Next Article in Journal
Genetic Characterization of an Endangered Chilean Endemic Species, Prosopis burkartii Muñoz, Reveals its Hybrids Parentage
Next Article in Special Issue
Comparison of Biostimulant Treatments in Acmella oleracea Cultivation for Alkylamides Production
Previous Article in Journal
Allelopathic Effects of Bidens pilosa L. var. radiata Sch. Bip. on the Tuber Sprouting and Seedling Growth of Cyperus rotundus L.
Previous Article in Special Issue
Foliar Application of an Amino Acid-Enriched Urea Fertilizer on ‘Greco’ Grapevines at Full Veraison Increases Berry Yeast-Assimilable Nitrogen Content
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 9
Issue 6
10.3390/plants9060743
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Role of Microbial Inoculants on Plant Protection, Growth Stimulation, and Crop Productivity of the Olive Tree (Olea europea L.)

by
Georgios Bizos
1,
Efimia M. Papatheodorou
2,*,
Theocharis Chatzistathis
3,
Nikoletta Ntalli
4,
Vassilis G. Aschonitis
3 and
Nikolaos Monokrousos
1,*
1
Laboratory of Molecular Ecology, International Hellenic University, 57001 Thessaloniki, Greece
2
Department of Ecology, School of Biology, Aristotle University, 54124 Thessaloniki, Greece
3
Institute of Soil and Water Resources, Hellenic Agricultural Organization-Demeter, 57001 Thessaloniki, Greece
4
Department of Pesticides Control and Phytopharmacy, Benaki Phytopathological Institute, 8 S. Delta Str., 14561 Athens, Greece
*
Authors to whom correspondence should be addressed.
Plants 2020, 9(6), 743; https://doi.org/10.3390/plants9060743
Submission received: 6 May 2020 / Revised: 9 June 2020 / Accepted: 10 June 2020 / Published: 12 June 2020
(This article belongs to the Special Issue Biostimulants in Plants Science)
Browse Figure
Versions Notes

Abstract

:
The olive tree (Olea europaea L.) is an emblematic, long-living fruit tree species of profound economic and environmental importance. This study is a literature review of articles published during the last 10 years about the role of beneficial microbes [Arbuscular Mycorrhizal Fungi (AMF), Plant Growth Promoting Rhizobacteria (PGPR), Plant Growth Promoting Fungi (PGPF), and Endophytes] on olive tree plant growth and productivity, pathogen control, and alleviation from abiotic stress. The majority of the studies examined the AMF effect using mostly Rhizophagus irregularis and Glomus mosseae species. These AMF species stimulate the root growth improving the resistance of olive plants to environmental and transplantation stresses. Among the PGPR, the nitrogen-fixing bacteria Azospirillum sp. and potassium- and phosphorous-solubilizing Bacillus sp. species were studied extensively. These PGPR species were combined with proper cultural practices and improved considerably olive plant’s growth. The endophytic bacterial species Pseudomonas fluorescens and Bacillus sp., as well as the fungal species Trichoderma sp. were identified as the most effective biocontrol agents against olive tree diseases (e.g., Verticillium wilt, root rot, and anthracnose).

Graphical Abstract

1. Introduction

The olive tree (Olea europaea L.) is one of the most ancient cultivated crop species and the only one of the Oleaceae family that produces edible fruits [1]. It is an emblematic, long-living woody plant [2,3] of profound economic, societal, and environmental significance [4]. It is extensively cultivated in Mediterranean environments, and in several subtropical regions of South America, Australia, and Southern Africa. Currently, there is a worldwide increase in olive production due to the resilience of olive trees to climate change, and the growing demand for table olives and oil [5]. This demand is mostly generated by its tremendous nutritional value [6,7].
The olive plant can grow in very diverse environments [8] of soil pH (5.5–8.5) [1] and humidity, from arid to semi-arid regions [4] due to its high tolerance and high adaptability to poor soils, drought [9], salinity, and excess of boron and chlorine [1]. The enhancement of soil fertility and the fulfillment of its water requirements are crucial factors to attain high productivity [10]. The olive tree is widely known for its strong tendency for alternate bearing, with higher yields being produced every second year. Low soil fertility and many abiotic stresses, such as high temperatures and drought enhance this tendency [11]. Several abiotic stresses, especially water stress, are strongly related to the transplantation shock that occurs when olive cuttings or seedlings are transplanted in the field decreasing their survival rate [12]; this failure of the young olive plants to root well forces them to expend additional energetic cost in order to adapt to the new environmental conditions [13]. Meddad-Hamza et al. [14] showed that when young olive plants, with low root to shoot ratio, were transplanted into natural soil conditions without fertilizers, there was an abrupt decrease of the mineral uptake by the plant, causing stunted growth and increased plant mortality. Furthermore, the intensification in agricultural practices of olive cultivation, like the establishment of orchards with high tree densities for increasing olive production (in countries such as Spain, Italy, or Greece) caused the increase in both incidence and severity of olive pests and soil-borne diseases [1]. Verticillium dahliae and other soil borne pathogenic fungi like Fusarium oxysporum, F. solani, Rhizoctonia solani, and Pythium sp. are responsible for root rot and wilt diseases, with the wilting disease caused by Verticillium dahliae being the most severe disease of olive trees worldwide [15]. Olive knot disease caused by the Gram-negative bacterium Pseudomonas savastanoi pv. savastanoi is another common and important disease that infects the aerial parts of olive plant and causes severe damage and extensive production losses [16]. Similar implications may also occur due to Anthracnose disease, caused by the pathogenic fungi Colletotrichum acutatum and Colletotrichum gloeosporioides. It infects several parts of the olive tree such as flowers, leaves, shoots and fruits leading to severe yield losses. It also affects oil quality by increasing oil’s free acidity and peroxide level and deteriorates its organoleptic properties [17].
For these reasons, every year a large portion of the farmers’ revenue is spent on agrochemicals to promote olive trees’ growth, to control plant pathogens, and to increase the nutritional value and quality of the olive products. The public concern on the use of agrochemicals (i.e., chemically-based fertilizers, fungicides, insecticides, etc.) has increased in recent years, due to the negative effects on the environment (e.g., soil and groundwater pollution), the ecosystem’s biodiversity, and human and animal health [18,19]. The widespread use of fungicides or bactericides can lead to resistance increase of pathogenic fungi and bacteria to these chemicals and to the decrease of their efficacy, which in turn leads to their increasing use in order to maintain the same level of protection [20].
Consequently, several researchers have focused their efforts on the development of alternative, eco-friendly practices aiming to increase olive crop yield, to control biotic threats, and to ameliorate olive tree’s health [18]. An essential aspect of sustainable agricultural management is the development and implementation of eco-friendly methods and strategies that promote a soil’s biological processes, decrease agricultural inputs [21], and improve soil structure and fertility [22]. Towards this aim, microorganisms of plant’s rhizosphere could play a crucial role in plant health and growth [23]. Such microorganisms are the Arbuscular Mycorrhizal Fungi (AMF), the Plant Growth Promoting Rhizobacteria (PGPR), the Plant Growth Promoting Fungi (PGPF), and the Endophytes. The olive plant forms a strong relationship with these beneficial soil microbes, which enables the plant to grow not only in limiting nutrient soils but also under various abiotic stresses, such as water scarcity [6,9].
The objective of this study is to provide a review based on a literature survey of articles published during the last 10 years about the role of beneficial microorganisms (AMF, PGPR, PGPF, and Endophytes) as microbial inoculants on olive trees for supporting their growth, for their alleviation from abiotic and transplantation stresses and for the biological control of olive plant diseases.

2. Categorization of Studies

The search of the relevant literature published during the last 10 years (2009–March 2020) was conducted using reliable scientific databases of peer-reviewed, academic literature such as Scopus, Web of Science, and Google scholar. Overall, 67 research papers were identified that studied the effect of microbial inoculants on the olive tree’s growth and nutrition, quality of olive products, several types of abiotic stress, and olive plant diseases (Table S1). The keywords used in our search were: (“Arbuscular Mycorrhizal Fungi” or “AM fungi” or “AMF” or “Plant Growth Promoting Rhizobacteria” or “Promoting Rhizobacteria” or “PGPR” or “Plant Growth Promoting Fungi” or “Promoting Fungi” or “PGPF” or “Endophytes” or “endophytic microorganisms”) and (“olive” or “Olea europaea”) and (“growth” or “productivity” or “nutrition” or “water stress” or “drought” or “transplantation stress” or “salinity” or “saline stress” or “toxicity” or “biocontrol”). The results of our search were used to create our manuscript’s tables illustrating which microbial inoculants were used in olive tree studies over the last 10 years.
AMF and PGPR were the main subject of study (28 and 17 studies, respectively), followed by endophytes (nine), PGPF (six), and co-inoculants (seven). Furthermore, 27 studies examined the effect of microbial inoculants on biocontrol efficacy (biotic stress), 22 on olive tree growth, physiology, and crop productivity, 15 studies on the alleviation from abiotic stresses, and three on the alleviation from transplantation stress. The majority of the research studies were conducted in countries located in the Mediterranean basin (57), while the rest were conducted in South America (10). In North African countries such as Tunisia, Egypt, Morocco, and Algeria, where dry and calcareous soils are prevalent, 12, nine, six, and three studies were identified, respectively. These studies were mainly focused on increasing olive tree’s productivity in these types of soils. On the contrary, in the southern European countries such as Spain, Italy, and Greece (18, three, and two studies, respectively), as well as in Turkey (two studies), where olive cultivation is intensified, the studies mainly focused on the use of microbial inoculants as biocontrol agents against olive tree diseases.

3. Beneficial Microorganisms and Olive Tree’s Growth, Physiology, and Productivity

Most of the experimental studies focused on the beneficial role of AMF inoculation alone or with other microbes on olive trees’ growth, physiology, and productivity (Table 1). In these experiments, the Glomus species, and especially Rhizophagus irregularis, were the most frequently studied. In the mutual symbiosis with young olive plants, Glomus sp., Glomus mosseae, and Glomus clarum favored the augmentation of shoot and root biomass [6,24,25,26]. Similar observations were also made for Gigaspora rosea and Scutelospora scrobiculata [25]. Glomus sp. favored mineral nutrition and G. Mosseae activated olive plant’s defense system, by inducing the exchange of photosynthates and favoring the increase of phenol content [6,24]. According to Seifi et al. [6], the leaf chlorophyll content was higher when the olive plantlets were inoculated with G. mosseae or R. irregularis. Chenchouni et al. [26] demonstrated that a local AMF strain of Glomus sp. and a commercial strain of R. irregularis were the most effective ones on olive plantlet’s growth traits, in comparison to Funneliformis mosseae, Septoglomus constrictum, and Gigaspora margarita.
R. irregularis showed a higher percentage of root colonization compared to other species and it was more effective than Glomus sp. in promoting the young olive plant’s biomass [6,24,26]. It improved the nutritional status of olive plant, by influencing the increase of carbohydrate contents in the root, and by enhancing of P, K, Ca, Mg, Mn, Fe, and Zn uptake [27,28]. Sugar analysis of the olive roots showed that fructose and sucrose content was higher in the inoculated plants with R. irregularis, while glucose content was not affected [28,29]. The increased content of phenols and flavonoids in young olive plant roots is immensely significant in the plant-microbe symbiosis and they act as antimicrobial and antifungal plant defense agents [6,29]. The increased sink strength of mycorrhizal roots leads to enhanced translocation of sugars from source to leaves, which enables higher photosynthetic rates [28].
The effectiveness of an AMF species is even greater when it is co-inoculated with another AMF species. The co-inoculation of R. irregularis and Glomus sp. was more effective than Glomus sp. alone in promoting the increase in olive’s shoot biomass [24]. R. irregularis in combination with G. mosseae favors the increase of young olive plant height, root, and shoot biomass and improves P and K content [30]. Additionally, Chatzistathis et al. [31] found that AMF species (Glomus sp. and Gigaspora sp.) increased young olive plant growth and nutrient uptake in three olive genotypes. Furthermore, a mycorrhizal consortium of Glomus, Acaulospora, Gigaspora, Entrophospora, and Scutellospora species, increased the Na, Ca, and P concentrations in nutrient contents of ‘Haouzia’ olive cultivars under sandy loam soil conditions [32] and it was responsible for young olive plant-growth enhancement [12,32,33].
As regards PGPR inoculation studies, Bacillus, Azospirillum, and Pseudomonas, were the most commonly used genera (Table 1). Abd-Alhamid et al. [22] reported that the reduced application of nitrogen fertilization (75%) in combination with three bacteria species (Azotobacter chrococcum, B. megaterium, and B. circulans) increased the yield and several fruit physical parameters (e.g., weight, volume, length and diameter, fruit oil content, oil quality, and total microbial count) in comparison to the standard orchard practice. Haggag and Merwad [34] showed that the reduction of the recommended dose of mineral fertilization (N, P, K) by 50%, combined with three biofertilizer products, containing Azospirillum sp., Bacillus mucilaginosus, and Bacillus megatherium, increased the young plant’s root system. The bacterial strains Pseudomonas fluorescent P19 or P21 [35] Chryseobacterium sp. AG13, Chryseobacterium sp. CT348, Pseudomonas sp. CT364 and Azospirillum brasilense Cd [36,37] promoted root induction and formation to a similar or greater extent than the control plants treated with indole-3-butyric acid, due to their ability to synthesize at low rates and secrete continually indole-3-acetic acid (IAA) [35,36].
Ramasamy et al. [38] stated that PGPR and AMF co-inoculation can be more beneficial for plant growth and nutrient uptake than a single inoculation, probably because PGPR can enhance the AMF establishment, by stimulating the hyphal growth through the production of vitamins and enzymes or by increasing the permeability of root epidermis cell wall [39]. The reduction of the recommended dose of mineral fertilization (N, P, K) by 50% to 70% , combined with a mixed inoculant containing PGPR (Azotobacter chroococcum, Azospirillum brasilense, Bacillus megaterium var. phosphaticum, Bacillus cereus, Pseudomonas sp.) and AMF strains (G. mosseae NRC31 Glomus fasciculatum NRC15) stimulated plant growth and enhanced the nutritional status of the olive seedlings [10]. Costa and Melloni [40] also showed that the co-inoculation of PGPR (Pseudomonas sp. and Paenibacillus sp.) with AMF species (Acaulospora scrobiculata, Gigaspora rosea, and Rhizophagus clarus) could effectively promote the nutritional status and growth of young olive plants. Furthermore, Shaheen and Taweel [21] showed that the reduction of the standard dose of mineral fertilization by 50% in combination with Bacillus polymyxa and fungus yeast Saccharomyces cerevicisiae foliar co-inoculation, increased significantly olive fruit length, weight, and width. The foliar application of S. cerevicisiae combined with AMF root colonization, also showed higher values of leaf N, K, Fe, and Mn content and higher values of auxin and gibberellin contents in these treatments, compared to un-inoculated control plants [41].
The aforementioned studies showed that the use of inoculants with multiple AMF species was more efficient for promoting plant biomass and productivity than individual species’ use. In the case of PGPR and AMF, their effects were examined in cases where inorganic fertilizers were also applied, but further studies without fertilizers were recommended by the authors in order to test whether they are also effective in nutrient-limited soils.

4. Beneficial Microbes and a Plant’s Response to Abiotic and Transplantation Stress

Inoculation with AMF species was also the focus of studies that investigated plant alleviation from abiotic and transplantation stresses. Once again, the most frequently beneficial AMF species used, under abiotic and transplantation stress, were Glomus sp. and R. irregularis (Table 2). Glomus claroideum and G. mosseae reduced the detrimental effects of salinity and strengthened the young olive plant’s capacity to resist water stress [14,42]. G. mosseae favored K acquisition by plants, which plays a major role in regulating the osmotic processes reducing significantly the saline stress [42]. It stimulated more the root growth than the shoot growth, where the higher root/shoot ratio causes better hydro-mineral nutrition, reinforcing the capacity of the young olive plants to resist not only water stress [41] but also transplantation stress [43]. R. irregularis was superior to G. mosseae in terms of root colonization on young olive plant roots under saline stressed conditions [44]. R. irregularis favors K uptake by the plants and reduces the effects of saline stress but not to the same extent as G. mosseae [42]. In addition, the co-inoculation with two R. irregularis strains (GC2 and GA5) also protected the olive plant from saline stress by decreasing the malondialdehyde content and by activating the antioxidant defenses of the plant [13,45]. M’barki et al. [46] showed clearly that chlorophyll and carotenoid contents (essential for photosynthesis) were significantly enhanced when the roots were colonized by R. irregularis. The higher level of root colonization by R. irregularis leads to the creation of an ample hyphal network in the rhizosphere, thus establishing better transport of nutrients to the plant [14]. R. irregularis favored root development when olive plantlets were grown in phosphorus poor soils, while in P rich soils, the inoculation with AMF resulted in reduced shoot growth compared to untreated control plants [47]. The olive plant has low phosphorus requirements and the excess of P can have adverse effects, such as a reduction of shoot growth and a possible reduction of AMF colonization [47].
In soils with high levels of gypsum, the mycelial hyphae of R. irregularis mitigated the ascent of the toxic gypsum sulfate ions from the roots to the shoots [48]. Furthermore, Briccoli Bati et al. [49] demonstrated that a microbial inoculant containing AMF species (Glomus sp., Scutellospora heterogama, Paraglomus laccatum, and Diversispora celata) instigated a protective effect against heavy metal toxicity caused by high soil Mn concentration. The major part of Mn was retained in the fungal and spore cell walls, bound to components such as chitin, cellulose, and cellulose derivatives.
The extra-radical hyphae created by the inoculation with six different Glomus species (G. etunicatum, G. microaggregatum, G. geosporum, G. claroideum, G mosseae, and R. irregularis) favored the ability of the root to expand in a larger volume of soil and to regulate stomatal conductance and root hydraulic conductivity, thus improving the gas exchanges and water relation status of the young olive plants [4,50]. Ouledali et al. [4] suggested that stomata closure in inoculated olive plants may be mediated by a putative mycorrhiza-dependent metabolite replacing the phytohormone abscisic acid, which controls stomatal opening. This metabolite may be produced by the fungus itself or by the plant. The accumulation of this metabolite is a result of the AM fungal symbiosis [4] and supports plants’ growth under drought conditions.
PGPRs can also be used in the alleviation of abiotic stresses, such as increased soil calcicity, which is frequently encountered in the Mediterranean region [19], and they can operate optimally in a wide spectrum of temperatures and soil pH [51]. The bacterial strains Azospirillum brasilense BR11001t, Azospirillum amazonense BR11040t, Herbaspirillum seropedicae BR11175t, and Burkholderia brasilensis BR11340t favored root induction in a wide range of pH (5–9) and temperature (15–35 °C) conditions [51]. The application of Bacillus megatherium along with antioxidants (e.g., ascorbic and citric acid) improved olive yield, fruit weight, and flesh oil content in calcareous soils. This was attributed to B. megatherium’s phosphate solubility and the antioxidant auxinic action that improved the P level of the olive plants [52]. The inoculation with Azotobacter chroococcum had a similar effect on the olive plant in calcareous soils, where the bacteria improved biomass production through the production of phytohormones and enhanced transfer of essential nutrients like N, P, and K from soil to plant [19].
El-Shazly and Ghieth [53] demonstrated that the interaction of PGPR (Azotobacter chroococcum) and AMF (Glomus macrocarbium), combined with the application of humic acid, reduced the negative impact of salinity. The combined treatment showed higher values of total microbial counts, bacterial densities, AMF infection percentage, and soil enzymatic activity. The study suggested that the production of phytohormones such as IAA, gibberellins, cytokinins and ethylene, nitrogen fixation, phosphates, and nutrient solubilization was the cause for these increases.
The majority of the aforementioned studies, examined the ability of the microbial inoculants to support the growth of olive plants in abiotically stressed environments (e.g., in saline soils, in calcareous soils, in soils with an excess of heavy metals or in drought conditions). In most cases, the studies investigated the combined inoculation of AMF and PGPR strains, applied either alone or together with other constituents, such as antioxidants or humid acids.

5. Beneficial Microorganisms Against Pathogens

Over the last decade, PGPR (10 studies), endophytes (nine), and PGPF (six) have been the center of attention for their biocontrol potential against major olive plant diseases, whereas only two studies with AMF were conducted for this purpose (Table 3). Many strains of Bacillus and Pseudomonas have been used in agriculture as biocontrol agents against several diseases caused either by fungi or bacteria [54]. Sanei [55] reported that eight isolates of Pseudomonas fluorescens inhibited Verticillium’s microsclerotia germination. The long-term endurance of microsclerotia and the fact that they cause the initial infections, make them direct targets of biocontrol of Verticillium dahliae [15,55]. Furthermore, Markakis et al. [56] showed that the application of Paenibacillus alvei K165 was also associated with the reduction of microsclerotia germination. The application of this bacterial strain in ‘Kalamon’ cultivar (highly tolerant to V. dahliae) was very effective against Verticillium wilt. Gómez-Lama Cabanás et al. [23] reported that three Pseudomonas strains (PIC25, PIC105, and PICF141) and three novel bacteria strains Paenibacillus polymyxa, Paenibacillus terrae, and Bacillus sp. PIC28 [15] demonstrated effectiveness against the highly virulent V. dahliae isolate (D pathotype), with the strain PICF141 being the most effective. Their biocontrol abilities rely on the production of cell wall-degrading enzymes (protease, cellulase, phytase amylase, etc.), siderophores, indole acetic acid, and ammonia [23].
Strains of Bacillus subtilis were very effective against Verticillium wilt, root rot, olive knot, and anthracnose [17,54,57]. B. subtilis Y1336 strain significantly reduced the disease incidence of V. dahliae and other soil-borne diseases like Fusarium oxysporum, Fusarium solani, Rhizoctonia solani, and Pythium sp. [57]. B. subtilis 2515-1 strain decreased the tumors in olive’s stems caused by Pseudomonas savastanoi pv. Savastanoi 2064-8 strain [54]. B. subtilis QST 713 strain significantly reduced the percentage of latent infections of anthracnose on olive fruits, caused by Colletotrichum acutatum and Colletotrichum gloeosporioides [17]. The effectiveness of these strains relies on the ability of Bacillus species to promote growth by increasing nutrient availability [57] and on their high, antibacterial specificity with Pseudomonas savastanoi pv. savastanoi strains [54]. They can also be used as an alternative to chemical or other Cu-based products that are mainly used to treat the symptoms of anthracnose [17].
Co-inoculation with bacterial strains Azotobacter sp. AZM1, Bacillus cereus BCM8, B. megaterium BMM5, and B. subtilis BSM1 had positive results against F. oxysporum, F. solani, and R. solani in olive transplants [58], suggesting that such consortiums should be further investigated in the future. Root rot caused by Fusarium solani and oxysporum can be greatly reduced by Bacillus licheniformis and Enterobacter colcae in combination with carbendazim (fungicide), suggesting that this can be an alternative method to the use of synthetic fungicide alone, reducing the risk of the occurrence of fungicide resistance and its harmful impact to the environment [59].
The endophytic Pseudomonas fluorescens PICF7 strain was the most frequently used microorganism as biocontrol agent in olive trees (Table 3). P. fluorescens PICF7 can penetrate (through root hairs) and colonize olive root tissues and trigger a wide array of defense responses, both local (roots) and systemic (aerial tissues), which explain its biocontrol effectiveness against diseases such as Verticillium wilt [2,60,61]. The effective application of this endophyte requires its presence in both the surface and the interior of olive roots before colonization by V. dahliae and eventually its direct contact with the pathogen [62,63]. Apart from P. fluorescens PICF7, another Pseudomonas strain that is highly competent in colonizing the rhizosphere and able to suppress the deleterious effects of Verticillium wilt is the Pseudomonas putida PICP2 strain [2]. In the case of anthracnose, which affects the flowers and the fruits of the olive plant, a spray application at the blooming stage of three endophytic isolates of yeast-like fungus Aureobasidium pullulans (well adapted in the phyllosphere), significantly reduced the percentage of latent infections of the disease compared to the untreated control [17]. These researchers suggested that the endophyte should be applied at the blooming stage because it can colonize living plant tissues and produce antifungal and antibacterial compounds.
Furthermore, two very promising candidates with biocontrol abilities are the endophytic Bacillus strains, B. licheniformis LMRE 36 [64] and B. velezensis OEE1 [65]. Bacillus licheniformis LMRE 36 strain inhibited Fusarium solani strains Fso6 and Fso7 progression up to 75% compared to the untreated plants suggesting that secondary metabolites from Bacillus strongly interfere with fungal pathogens [64]. B. velezensis OEE1 strain was more effective in reducing the disease severity of Fusarium Solani compared to commercial fungicides [65]. These beneficial effects could be explained by phosphate solubilization, nitrogen fixation, and IAA production that are attributed to B. velezensis OEE1 endophytic lifestyle.
Trichoderma harzianum Ths97 strain was very effective against Fusarium solani strain Fso14, which is responsible for the root rot in olive plants [5]. T. harzianum produces antibiotics and hydrolytic enzymes that are usually regulated by jasmonic acid and ethylene dependent signaling pathway that triggers a variety of plant defense responses [5]. Trichoderma asperellum Bt3 and T25 strains delayed the disease outbreak and decreased the total severity of Verticillium wilt [66]. These researchers advocated that the successful root colonization by the Trichoderma strain is a major requirement for plant defense system. The difference of the root colonization was also influenced by the application method since T. harzianum CECT 2413 strain was unable to colonize the olive roots of ‘Picual’ cultivar when it was applied as (pregerminated) conidia suspensions [66,67]. Conidia can be highly sensitive to soil fungistasis and have a slow survival rate, especially under natural conditions. These limitations can be overcome by the use of cornmeal sand mixture soil medium [68]. Trichoderma species can be very effective when they are combined with field applications, such as solarization, as this combination decreased the microsclerotia of Verticillium [69].
Boutaj et al. [70] reported that Glomus irregulare was very effective at reducing the disease symptoms caused by Verticillium wilt. These authors suggested that the induction of systemic resistance caused by the accumulation of phenolic compounds and flavonoids in the roots is the main mechanism of disease. Co-inoculation with Lactobacillus plantarum, Lactobacillus casei, Rhodobacter sphaeroides, Rhodopseudomonas palustris, Saccharomyces sp., Streptococcus lactis, and Streptomyces sp. in combination with solid οlive oil waste compost (with urea as nitrogen source) was effective against the highly virulent V. dahliae isolate V024 and reduced the disease incidence to 80% [71]. Moreover, a co-inoculation of T. harzianum Rifai strain KRL-AG2 with several AM fungi (R. irregularis, G. aggregatum, G. mosseae, G. clarum, G. monosporus, G. deserticola, G. brasilianum, G. etunicatum, and G. margarita) also significantly decreased the Verticillium wilt severity in a field experiment [72]. Lastly, Mulero-Aparicio et al. [73] showed that Fusarium oxysporum FO12 strain significantly reduced significantly the disease incidence in young olive plants and adult trees.
Based on the aforementioned studies, several mechanisms were reported as crucial ones for the control of pathogens, especially for Verticillium wilt, which was the most studied disease in olive trees. PGPR acted mostly by inhibiting Verticillium’s microsclerotia germination, or by producing cell wall-degrading enzymes. AMF induced the accumulation of phenolic compounds and flavonoids in roots, making the plants less vulnerable to diseases, while endophytes induced plant defense mechanisms mainly related to phosphate solubilization, nitrogen fixation, and/or IAA production.

6. Inoculum-Cultivar Specificity

There is a strong interaction between the effectiveness of a microbial inoculant and the olive cultivar. The AMF genera may differently affect olive cultivars, growing under the same soil conditions, in terms of vegetative growth and nutritional status since mycorrhiza affect the root system morphology [31]. Gigaspora sp. colonized the root system of ‘Chondrolia Chalkidikis’, ‘Koroneiki’, and ‘Kothreiki’, while Glomus sp. colonized only the root system of ‘Koroneiki’ [31]. ‘Chemlaly’, ‘Quartina’, and ‘Coronaki’ olive cultivars showed different responses to vegetative growth and leaf nutrient content when they were inoculated by the same fungi [41]. In this context, ‘Koroneiki’ demonstrated higher AMF colonization rate compared to ‘Valanolia’, which led to higher growth attributes in ‘Koroneiki’ (higher height and a higher number of lateral shoots and leaves, as well as higher oil phenol content); in contrast, ‘Valanolia’ showed higher leaf area [6]. The intensity of colonization depends on the cultivar and inoculum [49]. Glomus clarum, Gigaspora rosea, and Scutelospora scrobiculata stimulated plant growth in ‘Arbequina’ and ‘Grappolo’ cultivars, whereas ‘Maria da Fé’ variety had low mycorrhizal dependency [25]. The same bacterial strains induced rooting in ‘Hojiblanca’ but not in ‘Arbequina’ and ‘Picual’ [36]. The same combined treatment (PGPR and AMF) applied on ‘Arbequina’ and ‘Maria da Fé’ cultivars promoted high growth (height and diameter), fresh root, and shoot dry matter production in ‘Arbequina’ and improvement of nutritional status (higher nitrogen contents in the shoot) in ‘Maria da Fé’ [40]. Boutaj et al. [32], who investigated the inoculation of the olive cultivar ‘Picholine Marocaine’ with an autochthonous mycorrhizal inoculum, and with the commercial pure strain Glomus irregulare, found that root colonization and mycorrhizal frequency and intensity were greatly improved in both the autochthonous consortium (100% and 58.91%, respectively) and Glomus irregulare (97.77% and 57.77%, respectively) compared to the control plants.
From all the above quoted information, it is clear that the inoculum-olive cultivar specificity plays a crucial role not only on boosting plant growth, modifying root morphology, and enhancing plant nutrition, but also on improving the qualitative characteristics of olive products (e.g., high polyphenol olive oil). Thus, more emphasis should be given in the near future on the optimum interaction among soil and cultivation management techniques (which influence soil microbiology and AMF abundance) and choice of suitable genotype(s) (showing high qualitative characteristics) to maximize the benefits for the consumers’ health. Furthermore, because of the idiosyncratic interactions between olive cultivar and AMF, PGPR, or endophytes’ species, it is suggested to use a mixed inoculum, where various microbial species/strains of the above categories could be applied simultaneously. In that case, the cultivar has the chance to interact with the most successful microbial species to overcome difficulties in growth.

7. Microbial Inoculation under Nursery and Field Conditions

The microbial inoculation in the nurseries before their transplantation into the field is a beneficial strategy for olive plant growth promoting its resistance against biotic and abiotic stresses [12,42]. Growing young plants in nurseries, and applying the experimental inoculants under totally controlled soil conditions offers a great advantage in terms of root colonization. This literature review showed that most of the AMF experiments were conducted in nurseries under either unstressed or stressed conditions. An early mycorrhizal inoculation of olive seedlings during nursery propagation can be extremely beneficial for the early plant establishment and crop productivity, as commercial yields would be reached earlier [6,29,30]. Jiménez-Moreno et al. [47] showed that it is much more advantageous to apply the AMF inoculum in the nursery than directly in the cultivation field, due to the increased root volume of the plant before transplantation. The benefit of AMF inoculation at the early plant stages can be effective for a long time (in most cases at least four years after transplantation, expressed with a high commercial yield) [44]. Furthermore, AMF inoculation in the nursery can reduce the harmful effect of Verticillium wilt and can produce more vigorous plants with enhanced resistance against the pathogen [70]. This is associated to the competition for space on plants’ roots between the pathogen and the AMF; the AMF occupy the root surface area, and do not allow the pathogen to infest it, thus reducing the occurrence of the symptoms caused by the soil-borne pathogens in the field.
The effect of biocontrol agents against olive plant diseases has rarely been investigated under field conditions. The application of microbial biocontrol agents against olive plant pathogens, at the propagation stage (greenhouse or nursery) is once again the most recommended approach, not only because it is an effective, preventive strategy (by transferring into the field the plants with the defense mechanisms ‘activated’ and/or harboring a cohort of effective antagonists), but also because the use of biological control agents under these conditions is easier, cheaper, and less time-consuming than large-scale field treatments [15]. Hibar et al. [57] suggested that an earlier treatment (in the nursery) with biofungicide can significantly reduce the occurrence of symptoms caused by soil borne-pathogens in the field.
Some studies tried to emulate in the nursery the field conditions by using various soil mediums, with the cornmeal sand mixture medium resulting to be the best [67,68]. Even though this approach was characterized successful in terms of emulating the soil conditions, the researchers acknowledged that the natural field conditions were difficult to be replicated as the infestation speed differed considerably.

8. Future Perspectives

In order to evaluate thoroughly the efficacy of a biological control agent, more field experiments should be conducted, which is the last stage of a BCA’s efficacy assessment, because the pathogenic inoculum density usually recorded in the field is very difficult to be replicated in a controlled nursery experiment. Moreover, more studies should be conducted assessing the biocontrol efficacy of AMF against olive plant diseases, as well as to examine the effectiveness of biocontrol agents that combine AMF species with other microbial inoculants, such endophytes, against olive plant diseases that infect the aerial part of the plant. Nevertheless, the most important challenge would be the assessment of the microbial inoculants’ influence on the phenolic content of olive products, which is among the most important qualitative characteristics of extra virgin olive oil. Finally, our search showed that several combined AMF, PGPR, or endophyte inoculant consortia showed promising results and they should be considered for further production by the biofertilizer industry.

9. Conclusions

Based on the literature review of the last 10 years, it was observed that the majority of the studies in Olea europaea L. focused on AMF inoculation, due to its high ability to stimulate olive plant’s growth and nutritional status, ameliorate its antioxidant capacity, and reduce the impact of abiotic and biotic stresses. Nevertheless, this efficacy is strongly correlated to the AMF genera and the type of cultivar. R. irregularis and G. mosseae, mainly in co-inoculants, were the most effective agents. Glomus irregulare was also very effective against Verticillium wilt. Furthermore, the impact of AMF inoculation is greater in the first stages of plant development. Regarding PGPR, the majority of the microbial inoculants contained nitrogen-fixing bacteria (e.g., Azospirillum sp.) and potassium or phosphorous solubilizing bacteria (mainly Bacillus species). These microbial inoculants combined with mineral fertilizers or manure supply were very effective in enhancing olive plants’ growth and with less agricultural inputs.
As regards the studies on biotic stress, most of them were focused on bacteria, endophytes, and fungi that belong to Pseudomonas, Bacillus, and Trichoderma species. Bacterial, endophytic strain Pseudomonas fluorescens PICF7 was the most studied and the most effective biocontrol agent against Verticillium wilt. It was more effective when it was present in both the surface and the interior of olive organs and in direct contact with the pathogen. The application of biological control in olive plants, at the propagation stage, is the most recommended approach because an earlier treatment (in the nursery) with bio-fungicide can significantly reduce the occurrence of symptoms caused by pathogens in the field.

Supplementary Materials

The following are available online at https://www.mdpi.com/2223-7747/9/6/743/s1, Table S1: List of all the research articles used in our study.

Author Contributions

G.B., E.M.P., and N.M. conceptualized the review and wrote the paper. T.C., N.N., and V.G.A. read and critically commented on the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. López-Escudero, F.J.; Mercado-Blanco, J. Verticillium wilt of olive: A case study to implement an integrated strategy to control a soil-borne pathogen. Plant Soil 2011, 344, 1–50. [Google Scholar] [CrossRef] [Green Version]
  2. 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] [PubMed] [Green Version]
  3. 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]
  4. Ouledali, S.; Ennajeh, M.; Zrig, A.; Gianinazzi, S.; Khemira, H. Estimating the contribution of arbuscular mycorrhizal fungi to drought tolerance of potted olive trees (Olea europaea). Acta Physiol. Plant. 2018, 40, 81. [Google Scholar] [CrossRef]
  5. Ben Amira, M.; Lopez, D.; Triki Mohamed, A.; Khouaja, A.; Chaar, H.; Fumanal, B.; Gousset-Dupont, A.; Bonhomme, L.; Label, P.; Goupil, P.; et al. Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biol. Control. 2017, 110, 70–78. [Google Scholar] [CrossRef]
  6. Seifi, E.; Teymoor, Y.S.; Alizadeh, M.; Fereydooni, H. Olive mycorrhization: Influences of genotype, mycorrhiza, and growing periods. Sci. Hortic. 2014, 180, 214–219. [Google Scholar] [CrossRef]
  7. Kara, Z.; Arslan, D.; Güler, M.; Güler, Ş. Inoculation of arbuscular mycorrhizal fungi and application of micronized calcite to olive plant: Effects on some biochemical constituents of olive fruit and oil. Sci. Hortic. 2015, 185, 219–227. [Google Scholar] [CrossRef]
  8. Calvo-Polanco, M.; Sánchez-Castro, I.; Cantos, M.; García, J.L.; Azcón, R.; Ruiz-Lozano, J.M.; Beuzón, C.R.; Aroca, R. Effects of different arbuscular mycorrhizal fungal backgrounds and soils on olive plants growth and water relation properties under well-watered and drought conditions. Plant Cell Environ. 2016, 39, 2498–2514. [Google Scholar] [CrossRef] [Green Version]
  9. Fouad, M.O.; Essahibi, A.; Benhiba, L.; Qaddoury, A. Effectiveness of arbuscular mycorrhizal fungi in the protection of olive plants against oxidative stress induced by drought. Span. J. Agric. Res. 2014, 12, 763–771. [Google Scholar] [CrossRef] [Green Version]
  10. Merwad, M.A.; Shahin, M.F.M.; Haggag, L.F. Optimizing growth of “Picual” olive seedlings by using organic and biofertilizers as soil application under greenhouse condition. Int. J. Chemtech Res. 2015, 8, 36–42. [Google Scholar]
  11. Kour, D.; Bakshi, P.; Wali, V.K.; Sharma, N.; Sharma, A.; Iqbal, M. Alternate Bearing in Olive—A Review. Int. J. Curr. Microbiol. Appl. Sci. 2018, 7, 2281–2297. [Google Scholar] [CrossRef]
  12. Sidhoum, W.; Fortas, Z. Effect of Arbuscular mycorrhizal fungi on growth of semi-woody olive cuttings of the variety “Sigoise” in Algeria. Am. J. Res. Commun. 2013, 1, 244–257. [Google Scholar]
  13. Bompadre, M.J.; Pérgola, M.; Fernández Bidondo, L.; Colombo, R.P.; Silvani, V.A.; Pardo, A.G.; Ocampo, J.A.; Godeas, A.M. Evaluation of arbuscular mycorrhizal fungi capacity to alleviate abiotic stress of olive (Olea europaea L.) plants at different transplant conditions. Sci. World J. 2014, 6, 378950. [Google Scholar]
  14. Meddad-Hamza, A.; Beddiar, A.; Gollotte, A.; Lemoine, M.C.; Kuszala, C.; Gianinazzi, S. Arbuscular mycorrhizal fungi improve the growth of olive trees and their resistance to transplantation stress. Afr. J. Biotechnol. 2010, 9, 1159–1167. [Google Scholar]
  15. 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]
  16. 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, 337. [Google Scholar] [CrossRef]
  17. Nigro, F.; Antelmi, I.; Labarile, R.; Sion, V.; Pentimone, I. Biological control of olive anthracnose. Acta Hortic. 2018, 1199, 439–444. [Google Scholar] [CrossRef]
  18. Ruano-Rosa, D.; Valverde-Corredor, A.; Gómez-Lama Cabanás, C.; Sesmero, R.; Mercado-Blanco, J. What Lies Beneath: Root-Associated Bacteria to Improve the Growth and Health of Olive Trees. In Soil Biological Communities and Ecosystem Resilience; Lukac, M., Grenni, P., Gamboni, M., Eds.; Springer: Cham, Switzerland, 2017; pp. 107–122. [Google Scholar]
  19. Maksoud, M.A.; El-Shamma, M.S.; Saleh, M.A.; Zaied, N.S.; Hafez, O.M. Effect of different compost sorts and biofertilizers on chemlali olive trees grown in calcareous soil. Middle East. J. Sci. Res. 2012, 12, 1046–1049. [Google Scholar]
  20. Garnault, M.; Duplaix, C.; Leroux, P.; Couleaud, G.; Carpentier, F.; David, O.; Walker, A.S. Spatiotemporal dynamics of fungicide resistance in the wheat pathogen Zymoseptoria tritici in France. Pest. Manag. Sci. 2019, 75, 1794–1807. [Google Scholar] [CrossRef]
  21. Shaheen, S.A.; El Taweel, A.A.; Omar, M.N.A. Effect of inoculation by some plant growth promoting rhizobacteria (PGPR) on production of “Manzanillo” olive trees. Acta Hortic. 2014, 1018, 245–254. [Google Scholar] [CrossRef]
  22. Abd-Alhamid, N.; Hassan, H.S.A.; Haggag, L.F.; Hassan, A.M. Effect of mineral and bio-fertilization on vegetative growth, leaf mineral contents and flowering of manzanillo olive trees. Int. J. Chemtech. Res. 2015, 8, 51–61. [Google Scholar]
  23. Cabanás, C.G.L.; Legarda, G.; Ruano-Rosa, D.; Pizarro-Tobías, P.; Valverde-Corredor, A.; Niqui, J.L.; Triviño, J.C.; Roca, A.; Mercado-Blanco, J. Indigenous Pseudomonas spp. Strains from the Olive (Olea europaea L.) rhizosphere as effective biocontrol agents against Verticillium dahliae: From the host roots to the bacterial genomes. Front. Microbiol. 2018, 9, 277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Del Mar Alguacil, M.; Torrecillas, E.; Kohler, J.; Roldàn, A. A molecular approach to ascertain the success of “in situ” AM fungi inoculation in the revegetation of a semiarid, degraded land. Sci. Total Environ. 2011, 409, 2874–2880. [Google Scholar] [CrossRef] [PubMed]
  25. Ferreira, G.M.D.R.; Melloni, R.; da Silva, L.F.D.O.; Martins, F.B.; Gonçalves, E.D. Arbuscular mycorrhizal fungi in seedling development of olive (Olea europaea L.) in the south of Minas Gerais, Brazil. Rev. Bras. Cienc. Do Solo 2015, 39, 361–366. [Google Scholar] [CrossRef] [Green Version]
  26. Chenchouni, H.; Mekahlia, M.N.; Beddiar, A. Effect of inoculation with native and commercial arbuscular mycorrhizal fungi on growth and mycorrhizal colonization of olive (Olea europaea L.). Sci. Hortic. 2020, 261, 108969. [Google Scholar] [CrossRef]
  27. Mechri, B.; Attia, F.; Tekaya, M.; Cheheb, H.; Hammami, M. Colonization of olive trees (Olea europaea L.) with the arbuscular mycorrhizal fungus Glomus sp. modified the glycolipids biosynthesis and resulted in accumulation of unsaturated fatty acids. J. Plant Physiol. 2014, 171, 1217–1220. [Google Scholar] [CrossRef]
  28. Tekaya, M.; Mechri, B.; Mbarki, N.; Cheheb, H.; Hammami, M.; Attia, F. Arbuscular mycorrhizal fungus Rhizophagus irregularis influences key physiological parameters of olive trees (Olea europaea L.) and mineral nutrient profile. Photosynthetica 2017, 55, 308–316. [Google Scholar] [CrossRef]
  29. Mechri, B.; Tekaya, M.; Cheheb, H.; Attia, F.; Hammami, M. Accumulation of flavonoids and phenolic compounds in olive tree roots in response to mycorrhizal colonization: A possible mechanism for regulation of defense molecules. J. Plant Physiol. 2015, 185, 40–43. [Google Scholar] [CrossRef]
  30. Dag, A.; Yermiyahu, U.; Ben-Gal, A.; Zipori, I.; Kapulnik, Y. Nursery and post-transplant field response of olive trees to arbuscular mycorrhizal fungi in an arid region. Crop. Pasture Sci. Crop. Pasture Sci. 2009, 60, 427–433. [Google Scholar] [CrossRef]
  31. Chatzistathis, T.; Orfanoudakis, M.; Alifragis, D.; Therios, I. Colonization of Greek olive cultivars’ root system by arbuscular mycorrhiza fungus: Root morphology, growth, and mineral nutrition of olive plants. Sci. Agric. 2013, 70, 185–194. [Google Scholar] [CrossRef] [Green Version]
  32. Boutaj, H.; Meddich, A.; Wahbi, S.; Moukhli, A.; El Alaoui-Talibi, Z.; Douira, A.; Filali-Maltouf, A.; El Modafar, C. Improvement of growth and development of olive tree by mycorrhizal autochthonous inoculum. Res. J. Biotechnol. 2020, 15, 76–84. [Google Scholar]
  33. Semane, F.; Chliyeh, M.; Talbi, Z.; Touati, J.; Selmaoui, K.; Touhami, A.O.; Filali-Maltouf, A.; El Modafar, C.; Moukhli, A.; Benkirane, R.; et al. Effects of a Composite Endomycorrhizal Inoculum on Olive Cuttings under the Greenhouse Conditions. Int. J. Environ. Agric. Biotechnol. 2017, 2, 1070–1083. [Google Scholar] [CrossRef]
  34. Haggag, L.F.; Merwad, M.A. Effect of NPK and bio-fertilers as soil application on promoting growth of “Toffahi” olive seedlings under greenhouse condition. J. Agric. Tech. 2014, 10, 1607–1617. [Google Scholar]
  35. Peyvandi, M.; Farahani, F.; Hosseini Mazinani, M.; Noormohamadi, Z.; Ataii, S.; Asgharzade, A. Pseudomonas fluorescent and its ability to promote root formation of olive microshoots. Int. J. Plant Prod. 2010, 4, 63–66. [Google Scholar]
  36. Montero-Calasanz, M.C.; Santamaría, C.; Albareda, M.; Daza, A.; Duan, J.; Glick, B.R.; Camacho, M. Alternative rooting induction of semi-hardwood olive cuttings by several auxin-producing bacteria for organic agriculture systems. Span. J. Agric. Res. 2013, 11, 146–154. [Google Scholar] [CrossRef]
  37. Rosa, D.D.; Villa, F.; Da Silva, D.F.; Corbari, F. Rooting of semihardwood cuttings of olive: Indolbutyric acid, calcium and Azospirillum brasilense. Comun. Sci. 2018, 9, 34–40. [Google Scholar] [CrossRef] [Green Version]
  38. Ramasamy, K.; Joe, M.M.; Kim, K.-Y.; Lee, S.-M.; Shagol, C.; Rangasamy, A.; Chung, J.-B.; Islam, M.R.; Sa, T.-M. Synergistic Effects of Arbuscular Mycorrhizal Fungi and Plant Growth Promoting Rhizobacteria for Sustainable Agricultural Production. Korean J. Soil Sci. Fertil. 2011, 44, 637–649. [Google Scholar] [CrossRef] [Green Version]
  39. Lies, A.; Ferhout, H.; Wahbi, S.; Hafidi, M.; Prin, Y.; Duponnois, R. Selection of efficient microbial biofertilizers from Moroccan soils. Acta Hortic. 2016, 1148, 115–126. [Google Scholar] [CrossRef]
  40. Costa, S.M.L.; Melloni, R. Relationship of arbuscular mycorrhizal fungi and rhizobacteria on the growth of olive tree seedlings (Olea europaea). Cienc. Florest. 2019, 29, 169–181. [Google Scholar] [CrossRef]
  41. Hafez, O.M.; Saleh, M.A.; El-Lethy, S.R. Response of some seedlings olive cultivars to foliar spray of yeast and garlic extracts with or without vascular arbuscular mycorrhizal fungi. World Appl. Sci. J. 2013, 24, 1119–1129. [Google Scholar]
  42. 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]
  43. Chliyeh, M.; Ouazzani Touhami, A.; Filali-Maltouf, A.; El Modafar, C.; Moukhli, A.; Oukabli, A.; Benkirane, R.; Douira, A. Effect of a composite endomycorrhizal inoculum on the growth of olive trees under nurseries conditions in Morocco. Int. J. Pure Appl. Biosci. 2014, 2, 1–14. [Google Scholar]
  44. Kapulnik, Y.; Tsror, L.; Zipori, I.; Hazanovsky, M.; Wininger, S.; Dag, A. Effect of AMF application on growth, productivity and susceptibility to Verticillium wilt of olives grown under desert conditions. Symbiosis 2010, 52, 103–111. [Google Scholar] [CrossRef]
  45. Bompadre, M.J.; Rios De Molina, M.C.; Colombo, R.P.; Fernandez Bidondo, L.; Silvani, V.A.; Pardo, A.G.; Ocampo, J.A.; Godeas, A.M. Differential efficiency of two strains of the arbuscular mycorrhizal fungus Rhizophagus irregularis on olive (Olea europaea) plants under two water regimes. Symbiosis 2013, 61, 105–112. [Google Scholar] [CrossRef]
  46. M’barki, N.; Chehab, H.; Aissaoui, F.; Dabbaghi, O.; Attia, F.; Mahjoub, Z.; Laamari, S.; Chihaoui, B.; del Giudice, T.; Jemai, A.; et al. Effects of mycorrhizal fungi inoculation and soil amendment with hydrogel on leaf anatomy, growth and physiology performance of olive plantlets under two contrasting water regimes. Acta Physiol. Plant. 2018, 40, 116. [Google Scholar] [CrossRef]
  47. Jiménez-Moreno, M.J.; Moreno-Márquez, M.d.C.; Moreno-Alías, I.; Rapoport, H.; Fernández-Escobar, R. Interaction between mycorrhization with Glomus intraradices and phosphorus in nursery olive plants. Sci. Hortic. 2018, 233, 249–255. [Google Scholar] [CrossRef]
  48. Khabou, W.; Hajji, B.; Zouari, M.; Rigane, H.; Abdallah, F. Ben Arbuscular mycorrhizal fungi improve growth and mineral uptake of olive tree under gypsum substrate. Ecol. Eng. 2014, 73, 290–296. [Google Scholar] [CrossRef]
  49. Briccoli Bati, C.; Santilli, E.; Lombardo, L. Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 2014, 25, 97–108. [Google Scholar] [CrossRef] [PubMed]
  50. Ouledali, S.; Ennajeh, M.; Ferrandino, A.; Khemira, H.; Schubert, A.; Secchi, F. Influence of arbuscular mycorrhizal fungi inoculation on the control of stomata functioning by abscisic acid (ABA) in drought-stressed olive plants. South. Afr. J. Bot. 2019, 121, 152–158. [Google Scholar] [CrossRef]
  51. Silva, T.F.; Melloni, R.; Melloni, E.G.P.; Gonçalves, E.D. Non-symbiotic diazotrophic bacteria and the rooting of olive semi-hardwood cuttings (Olea europaea L.). Cienc. Florest. 2017, 27, 61–71. [Google Scholar] [CrossRef] [Green Version]
  52. Maksoud, M.A.; Saleh, M.A.; Fouad, A.A. The Beneficial Effect of Biofertilizers and Antioxidants on Olive Trees under Calcareous Soil Conditions. World J. Agric. Sci. 2009, 5, 350–352. [Google Scholar]
  53. El-Shazly, M.M.; Ghieth, W.M. Effect of Some Biofertilizers and Humic Acid Application on Olive Seedlings Growth under Irrigation with Saline Water. Alex. Sci. Exch. J. 2019, 40, 263–279. [Google Scholar] [CrossRef] [Green Version]
  54. Bouaichi, A.; Benkirane, R.; El-Kinany, S.; Habbadi, K.; Lougraimzi, H.; Sadik, S.; Benbouazza, A.; Achbani, E.H. Potential effect of antagonistic bacteria in the management of olive knot disease caused by Pseudomonas savastanoi pv. savastanoi. J. Microbiol. Biotechnol. Food Sci. 2019, 8, 1035–1040. [Google Scholar] [CrossRef] [Green Version]
  55. Sanei, S. Suppression of Verticillium Wilt of Olive by Pseudomonas fluorescens. Am. J. Exp. Agric. 2011, 1, 294–305. [Google Scholar] [CrossRef]
  56. 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]
  57. Hibar, K.; Gamaoun, W.; Triki, M.A. Isolation, identification and biological control of the major pathogens causing root rot and wilt diseases of young olive trees in. J. New Sci. 2017, 39, 2121–2130. [Google Scholar]
  58. Abdel-Monaim, M.F.; El-Morsi, M.E.A.; Hassan, M.A.E. Control of root rot and wilt disease complex of some evergreen fruit transplants by using plant growth promoting rhizobacteria in the New Valley Governorate, Egypt. J. Phytopathol. 2014, 1, 23–33. [Google Scholar]
  59. Bouzoumita, A.; Metoui, M.; Jemni, M.; Kabaeir, N.; Belhouchette, K.; Ferchichi, A. The efficacy of various bacterial organisms for biocontrol of fusarium root rot of olive in tunisia. Pol. J. Environ. Stud. 2020, 29, 11–16. [Google Scholar] [CrossRef]
  60. Prieto, P.; Schilirò, E.; Maldonado-González, M.M.; Valderrama, R.; Barroso-Albarracín, J.B.; Mercado-Blanco, J. Root Hairs Play a Key Role in the Endophytic Colonization of Olive Roots by Pseudomonas spp. with Biocontrol Activity. Microb. Ecol. 2011, 32, 435–445. [Google Scholar] [CrossRef] [Green Version]
  61. Maldonado-González, M.M.; Prieto, P.; Ramos, C.; Mercado-Blanco, J. From the root to the stem: Interaction between the biocontrol root endophyte Pseudomonas fluorescens PICF7 and the pathogen Pseudomonas savastanoi NCPPB 3335 in olive knots. Microb. Biotechnol. 2013, 6, 275–287. [Google Scholar] [CrossRef] [Green Version]
  62. 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] [PubMed] [Green Version]
  63. Cabanás, C.G.L.; Sesmero, R.; Valverde-Corredor, A.; Javier López-Escudero, F.; Mercado-Blanco, J. A split-root system to assess biocontrol effectiveness and defense-related genetic responses in above-ground tissues during the tripartite interaction Verticillium dahliae-olive-Pseudomonas fluorescens PICF7 in roots. Plant Soil 2017, 417, 433–452. [Google Scholar] [CrossRef]
  64. Slama, H.B.; Triki, M.A.; Bouket, A.C.; Mefteh, F.B.; Alenezi, F.N.; Luptakova, L.; Cherif-Silini, H.; Vallat, A.; Oszako, T.; Gharsallah, N.; et al. Screening of the high-rhizosphere competent limoniastrum monopetalum’ culturable endophyte microbiota allows the recovery of multifaceted and versatile biocontrol agents. Microorganisms 2019, 7, 249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Cheffi, M.; Bouket, A.C.; Alenezi, F.N.; Luptakova, L.; Belka, M.; Vallat, A.; Rateb, M.E.; Tounsi, S.; Triki, M.A.; Belbahri, L. Olea europaea L. Root endophyte Bacillus Velezensis oee1 counteracts oomycete and fungal harmful pathogens and harbours a large repertoire of secreted and volatile metabolites and beneficial functional genes. Microorganisms 2019, 7, 314. [Google Scholar] [CrossRef] [Green Version]
  66. 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]
  67. Ruano-Rosa, D.; Prieto, P.; Rincón, A.M.; Gómez-Rodríguez, M.V.; Valderrama, R.; Barroso, J.B.; Mercado-Blanco, J. Fate of Trichoderma harzianum in the olive rhizosphere: Time course of the root colonization process and interaction with the fungal pathogen Verticillium dahliae. BioControl 2016, 61, 269–282. [Google Scholar] [CrossRef]
  68. Varo, A.; Moral, J.; Lozano-Tóvar, M.D.; Trapero, A. Development and validation of an inoculation method to assess the efficacy of biological treatments against Verticillium wilt in olive trees. BioControl 2016, 61, 283–292. [Google Scholar] [CrossRef]
  69. Otero, M.L.; Roca, M.; Zapata, R.; Ladux, J.L.; Ortiz, J.; Zanelli, M.; Matías, A.C.; Pérez, B.A. Effect of solarization, organic matter, and Trichoderma on the severity of Verticillium wilt in olive trees (Olea europaea L.) and soil inoculum density. Acta Hortic. 2014, 1057, 121–126. [Google Scholar] [CrossRef]
  70. Boutaj, H.; Meddich, A.; Wahbi, S.; Moukhli, A.; El Alaoui-Talibi, Z.; Douira, A.; Filali-Maltouf, A.; El Modafar, C. Effect of arbuscular mycorrhizal fungi on verticillium wilt development of olive trees caused by Verticillium dahliae. Res. J. Biotechnol. 2019, 14, 79–88. [Google Scholar]
  71. Varo-Suárez, A.; Raya-Ortega, M.C.; Agustí-Brisach, C.; García-Ortiz-Civantos, C.; Fernández-Hernández, A.; Mulero-Aparicio, A.; Trapero, A. Evaluation of organic amendments from agro-industry waste for the control of verticillium wilt of olive. Plant Pathol. 2018, 67, 860–870. [Google Scholar] [CrossRef]
  72. Arici, S.E.; Demirtas, A.E. The effectiveness of rhizosphere microorganisms to control Verticillium wilt disease caused by Verticillium dahliae Kleb. in olives. Arab. J. Geosci. 2019, 12, 781. [Google Scholar] [CrossRef]
  73. 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]
Table
Table 1. Microbial inoculant applied to improve olive tree’s growth, physiology, and crop productivity. AMF: Arbuscular Mycorrhizal Fungi; PGPR: Plant Growth Promoting Rhizobacteria.
Table 1. Microbial inoculant applied to improve olive tree’s growth, physiology, and crop productivity. AMF: Arbuscular Mycorrhizal Fungi; PGPR: Plant Growth Promoting Rhizobacteria.
Microbial InoculantTypeProductEffectApplicationAgeLocationReferences
Rhizophagus irregularis, Glomus mosseaeAMF-GrowthRootYoungNursery[6]
R. irregularisAMF-Growth and Nutrition *RootYoungNursery[7]
Glomus sp., Acaulospora sp.,
Glomus macrocarpum, Glomus multicaulis,
Scutellospora sp.		AMF-GrowthRootYoungNursery[12]
Glomus sp., R. irregularisAMF-GrowthRootYoungExperimental Field[24]
Glomus clarum, Gigaspora rosea,
Scutellospora scrobiculata		AMF-GrowthRootYoungNursery[25]
Glomus sp., Septoglomus constrictum,
R. irregularis, Funneliformis mosseae,
Gigaspora margarita		AMF-GrowthRootYoungNursery[26]
R. irregularisAMF-Growth and NutritionRootYoungNursery[27]
R. irregularisAMF-Growth and Nutrition **RootYoungNursery[28]
R. irregularisAMF-Growth and Nutrition **RootYoungNursery[29]
R. irregularis, G. mosseaeAMF-Growth and NutritionRootYoungNursery [30]
Glomus sp., Gigaspora sp.AMF-Growth and NutritionRootYoungNursery[31]
Glomus sp., Acaulospora sp., Gigaspora sp., Entrophospora sp., Scutellospora sp., Glomus irregulare DAOM 197198AMF-Growth and NutritionRootYoungNursery[32]
Acaulospora scrobiculata,
G. macrocarpum, R. irregularis,
Glomus versiforme, Gigaspora sp., Scutellospora fulgida, Glomus geosporum,
Glomus aureum, Glomus microcarpum,
Glomus aurantium, G. corymbiforme,
G. clarum, Scutellospora heterogama		AMF-GrowthRootYoungNursery[33]
Azotobacter chrococcum,
Bacillus megaterium, Bacillus circulans		PGPR-GrowthRootAdultOrchard[22]
Azospirillum sp., Bacillus mucilaginosus,
B. megatherium		PGPR-Growth and NutritionRootYoungNursery[34]
Pseudomonas fluorescent P19, P21PGPR-GrowthRootYoungNursery[35]
Pantoea sp. AG9, Chryseobacterium sp. AG13, Pseudomonas sp. CT364, Chryseobacterium sp. CT348, Azospirillum brasilense CdPGPR-GrowthRootYoungNursery[36]
Azospirillum brasilensePGPRAzototal®GrowthRootYoungNursery[37]
Azotobacter chroococcum,
Azospirillum brasilense,
B. megaterium var. phosphaticum,
G. mosseae NRC31, Pseudomonas sp.,
Bacillus cereus, Glomus fasciculatum NRC15		AMF and PGPR-Growth and NutritionRootYoungNursery[10]
Pseudomonas sp., Paenibacillus sp.,
Acaulospora scrobiculata,
Gigaspora rosea, Rhizophagus clarus		AMF and PGPR-Growth and NutritionRootYoungNursery[40]
Bacillus polymyxa,
Saccharomyces cereivisea		PGPR and FungiBiovine®Growth and NutritionFoliarAdultOrchard[21]
AMF consortium, S. cerevisiaeAMF and Fungi-Growth and NutritionRoot/FoliarYoungNursery[41]
* Enhancement of the nutritional value of the olive fruit with the increase of antioxidants with health benefits ** Enhancement of the antioxidant capacity of the olive tree with the increase of phenols and flavonoids.
Table
Table 2. Microbial inoculant studies aiming on the alleviation of abiotic and transplantation stresses.
Table 2. Microbial inoculant studies aiming on the alleviation of abiotic and transplantation stresses.
Microbial InoculantTypeProductStress ConditionsApplicationAgeLocationReferences
G. etunicatum, G. microaggregatum,
R. irregularis, G. claroideum,
G. mosseae, G. geosporum		AMFSymbivit®Water StressRootYoungExperimental Field[4]
Glomus sp., R. irregularis,
Dominikia sp., Funneliformis sp., Funneliformis geosporum, Septoglomus constrictum, Septoglomus viscosum		AMF-Water StressRootYoungNursery[8]
Rhizophagus manihotis,
Funneliformis mosseae		AMF-Water StressRootYoungNursery[9]
R. irregularis GC2, GA5AMF-TransplantationRootYoungNursery[13]
G. mosseae, R. irregularisAMF-TransplantationRootYoungNursery[14]
G. mosseae, R. irregularis, G. claroideumAMF-SalinityRootYoungNursery[42]
R. irregularis, G. trimurales, G. manihoti, G. diaphanum, G. pansihalos,
G. geosporum, G. glomerulatum,
G. fasciculatum, G. etunicatum,
Acaulospora sp., Acaulospora mellea,
Entrophospora kentinensis,
Scutellospora nigra,
Scutellospora fulgida,
Scutellospora heterogama, 		AMF-TransplantationRootYoungNursery[43]
R. irregularis, G. mosseaeAMF-SalinityRootYoungExperimental Field[44]
R. irregularis GC2, GA5AMF-Water StressRootYoungNursery[45]
R. irregularisAMF-Water StressRootYoungNursery[46]
R. irregularisAMF-Nutrient stressRootYoungNursery[47]
R. irregularisAMF-ToxicityRootYoungNursery[48]
Glomus sp., Scutellospora heterogama, Paraglomus laccatum, Diversispora celataAMFEndorize IV®ToxicityRootYoungNursery[49]
R. irregularis, G. etunicatum,
G. microaggregatum, G. claroideum,
G. mosseae, G. geosporum		AMFSymbivit®Water StressRootYoungNursery[50]
Azotobacter chrococcumPGPR-ToxicityRootYoungNursery[19]
Azospirillum brasilense BR11001t,
Azospirillum amazonense BR11040t, Herbaspirillum seropedicae BR11175t,
Burkholderia brasiliensis BR11340t		PGPR-Temperature and pHRootYoungNursery[51]
B. megatheriumPGPRPhosphorine®ToxicityRootYoungNursery[52]
Azotobacter chroococcum,
G. macrocarbium		PGPR and AMF-SalinityRootYoungExperimental Field[53]
Table
Table 3. Microbial inoculants used as biocontrol agents. PGPF: Plant Growth Promoting Fungi.
Table 3. Microbial inoculants used as biocontrol agents. PGPF: Plant Growth Promoting Fungi.
Microbial InoculantTypeProductDiseaseApplicationAgeLocationReferences
Pseudomonas fluorescens PICF7Endophyte-Verticillium wiltRootYoungNursery[2]
P. fluorescens PICF7Endophyte-Verticillium wiltRootYoungNursery[3]
Trichoderma harzianum Ths97PGPF-Root rotRootYoungNursery[5]
Paenibacillus polymyxa, Paenibacillus terrae, Bacillus sp. PIC28, P. fluorescensPICF7, Pseudomonas sp. PICF141PGPR-Verticillium wiltRootYoungNursery[15]
Bacillus mojavensis A-BC-7PGPR-Olive knotStemYoungNursery[16]
B. subtilis QST 713, Aureobasidium pullulans A3, A5, A6PGPR EndophyteSerenade Max®AnthracnoseFoliarAdultOrchard[17]
Pseudomonas spp. PIC25, PIC105, PICF141PGPR-Verticillium wiltRootYoungNursery[23]
R. irregularis, G. mosseaeAMF-Verticillium wiltRootYoungExperimental Field[44]
B. subtilis 2515-1PGPR-Olive knotStemYoungNursery[54]
P. fluorescensPGPR-Verticillium wiltRootYoungNursery[55]
Paenibacillus alvei K165PGPR-Verticillium wiltRootYoungExperimental Field[56]
B. subtilis Y1336PGPRBiobac®Root rot and wiltRootYoungNursery[57]
Azotobacter sp. AZM1, B. cereus BCM8, B. megatherium BMM5, B. subtilis BSM1PGPR-Root rotRootYoungNursery[58]
B. licheniformis, Enterobacter colcaePGPR-Root rotRootYoungNursery[59]
P. fluorescens PICF7,
P. putida PICP2		Endophyte-Verticillium wiltRootYoungNursery[60]
P. fluorescens PICF7Endophyte-Olive knotRootYoungNursery[61]
P. fluorescens PICF7Endophyte-Verticillium wiltRootYoungNursery[62]
P. fluorescens PICF7Endophyte-Verticillium wiltRootYoungNursery[63]
B. licheniformis LMRE 36Endophyte-Root rotRootYoungNursery[64]
B. velezensis OEE1Endophyte-Olive knotRootYoungNursery[65]
Trichoderma asperellum Bt3, T25PGPF-Verticillium wiltRootYoungNursery[66]
T. harzianum CECT 2413PGPF-Verticillium wiltRootYoungNursery[67]
Fusarium oxysporum FO12,
Phoma sp. Ph02		PGPF-Verticillium wiltRootYoungNursery[68]
T. harziarumPGPF-Verticillium wiltRootAdultOrchard[69]
Glomus sp., Acaulospora sp., Gigaspora sp., Entrophospora sp., Scutellospora sp., G. irregulare DAOM 197198AMF-Verticillium wiltRootYoungNursery[70]
Fusarium oxysporum FO12, Lactobacillus plantarum, Lactobacillus casei, Rhodobacter sphaeroides, Rhodopseudomonas palustris Saccharomyces sp.,
Streptococcus lactis, Streptomyces sp.		PGPR and FungiEM-1®Verticillium wiltRootYoungNursery[71]
G. aggregatum, G. mosseae,
G. clarum, G. monosporus, G. deserticola,
G. brasilianum, G. etunicatum,
G. margarita, R. irregularis,
T. harzianum Rifai KRL-AG2		AMF and PGPFT-22Planter Box®Verticillium wiltRootAdultOrchard[72]
Fusarium oxysporum FO12PGPF Verticillium wiltRootYoung/AdultNursery/Orchard[73]

Share and Cite

MDPI and ACS Style

Bizos, G.; Papatheodorou, E.M.; Chatzistathis, T.; Ntalli, N.; Aschonitis, V.G.; Monokrousos, N. The Role of Microbial Inoculants on Plant Protection, Growth Stimulation, and Crop Productivity of the Olive Tree (Olea europea L.). Plants 2020, 9, 743. https://doi.org/10.3390/plants9060743

AMA Style

Bizos G, Papatheodorou EM, Chatzistathis T, Ntalli N, Aschonitis VG, Monokrousos N. The Role of Microbial Inoculants on Plant Protection, Growth Stimulation, and Crop Productivity of the Olive Tree (Olea europea L.). Plants. 2020; 9(6):743. https://doi.org/10.3390/plants9060743

Chicago/Turabian Style

Bizos, Georgios, Efimia M. Papatheodorou, Theocharis Chatzistathis, Nikoletta Ntalli, Vassilis G. Aschonitis, and Nikolaos Monokrousos. 2020. "The Role of Microbial Inoculants on Plant Protection, Growth Stimulation, and Crop Productivity of the Olive Tree (Olea europea L.)" Plants 9, no. 6: 743. https://doi.org/10.3390/plants9060743

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop