Physicochemical parameters of Ogliarola olive oil and Cellina olive oil after ozonization procedure.
\\n\\n
Dr. Pletser’s experience includes 30 years of working with the European Space Agency as a Senior Physicist/Engineer and coordinating their parabolic flight campaigns, and he is the Guinness World Record holder for the most number of aircraft flown (12) in parabolas, personally logging more than 7,300 parabolas.
\\n\\nSeeing the 5,000th book published makes us at the same time proud, happy, humble, and grateful. This is a great opportunity to stop and celebrate what we have done so far, but is also an opportunity to engage even more, grow, and succeed. It wouldn't be possible to get here without the synergy of team members’ hard work and authors and editors who devote time and their expertise into Open Access book publishing with us.
\\n\\nOver these years, we have gone from pioneering the scientific Open Access book publishing field to being the world’s largest Open Access book publisher. Nonetheless, our vision has remained the same: to meet the challenges of making relevant knowledge available to the worldwide community under the Open Access model.
\\n\\nWe are excited about the present, and we look forward to sharing many more successes in the future.
\\n\\nThank you all for being part of the journey. 5,000 times thank you!
\\n\\nNow with 5,000 titles available Open Access, which one will you read next?
\\n\\nRead, share and download for free: https://www.intechopen.com/books
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Preparation of Space Experiments edited by international leading expert Dr. Vladimir Pletser, Director of Space Training Operations at Blue Abyss is the 5,000th Open Access book published by IntechOpen and our milestone publication!
\n\n"This book presents some of the current trends in space microgravity research. The eleven chapters introduce various facets of space research in physical sciences, human physiology and technology developed using the microgravity environment not only to improve our fundamental understanding in these domains but also to adapt this new knowledge for application on earth." says the editor. Listen what else Dr. Pletser has to say...
\n\n\n\nDr. Pletser’s experience includes 30 years of working with the European Space Agency as a Senior Physicist/Engineer and coordinating their parabolic flight campaigns, and he is the Guinness World Record holder for the most number of aircraft flown (12) in parabolas, personally logging more than 7,300 parabolas.
\n\nSeeing the 5,000th book published makes us at the same time proud, happy, humble, and grateful. This is a great opportunity to stop and celebrate what we have done so far, but is also an opportunity to engage even more, grow, and succeed. It wouldn't be possible to get here without the synergy of team members’ hard work and authors and editors who devote time and their expertise into Open Access book publishing with us.
\n\nOver these years, we have gone from pioneering the scientific Open Access book publishing field to being the world’s largest Open Access book publisher. Nonetheless, our vision has remained the same: to meet the challenges of making relevant knowledge available to the worldwide community under the Open Access model.
\n\nWe are excited about the present, and we look forward to sharing many more successes in the future.
\n\nThank you all for being part of the journey. 5,000 times thank you!
\n\nNow with 5,000 titles available Open Access, which one will you read next?
\n\nRead, share and download for free: https://www.intechopen.com/books
\n\n\n\n
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2020",datePublished:"April 8th 2020",book:{id:"8004",title:"Nitrogen Fixation",subtitle:null,fullTitle:"Nitrogen Fixation",slug:"nitrogen-fixation",publishedDate:"April 8th 2020",bookSignature:"Everlon Cid Rigobelo and Ademar Pereira Serra",coverURL:"https://cdn.intechopen.com/books/images_new/8004.jpg",licenceType:"CC BY 3.0",editedByType:"Edited by",editors:[{id:"39553",title:"Prof.",name:"Everlon",middleName:"Cid",surname:"Rigobelo",slug:"everlon-rigobelo",fullName:"Everlon Rigobelo"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:[{id:"158046",title:"Dr.",name:"Elaine Maria Silva Guedes",middleName:"Guedes",surname:"Lobato",fullName:"Elaine Maria Silva Guedes Lobato",slug:"elaine-maria-silva-guedes-lobato",email:"elaine.guedes@ufra.edu.br",position:null,institution:null},{id:"313880",title:"Dr.",name:"Barbara",middleName:null,surname:"Rodrigues Quadros",fullName:"Barbara Rodrigues 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Herbal medicine is commonly used to treat skin disorders, and the ethnobotanical remedies are developed in different regions, based on local plants. In particular, two different systems, Ayurvedic herbs, estabilished in India, and the traditional Chinese medicine, which uses the combination of different herbs, are known. In the occidental world, the use of herbal medicine is relative to purified extracts, often substituted for synthetic chemical drugs. In the last years, we assisted an intense return, in the occidental world, to herbal medicine, probably because we are living in the green revolution [1]. The use of vegetable raw materials in the preparation of products for local application on the skin dates back to ancient times. The term phytocosmetics, from Greek kosmesis, which means adorn, and phytos, which means plant, is used to indicate the predominant and preferential use of botanical derivatives in cosmetic products. The vegetable field is an inexhaustible source of raw materials that, transformed by various processes, find many applications, both as functional substances and as excipients of the products. Contrary to some 50 years ago, when the cosmetic use of medicinal herbs was largely based on the mere observation of the traditional use, today, numerous scientific studies on the properties of plant-based drugs, as well as advanced knowledge on technical-scientific ones that allow to extract the active principles contained in the plants, are available. The herbal phytonutrient offers an enormous amount and heterogeneity of substances, which, by means of various extracellular processes, give rise to extracts with various functional applications. The active constituents of plants are in fact represented by a complex mixture of substances of different chemical nature (tannins, pectins, saponins, flavonoids, essences, fixed oils, etc.) whose concentration in the extract is essentially linked to the particular extraction process. The most widely used vegetable extracts are glycolic extracts, hydroalcoholic extracts, distilled water, dried extracts, oily extracts, essential oils, and vegetable oils. Vegetable oils are obtained by cold squeezing of plant drugs whose active ingredients are characterized by oily texture. The oil is predominantly made up of polyunsaturated fatty acids rich in triglycerides and also contains antioxidant substances, liposoluble vitamins, and the so-called insaponifiable fraction, a complex mixture of substances of extreme interest both from the dermatological and cosmetic field. Olive oil, coconut oil, wheat germ oil, borage oil, and almond oil are the main types of vegetable oils used in cosmetics. Compared to other types of oily ingredients, the advantage of using vegetable oils in cosmetics and cosmeceuticals lies primarily in their particular lipid composition, which is very close to the structure and function of that of the physiologic sebum present in the interstices and the surface of the corneal layer of the epidermis. The very high affinity to the skin sebum gives them an excellent ability to restore the physiological skin barrier by means of a protective, filmogenic, and emollient action. In this chapter, we describe the advantageous effects of ozonated olive oil in the treatment of skin disorders; in fact, olive oil is considered one of the most excellent foods for diet, but it has anti-inflammatory action, so it is used for skin disease. In the chapter, we report information about the safety and mechanism of action on microorganism and on wound healing.
Olive oil consists of glycerides, such as oleic, arachidic, palmitic, linoleic, and stearic acids, and of phenolic compounds. It is very important in the culinary use, but it has important applications in cosmetic and pharmaceutical fields. The olive tree Olea europaea is a common feature of the Mediterranean landscape, with the olive fruit and olive oil being the basic elements in the nutrition of civilizations around the Mediterranean basin for millennia. The principal reason is due to the tree’s climatic requirements, which are found in limited areas of the earth’s surface [2]. This longevous tree integrates and identifies economically, socially, and culturally with the inhabitants of this land and determines its rural landscape [3]. Even olive leaves have been used in popular medicine. The therapeutic and health properties of olive oil have been known for millennia so much that Hippocrates advised the juice of fresh olives to cure mental illness and wraps to heal ulcers. During the Middle Ages and during the Renaissance, olive oil was used to cure gynecological infections and was considered useful in the treatment of heart disease, fever, and hypertension.
Virgin olive oil has been and still is the subject of numerous studies that have attributed great properties to it, both in the field of health and in cosmetology. Various epidemiological studies have shown that the incidence of inflammatory, cardiovascular, and tumor illnesses is generally lower in Mediterranean European countries (such as Greece, Italy, and Spain) than in other western and northern countries [4]. This can be attributed to the high consumption of olive oil in the Mediterranean diet, which contributes to the daily requirement of vitamin E, essential fatty acids, and specific antioxidants, particularly represented by phenolic compounds and tocopherols. In addition, antioxidants have a primary role in resistance to oxidation and hence in the stability of olive oil and have been shown to exert numerous beneficial effects on the human body. The antioxidants’ protective effect is mainly due to their ability to inhibit the action of oxygen free radicals, indicated by the acronym ROSs [5]. ROSs are highly reactive species represented by atoms or molecules with one or more electrons being dissipated, capable of generating the so-called oxidative stress. When the organism is subject to an increase in oxidative stress, an increase of F2-isoprostanes (IsoPs) in plasma levels and of urinary excretion is observed. IsoPs are a type of novel compound, structurally similar to prostaglandins, biosynthesized in vivo from the free radical–catalyzed peroxidation of arachidonate independent of the cyclooxygenases (COX) [6]. Oxidative stress seems to be the main reason for many chronic and degenerative diseases and skin aging. More specifically, ROSs induce (i) DNA mutations and protein alterations that are the basis of carcinogenesis [7]; (ii) oxidation of low density lipoproteins (LDL) involved in the formation of atherosclerotic plaques [8]; (iii) the onset of chronic intestinal inflammatory diseases, such as Crohn’s disease [9]; (iv) probable onset of neurodegenerative diseases, such as Parkinson’s disease [10]; and (v) cellular aging, by lipid peroxidation of the membranes, which become more permeable and less effective. All this evidence allows us to understand the importance of antioxidants, even from exogenous sources such as diet. The beneficial effects, and in particular the antitumor activity, of olive oil on human health are attributed to the high content of phenolic substances with high antioxidant power [11]. Phenolic compounds, in synergy with α-tocopherol and coenzyme Q, protect cells from oxidative damage by contrasting the toxic effects of ROS [12]. Through various epidemiological studies, the correlation between the consumption of virgin olive oil and the risk of onset of certain types of cancer has been demonstrated, such as breast [13], lung [14], colon [15], ovary [16], pancreas [17], and prostate cancer [18]. It has been shown that among the phenolic compounds, one of the most biologically active is hydroxytyrosol (3,4-DHPEA) that is able to inhibit the 5-lipoxygenase enzyme, by reducing the production of leukotriene B4 in the leukocytes, originating from the metabolism of the eicosanoids [19]. In addition, hydroxytyrosol is able to inhibit in vitro the oxidation of LDL [20] and in vivo [21] the aggregation of platelets [22]. Some experimental studies have also shown that the phenolic extract of virgin olive oil and two isolated compounds, the dialdehyde form of hydroxytyrosol (3,4-DHPEA-EDA) and thiol (p-HPEA-EDA), are able to inhibit uncontrolled cellular proliferation by blocking the cell cycle at G0/G1 and to induce apoptosis in some lines of cancer cells, as demonstrated for HL60 cells of promyelocytic human leukemia [23, 24]. However, compounds with greater biological activity are those containing the ortho-diphenol residues; it has been shown that 3,4-DHPEA and 3,4-DHPEA-EDA are more effective than p-HPEA and p-HPEA-EDA in protecting DNA from damage caused by oxidation [25]. In an in vitro study, by examining different virgin olive oil extracts, a chemoprotective effect was demonstrated on HL60 cell lines in relation to their composition but not to the total content of phenolic substances [26]. ROS production is also closely related to inflammatory processes in which the cyclooxygenase enzymes (COX-1 and COX-2), belonging to the oxidoreductase class, catalyze the conversion of arachidonic acid into prostaglandins. The p-HPEA-EDA, also called oleocanthal, has the ability to inhibit the activity of such enzymes and has a pharmacological effect similar to that of ibuprofen, which belongs to the class of nonsteroidal anti-inflammatory drugs [27]. It has also been shown that the consumption of olive oil may improve blood pressure regulation and cholesterol content in the blood; these events, together with the inhibition of platelet aggregation and the reduction of LDL oxidation, are important to prevent the onset of atherosclerotic plaques and, in general, cardiovascular pathologies [28, 29]. Olive oil also contains many monounsaturated fatty acids, including oleic acid, which is a key component of cellular membranes and can progressively replace polyunsaturated fatty acids. Membranes rich in monounsaturated fatty acids are more fluid and less subject to lipid peroxidation [30]. Some studies have also shown that regular intake of this food may result in a reduction in the risk of developing diabetes [31]. The therapeutic properties of olive oil include a laxative effect and stimulation of biliary function [32]. Finally, some studies on animal models have shown that the intake of olive oil can help to counteract the damage caused by epidermal ultraviolet radiation [33].
In recent years, in a number of fields, including cosmetics, there has been a renewed interest in materials of natural origin, particularly those of vegetable origin. Since ancient times, olive oil has been known not only for its high nutritional power but also for its cosmetic and therapeutic properties [34]. In 1971, Thiers was still pointing to its potential use in the cosmetic sector. To date, olive oil is certainly the most appreciated natural ingredient, alongside jojoba and avocado oils. The topical application of olive oil may be advised for its soothing action and its beneficial effects on eczema, surface wounds, and burns [35, 36]. In particular, the presence of phytosterols and triterpenoid compounds offers revitalizing and soothing properties for the skin. Vitamins E and A have an intense antioxidant action and have the ability to prevent irritation and aging of the skin, to help maintain its softness, smoothness, stability, and elasticity. As a result, in the cosmetic field, olive oil can be used to prevent signs of aging as a soothing emollient for dry skin and to strengthen hair [37]. Indeed, it is very often a component of lotions, lip balms, shampoos, bath oils, and massage oils. From a dermatologic point of view, olive oil has also proven to have antimicrobial activity, in vitro, against some positive and negative Gram and various types of fungi, including Candida spp. [38]. Some components of olive oil, especially certain aliphatic aldehydes, inhibit elastase activity; this enzyme is involved in the virulence process [39]. Olive oil is an important component of some topical formulations used in the treatment of inflammatory and mycotic skin diseases [40]. The unsaponifiable fraction is rich in numerous active ingredients with sebum-regulating and moisturizing properties, as well as emollients; it can be a component of cosmetic products (in the form of creams, balms, gels, etc.) for the treatment of delicate, dry, and cracked skin. In fact, the unsaponifiable fraction is very useful in the case of particularly vulnerable skin, such as that of infants and children, or in the case of xerotic skin, such as that of the elderly. Skin hydration is above all important in the neonatal period and especially in premature infants: some clinical trials have been conducted to highlight the beneficial effects of emollient topical treatment [41, 42]. Furthermore, the unsaponifiable fraction exerts a good photoprotective effect on ultraviolet exposed skin: various studies have shown that the application of olive oil may reduce the incidence of skin epithelial tumors on UV-B–exposed mice compared to a control group [43, 44]. The unsaponifiable fraction can also be an additive in makeup products with the purpose of making them easier to apply, softer, and smoother. Butter contains high quantities of squalene (which is the most important constituent of sebum), waxes, and esters that guarantee high penetration of the skin. Butter is ideal for massages or as a vehicle for other active ingredients used in skin care. It acts also as an emollient and moisturizing agent, promoting skin elasticity and preventing the onset of wrinkles. Finally, it can be used as an additive in photoprotective products or in skin hygiene products due to its ability to neutralize aggressive detergent action.
An interesting and powerful way to use extra virgin olive oil is with ozone. The process of ozonization allows the properties of ozone gas to be combined with those of olive oil; the result is a peerless compound. Since ancient times, ozone has also been used in a large number of medical indications [45, 46, 47, 48, 49].
Ozone is an oxygen derivative and is known primarily for its ecological role in the Earth’s balance, absorbing most of the ultraviolet radiation from the sun and preventing it from reaching humans in a harmful way. It is an unstable gas that cannot be stored; in fact, it dissolves in very short time. Ozone is totally neutral to the human body, and in fact, it does not (i) modify pH, (ii) irritate skin or mucous membranes, (iii) damage hair or clothing, (iv) interact with drugs, and (v) cause allergic reactions. This molecule has been subjected to countless studies, and in particular, its strong oxidation capacity has been tested in order to underline its disinfectant and sanitizing properties principally applied as a disinfectant of drinking and waste water [45, 46, 47]. To this purpose, the dedicated design and construction of equipment for the production of gaseous ozone for air and water purification are increasing. But research into the properties of ozone has yielded promising results in biological applications, thus confirming the ozone activity in stimulating natural cell defenses and increasing their energy availability. Indeed, since ancient times, ozone has also been used in a large number of medical indications [48, 49]. Scientific studies have shown that ozone, while being highly unstable, can be trapped inside vegetable oils. These are composed of triglycerides in which saturated and unsaturated fatty acids are present, which have the ability to retain ozone, thus allowing them to prolong their use. In addition, the greater the amount of unsaturated fats present, the greater the amount of ozone that will be retained [50]. Therefore, when extra virgin olive oil is ozonated, the produced product combines the beneficial properties of extra virgin olive oil with those of ozone. There are countless ozone-based products on the market, and in particular, in our laboratory, we have developed Bioxoil™, an ozonated extra virgin olive oil available in pharmacies. This product is exclusively made from olive cultivars from Puglia and Salento and the oil is ozonated by an innovative patented method (number: M2011A001045 titled: “Process for the ozonization of a vegetable oil“) that confers quality and efficiency in various fields of application; in particular, Bioxoil™ is indicated for the treatment of acne, herpes, psoriasis, fungal infections, bed sores, and wounds in general, due to its healing and disinfectant properties (Figure 1).
Bioxoil™ products. The Bioxoil products have different applications. Bioxoil with a red label is indicated for bed sores; the sky blue label is indicated as soothing medication; the green label is indicated for herpes labialis; the pink label is indicated for acne; and the orange tag is indicated for mycosis.
Bioxoil™ is produced from extra virgin olive oils from two local cultivars, Ogliarola and Cellina, in Salento (Apulia, Italy). The ozone reacts with unsaturated compounds through the known Criegee mechanism. The quality of extra virgin oil is very important to obtain a higher grade of ozonization; for this reason, during the process, it is necessary to control different physical and chemical parameters. Of these parameters, the most important is the temperature, and in fact, during the reaction, the temperature increases provoking an alteration of antioxidant content. The oils’ peroxide content and acidity value that indicate the level of hydrolytic modification and primary and secondary oxidation of oil are analyzed and reported in Table 1. Peroxide index (PI) and acidity index (AI) after ozonization of oils increase with respect to relative controls. In particular, Cellina’s oil sample has an acidity index of 0.2% and a peroxide index of 12 mmol O2 kg−1, while related ozonated oil has an AI of 1.8% and a PI of 533 mmol O2 kg−1. Ogliarola’s oil sample presents an acidity index of 0.3% and a peroxide index of 13 mmoli O2 kg−1, while respective ozonated oil has an AI of 1.3% and the PI increases to 677 mmoli O2 kg−1.
Sample | Acidity index (AI), % (means ± SD) | Peroxide index (PI), mmol O2 kg−1, (means ± SD) |
---|---|---|
Ogliarola olive oil | 0.2 ± 0.03 | 12 ± 1.2 |
Ozonated Ogliarola olive oil | 1.8 ± 0.02 | 533 ± 1.5 |
Cellina olive oil | 0.3 ± 0.02 | 13 ± 1.5 |
Ozonated Cellina olive oil | 1.3 ± 0.01 | 677 ± 1.6 |
Physicochemical parameters of Ogliarola olive oil and Cellina olive oil after ozonization procedure.
In our experiments, the ability of ozone to react with olive oil and in particular with the carbon-carbon double bonds present in unsaturated fatty acids was demonstrated by gas liquid chromatography (GLC). The composition of fatty acids of each olive oil and respective ozonated oil are analyzed by GLC. Data demonstrate that the amount of oleic acid decreases in both ozonized oil samples: in Cellina’s ozonated oil, we observed a 30% reduction, while in Ogliarola’s ozonized oil, the reduction was about 26% (Table 2). During the ozonization reaction, ozone etches mainly the double bond of acid oleic, the most abundant fatty acid in olive oil (about 80%). This explains the decrease in oleic acid and the contemporary appearance of new compounds, which are the reaction’s products, among which are nonanal aldehyde and nonanoic acid, both compounds with nine carbon atoms (Table 2). In both cultivar ozonized oils, the composition of fatty acids changes, showing a gradual decrease in unsaturated fatty acids (C 18:1, C 18:2), with a gradual increase in ozone doses.
Composition of fatty acids (%) | Cellina | Cellina | Ogliarola | Ogliarola |
---|---|---|---|---|
Control | Ozonated oil | Control | Ozonated oil | |
Palmitic acid | 12.45 | 11.91 | 11.89 | 11.30 |
Linolenic acid | 5.57 | 2.19 | 4.96 | 2.06 |
Cis-oleic acid | 70.27 | 39.82 | 67.00 | 41.25 |
Trans-oleic acid | 8.22 | 6.68 | 7.88 | 7.2 |
Stearic acid | 3.48 | 1.29 | 3.32 | 3.22 |
Nonanal | 0 | 11.69 | 0 | 10.07 |
Nonanoic acid | 0 | 1.36 | 0 | 1.98 |
Composition of fatty acids in olive oil samples Cellina and Ogliarola.
The skin is the largest organ of the body and is the major barrier between the inside and outside of our body. It is formed of two main layers: the epidermis, a thin outer portion, and the dermis, the connective tissue layer of skin. This portion is involved in the thermoregulation process, and the resident dermal fibroblasts secrete collagen, elastin, and substances that offer support and elasticity of the skin. The epidermis is subdivided into four layers: (i) the stratum germinativum (SG) that provides the germinal cells necessary for the regeneration of epidermidis; (ii) the stratum spinosum (SS), in which the cells divided in the SG start to accumulate many desmosomes on their surface; (iii) the stratum granulosum (SGR), in which the keratinocytes accumulate dense basophilic keratohyalin granules that contain lipids, which help to form a waterproof barrier; and (iv) the stratum corneum (SC), the outermost layer, in which the cells are dead. The skin is constantly exposed to the environmental stress of pollutants or cigarette smoke, for example, so it is necessary for the wellness of the skin to preserve it from oxidative stress. To this purpose, there are a variety of antioxidants that include glutathione peroxidase, superoxide dismutase, catalases, and nonenzymatic low-molecular weight antioxidants such as vitamin E isoforms, vitamin C, glutathione (GSH), uric acid, and ubiquinol. Interestingly, the distribution of antioxidants in the SC follows a gradient with higher concentrations in deeper layers [51].
The biocompatibility of Bioxoil™ was investigated by MTT assay on fibroblast 3T3 and on keratinocytes HaCaT and compared with ozonated dulcis almond oils and nonozonated olive oil as controls. The MTT test values the cell metabolic activity and, in particular, measures the activity of oxidoreductase by reduction of the tetrazolium bromide dye in formazan. The dulcis almond oil was chosen because it is largely used in cosmetics, and as it is an oil, it is a possible vector of ozone. Data reported in Figure 2 demonstrate the Bioxoil™ biocompatibility for both cell types. The viability of cells never significantly decreased in relation to the control and was the same as the nonozonated oil. Conversely, once ozonated, 10% of dulcis almond oil had a very significant negative effect on the viability of fibroblasts and keratinocytes but not when dulcis almond oil was nonozonated. Interestingly, the vitality test demonstrated that when these cells are exposed to a mixture of ozonated olive oil and 10% of ozonated dulcis almond oil (3:1), the adverse event induced by the ozonated almond oil alone was partially prevented (Figure 2).
MTT assay on fibroblasts and keratinocytes.
By combining the beneficial properties of extra virgin olive oil with that of ozone, the ozonated extra virgin olive oil becomes very powerful for the topical treatment of acute and chronic skin lesions. The ozonides generated during the ozonization procedure possess many properties including a high germicidal activity on fungi, yeasts, viruses, and bacteria; activation of local microcirculation; stimulation of granulation and tissue growth; and revitalization of epithelial tissues.
The excessive consumption of antibiotics for the treatment of infectious diseases has fuelled the drug resistance phenomenon, i.e., the microorganisms are resistant to antibiotics. Therefore, it is necessary to develop new molecules with antibiotic properties, preferably natural and nonsynthetic. In fact, this research is divided into the field of synthetic molecules produced by the chemical/pharmaceutical industry and the field of natural active compounds, in which plant extracts are studied also by the use of green chemistry. The plants are able to withstand fungal and bacterial infections and therefore their secondary metabolites can be applied in the field of medicinal herbs. Maoz and Neeman in their research reported an antifungal action of olive oil due to the high content of oleic acid [52]. The ozonated oil increases this natural capacity, because ozone acts on microorganisms, thanks to its greater oxidizing power; in fact, it is able to break down the macromolecules that are the basis of the vital integrity of bacterial cells, fungus, protozoa, and viruses. The ozone in contact with the microorganism’s lipoproteins forms H2O2 and the final products of lipid oxidation (LOP); H2O2 assures bacteriostatic and bactericidal activity, while final lipid oxidation products have induction activity and reactivate metabolic functions (Figure 3). Nagayoshi et al. [53] reported the capability of ozone to destroy Gram-positive and -negative microorganisms, and in particular, Gram-negative bacteria are more sensitive.
Molecular mechanism of antimicrobial activity of ozonides: the oxygen internalized from ozonides reacts with the proton/protons in order to form H2O2 that has a bacteriostatic and bactericidal activity.
For virus inactivation, a higher gas dosage than that required for bacteria is necessary. The ozone oxidates and subsequently inactivates the specific viral receptors used to bind the cell wall for virus invasion [54]. We tested the antibacterial activity of Bioxoil™ on mycete Epidermophyton floccosum, demonstrating its efficacy in the inhibition of mycete’s growth in liquid and agar medium; the bacteriostatic effect is obtained in the presence of 5 μl/ml of ozonated olive oil, and the bactericidal effect is obtained in the presence of 15 μl/ml (Figure 4).
Growth curves of mycete Epidermophyton floccosum in liquid culture medium: 1A, 2A, and 3A are the positive controls with 12.5, 25, and 50 mg/ml of nonozonized olive oil, respectively; 1B, 2B, and 3B are ozonized olive oil samples with 12.5, 25, and 50 mg/ml of ozonized olive oil, respectively; 4 is the negative control.
The antibacterial activity of Bioxoil™ was also tested on Staphylococcus aureus and Staphylococcus epidermidis, and its efficacy in inhibiting microbes growing both in liquid medium culture and in agar medium was demonstrated. We defined the minimal inhibitory concentration (MIC) of 50 mg⋅ml−1 for S. aureus and of 25 mg⋅ml−1 for S. epidermidis. This study confirms that ozonated olive oil has antimicrobial properties, which can be exploited for cutaneous infections, by slow release of O3, which displays effective disinfectant and stimulatory activities that lead to rapid healing.
The ozonides easily penetrate the cell membrane and, thanks to their biological properties, stimulate skin cells and improve the tropism of the skin by promoting wound healing and repair of ulcers of various kinds; from the experiments, it was found that topical application of products based on ozonides has determined a considerable increase of fibroblasts resulting in increased production of collagen, glycosoaminoglycans, and formation of elastic and reticular fibers. The healing of skin lesions includes complex movements like tissue hemorrhage, inflammation, re-epithelialization, granulation tissue, and finally remodeling. These events involve the coordination of many cell types and matrix proteins, which are important for the control of the various stages of tissue repair. Previous studies have shown that endogenous growth factors, such as fibroblast growth factor (FGF), growth factor derived from platelets (PDGF), the TGF-β factor, and vascular endothelial growth factor (VEGF) are important regulators in the healing of wounds [55]. They are released by macrophages, fibroblasts, and keratinocytes at the site of injury and participate in the regulation of re-epithelialization, formation of granulation tissue, collagen synthesis, and neovascularization [56, 57, 58]. The beneficial effects of ozone in the treatment of sores are due to the decrease of bacterial infection and the increasing oxygen tension in the wound. In the literature, it is reported that after exposure to ozone transcription factors are activated, such as NF-kB, and these are important regulators of the inflammatory response and tissue repair process [58]. In conclusion, the ozonated olive oil can accelerate acute cutaneous wound repair, by stimulation of dermal fibroblast, and the ozonized oil has shown to be effective against Gram-negative and -positive bacteria, mycetes, and viruses, so it can be used for the cure of infections.
The goal of pharmacological research has always been that of finding drugs that can cure diseases or soothe the pain that derives from them, and this research has evolved over the years in an extraordinary way both in the field of medical knowledge and scientific studies that are more and more powerful and sophisticated. Medicinal herbs, long popular in many parts of the world, are increasingly spreading in the western world and represent a large commercial market with an estimated annual growth of 25%, often replacing synthetic drugs. Among the medicinal herbs, particular interest is reserved to olive oil, called “yellow gold” by the Egyptians for its innumerable beneficial properties. Herbal trade today sees many products based on olive oil for both hygiene and personal care. In the field of oil-based products, particular interest is directed to products containing ozonated oil; these products are the result of the union of the beneficial properties of olive oil with those of ozone. Ozonated oil is the most practical, innovative, harmless, and noninvasive of the techniques of application developed in the field of ozone therapy over the last 130 years. It has demonstrated interesting therapeutic results. The biological effects of ozone include antimicrobial activity (antibacterial, antiviral, and antifungal), antalgic action, and improved O2 metabolism [59]. In this chapter, the possible applications of the Bioxoil™ products, already distributed in pharmacies and herbalist’s shops, have been described; its production line includes five different products characterized by different concentrations of ozonides such as to allow the use for the most varied skin affections. Bioxoil with the highest content of ozonides is indicated for the treatment of bedsores at first and second stages, thanks to its anti-inflammatory and cicatrizing properties, Bioxoil with medium concentrations, but different from each other, is indicated for the treatment of herpes labialis, mycosis, and onychomycosis and for acne due to its antimicrobial action. Finally, Bioxoil with the lowest ozonide content is indicated to soothe contact or allergic irritations. The exceptional usability of the product and its completely natural origin offers a vast market.
ROS | reactive oxygen species |
IsoPs | F2-isoprostanes |
COX | cyclooxygenase |
LDL | low density lipoprotein |
3,4-DHPEA | hydroxytyrosol |
3,4-DHPEA-EDA | 3,4-dihydroxyphenylethanol-elenolic acid dialdehyde |
p-HPEA-EDA | 2-(4-hydroxyphenyl)ethyl (4E)-4-formyl-3-(2-oxoethyl)hex-4-enoate |
COX-1 | cyclooxygenase 1 |
COX-2 | cyclooxygenase 2 |
PI | peroxide index |
AI | acidity index |
SG | stratum germinativum |
SS | stratum spinosum |
SGR | stratum granulosum |
SC | stratum corneum |
GSH | glutathione |
LOP | lipid oxidation |
MIC | minimal inhibitory concentration |
Water scarcity jeopardizes not only originally arid, semi-arid regions but also agricultural areas in which farmers obtain flourishing horticulture based on adequate water resources. Nonetheless, ongoing climate change supposed to amplify the frequency and severity of drought in different regions of the globe [1] can wipe out the so far achievements. Drought is the most devastating stress that remarkably diminishes crop productivity more than any other stress factor [2]. Water constraints provoke stomatal closure with a subsequent reduction of CO2 influx resulting in a decrease in photosynthetic activity and carbon partitioning [3]. Also, water scarcity has a negative influence on nutrient supply, reducing phosphate availability. Severe drought profoundly affects plant physiology, growth, development, and reproduction, and exerts substantial losses in crop yield as well as reduces crop quality. In fact, over the past 35 years, worldwide drought inflicted yield decrease by 40% in maize and 21% in wheat production [4]. Thus, there is an urgent need to develop strategies to make agriculture more resilient and to alleviate the adverse impacts of water scarcity on crop yield. Among these strategies, there has been an increasing interest in beneficial soil microbes including arbuscular mycorrhizal (AM) fungi.
\nNotably, under natural conditions, plants frequently interact with microbes, which directly mediate plant responses to environmental adversities. Some microbe-plant interactions lead to a mitigation of stress-related damages and improvement of plant tolerance to stressful conditions [5]. As a crucial element of soils, microbes are an integral part of the agricultural ecosystem. Arbuscular mycorrhizal fungi (AMF) are ubiquitous soil microorganisms, which can form a symbiotic association with most terrestrial plants. These beneficial microbes have been proved to offer an array of benefits to host plants [6]. During mycorrhization, besides significant improvement of plant nutritional status, AMF can enhance plant performance and tolerance against several stresses, particularly drought stress [7]. The exploitation of AMF is considered as one of the most efficient practices to increase plant tolerance to environmental stresses [8]. Previous studies illustrate the substantial contribution of AM symbiosis to improved stress plant tolerance to water deficit by various mycorrhizal benefits such as strengthened water and nutrient uptake, alterations in host physiology, for example, photosynthesis, osmotic adjustment, phytohormones, and more efficient antioxidative systems [9, 10, 11]. This chapter presents the current knowledge on AMF application to crop production under water deficit. Variable benefits of AMF are also discussed to explain the reason why positive outcomes of AM colonization are not always the case. Finally, challenges of the fungal symbiont application are highlighted for practical use in crop production.
\nAMF are obligate root symbionts inhabiting almost all terrestrial ecosystems. They can form a symbiotic association with around 80% of vascular plants and with approximately 90% of agricultural plants [12]. In this mutual association, the fungus receives 10–20% of total photosynthates [13] and lipids [14] from the host plant, whereas the plant is enhanced through uptake of water and mineral nutrient by the mycorrhizal partner [12]. AMF are the most common fungi in soils and represent 9–55% of the soil microbe biomass and 5–36% of the total soil biomass [15]. These fungi play a vital role in agricultural ecosystems, since they can improve plant nutrient, water status, and plant growth [12], enhance survival rate and development of seedlings, crop uniformity, and reproductive capacity [16], decrease the input of P and N fertilizer, and increase resistance or tolerance to environmental adversities [8, 17].
\nCurrently, AMF are classified as a member of phylum Glomeromycota including four orders (Archaeosporales, Diversisporales, Glomerales, and Paraglomerales), with 11 families, 25 genera, and nearly 250 species [18]. However, data based on next-generation sequencing of root samples [19] and recent results [20] suggest that its number may be an order of magnitude higher. Spores of AMF which are the major survival units of AMF have multi-nucleate, heterokaryotic structures [21], and are formed singly, in clusters or sporocarps in the soil, and within root tissue in some mycorrhiza species as well (Figure 1A–C). The development of AM symbiosis starts with signaling taking place before physical contact between the plant and the fungus. Both partners produce molecular signals triggering preparative responses in the other [22]. The mycorrhization process can be divided into distinct steps, consisting of germinating spores, hyphae differentiation, appressorium formation, penetration of the host root, intraradical hyphae formation, intercellular growth along with developed external mycelium (extraradical hyphae), and arbuscule formation, subsequently exchanging nutrients and carbohydrates between the host and fungus [23].
\nTomato roots without (A) and with (B–D) staining showing AM fungal structures. The presence of arbuscular mycorrhiza (AM) structures (arbuscules, vesicles, intraradical hyphae, and spore) was assessed by means of an Olympus BX51 light microscope with Nomarski interference contrast optics, using an objective of 40×. Scale Bar representing 20 μm.
The primary structures of AMF consist of coenocytic hyphae with unlimited growth in the rhizosphere called external hyphae, which penetrate the cortex layer of roots and form different organs. The extraradical hyphae merely in some species of Diversisporales [18] producing auxiliary cells could have functions in reproduction or nutrition and storage [24]. Mycelium outside the roots absorb mineral nutrients and water and subsequently transport them to the host plant via intraradical hyphae (Figure 1C,D) growing inside root cells [6]. Hyphae growing within roots form either the Paris-type or the Arum-type. The Paris-type is featured by intracellular mycelium development to shape coils, whereas the Arum-type is characterized by intercellular hyphae growth forming arbuscules [12] (Figure 1D), thereby establishing the nutrient exchange sites between AMF and the host plant [25]. Vesicles containing high quantity of lipids and glycogen are formed from intraradical hyphae at intercalary position (their terminal) in the root, functioning as nutrient storage, and propagules [23] but not all AMF produce vesicles.
\nAMF species isolates differ in the ability to spread mycelia, the viability, structure, and possibility of anastomosis [26, 27]. Taxonomic variation in mycelium structure among AMF families was also observed [28]. Gigasporaceae are prone to possess vigorous, thickly aggregated mycelium with densities from 6 to 9 m cm−3, while Acaulosporaceae and Glomeraceae show a tendency to maintain thinly dispersed mycelium with densities from 1 to 2 m cm−3.
\nAlthough a majority of plants are responsive to AMF, plant species in families Amaranthaceae, Brassicaceae, Caryophyllaceae, Chenopodiaceae, Cyperaceae, Juncaceae, and Urticaceae are rarely or never colonized by the symbiotic fungus [29]. How AMF evaluate the AM host and nonhost status of plant species is not well known. The current hypothesis proposes that nonmycorrhizal plant species lost orthologs of important putative genes, required for symbioses [30], and/or cannot synthesize or degrade strigolactones, essential signals for symbiosis establishment [31], and/or their root exudates constitute antifungal products [29]. Under certain conditions, some nonhost species develop rudimentary AM phenotypes described by Cosme et al. [30] giving a more in-depth explanation of this question.
\nUtilization of AMF has become an appealing tool for sustainable agriculture due to the positive attributes of mycorrhizal symbiosis. Nevertheless, the opposite or neutral influence of AMF has also been found [32]. The obligate biotrophic life cycle of AMF which relies on photosynthates supplied by a nurturing autotrophic host is the key point; therefore, choosing the right partner (target plant) is crucial. Even though this widespread symbiont is thought to be a generalist due to low host specificity, each AMF species highly varies in the responsiveness to the host plant. Hence, the variable benefits of AM symbiosis exist among mycorrhiza species [10, 33]. The interaction between the host plant and AMF could range from mutualism to parasitism in which colonized plants exhibit a decrease in growth [34] owing to the carbon drainage in the host inflicted by the fungus [35]. Many factors that can affect the AM benefits to target plants include host plant genotypes, AMF species, and environmental conditions. Dissimilar plant responses to different AMF species under environmental adversities have been observed [11, 36]. Fascinatingly, AM benefits for plant fitness augment with adversity, supporting the concept of AM colonization as a ‘health insurance’ for host plants, in which the beneficial effects of AMF become more obvious under stressful environments [36]. Metabolites differentially accumulated in roots colonized by different fungal symbionts (Rhizophagus irregularis, Funneliformis mosseae, and Claroideoglomus etunicatum) under abiotic stresses, which may underlie their enhanced stress tolerance in host plants [36]. Cultivar differences in response to mycorrhizas have been reported in many crops such as tomato [37], pepper [38], wheat [39], maize [40], and some other crops [41]. For chickpea, only three of thirteen varieties with different genotypes and phenotypes were more positively responsive to AM mixed inoculation with Diversispora eburnea, Claroideoglomus etunicatum, and Glomus sp. [42]. More recently, twenty geographically different barrel clover (Medicago truncatula) accessions showed differences in their growth, stomatal conductance (gs), and AM colonization in response to Funneliformis mosseae treatment [43]. Also, root hydraulic conductivity, expression of the mycorrhiza-induced phosphate transporter gene (MtPT4), and five aquaporin genes (MtAQP1, MtPIP1, MtPIP2, MtNIP1, and MtNIP4) vary with mycorrhizal treatment during further analysis of five accessions. In the case of wheat, old accessions have been shown to be more responsive to AMF than new ones [39].
\nSelection and breeding programs generally tend to maximize plant performance and crop yield under high-input production systems, which could cause the loss of genes, phytochemicals, and/or other plant traits which are necessary for the establishment of efficient symbioses. Modern cultivars could absorb phosphate without the AM assistance in soils with high phosphorus availability, decreasing the degree of AM dependence. As a consequence, AMF are less responsive to new lines. Recent research has proved that domestication decreased AM benefits for domesticated crops in exposure to high P supply [44]. However, in maize, which is highly mycorrhizal-dependent, modern breeding programs do not necessarily result in the less mycorrhizal colonization. Replicated field experiments with 225 genotypes consisting of hybrids, inbred lines, and landraces originating from different locations were conducted for two consecutive years to explore the variation in mycorrhizal colonization [40]. The findings showed that AM colonization differed profoundly and continuously among genotypes, with substantially greater values in modern hybrids than old landraces and inbred lines.
\nIt is well known that AMF offer indispensable advantages to the host plant subjected to water shortage, with two major strategies that mycorrhizal plants use to deal with water deficit: drought mitigation and drought tolerance. Drought mitigation strategy is involved in indirect AM benefits and enhanced water uptake through the extensive hyphae network, enabling host plants to suffer less stress than non-AM plants, whereas drought tolerance includes a combination of direct AM benefits that improve plant’s innate ability to cope with the stress (Figure 2).
\nStrategies of mycorrhizal plants to cope with water scarcity, that is, drought mitigation and drought tolerance. Multiple benefits/mechanisms could be simultaneously induced by arbuscular mycorrhizal fungi in the host plant exposed to water deficit. The blue arrows show increase/up-regulation, whereas the orange arrows indicate decrease/down-regulation, relative to control non-mycorrhizal plants. Italic words indicate genes. ABA, abscisic acid; AQP, aquaporin; Car, carotenoids; Chla, chlorophyll a; Chlb, chlorophyll b; Fv/Fm, maximum quantum efficiency of PSII; gs, stomatal conductance; IAA, indole-3-acetic acid; iWUE, intrinsic water use efficiency; JAs, jasmonates; LWP, leaf water potential; MDA, malondialdehyde; MeJA, methyl jasmonate; PN, net photosynthesis rate; ROS, reactive oxygen species; RWC, relative water content; SLs, strigolactones.
An important benefit of AM colonization to the host plant under drought stress is a superior water allocation mediated by the fungal hyphal network, facilitating the colonized root access to water in a lower soil water potential [45]. Indeed, the host root system is extended by widespread extraradical mycelia, enabling colonized roots to reach more water and nutrient pools unavailable to uncolonized roots. Fungal hyphae diameters (3–7 μm) are much smaller than those of fine root hairs (5–20 μm); nevertheless, hyphal densities are ten-hundred times higher than root densities [46]. Hence, the absorption surface of mycorrhizal roots is improved substantially. It is calculated that the rate of water transport from external hyphae to the root ranged from 0.1 [47] to 0.76 μl H2O h−1 per hyphal infection point [48], which is adequate to alter plant water relations [47]. Lettuce plants pretreated by Rhizophagus irregularis, Funneliformis mosseae, Funneliformis coronatum (formerly Glomus coronatum), and Claroideoglomus claroideum (G. claroideum) obtained 3–4.75 ml H2O plant−1 day−1 higher than uncolonized plants, which might be related to the amount of extraradical mycelium and root colonization frequency [45]. Furthermore, AMF contribute approximately 20% to total plant water uptake [49], highlighting the role of the symbiosis in the water status of host plants.
\nThe widespread extraradical mycelia also enhance the absorption of mineral nutrients in soils, which is more critical for host plants under water-stress conditions where nutrient mobility is limited. As soon as external hyphae transport water to the host, mineral nutrients also follow the water flow to the plant from the soil-root interface [50]. AM colonization is well known to improve phosphorus (P) nutrient into the host plants particularly under low-nutrient conditions, increasing stress tolerance in plants. Interestingly, plants possess a symbiotic inorganic phosphate (Pi) uptake pathway, and AM symbiosis has been proved to specifically induce the expression of genes encoding plant Pi transporters to enhance P acquisition, for instance, LjPT4 in Lotus japonicus and MtPT4 in Medicago truncatula [51], recently LbPT3, LbPT4, and LbPT5 in Lycium barbarum [52]. Under water restrictions (moderate and severe), different expressions of five tomato PT genes (LePT1-LePT5) in the absence/presence of Rhizophagus irregularis or F. mosseae were observed [53]. LePT4 was overexpressed in R. irregularis-colonized plants exposed to both water-stress levels, while this upregulation was in F. mosseae-infected plants subjected to severe water stress. A role of PT4 genes in root tips, creating a connection among root branching, Pi-signaling mechanisms, and Pi-perception has been proposed [51]. In addition, on the fungal side, R. irregularis PT gene was up-regulated under moderate drought conditions [53]. Phosphate is taken up by mycorrhizal phosphate transporters and assimilated to polyphosphate translocated toward the plant. This process is facilitated by the activation of fungal aquaporins [54].
\nApart from that, AM colonization enhances the rate of nitrogen (N)-assimilation of plants under drought [55] as a result of the direct uptake of NO3− or NH4+ by fungal hyphae [56]. Several NO3− and NH4+ transporters and metal transporters in AMF [57, 58] while mycorrhiza-inducible ammonium transporters in some plants have been identified [59, 60]; therefore, AMF considerably contribute to the total N uptake of the host. Increased N nutrient could promote protein synthesis and higher levels of compatible osmolytes in stressed AM plants. Other studies also confirmed that inadequacy of necessary macro- and micro-nutrients could be alleviated in mycorrhizal plants under water deficit [61, 62]. Hydraulic conductivity of colonized roots was enhanced to absorb more N, P, and K, leading to a higher protein concentration in host plants under drought stress [63]. Thus, more vigorous uptake of water and nutrients may provide adequate necessary substances for better growth of mycorrhizal plants under such stress.
\nThe negative water potential in dried soils exerts the problem for plants to obtain adequate water amount, a process where aquaporins (AQPs) get involved in [64]. AQPs belonging to the large major intrinsic protein family of transmembrane proteins functioning as water channels are crucial in osmoregulation [64]. On top of that, their regulation of transcellular movement of many molecules such as small alcohols, boron, and osmolytes has been reported [65]. In AMF, the first AQP gene GintAQP1 of Rhizophagus irregularis was cloned, with evidence of a compensatory mechanism between GintAQP1 expressions and the host aquaporins under drought stress [66]. Furthermore, two AQP genes GintAQPF1 and GintAQPF2 present in Rhizophagus irregularis were upregulated under osmotic stress, assisting the fungus survival and contributing to the host plant tolerance to water stress [67, 68]. Upregulation of RiAQPF2 in Rhizophagus irregularis was also found under water deficit [10], suggesting its putative involvement in host plant tolerance in response to drought.
\nOn the plant side, AMF could induce changes in the expression of various AQP genes in the host in order to strengthen root hydraulic conductivity and host tolerance under water-stress conditions in several plants, such as maize [69, 70, 71], tomato [10, 11], black locust [72], trifoliate orange [73], olive [74], and Populus x canadensis plants [75]. AM-induced alterations in expression of plant AQPs could depend on stress duration as the observation in maize plants [69]. Under short-term water deficit, the AM symbiosis upregulated ten AQP genes with diverse aquaporin classes in roots inoculated with Rhizophagus intraradices, stimulating more water uptake in the host [69]. By contrast, under sustained water-stress conditions, AM-mediated downregulation of 6 different AQP genes was found, restricting plant water loss [69]. Intriguingly, drought-sensitive cultivars may gain higher physiological benefit from AM inoculation than drought-tolerant cultivars [71]. Downregulation of genes TIP1;1, TIP2;3, PIP1;1, PIP1;3, PIP1;4, PIP1;6, PIP2;2, and PIP2;4 whereas only upregulation of TIP4;1 were observed in drought-sensitive cultivar colonized by Rhizophagus irregularis, supporting the decrease in water loss in host plants subjected to drought stress [71]. Recent research also revealed a significant shift in the transcriptional regulation profiles with AQP genes as potential targets in mycorrhizal roots, in comparison to non-AM ones during a water stress event, which may influence some key metabolic pathways linked with drought response [76]. In parallel, it has been proposed that during drought stress a controlled mechanism mediated by the presence of arbuscules at cortical cells in roots fine-tuned the gene expression regulation in the host plant [76].
\nIn general, fungal and plant AQPs work together in mycorrhizal plants under water restrictions. The simultaneous induction of both fungal and plant AQP genes together with differential regulation of drought-responsive genes in host plant indicates that AMF mediate colonized plant responses to drought stress.
\nNumerous reports illustrate that AMF could increase photosynthetic activity or protect the photosynthetic apparatus under water stress conditions [77, 78]. In fact, AM colonization considerably influences the stomatal behavior in the leaves of host plants, determining the water vapor efflux, CO2 gas exchange, and thus photosynthetic activity [79]. Stomatal conductance changed by AM inoculation is closely connected to leaf water potential and relative water content in host plants. Under water restrictions, the first response of plants is stomatal closure to limit water loss through transpiration. Additionally, reduction of CO2 uptake and carbon assimilation whereas favoring photorespiration may occur in plants [80]. Upregulation of LeEPFL9 involved in the regulation of stomatal development together with greater stomatal density was found in tomato plants colonized by R. irregularis [10]. Inoculation of Septoglomus deserticola or S. constrictum sustained stomatal opening in host plants under drought conditions, substantially contributing to the carbon assimilation [11]. Improvement of stomatal conductance (gs) in mycorrhizal castor bean [78], black locust [72], and strawberry [81] plants exposed to water stress has been detected.
\nOne of the widely known benefits of mycorrhizal inoculation is the improvement of host water status under drought stress. Leaf water potential (LWP) and relative water content (RWC) of plants were substantially higher in the presence of mycorrhiza [11, 81]. Several studies illustrated a higher water use efficiency or intrinsic water use efficiency in AM plants during water stress [10, 81, 82]. It is believed that photosynthetic activity correlates with chlorophyll content and stomatal conductance, which have been enhanced by AMF. Drought stress changes photosynthetic pigments and damages chloroplasts. Nonetheless, AM inoculation alleviates the damage of these parameters caused by the stress [77]. Rhizophagus irregularis-colonized castor bean plants subjected to water restriction increased contents of chlorophyll a (by 26%), b (30%), carotenoid (by 28.5%), and total chlorophyll (25.5%) in comparison to counterparts of non-AM plants [78]. These increases in AM plants may be attributed to the improved nutrient uptake, particularly N and Mg that are structural components of chlorophyll.
\nMycorrhizal colonization has been found to alleviate the adverse impacts of drought stress on photochemical efficiency and photosystem II (PSII) reaction center [77, 83]. Under water deficit, application of AMF promoted a higher maximum quantum efficiency of PSII (Fv/Fm) [11], greater photosynthetic efficiency [84], transpiration rate, and net photosynthesis rate (PN) [10, 81]. Although mycorrhizal plants usually have higher photosynthetic capacities, environmental factors such as high atmospheric drought or low radiation can decide the beneficial effects of mycorrhiza on photosynthesis [85].
\nPhytohormones not only modulate a plethora of events during plant development but also are essential signaling molecules for interaction between plants and AMF [86]. Changes in plant hormone homeostasis also affect plant tolerance against abiotic stresses [87, 88]. During mycorrhization, changes in levels of several plant hormones have been reported [86], hence may contribute to the improved host plant tolerance to subsequent stresses.
\nAbscisic acid (ABA) is the most fundamental stress hormonal signal, modulating transpiration rate, root hydraulic conductivity, and aquaporin expression [89]. The concentration of ABA is heightened in plant tissues under drought stress to induce stomatal closure for reduction of water loss and activate different stress-responsive genes, increasing plant tolerance to drought [90]. A lower ABA concentration was found in roots and leaves of mycorrhizal plants versus nonmycorrhizal plants under drought stress [9, 10, 91]. Downregulation of SlNCED gene, a critical ABA biosynthetic gene, in Septoglomus constrictum-infected roots under water stress concurred with the greater gs and higher water status of tomato plants, indicating a higher stress tolerance in colonized plants compared to uninoculated plants [11]. Nonetheless, an increase in ABA concentration in trifoliate orange plants colonized by F. mosseae was also observed under drought stress [73]. The reason for this remains poorly understood, which requires further research.
\nThe role of jasmonate (JA) in water uptake and transport, exerting influence on stomatal conductance, root hydraulic conductance, and regulating the expression and abundance of aquaporins in tomato plants has been revealed [91]. Tomato plants defective in JA synthesis altered the AM impacts on the host plant, interfering phytohormones and expression of AM-induced aquaporin genes. The content of JA and its precursors was higher in leaves of Digitaria eriantha plants infected by Rhizophagus irregularis under water deficit, relative to noninfected plants, which could enhance plant tolerance to the stress [92]. Likewise, mycorrhizal inoculation substantially increased methyl jasmonate (MeJA) in trifoliate orange plants exposed to drought stress [93]. Under water-stress conditions, significantly higher expression levels of JA-biosynthetic gene SlLOXD in roots and leaves of colonized tomato plants were detected, supporting plant response to drought stress by triggering a LOXD-mediated pathway [10, 11].
\nStrigolactones (SLs), as phytohormones, not only modulate the coordinated development of plants exposed to nutrient shortages but are also host detection signals for AM establishment in the host plant [94]. Upregulation of the SL-biosynthesis gene SlCCD7 together with a greater content of SLs was found in Rhizophagus irregularis-inoculated tomato roots subjected to water-stress conditions, correlated with the increase in AM colonization rate [9]. The stimulated production of SLs promoting symbiosis establishment as a strategy of plants to cope with drought stress has been proposed.
\nAuxin is a key regulator in root-hair initiation, growth, and developmental processes [95, 96]. In a recent study, an increased content of indole-3-acetic acid (IAA) which is the dominant naturally occurring auxin was found in mycorrhizal tomato plants exposed to drought [91]. Similarly, stimulation of biosynthesis and transport of IAA in roots of trifoliate orange under water restrictions were demonstrated [97]. Under drought conditions, AM colonization overexpressed PtYUC3 and PtYUC8 involved in IAA biosynthesis, and downregulated auxin efflux carriers (PtPIN1 and PtPIN3), while up-regulated auxin-species influx carriers (PtABCB19 and PtLAX2) in roots, leading to significantly higher IAA accumulation in mycorrhizal roots versus non-AM roots [97]. Together with higher IAA, colonized trifoliate orange plants showed a significant increase in MeJA, nitric oxide, and calmodulin in roots, supporting greater root adaptation of morphology as a crucial strategy for drought adaptation [93].
\nAlthough important roles of phytohormones are irrefragable in plant responses to water stress, little attention has been paid to them in mycorrhizal plants. Previous studies have just revealed changes in concentrations and expression of genes encoding biosynthesis of few hormones in colonized plants during drought stress; thereby, further research is required to understand it.
\nIn response to drought stress, plants accumulate compatible solute compounds or osmolytes functioning for osmotic adjustment to maintain a favorable gradient for water uptake [98]. Osmotic adjustment is essential for water influx, turgor maintenance, sustaining physiological activity in plants such as stomatal opening, photosynthesis, cellular expansion, and growth during the stress [98]. Compatible solutes include a variety of sugars, proline, glycine betaine, polyamines, and organic acids such as oxalate and malate [99]. Interestingly, discrepant observations in osmolyte accumulation have been reported in a wide range of mycorrhizal plants [10, 83, 100, 101].
\nProline, an amino acid, plays a crucial role in osmoregulation and acts as an efficient scavenger of reactive oxygen species (ROS) [102] (discussed in Section 4.1.7). Enhanced drought tolerance with a higher proline concentration in mycorrhizal plants has been shown in many studies [10, 78, 100]; nevertheless, opposite results have also been reported [81, 83]. Inoculation of either F. mosseae or Paraglomus occultum in trifoliate orange plants substantially reduced leaf proline content but improved the host plant growth under water deficit [103]. These results suggest that AMF strongly altered leaf proline metabolism through regulating proline-metabolized enzymes, which is important for osmotic adjustment of the host plants.
\nSugars are osmoprotectants, which contribute up to 50% of osmotic potential in plants [104, 105]. In general, under water stress, the higher accumulation of total soluble sugars offers a defense mechanism in mycorrhizal plants such as watermelon [100] and flax [106]. Concentrations of sucrose, glucose, and fructose were significantly heightened in leaves of mycorrhizal trifoliate orange seedlings exposed to drought, which could function as osmolytes to stabilize and protect structures and macromolecules in plants from the stress, therefore improving host plant tolerance [103]. AMF-mediated increases in leaf sugar metabolism by modulating sugar-metabolized enzymes notably contribute to the osmotic adjustment of colonized plants. However, contrast observations have been shown in olive trees [101] and maize [107] colonized by AMF, which may be due to the fact that host plants suffer less stress. Noticeably, under severe drought inoculation with Rhizophagus clarus significantly reduced soluble sugars in leaves of strawberry plants, but this parameter was remarkably enhanced in roots in response to mild and severe water stress [81]. These changes together with an improved water status and plant biomass suggest different strategies for the enhanced water status triggered by AMF in roots and leaves of strawberry.
\nIn summary, increased accumulation of compatible solutes in AM-inoculated plants in exposure to water deficit is supposed to protect plants from the stress and curtail the plant osmotic potential, whereas the lower osmolyte accumulation in host plants is thought to be due to colonized plants successfully gaining drought mitigation.
\nOne of the consequences of water stress is the overproduction of reactive oxygen species (ROS) such as hydroxyl radicals (˙OH), superoxide radicals (O2˙–), singlet oxygen (1O2), and hydrogen peroxide (H2O2) mainly in chloroplasts and mitochondria. The excessive ROS results in unbalanced cellular homeostasis and then oxidative stress, damaging membrane lipids, proteins, and nucleic acids and even causing the death of cells [108]. To cope with oxidative stress, plants have evolved ROS scavengers in both nonenzymatic and enzymatic defense systems. Nonenzymatic antioxidants comprise phenolic compounds, glutathione, ascorbic acid, alkaloids, carotenoids, and tocopherol [109], which not only play a direct role in ROS removal but also serve as a substrate for the antioxidant enzymes in scavenging ROS [110]. Under water deficit, AMF ameliorate oxidative damage through augmented production of phenolic compounds and secondary metabolites detoxifying ROS in various plants [111, 112, 113]. AM inoculation also significantly increased the concentrations of anthocyanins and carotenoids [106] and ascorbic acid [82, 106] in plants in exposure to water constraints.
\nAnother important ROS scavenger system is enzymatic antioxidants which could be enhanced in mycorrhizal plants including superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), guaiacol peroxidase, ascorbate peroxidase (APX), glutathione reductase (GR), dehydroascorbate reductase (DHAR), and monodehydroascorbate reductase (MDHAR) [110]. The AM symbiosis has been reported to improve plant protection against oxidative stress by decreasing the level of lipid peroxidation (MDA) and H2O2 accumulation by strengthening significantly antioxidative enzymes SOD, POD, and CAT in roots and leaves under mild and severe drought [11, 81]. SOD and CAT are the most important ROS scavenging enzymes among the enzymatic antioxidants. These enzymes together with the cooperative enzymes (GR, MDHAR, DHAR, and APX) in the ascorbate-glutathione (ASA-GSH) cycle play pivotal roles in controlling overproduced ROS to maintain cellular homeostasis [114, 115, 116]. Remarkable increases in SOD, CAT, GR, APX, and MDHAR at transcription and enzymatic level correlated with lower O2˙−, H2O2, and MDA have been revealed in drought-stressed mycorrhizal plants versus counterparts of non-AM plants, improving host protection against oxidative damage [101].
\nHigher nonenzymatic and enzymatic antioxidants in colonized plants help for the rapid and efficient elimination of excess ROS. Nevertheless, discrepant results, no change or decrease in ROS scavengers, have also been demonstrated [70, 117]. Results are not entirely consistent with all reports because of different ages of host plants [118] and/or the specific combination of mycorrhizal strains and plant species, even cultivars [11] (as discussed in Section 3) or successful drought mitigation in colonized plants.
\nThe hyphal network of AMF is believed to improve soil water retention properties in the mycorrhizosphere through its physical, biological, and chemical influences. It has been reported that AMF produce polysaccharides, glomalin, mucilages, and hydrophobins that act to bind soil particles, leading to soil aggregation with enhanced water-holding capacity in soil [119]. Glomalin, a stable glycoprotein, highly persists in the soil, defined as glomalin-related soil protein (GRSP) [120]. The higher amounts of GRSP in the soil, the more enhanced capacity of water retention was found since soil aggregation increased protection of C-rich debris from the decomposition of soil microbes [120, 121]. Indeed, fungal hyphae coated by GRSP sharp a hydrophobic layer into the aggregate surface, hence decreasing water loss within soil aggregates [122]. When the fungal hyphae form branching structures with glomalin, they physically stick micro-aggregates with macro-aggregates [119]. The physical interaction of external hyphae on soil particles forms stable aggregates [123] in general and under water deficit [124]. Moreover, mycorrhizosphere also influences soil aggregation through alterations in the soil microbial food web, habitats for soil microbes, and biological activities in the host rhizosphere, which could result in an enhancement in microaggregate soil structure [125]. Thus, soils possess well-structured property in the presence of AMF, maintaining relatively higher available water than poorly structured soils without mycorrhizal presence under water stress [126]. Notably, in artificial substrates, an enhancement in water retention and water transport within substrates inoculated with AMF was observed under severe drought, suggesting that host plants perceive less stress at the root surface as reducing substrate moisture [127]. Hence, AMF postponed the physiological stress response in host plants.
\nIt is often found that AM symbiosis can improve plant growth in numerous plants, such as lettuce [9], tomato [9, 11], strawberry [81], maize [128], black locust [72], digitgrass (Digitaria eriantha), a source of forage [92], and damask rose [129]. The substantial improvement in the growth of mycorrhizal plants could be a result of a combination of AMF-induced mechanisms of plant tolerance under drought conditions, notably enhanced water and nutrient uptake in host plants [60, 117], and increased photosynthetic activity (as discussed in Section 4.1.3) since plant size closely links with measured physiological parameters [11]. It is important because nutrient supply may improve plant drought tolerance for better plant establishment. The increased plant biomass and nutrient uptake in AM plants could be more pronounced during seedling growth stages and in a longer stress duration. For instance, significant increases in shoot dry weight (by 128–242%) and root dry weight (185–328%) in French lavender (Lavandula dentata) plants treated by either single autochthonous AMF (Septoglomus contrictum, Diversispora aunantia, Archaespora trappei, Glomus versiforme, and Paraglomus occultum) or their mixture were recorded, compared to uninoculated plants after 6 months of growth under drought conditions [60].
\nBesides positive mycorrhizal effects on plant growth, discrepant observations have also been reported. Four tomato recombinant inbred lines (RIL 20, 40, 66 and 100) and one commercial cultivar inoculated with Rhizophagus irregularis showed variable results under water stress [37]. AM application remarkably increased shoot dry weight of RIL 40 and RIL 60 lines under drought conditions while no changes were recognized in plants colonized by other AMF. Similar results were found in soybean using single isolates of Septoglomus constrictum, Glomus sp., Glomus aggregatum, or their mixture [130]. Taken together, the benefits of AMF application under water deficit are dependent on the specific combination of plant genotypes and AM isolates.
\nAnother significant benefit of mycorrhizal inoculation is to increase crop yield in exposure to water constraints compared to nonmycorrhizal plants. An array of observations shows a significantly higher yield, importantly marketable yield in mycorrhizal plants subjected to water scarcity in maize [128], tomato [82], flax [131], cowpea [132], and damask rose [129]. Furthermore, AM symbiosis has shown to accelerate flowering and fruit development [133]. Interestingly, re-inoculation of AMF after transplanting seedlings in the field appears to be necessary to strengthen mycorrhizal benefits. This could be seen in the field investigation which with twice application of AMF considerably heightened the marketable fruit yield (by 51–71%) in plants subjected to 50% water supply regime in comparison with those with mycorrhizal inoculation once at sowing and uninoculated ones [82]. The beneficial effect of AMF application on relative water content and nutritional status in plants as well as enhanced shoot accumulation of photoassimilates through higher photosynthetic activity, and improved stress tolerance in the presence of drought could result in higher productivity in colonized plants. Also, fruits are often the main sink for P; therefore, enhanced P nutrient in host plants promotes higher fruit yield.
\nAs a result of physiological changes during mycorrhization, both transcriptional and metabolic changes occur in host plants influencing crop quality as well. AM symbiosis not only modulates gene expression in tomato fruit, through a systemic impact, but also changes the phenology of flowering and fruit ripening as well as in the amino acid profile [133]. Under water shortage, AMF treatment has been explored to improve quality attributes including antioxidant compounds, carotenoids and anthocyanins [82, 134], essential oils [135], and alteration in seed quality of flax [131], hence highlighting the potential of using AMF in crop production, producing industrial and oil plants.
\nMicrobial symbionts of plants such as AMF represent a huge, but an unrealized resource for improving yields, especially in the tropics [136]; however, lower benefits to plants than the potential of these microorganisms are often found. To predict real benefits as well as all potentials of the fungal inoculation, implementation of field trials before AMF application on a large scale is indispensable in order to choose suitable inoculum or appropriately tune the best AM combination for target crop production systems. Moreover, various environmental factors influence the success of AMF application into the field.
\nAnother critical issue is whether generic or tuned AM products should be utilized in sustainable crop production. One of the challenges of AMF inoculation under open field conditions is the native populations of AMF in soils, which are able to remarkably compete colonization niche with the introduced symbionts. Despite the fact that commercial AMF inoculants are usually advertised as compatible for a variety of host plants and field-cultivation conditions, the AM-induced benefits for crops are not always as expected [137]. The bridge between research and AM suppliers should be strengthened to recommend appropriate AM inocula for most benefits. Due to the specificity of AMF-host plant interaction as described in several places in the chapter, an attempt to exploit advantageous combinations is necessary. Fine-tuning commercial mycorrhizal products is vital to obtain optimum beneficial effects from mycorrhizal inoculation.
\nEven in some circumstances, the symbiotic effectiveness and adaptability of the indigenous fungi are more dominant than non-native ones [138, 139]; therefore, introduced AMF isolates could be less profitable than native ones [140]. Besides, there is an existence of functional diversity among different AMF species [36]. Remarkable differences in performance even among different geographical isolates belonging to the same mycorrhizal species have been described [141]. In such cases, isolation of indigenous mycorrhizal strains for inoculum production, then large-scale reintroduction of these native fungi in the field could be a feasible solution for a useful AMF application [142]. It is worth mentioning that selection of specific AM taxa for particular crops is the best approach to improve crop growth, and there is no ‘one-size-fits-all’ AMF [143]. In controlled environments, application of a single AMF is more effective than using a mixture of different AM taxa [143].
\nDuring the last decades, several molecular techniques have been used to characterize entire communities of mycorrhiza in soil [144, 145] and AMF inocula [146, 147, 148]. These techniques enable to monitor the introduced fungal symbiont both inside and outside the host during plant growth [149, 150]. Tracing the introduced AMF temporally and spatially could be implemented by high-throughput next-generation sequencing, which possibly verifies whether the introduced fungi favor substantial levels of colonization and explores how the inoculated AMF coexist and interact with the local community of AMF [136]. Advances in molecular techniques can further assist the adjustment or tuning of commercial inoculants to specific AMF combinations with host plants under crop production systems.
\nAnother major limitation of mycorrhizal inoculation in horticulture and agriculture is farmer’s awareness and acceptance and the relatively high cost of it. Furthermore, conventional breeding programs have overlooked plant characteristics facilitating mycorrhizal association, and plant breeders have selected varieties in favor of acquiring nutrients in high-input crop production systems without respect to the AMF role in soil nutrient management [151], resulting in the primary challenge to AMF application. Hence, modern breeding programs should consider AMF as an essential component of breeding traits in new cultivars, particularly those cultivated under environmental adversities such as drought stress in which AMF application has been proved to stimulate higher crop tolerance.
\nAM inoculation can offer multiple advantages to host plants in exposure to water scarcity, which could enable inoculated plants to avoid drought stress or tolerate water deficit better than nonmycorrhizal plants. Indeed, various direct and indirect AM-induced mechanisms in mycorrhizal plants could contribute to drought mitigation or tolerance. More importantly, improved crop yield and quality attribute in colonized plants under drought stress highlight the importance of AMF application in crop production as one of the promising practices under water constraints. However, variable plant responses to AMF and the discussed major challenges hinder possible fruitful outcomes of AM inoculation. Identification of the most appropriate combination of fungal inoculants and a given variety, cultivar, or accession grown under water scarcity, and understanding environmental factors deciding the positive results of the inoculation are crucial determinants for successful AMF application. Compatible combination of AMF with other beneficial microbes such as plant growth-promoting bacteria and/or Trichoderma offering synergistic effects on plant tolerance to stressful environments including drought stress is also a bright perspective [38, 106]. Besides that, further research is necessary to shed light on the specific functions of genes mediated by mycorrhiza, which could explore the exact AM-triggered mechanisms of plant adaptation under water deficit. Studies on quantitative trait loci (QTL) involved in mycorrhizal plant responses to drought stress are needed for breeding programs to create new cultivars with a combination of drought-tolerant traits and AM benefits.
\nThis work was supported by 1783-3/2018/FEKUTSTRAT Program awarded by the Ministry of Human Capacities and by the National Research Development and Innovation Office (2017-1.3.1-VKE-2017-00022).
\nWe declare that we do not have any conflict of interest.
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