi populations, through the decrease of production of necrotic tumours [116]. Isolates from Bacillus spp. have an inhibitory effect on S. oleagina conidial germination, controlling the olive leaf spot propagation [117].
Table 2. Biostimulants used in the control of some olive diseases.
Table 2. Biostimulants used in the control of some olive diseases.
BiostimulantPathogenEffectsReference
T. asperellum, T. harzianum,
T. asperellum + T. gamsii
V. dahliae
  • Reduce pathogen growth and help to decrease disease progression
[108]
F. oxysporumV. dahliae
  • Reduce the inoculum density of V. dahliae and disease progression
[107]
P. alveiV. dahliae
  • Reduce the disease progression curve and disease severity index
[109]
P. fluorescens and P. putidaV. dahliae
  • Decrease disease incidence and severity, and promote olive growth
  • Upregulate genes related to (a)biotic stress response (e.g., genes involved in plant hormones and phenylpropanoids biosynthesis, like PAL, ACL, LOX-2, and oxidative stress, like catalase), and induce several transcription factors (e.g., bHLH, WRKYs and GRAS1)
[110,111,112,113,114]
Ulva lactucaV. dahliae
  • Limit pathogen spread
  • Stimulate the activity of PAL and accumulation of phenolic and lignin
  • Delay the senescence symptoms
[101]
Plant extractsV. dahliae
  • Some inhibitory effects on pathogen micellar growth
[107]
B. cereus
B. subtilis
B. megaterium
S. oleaginea
  • Inhibit conidial germination
[117,119]
B. mojavensisP. savastanoi pv. Savastanoi
  • Decrease knot weights and pathogen population size
  • Production of less necrotic tumours
[116]
B. subtilisC. acutatum
  • Reduction of the incidence of latent infections on drupes
[120]

4.2.2. Abiotic Stress Tolerance

The use of several types of biostimulants (Trichoderma spp., micro-algae, seaweed mixtures and glycine) to improve olive performance to drought and high temperatures (heat) was described by Graziani et al. [121]. The biostimulants’ positive effects were evident under water deficit conditions, with particular increase in the number of leaves and leaf area, total antioxidant capacity and phenolics contents (e.g., oleuropein and hydroxytirosol) in the cv ‘Salella’ treated with a mixture of microalgae and seaweed and with glycine betaine. Similar results were observed in the cv ‘Galega’ and ‘Arbequina’ treated with the commercial product Fitoalgas Green, based on A. nodosum [122]. This seaweed improved the olive physiological performance under drought conditions by maintaining the leaf water content and promoting the accumulation of starch and antioxidants (such as total phenols and flavonoids). Also under salinity stress, the treatment of olive plants (cv ‘Arbequina’) with the commercial biostimulant Megafol (based on vitamins, amino acids, proteins betaine and growth regulators) helped the plants to maintain a photosynthetic rate, leaf water availability and pigment content similar to the control (above those under salinity stress), and also stimulated the antioxidant system (e.g., SOD activity) leading to membrane protection (lower lipid peroxidation and H2O2 production) [123].
Greenhouse experiments with potted olive plants, cv ‘Picual’ (5-month-old), inoculated with Pseudomonas ssp. PICF6 and Pseudomonas simiae PICF7, together or individually improved the content of leaf flavonoids under drought and salinity stress [124]. Also, under salinity conditions (100 and 200 mM NaCl), the application of the amino acid proline to potted olive plants (2-years-old) enhanced stress tolerance by improving the leaf water status (leaf relative water content and water potential), upregulating the antioxidant enzymes (SOD, APC and CAT), enhancing the levels of chlorophylls, and improving the gas exchange parameters (photosynthesis, stomatal conductance and transpiration rate) [125]. On the other hand, olive roots colonization with Glomus mosseae, Glomus intraradices or Glomus claroideum enhanced nutrients uptake, leading to higher area root surface and biomass under saline conditions [126]. The use of two commercial mycorrhizal fungi (one containing the propagules of Rhizophagus irregularis, Funneliformis mosseae, Funneliformis geosporum, Funneliformis coronatum and Claroideoglomus claroideum, and the other containing Pisolithus tinctorius, Rhizopogon spp., Scleroderma spp. and Laccaria spp.) to alleviate the drought summer stress conditions in young olive trees was very effective, improving growth and photosynthesis [127].

4.3. Other Strategies and Techniques to Improve Olive Stress Performance

Beside the use of biostimulants (Section 4.2), other strategies to improve olive tolerance to stress have been studied. For instance, melatonin, a hormone-like compound found in plants, has been used to enhance salt tolerance in several fruit crops including olive [128]. The application of melatonin in potted olive plants, cv ‘Zard’, exposed to salinity stress, improved olive leaf water status, biomass, and antioxidant system (CAT, SOD and APX). Moreover, these authors also described that this compound protected the photosynthetic pigments and the membranes (decreased the levels of H2O2 and lipid peroxidation), reduced Na+/K+ ratio, and increased the accumulation of proline, glycine betaine, soluble sugars, abscisic acid and indole acetic acid [128]. Also, the use of other compounds like the phytohormones salicylic acid and abscisic acid, and kaolin to alleviate olive summer stress has been investigated [129,130,131,132,133]. The foliar application of these compounds showed to be efficient to prevent the negative effects induced by summer stress in olive trees performance, by the modulation of several physiological and biochemical responses (e.g., increase of photosynthesis, soluble sugars and pigments).
A different approach using shoots of transgenic olive lines expressing osmotin gene was described by Silvestri et al. and Bashir et al. [134,135]. Osmotin is a cationic protein that seems to confer some tolerance to salinity stress, by enhancing the accumulation of osmolytes (e.g., proline and glycine betaine) [135]. Bashir et al. [135] used in vitro cultures of two olive cvs ‘Canino’ and ‘Sirole’ and two transgenic lines of ‘Canino’ (AT17-1 and AT17-2 expressing tobacco the osmotin gene) and treated them with NaCl solutions (ranging from 0 to 200 mM). The transgenic lines showed more tolerance to salinity (no injuries on growth and increase of the O-acetyl serine(thiol)lyase). Under drought stress condition, also the transgenic olive lines (cv ‘Canino’) expressing osmotin gene showed a higher growth and less lipid peroxidation [134].
Despite the results obtained in the above mentioned studies, the use of these strategies and technics (e.g., genetic manipulation) to improve olive performance and application in agriculture/orchards systems required more knowledge. Genetic improvement for (a)biotic stress tolerance is an interesting and promising strategy, but the long term direct and indirect implications associated are not well known. Moreover, the action mode of some of these substances differ from the biostimulants described above (Section 4.1). For instance, kaolin is applied in leaves forming a particle film that reduce light absorption and transpiration, nevertheless it raises some concerns related with photosynthesis impairments under specific environmental conditions (e.g., low radiation), as already highlighted by some authors [136].

4.4. Biostimulant Effect on Olive Fruits, Oil Yield and Quality

Similar to the reported for plant performance and growth, biostimulants can also affect olive fruit characteristics and oil composition [137]. However, some variability on the responses profile have been reported [137]. For instance, Chouliaras et al. [138] demonstrated that the application of seaweed extracts combined with boron improved the level of linoleic and oleic acids and peroxide value, but reduced the contents of palmitoleic, stearic and linoleic acids, and total phenols in olives from potted trees of the cv ‘Koroneiki’.
The treatment of olive trees, cv ‘Chemlali’, with two biostimulants, Alcygol (seaweed with boron) and Nectar intense (based on proteins), changed the olive oil quality profile [139]. For the Alcygol biostimulant, an increase of carotenoids and a reduction of peroxide value and total phenols was observed, while with the use of Nectar intense, the monounsaturated fatty acids (MUFAs) and carotenoids increased but the polyunsaturated fatty acids (PUFAs) decreased. Hernández-Hernandez et al. [140] showed that the application of biostimulants based on algae and amino acids supplemented with nutrients on olive plants from the cvs ‘Chemlali’ and ‘Arbequina’ (in high density orchards) improved fruit weight but not alter oil quality (e.g., fatty acids, polyphenols and tocopherols). In olive orchards, the application of A. nodosum reduced olive oil acidity (%) but improved to levels of total phenols [4]. Almadi et al. [46] did not report changes in the characteristics of olive fruits (fresh weight, pigmentation, water content, oil content and yield efficiency) from the cv ‘Leccino’ treated with a protein hydrolysate (Sinergon 3000, CIFO, Bologna, Italy).
Concerning biostimulant effects on olives yield, Tejada et al. [141] reported an improvement with the use of two biostimulants obtained from sewage sludge by fermentative processes using Bacillus licheniformis (ATCC 21415) in olive tree from orchards.

5. Concluding Remarks

Changes in agriculture production must be implemented to meet the Farm to Fork agricultural strategy of the EU, adapt to climate change and promote agroecosystems biodiversity. Therefore, the search of innovative and sustainable strategies to the agricultural system has increased in the last decades. The use of biostimulants, that are natural products, microorganisms or even nanomaterials, emerge as a sustainable strategy to achieve the objective of developing a more sustainable agricultural production, reducing the irrigation water requirements and the needs of agrochemicals under the actual context of climate change. In olive culture, the use of biostimulants remains very limited with respect to other crops, such as grape. However, the promising results obtained particularly in the control of some important olive diseases, open good perspectives for their application to other disease as well as to improve olive performance and productivity under abiotic stress conditions (like drought and heat). These results also pinpoint that more research must be conducted to better exploit the benefits of biostimulants in olive groves, as a complementary approach to other sustainable practices and the valorisation of more tolerant cultivars. Finally, the knowledge gained here may be useful in spreading the use of biostimulants to other economically important crops.

Author Contributions

Conceptualization, M.C.D.; investigation, M.C.D.; writing—original draft preparation, M.C.D., M.A., S.S. and C.S.; writing—review and editing, M.C.D., M.A., S.S. and C.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financed by Fundação para a Ciência a Tecnologia (FCT) and Ministério da Educação e Ciência through national funds and the co-funding by the FEDER, within the PT2020 Partnership Agreement, and COMPETE 2010, within the projects CEF UI0183–UID/BIA/04004/2020 and LAQV-REQUIMTE UIDB/50006/2020. M Araújo (SFRH/BD/116801/2016 and COVID/BD/151706/2021) was funded by FCT and MCDias (SFRH/BPD/100865/2014) and S Silva (SFRH/BPD/74299/2010) were funded by national funds (OE), through FCT, I.P., in the scope of the framework contract foreseen in the numbers 4–6 of the article-23, of the Decree-Law57/2016, August 29, changed by Law 57/2017, July 19.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data availability on request.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Mohanty, P.; Singh, P.K.; Chakraborty, D.; Mishra, S.; Pattnaik, R. Insight into the role of PGPR in sustainable agriculture and environment. Front. Sustain. Food Syst. 2021, 5, 667150. [Google Scholar] [CrossRef]
  2. Muluneh, M.G. Impact of climate change on biodiversity and food security: A global perspective—A review article. Agric. Food Secur. 2021, 10, 1–25. [Google Scholar] [CrossRef]
  3. IPCC. Climate Change and Land: An IPCC Special Report on Climate Change, Desertification, Land Degradation, Sustainable Land Management, Food Security, and Greenhouse Gas Fluxes in Terrestrial Ecosystems; Shukla, P.R., Skea, J., Calvo Buendia, E., Masson-Delmotte, V., Pörtner, H.-O., Roberts, D.C., Zhai, P., Slade, R., Connors, S., van Diemen, R., et al., Eds.; 2019; Available online: https://www.ipcc.ch/site/assets/uploads/sites/4/2021/07/210714-IPCCJ7230-SRCCL-Complete-BOOK-HRES.pdf (accessed on 1 September 2022).
  4. Leogrande, R.; El Chami, D.; Fumarola, G.; Di Carolo, M.; Piegari, G.; Elefante, M.; Perrelli, D.; Dongiovanni, C. Biostimulants for Resilient Agriculture: A Preliminary Assessment in Italy. Sustainability 2022, 14, 6816. [Google Scholar] [CrossRef]
  5. du Jardin, P. Plant biostimulants: Definition, concept, main categories and regulation. Sci. Hortic. 2015, 196, 3–14. [Google Scholar] [CrossRef] [Green Version]
  6. EBIC. Economic Overview of the Biostimulants Sector in Europe. Available online: https://biostimulants.eu/ (accessed on 2 August 2022).
  7. Reid, T.E.; Kavamura, V.N.; Abadie, M.; Torres-Ballesteros, A.; Pawlett, M.; Clark, I.M.; Harris, J.; Mauchline, T.H. Inorganic chemical fertilizer application to wheat reduces the abundance of putative plant growth-promoting Rhizobacteria. Front. Microbiol. 2021, 12, 642587. [Google Scholar] [CrossRef]
  8. Yakhin, O.I.; Lubyanov, A.A.; Yakhin, I.A.; Brown, P.H. Biostimulants in plant science: A global perspective. Front. Plant Sci. 2017, 7, 2049. [Google Scholar] [CrossRef] [Green Version]
  9. Shukla, P.S.; Mantin, E.G.; Adil, M.; Bajpai, S.; Critchley, A.T.; Prithiviraj, B. Ascophyllum nodosum-based biostimulants: Sustainable applications in agriculture for the stimulation of plant growth, stress tolerance, and disease management. Front. Plant Sci. 2019, 10, 655. [Google Scholar] [CrossRef] [Green Version]
  10. Obied, H.K.; Prenzler, P.D.; Ryan, D.; Servili, M.; Taticchi, A.; Esposto, S.; Robards, K. Biosynthesis and biotransformations of phenol-conjugated oleosidic secoiridoids from Olea europaea L. Nat. Prod. Rep. 2008, 25, 1167–1179. [Google Scholar] [CrossRef] [PubMed]
  11. Blázquez, J.M. The origin and expansion of olive cultivation. In World Olive Encyclopaedia; International Olive Oil Council: Madrid, Spain, 1996; pp. 19–58. ISBN 84-01-61881-9. [Google Scholar]
  12. Fraga, H.; Moriondo, M.; Leolini, L.; Santos, J.A. Mediterranean olive orchards under climate change: A review of future impacts and adaptation strategies. Agronomy 2021, 11, 56. [Google Scholar] [CrossRef]
  13. Brito, C.; Dinis, L.T.; Moutinho-Pereira, J.; Correia, C.M. Drought stress effects and olive tree acclimation under a changing climate. Plants 2019, 8, 232. [Google Scholar] [CrossRef]
  14. Alonso, A.D.; Krajsic, V. Food heritage down under: Olive growers as Mediterranean ‘food ambassadors’. J. Herit. Tour. 2013, 8, 158–171. [Google Scholar] [CrossRef]
  15. Valente, S.; Machado, B.; Pinto, D.C.G.A.; Santos, C.; Silva, A.M.S.; Dias, M.C. Modulation of phenolic and lipophilic compounds of olive fruits in response to combined drought and heat. Food Chem. 2020, 329, 127191. [Google Scholar] [CrossRef] [PubMed]
  16. Reis, P. O Olival em Portugal Dinâmicas, Tecnologias e Relação com o Desenvolvimento Rural; Associação Portuguesa para o Desenvolvimento Local: Lisboa, Portugal, 2014; Volume 33. [Google Scholar]
  17. Calabrese, G.; Artaglini, N.; Ladisa, G. Study on Biodiversity in Century-Old Olive Groves; CIHEAM-Mediterranean Agronomic Institute: Bari, Italy, 2012; pp. 1–108. [Google Scholar]
  18. Guerrero-Casado, J.; Carpio, A.J.; Tortosa, F.S.; Villanueva, A.J. Environmental challenges of intensive woody crops: The case of super high-density olive groves. Sci. Total Environ. 2021, 798, 149212. [Google Scholar] [CrossRef] [PubMed]
  19. Therios, I. Olives; Cambridge University Press: Wallingford, UK, 2009. [Google Scholar]
  20. Belaj, A.; de la Rosa, R.; León, L.; Gabaldón-Leal, C.; Santos, C.; Porras, R.; de la Cruz-Blanco, M.; Lorite, I.J. Phenological diversity in a world olive germplasm bank: Potential use for breeding programs and climate change studies. Span. J. Agric. Res. 2020, 18, e0701. [Google Scholar] [CrossRef] [Green Version]
  21. Lo Bianco, R.; Proietti, P.; Regni, L.; Caruso, T. Planting systems for modern olive growing: Strengths and weaknesses. Agriculture 2021, 11, 494. [Google Scholar] [CrossRef]
  22. International Olive Council. Book of the IOC Network of Germplasm Banks; UCOLIVO—Universidad de Córdoba: Córdoba, Spain, 2019. [Google Scholar]
  23. Silva, S.; Santos, C.; Serôdio, J.; Silva, A.M.S.; Dias, M.C. Physiological performance of drought-stressed olive plants when exposed to a combined heat–UV-B shock and after stress relief. Funct. Plant Biol. 2018, 45, 1233–1240. [Google Scholar] [CrossRef]
  24. Regni, L.; Del Pino, A.M.; Mousavi, S.; Palmerini, C.A.; Baldoni, L.; Mariotti, R.; Mairech, H.; Gardi, T.; D’Amato, R.; Proietti, P. Behavior of four olive cultivars during salt stress. Front. Plant Sci. 2019, 10, 867. [Google Scholar] [CrossRef]
  25. Rapoport, H.F.; Fabbri, A.; Sebastiani, L. The Olive Tree Genome; Springer: Berlin/Heidelberg, Germany, 2016; pp. 13–26. [Google Scholar] [CrossRef]
  26. Tripepi, M.; Pöhlschroder, M.; Bitonti, M.B. Diversity of Dehydrins in Oleae europaea Plants Exposed to Stress. Open Plant Sci. J. 2011, 5, 9–13. [Google Scholar] [CrossRef]
  27. Chartzoulakis, K.S. Salinity and olive: Growth, salt tolerance, photosynthesis and yield. Agric. Water Manag. 2005, 78, 108–121. [Google Scholar] [CrossRef]
  28. Orlandi, F.; Rojo, J.; Picornell, A.; Oteros, J.; Pérez-Badia, R.; Fornaciari, M. Impact of climate change on olive crop production in Italy. Atmosphere 2020, 11, 595. [Google Scholar] [CrossRef]
  29. Martinelli, F.; Remorini, D.; Saia, S.; Massai, R.; Tonutti, P. Metabolic profiling of ripe olive fruit in response to moderate water stress. Sci. Hortic. 2013, 159, 52–58. [Google Scholar] [CrossRef]
  30. Ben-Gal, A. Salinity and olive: From physiological responses to orchard management. Isr. J. Plant Sci. 2011, 59, 15–28. [Google Scholar] [CrossRef]
  31. Petridis, A.; Therios, I.; Samouris, G.; Koundouras, S.; Giannakoula, A. Effect of water deficit on leaf phenolic composition, gas exchange, oxidative damage and antioxidant activity of four Greek olive (Olea europaea L.) cultivars. Plant Physiol. Biochem. 2012, 60, 1–11. [Google Scholar] [CrossRef] [PubMed]
  32. Koubouris, G.C.; Kavroulakis, N.; Metzidakis, I.T.; Vasilakakis, M.D.; Sofo, A. Ultraviolet-B radiation or heat cause changes in photosynthesis, antioxidant enzyme activities and pollen performance in olive tree. Photosynthetica 2015, 53, 279–287. [Google Scholar] [CrossRef]
  33. Araújo, M.; Santos, C.; Dias, M.C. Can young olive plants overcome heat shock? In Theory and Practice of Climate Adaptation; Alves, F., Leal Filho, W., Azeiteiro, U., Eds.; Springer: Berlin, Germany, 2018; pp. 193–203. [Google Scholar]
  34. Dias, M.C.; Pinto, D.C.G.A.; Correia, C.; Moutinho-Pereira, J.; Oliveira, H.; Freitas, H.; Silva, A.M.S.; Santos, C. UV-B radiation modulates physiology and lipophilic metabolite profile in Olea europaea. J. Plant Physiol. 2018, 222, 39–50. [Google Scholar] [CrossRef]
  35. Piccini, C.; Cai, G.; Dias, M.C.; Romi, M.; Longo, R.; Cantini, C. UV-B Radiation Affects Photosynthesis-Related Processes of Two Italian Olea europaea (L.) Varieties Differently. Plants 2020, 9, 1712. [Google Scholar] [CrossRef]
  36. Piccini, C.; Cai, G.; Dias, M.C.; Araújo, M.; Parri, S.; Romi, M.; Faleri, C.; Cantini, C. Olive varieties under UV-B stress show distinct responses in terms of antioxidant machinery and isoform/activity of rubisco. Int. J. Mol. Sci. 2021, 22, 11214. [Google Scholar] [CrossRef]
  37. Caruso, G.; Gucci, R.; Urbani, S.; Esposto, S.; Taticchi, A.; Di Maio, I.; Selvaggini, R.; Servili, M. Effect of different irrigation volumes during fruit development on quality of virgin olive oil of cv. Frantoio. Agric. Water Manag. 2014, 134, 94–103. [Google Scholar] [CrossRef]
  38. Nissim, Y.; Shloberg, M.; Biton, I.; Many, Y.; Doron-Faigenboim, A.; Zemach, H.; Hovav, R.; Kerem, Z.; Avidan, B.; Ben-Ari, G. High temperature environment reduces olive oil yield and quality. PLoS ONE 2020, 15, e0231956. [Google Scholar] [CrossRef]
  39. Nissim, Y.; Shlosberg, M.; Biton, I.; Many, Y.; Doron-Faigenboim, A.; Hovav, R.; Kerem, Z.; Avidan, B.; Ben-Ari, G. A high temperature environment regulates the olive oil biosynthesis network. Plants 2020, 9, 1135. [Google Scholar] [CrossRef]
  40. Fernández-Lobato, L.; García-Ruiz, R.; Jurado, F.; Vera, D. Life cycle assessment, C footprint and carbon balance of virgin olive oils production from traditional and intensive olive groves in southern Spain. J. Environ. Manage. 2021, 293, 112951. [Google Scholar] [CrossRef] [PubMed]
  41. Wang, Y.; Jensen, C.R.; Liu, F. Nutritional responses to soil drying and rewetting cycles under partial root-zone drying irrigation. Agric. Water Manag. 2017, 179, 254–259. [Google Scholar] [CrossRef]
  42. Bedbabis, S.; Ben Rouina, B.; Boukhris, M.; Ferrara, G. Effects of irrigation with treated wastewater on root and fruit mineral elements of Chemlali olive cultivar. Sci. World J. 2014, 2014, 1–8. [Google Scholar] [CrossRef] [PubMed]
  43. Andrade, C.; Fonseca, A.; Santos, J.A. Are land use options in viticulture and oliviculture in agreement with bioclimatic shifts in Portugal? Land 2021, 10, 869. [Google Scholar] [CrossRef]
  44. IPMA. Acompanhamento do Clima. Available online: https://www.ipma.pt/pt/oclima/monitorizacao/index.jsp?selTipo=m&selVar=tt&selAna=me&selAno=2017 (accessed on 7 August 2020).
  45. IPMA. Boletim Climático Portugal Continental Janeiro 2022. Available online: https://www.ipma.pt/resources.www/docs/im.publicacoes/edicoes.online/20220204/FGdTvyAzNYKcsCOxBZMy/cli_20220101_20220131_pcl_mm_co_pt.pdf (accessed on 1 September 2022).
  46. Almadi, L.; Paoletti, A.; Cinosi, N.; Daher, E.; Rosati, A.; Di Vaio, C.; Famiani, F. A biostimulant based on protein hydrolysates promotes the growth of young olive trees. Agriculture 2020, 10, 618. [Google Scholar] [CrossRef]
  47. Ali, O.; Ramsubhag, A.; Jayaraman, J. Biostimulant properties of seaweed extracts in plants: Implications towards sustainable crop production. Plants 2021, 10, 531. [Google Scholar] [CrossRef]
  48. Franzoni, G.; Cocetta, G.; Prinsi, B.; Ferrante, A.; Espen, L. Biostimulants on crops: Their impact under abiotic stress conditions. Horticulturae 2022, 8, 189. [Google Scholar] [CrossRef]
  49. Bartucca, M.L.; Cerri, M.; Del Buono, D.; Forni, C. Use of biostimulants as a new approach for the improvement of phytoremediation performance—A Review. Plants 2022, 11, 1946. [Google Scholar] [CrossRef]
  50. Lau, S.-E.; Fei, W.; Teo, A.; Teoh, E.Y.; Tan, B.C. Microbiome engineering and plant biostimulants for sustainable crop improvement and mitigation of biotic and abiotic stresses. Discov. Food 2022, 2, 9. [Google Scholar] [CrossRef]
  51. Lynch, J.; Cain, M.; Frame, D.; Pierrehumbert, R. Agriculture’s contribution to climate change and role in mitigation is distinct from predominantly fossil CO2-emitting sectors. Front. Sustain. Food Syst. 2021, 4, 518039. [Google Scholar] [CrossRef]
  52. Rouphael, Y.; Colla, G. Editorial: Biostimulants in agriculture. Front. Plant Sci. 2020, 11, 40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Xu, L.; Geelen, D. Developing biostimulants from agro-food and industrial by-products. Front. Plant Sci. 2018, 871, 1567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Juárez-Maldonado, A.; Ortega-Ortíz, H.; Morales-Díaz, A.B.; González-Morales, S.; Morelos-Moreno, Á.; Cabrera-De la Fuente, M.; Sandoval-Rangel, A.; Cadenas-Pliego, G.; Benavides-Mendoza, A. Nanoparticles and nanomaterials as plant biostimulants. Int. J. Mol. Sci. 2019, 20, 162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Pereira, R.V.; Filgueiras, C.C.; Dória, J.; Peñaflor, M.F.G.V.; Willett, D.S. The effects of biostimulants on induced plant defense. Front. Agron. 2021, 3, 1–9. [Google Scholar] [CrossRef]
  56. Brouwers, E.; Draisma, M.; van Swam, K.; Veen, A.J.; Burger, L. Identification of the Seaweed Biostimulant Market (Phase 1); The North Sea Farm Foundation: AD Den Haag, The Netherlands, 2018; pp. 1–64. [Google Scholar]
  57. El Boukhari, M.E.M.; Barakate, M.; Bouhia, Y.; Lyamlouli, K. Trends in seaweed extract based biostimulants: Manufacturing process and beneficial effect on soil-plant systems. Plants 2020, 9, 359. [Google Scholar] [CrossRef] [Green Version]
  58. Van Oosten, M.J.; Pepe, O.; De Pascale, S.; Silletti, S.; Maggio, A. The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem. Biol. Technol. Agric. 2017, 4, 5. [Google Scholar] [CrossRef] [Green Version]
  59. Baltazar, M.; Correia, S.; Guinan, K.J.; Sujeeth, N.; Bragança, R.; Gonçalves, B. Recent advances in the molecular effects of biostimulants in plants: An overview. Biomolecules 2021, 11, 1096. [Google Scholar] [CrossRef]
  60. Bulgari, R.; Franzoni, G.; Ferrante, A. Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy 2019, 9, 306. [Google Scholar] [CrossRef] [Green Version]
  61. Cristiano, G.; Pallozzi, E.; Conversa, G.; Tufarelli, V.; De Lucia, B. Effects of an animal-derived biostimulant on the growth and physiological parameters of potted snapdragon (Antirrhinummajus L.). Front. Plant Sci. 2018, 9, 1–12. [Google Scholar] [CrossRef]
  62. Stirk, W.A.; Rengasamy, K.R.R.; Kulkarni, M.G.; van Staden, J. Plant biostimulants from seaweed. In The Chemical Biology of Plant Biostimulants; Gleelen, D., Xu, L., Eds.; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2020; pp. 31–55. [Google Scholar]
  63. Mukherjee, A.; Patel, J.S. Seaweed extract: Biostimulator of plant defense and plant productivity. Int. J. Environ. Sci. Technol. 2020, 17, 553–558. [Google Scholar] [CrossRef]
  64. Nanda, S.; Kumar, G.; Hussain, S. Utilization of seaweed-based biostimulants in improving plant and soil health: Current updates and future prospective. Int. J. Environ. Sci. Technol. 2021, 19, 12839–12852. [Google Scholar] [CrossRef]
  65. Ertani, A.; Francioso, O.; Tinti, A.; Schiavon, M.; Pizzeghello, D.; Nardi, S. Evaluation of seaweed extracts from laminaria and Ascophyllum nodosum spp. As biostimulants in Zea mays L. using a combination of chemical, biochemical and morphological approaches. Front. Plant Sci. 2018, 9, 428. [Google Scholar] [CrossRef] [PubMed]
  66. Cristofano, F.; El-Nakhel, C.; Rouphael, Y. Biostimulant substances for sustainable agriculture: Origin, operating mechanisms and effects on cucurbits, leafy greens, and nightshade vegetables species. Biomolecules 2021, 11, 1103. [Google Scholar] [CrossRef] [PubMed]
  67. Francesca, B.; Nicola, B.; Paolo, T.; Marcello, M. Classification of Biostimulants Origin Using Amino Acids Composition of Hydrolyzed Proteins. J. Hortic. Sci. Res. 2017, 1, 30–35. [Google Scholar] [CrossRef]
  68. Vaseva, I.I.; Simova-Stoilova, L.; Kostadinova, A.; Yuperlieva-Mateeva, B.; Karakicheva, T.; Vassileva, V. Heat-stress-mitigating effects of a protein-hydrolysate-based biostimulant are linked to changes in protease, DHN, and HSP gene expression in Maize. Agronomy 2022, 12, 1127. [Google Scholar] [CrossRef]
  69. Visconti, F.; de Paz, J.M.; Bonet, L.; Jordà, M.; Quiñones, A.; Intrigliolo, D.S. 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, 129–138. [Google Scholar] [CrossRef]
  70. Colla, G.; Hoagland, L.; Ruzzi, M.; Cardarelli, M.; Bonini, P.; Canaguier, R.; Rouphael, Y. Biostimulant action of protein hydrolysates: Unraveling their effects on plant physiology and microbiome. Front. Plant Sci. 2017, 8, 129–138. [Google Scholar] [CrossRef] [Green Version]
  71. Francesca, S.; Cirillo, V.; Raimondi, G.; Maggio, A.; Barone, A.; Rigano, M.M. A Novel protein hydrolysate-based biostimulant improves tomato performances under drought stress. Plants 2021, 10, 783. [Google Scholar] [CrossRef]
  72. Rouphael, Y.; Colla, G. Synergistic biostimulatory action: Designing the next generation of plant biostimulants for sustainable agriculture. Front. Plant Sci. 2018, 871, 1655. [Google Scholar] [CrossRef]
  73. Popa, D.G.; Lupu, C.; Constantinescu-Aruxandei, D.; Oancea, F. Humic substances as microalgal biostimulants—Implications for microalgal biotechnology. Mar. Drugs 2022, 20, 327. [Google Scholar] [CrossRef]
  74. Nephali, L.; Piater, L.A.; Dubery, I.A.; Patterson, V.; Huyser, J.; Burgess, K.; Tugizimana, F. Biostimulants for plant growth and mitigation of abiotic stresses: A metabolomics perspective. Metabolites 2020, 10, 505. [Google Scholar] [CrossRef] [PubMed]
  75. Aguiar, N.O.; Medici, L.O.; Olivares, F.L.; Dobbss, L.B.; Torres-Netto, A.; Silva, S.F.; Novotny, E.H.; Canellas, L.P. Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Ann. Appl. Biol. 2016, 168, 203–213. [Google Scholar] [CrossRef]
  76. Alsamadany, H. Physiological, biochemical and molecular evaluation of mungbean genotypes for agronomical yield under drought and salinity stresses in the presence of humic acid. Saudi J. Biol. Sci. 2022, 29, 103385. [Google Scholar] [CrossRef] [PubMed]
  77. Zanin, L.; Tomasi, N.; Cesco, S.; Varanini, Z.; Pinton, R. Humic substances contribute to plant iron nutrition acting as chelators and biostimulants. Front. Plant Sci. 2019, 10, 675. [Google Scholar] [CrossRef] [Green Version]
  78. Ferrara, G.; Loffredo, E.; Simeone, R.; Senesi, N. Evaluation of antimutagenic and desmutagenic effects of humic and fulvic acids on root tips of Vicia faba. Environ. Toxicol. 2000, 15, 513–517. [Google Scholar] [CrossRef]
  79. Ferrara, G.; Loffredo, E.; Senesi, N. Anticlastogenic, antitoxic and sorption effects of humic substances on the mutagen maleic hydrazide tested in leguminous plants. Eur. J. Soil Sci. 2004, 55, 449–458. [Google Scholar] [CrossRef]
  80. Canellas, L.P.; Olivares, F.L.; Aguiar, N.O.; Jones, D.L.; Nebbioso, A.; Mazzei, P.; Piccolo, A. Humic and fulvic acids as biostimulants in horticulture. Sci. Hortic. 2015, 196, 15–27. [Google Scholar] [CrossRef]
  81. Gemin, L.G.; Mógor, Á.F.; De Oliveira Amatussi, J.; Mógor, G. Microalgae associated to humic acid as a novel biostimulant improving onion growth and yield. Sci. Hortic. 2019, 256, 108560. [Google Scholar] [CrossRef]
  82. Jung, H.; Kwon, S.; Kim, J.H.; Jeon, J.R. Which traits of humic substances are investigated to improve their agronomical value? Molecules 2021, 26, 760. [Google Scholar] [CrossRef]
  83. Del Buono, D. Can biostimulants be used to mitigate the effect of anthropogenic climate change on agriculture? It is time to respond. Sci. Total Environ. 2021, 751, 141763. [Google Scholar] [CrossRef]
  84. Rai, N.; Rai, S.P.; Sarma, B.K. Prospects for abiotic stress tolerance in crops utilizing phyto- and bio-stimulants. Front. Sustain. Food Syst. 2021, 5, 455. [Google Scholar] [CrossRef]
  85. Etesami, H.; Maheshwari, D.K. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicol. Environ. Saf. 2018, 156, 225–246. [Google Scholar] [CrossRef] [PubMed]
  86. Leontidou, K.; Genitsaris, S.; Papadopoulou, A.; Kamou, N.; Bosmali, I.; Matsi, T.; Madesis, P.; Vokou, D.; Karamanoli, K.; Mellidou, I. Plant growth promoting rhizobacteria isolated from halophytes and drought-tolerant plants: Genomic characterisation and exploration of phyto-beneficial traits. Sci. Rep. 2020, 10, 1–15. [Google Scholar] [CrossRef]
  87. Miceli, A.; Moncada, A.; Vetrano, F. Use of microbial biostimulants to increase the salinity tolerance of vegetable transplants. Agronomy 2021, 11, 1143. [Google Scholar] [CrossRef]
  88. Begum, N.; Qin, C.; Ahanger, M.A.; Raza, S.; Khan, M.I.; Ashraf, M.; Ahmed, N.; Zhang, L. Role of Arbuscular Mycorrhizal Fungi in Plant Growth Regulation: Implications in Abiotic Stress Tolerance. Front. Plant Sci. 2019, 10, 1068. [Google Scholar] [CrossRef] [Green Version]
  89. Latef, A.A.H.A.; Miransari, M. Use of Microbes for the Alleviation of Soil Stresses. In Use of Microbes for the Alleviation of Soil Stresses: Alleviation of Soil Stress by Pgpr and Mycorrhizal Fungi; Miransari, M., Ed.; Springer: New York, NY, USA, 2014; pp. 23–38. [Google Scholar]
  90. Diagne, N.; Ngom, M.; Djighaly, P.I.; Fall, D.; Hocher, V.; Svistoonoff, S. Roles of arbuscular mycorrhizal fungi on plant growth and performance: Importance in biotic and abiotic stressed regulation. Diversity 2020, 12, 370. [Google Scholar] [CrossRef]
  91. Moradi Tarnabi, Z.; Iranbakhsh, A.; Mehregan, I.; Ahmadvand, R. Impact of arbuscular mycorrhizal fungi (AMF) on gene expression of some cell wall and membrane elements of wheat (Triticum aestivum L.) under water deficit using transcriptome analysis. Physiol. Mol. Biol. Plants 2020, 26, 143–162. [Google Scholar] [CrossRef] [PubMed]
  92. Silva, S.; Dias, M.C.; Silva, A.M.S. Titanium and zinc based nanomaterials in agriculture: A promising approach to deal with (a)biotic stresses? Toxics 2022, 10, 172. [Google Scholar] [CrossRef]
  93. Hassan, M.U.; Ghareeb, R.Y.; Nawaz, M.; Mahmood, A.; Shah, A.N.; Abdel-megeed, A.; Abdelsalam, N.R.; Hashem, M.; Alamri, S. Melatonin: A vital protectant for crops against heat stress: Mechanisms and prospects. Agronomy 2022, 12, 1116. [Google Scholar] [CrossRef]
  94. Hidangmayum, A.; Dwivedi, P. Chitosan based nanoformulation for sustainable agriculture with special reference to abiotic stress: A Review. J. Polym. Environ. 2022, 30, 1264–1283. [Google Scholar] [CrossRef]
  95. Regni, L.; Del Buono, D.; Micheli, M.; Facchin, S.L.; Tolisano, C.; Proietti, P. Effects of biogenic ZnO nanoparticles on growth, physiological, biochemical traits and antioxidants on olive tree in vitro. Horticulturae 2022, 8, 161. [Google Scholar] [CrossRef]
  96. Ntasiou, P.; Kerou, A.K.; Karamanidou, T.; Vlachou, A.; Tziros, G.T.; Tsouknidas, A.; Karaoglanidis, G.S. Synthesis and characterization of novel copper nanoparticles for the control of leaf spot and anthracnose diseases of olive. Nanomaterials 2021, 11, 1667. [Google Scholar] [CrossRef] [PubMed]
  97. Wang, Y.; Zhang, B.; Jiang, D.; Chen, G. Silicon improves photosynthetic performance by optimizing thylakoid membrane protein components in rice under drought stress. Environ. Exp. Bot. 2019, 158, 117–124. [Google Scholar] [CrossRef]
  98. Zhu, Y.; Jiang, X.; Zhang, J.; He, Y.; Zhu, X.; Zhou, X.; Gong, H.; Yin, J.; Liu, Y. Silicon confers cucumber resistance to salinity stress through regulation of proline and cytokinins. Plant Physiol. Biochem. 2020, 156, 209–220. [Google Scholar] [CrossRef]
  99. Morales-Díaz, A.B.; Ortega-Ortíz, H.; Juárez-Maldonado, A.; Cadenas-Pliego, G.; González-Morales, S.; Benavides-Mendoza, A. Application of nanoelements in plant nutrition and its impact in ecosystems. Adv. Nat. Sci. Nanosci. Nanotechnol. 2017, 8, 013001. [Google Scholar] [CrossRef]
  100. Muzzalupo, I.; Badolati, G.; Chiappetta, A.; Picci, N.; Muzzalupo, R. In vitro antifungal activity of Olive (Olea europaea) leaf extracts loaded in chitosan nanoparticles. Front. Bioeng. Biotechnol. 2020, 8, 151. [Google Scholar] [CrossRef] [Green Version]
  101. Salah, I.B.; Aghrouss, S.; Douira, A.; Aissam, S.; El Alaoui-Talibi, Z.; Filali-Maltouf, A.; El Modafar, C. Seaweed polysaccharides as bio-elicitors of natural defenses in olive trees against verticillium wilt of olive. J. Plant Interact. 2018, 13, 248–255. [Google Scholar] [CrossRef]
  102. Montes-Osuna, N.; Mercado-Blanco, J. Verticillium wilt of olive and its control: What did we learn during the last decade? Plants 2020, 9, 735. [Google Scholar] [CrossRef] [PubMed]
  103. Jiménez-Díaz, R.M.; Castillo, P.; Jiménez-Gasco, M.d.M.; Landa, B.B.; Navas-Cortés, J.A. Fusarium wilt of chickpeas: Biology, ecology and management. Crop Prot. 2015, 73, 16–27. [Google Scholar] [CrossRef]
  104. Tyśkiewicz, R.; Nowak, A.; Ozimek, E.; Jaroszuk-ściseł, J. Trichoderma: The current status of its application in agriculture for the biocontrol of fungal phytopathogens and stimulation of plant growth. Int. J. Mol. Sci. 2022, 23, 2329. [Google Scholar] [CrossRef]
  105. Carrero-Carrón, I.; Trapero-Casas, J.L.; Olivares-García, C.; Monte, E.; Hermosa, R.; Jiménez-Díaz, R.M. Trichoderma asperellum is effective for biocontrol of Verticillium wilt in olive caused by the defoliating pathotype of Verticillium dahliae. Crop Prot. 2016, 88, 45–52. [Google Scholar] [CrossRef]
  106. Carrero-Carrón, I.; Rubio, M.B.; Niño-Sánchez, J.; Navas-Cortés, J.A.; Jiménez-Díaz, R.M.; Monte, E.; Hermosa, R. Interactions between Trichoderma harzianum and defoliating Verticillium dahliae in resistant and susceptible wild olive clones. Plant Pathol. 2018, 67, 1758–1767. [Google Scholar] [CrossRef] [Green Version]
  107. Varo, A.; Raya-Ortega, M.C.; Trapero, A. Selection and evaluation of micro-organisms for biocontrol of Verticillium dahliae in olive. J. Appl. Microbiol. 2016, 121, 767–777. [Google Scholar] [CrossRef] [PubMed]
  108. Mulero-Aparicio, A.; Varo, A.; Agustí-Brisach, C.; López-Escudero, F.J.; Trapero, A. Biological control of Verticillium wilt of olive in the field. Crop Prot. 2020, 128, 104993. [Google Scholar] [CrossRef]
  109. Markakis, E.A.; Tjamos, S.E.; Antoniou, P.P.; Paplomatas, E.J.; Tjamos, E.C. Biological control of Verticillium wilt of olive by Paenibacillus alvei, strain K165. BioControl 2016, 61, 293–303. [Google Scholar] [CrossRef]
  110. Mercado-Blanco, J.; Rodríguez-Jurado, D.; Hervás, A.; Jiménez-Diaz, R.M. Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biol. Control 2004, 30, 474–486. [Google Scholar] [CrossRef]
  111. Prieto, P.; Navarro-Raya, C.; Valverde-Corredor, A.; Amyotte, S.G.; Dobinson, K.F.; Mercado-Blanco, J. Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microb. Biotechnol. 2009, 2, 499–511. [Google Scholar] [CrossRef] [Green Version]
  112. Deketelaere, S.; Tyvaert, L.; França, S.C.; Hofte, M. Desirable traits of a good biocontrol agent against Verticillium wilt. Front. Microbiol. 2017, 8, 1186. [Google Scholar] [CrossRef] [Green Version]
  113. Schilirò, E.; Ferrara, M.; Nigro, F.; Mercado-Blanco, J. Genetic responses induced in olive roots upon colonization by the biocontrol endophytic bacterium Pseudomonas fluorescens PICF7. PLoS ONE 2012, 7, e48646. [Google Scholar] [CrossRef]
  114. Cabanás, C.G.L.; Schilirò, E.; Valverde-Corredor, A.; Mercado-Blanco, J. The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Front. Microbiol. 2014, 5, 427. [Google Scholar] [CrossRef]
  115. Sharma, H.S.S.; Fleming, C.; Selby, C.; Rao, J.R.; 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, 465–490. [Google Scholar] [CrossRef]
  116. Ghanney, N.; Locantore, P. Potential biocontrol effect of the phylloplane bacterium Bacillus mojavensis ABC-7 on the olive knot disease. J. Plant Pathol. Microbiol. 2016, 7, 3–5. [Google Scholar] [CrossRef]
  117. Salman, M. Biological control of Spilocaea oleagina, the causal agent of olive leaf spot disease, using antagonistic bacteria. J. Plant Pathol. 2017, 99, 741–744. [Google Scholar] [CrossRef]
  118. Cabanás, C.G.-L.; Ruano-Rosa, D.; Legarda, G.; Pizarro-Tobías, P.; Valverde-Corredor, A.; Triviño, J.C.; Roca, A.; Mercado-Blanco, J. Bacillales members from the olive rhizosphere are effective biological control agents against the defoliating pathotype of Verticillium dahliae. Agriculture 2018, 8, 90. [Google Scholar] [CrossRef] [Green Version]
  119. Al-Khatib, M. Biological control of olive leaf spot (peacock spot disease) caused by Cycloconium oleaginum (Spilocea oleaginea). J. Microbiol. 2010, 2, 64–67. [Google Scholar]
  120. Nigro, F.; Antelmi, I.; Labarile, R.; Sion, V.; Pentimone, I. Biological control of olive anthracnose. Acta Hortic. 2018, 1199, 439–444. [Google Scholar] [CrossRef]
  121. Graziani, G.; Cirillo, A.; Giannini, P.; Conti, S.; El-Nakhel, C.; Rouphael, Y.; Ritieni, A.; Di Vaio, C. Biostimulants improve plant growth and bioactive compounds of young olive trees under abiotic stress conditions. Agriculture 2022, 12, 227. [Google Scholar] [CrossRef]
  122. Dias, M.C.; Figueiras, R.; Sousa, M.; Araújo, M.; Santos, C. Aplicação de bioestimulante na cultura de oliveira em rega deficitária. In Proceedings of IX Simpósio Nacional de Olivicultura, Oeiras, Portugal, 25 October 2021; Ramos, A.C., Pereira, J.A., Rodrigues, N., Eds.; Associação Portuguesa de Horticultura (APH): Lisboa, Portugal, 2021; p. 92. [Google Scholar]
  123. Del Buono, D.; Regni, L.; Del Pino, A.M.; Bartucca, M.L.; Palmerini, C.A.; Proietti, P. Effects of megafol on the olive cultivar ‘Arbequina’ grown under severe saline stress in terms of physiological traits, oxidative stress, antioxidant defenses, and cytosolic Ca2+. Front. Plant Sci. 2021, 11, 603576. [Google Scholar] [CrossRef]
  124. Montes-Osuna, N.; Cabanás, C.G.-L.; Valverde-Corredor, A.; Legarda, G.; Prieto, P.; Mercado-Blanco, J. Evaluation of indigenous olive biocontrol rhizobacteria as protectants against drought and salt stress. Microorganisms 2021, 9, 1209. [Google Scholar] [CrossRef]
  125. Ahmed, C.B.; Rouina, B.B.; Sensoy, S.; Boukhriss, M.; Abdullah, F.B. Exogenous Proline Effects on Photosynthetic Performance and Antioxidant Defense System of Young Olive Tree. J. Agr. Food Chem. 2010, 58, 4216–4222. [Google Scholar] [CrossRef]
  126. Porras-Soriano, A.; Soriano-Martín, M.L.; Porras-Piedra, A.; Azcón, R. Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J. Plant Physiol. 2009, 166, 1350–1359. [Google Scholar] [CrossRef] [PubMed]
  127. Lopes, J.I.; Arrobas, M.; Brito, C.; Gonçalves, A.; Silva, E.; Martins, S.; Raimundo, S.; Rodrigues, M.A.; Correia, C.M. Mycorrhizal Fungi were More Effective than Zeolites in Increasing the Growth of Non-Irrigated Young Olive Trees. Sustainability 2020, 12, 10630. [Google Scholar] [CrossRef]
  128. Zahedi, S.M.; Hosseini, M.S.; Fahadi Hoveizeh, N.; Gholami, R.; Abdelrahman, M.; Tran, L.-S.P. Exogenous melatonin mitigates salinity-induced damage in olive seedlings by modulating ion homeostasis, antioxidant defense, and phytohormone balance. Physiol. Plant. 2021, 173, 1682–1694. [Google Scholar] [CrossRef]
  129. Brito, C.; Dinis, L.T.; Silva, E.; Gonçalves, A.; Matos, C.; Rodrigues, M.A.; Moutinho-Pereira, J.; Barros, A.; Correia, C. Kaolin and salicylic acid foliar application modulate yield, quality and phytochemical composition of olive pulp and oil from rainfed trees. Sci. Hortic. 2018, 237, 176–183. [Google Scholar] [CrossRef] [Green Version]
  130. Brito, C.; Dinis, L.T.; Meijón, M.; Ferreira, H.; Pinto, G.; Moutinho-Pereira, J.; Correia, C. Salicylic acid modulates olive tree physiological and growth responses to drought and rewatering events in a dose dependent manner. J. Plant Physiol. 2018, 230, 21–32. [Google Scholar] [CrossRef]
  131. Brito, C.; Dinis, L.T.; Luzio, A.; Silva, E.; Gonçalves, A.; Meijón, M.; Escandón, M.; Arrobas, M.; Rodrigues, M.Â.; Moutinho-Pereira, J.; et al. Kaolin and salicylic acid alleviate summer stress in rainfed olive orchards by modulation of distinct physiological and biochemical responses. Sci. Hortic. 2019, 246, 201–211. [Google Scholar] [CrossRef] [Green Version]
  132. Brito, C.; Dinis, L.T.; Ferreira, H.; Coutinho, J.; Moutinho-Pereira, J.; Correia, C.M. Salicylic acid increases drought adaptability of young olive trees by changes on redox status and ionome. Plant Physiol. Biochem. 2019, 141, 315–324. [Google Scholar] [CrossRef]
  133. Brito, C.; Dinis, L.T.; Ferreira, H.; Moutinho-Pereira, J.; Correia, C.M. Foliar pre-treatment with abscisic acid enhances olive tree drought adaptability. Plants 2020, 9, 341. [Google Scholar] [CrossRef] [Green Version]
  134. Silvestri, C.; Celletti, S.; Cristofori, V.; Astolfi, S.; Ruggiero, B.; Rugini, E. Olive (Olea europaea L.) plants transgenic for tobacco osmotin gene are less sensitive to in vitro-induced drought stress. Acta Physiol. Plant. 2017, 39, 229. [Google Scholar] [CrossRef]
  135. Bashir, M.A.; Silvestri, C.; Coppa, E.; Brunori, E.; Cristofori, V.; Rugini, E.; Ahmad, T.; Hafiz, I.A.; Abbasi, N.A.; Shah, M.K.N.; et al. Response of olive shoots to salinity stress suggests the involvement of sulfur metabolism. Plants 2021, 10, 350. [Google Scholar] [CrossRef]
  136. Monteiro, E.; Gonçalves, B.; Cortez, I.; Castro, I. The role of biostimulants as alleviators of biotic and abiotic stresses in grapevine: A Review. Plants 2022, 11, 396. [Google Scholar] [CrossRef]
  137. Mazeh, M.; Almadi, L.; Paoletti, A.; Cinosi, N.; Daher, E.; Tucci, M.; Lodolini, E.M.; Rosati, A.; Famiani, F. Use of an organic fertilizer also having a biostimulant action to promote the growth of young olive trees. Agriculture 2021, 11, 593. [Google Scholar] [CrossRef]
  138. Chouliaras, V.; Tasioula, M.; Chatzissavvidis, C.; Therios, I.; Tsabolatidou, E. The effects of a seaweed extract in addition to nitrogen and boron fertilization on productivity, fruit maturation, leaf nutritional status and oil quality of the olive (Olea europaea L.) cultivar Koroneiki. J. Sci. Food Agric. 2009, 89, 984–988. [Google Scholar] [CrossRef]
  139. Zouari, I.; Mechri, B.; Tekaya, M.; Dabbaghi, O.; Cheraief, I.; Mguidiche, A.; Annabi, K.; Laabidi, F.; Attia, F.; Hammami, M.; et al. Olive oil quality influenced by biostimulant foliar fertilizers. Brazilian J. Biol. Sci. 2020, 7, 3–18. [Google Scholar] [CrossRef] [Green Version]
  140. Hernández-Hernandez, G.; Salazar, D.M.; Martínez-Tomé, J.; López-Cortés, I. The use of biostimulants in high-density olive growing: Quality and production. Asian J. Adv. Agric. Res. 2019, 10, 1–11. [Google Scholar] [CrossRef] [Green Version]
  141. Tejada, M.; Caballero, P.; Parrado, J. Effects of foliar fertilization of biostimulants obtained from sewage sludge on olive yield. Cogent Food Agric. 2022, 8, 2124702. [Google Scholar] [CrossRef]
Figure 1. Biostimulants used to control abiotic and biotic negative effects on olive tree.
Figure 1. Biostimulants used to control abiotic and biotic negative effects on olive tree.
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Dias, M.C.; Araújo, M.; Silva, S.; Santos, C. Sustainable Olive Culture under Climate Change: The Potential of Biostimulants. Horticulturae 2022, 8, 1048. https://doi.org/10.3390/horticulturae8111048

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Dias MC, Araújo M, Silva S, Santos C. Sustainable Olive Culture under Climate Change: The Potential of Biostimulants. Horticulturae. 2022; 8(11):1048. https://doi.org/10.3390/horticulturae8111048

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Dias, Maria Celeste, Márcia Araújo, Sónia Silva, and Conceição Santos. 2022. "Sustainable Olive Culture under Climate Change: The Potential of Biostimulants" Horticulturae 8, no. 11: 1048. https://doi.org/10.3390/horticulturae8111048

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