Development of agricultural bio-inoculants based on mycorrhizal fungi and endophytic filamentous fungi: co-inoculants for improve plant-physiological responses in sustainable agriculture

Biological Control 182 (2023) 105223 Available online 11 April 2023 1049-9644/© 2023 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Review Development of agricultural bio-inoculants based on mycorrhizal fungi and endophytic filamentous fungi: Co-inoculants for improve plant-physiological responses in sustainable agriculture María Díaz-Urbano a , Nieves Goicoechea b , Pablo Velasco a , Jorge Poveda c , * a Group of Genetics, Breeding and Biochemistry of Brassicas, Misi´ on Biol´ ogica de Galicia (MBG), Spanish National Research Council (CSIC), A Carballeira, 8, 36143 Pontevedra, Spain b Department of Environmental Biology, Plant Stress Physiology Group, Associated to CSIC (EEAD, Zaragoza), School of Sciences, University of Navarra-BIOMA, c/ Irunlarrea 1, 31008 Pamplona, Spain c Recognised Research Group AGROBIOTECH, Department of Plant Production and Forest Resources, University Institute for Research in Sustainable Forest Management (iuFOR), University of Valladolid, Av. de Madrid, 57, 34004 Palencia, Spain HIGHLIGHTS •Agricultural inoculant formulations consist of several microorganisms on a carrier. •Bioinoculants based on EFF* and MF** often act synergistically when co-inoculated. •EF-MF consortia improve crop yield and quality under optimal conditions and stress. •EF-MF consortia improve plant performance against biotic and abiotic stresses. *EFF: Endophytic filamentous fungi. **MF: Mycorrhizal fungi. ARTICLE INFO Keywords: Biological control Biostimulant Glomus Trichoderma Rhizophagus Piriformospora ABSTRACT A new more sustainable agricultural system needs to be developed to increase production without compromising human and animal health and preserving essential resources, such as soil, water and diversity. Bio-inoculants can be a tool to favor this transition, as they can replace or complement agrochemicals that do not meet the above premises. Bio-inoculants generated from endophytic filamentous fungi and mycorrhizal fungi, whether used individually, in combination with each other or with other microorganisms, stand out for their potential. This review provides information on how bio-inoculants based on these microorganisms have been shown to increase crop yield and quality through strategies, such as increasing nutrient uptake or levels of certain phytohormones. On how they can promote tolerance to abiotic stresses, including heavy metals, elevated temperatures, salinity or drought, through strategies, such as the accumulation of osmoregulatory substances or increasing the plant’s root surface, among others. And finally, in the ability to protect the plant against pathogens and pests, either by inducing defense systems, competing for space or synthesizing metabolites with antibiotic activity. It should be noted that, although there are already commercial products using these microorganisms for agricultural purposes, such as biological control agents or biostimulants, it is expected that a deeper understanding of the mechanisms of action of the microorganisms, together with improved technical production processes, will lead to more effective, safer and cheaper products. 1. Introduction Humankind faces a severe challenge, difficult to solve: ensuring food sovereignty. The world’s population has reached 7.9 billion people in 2023 and it is estimated that by 2050 the world’s population will reach 9.7 billion people (United Nations, 2019). This increase in population density must translate into an increase in available resources, such as food. In addition, climate change and global warming can be aggravating factors in this context, since an increase of extreme phenomena is predicted, such as torrential rains, droughts, heat and cold waves * Corresponding author. E-mail address: [email protected] (J. Poveda). Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon https://doi.org/10.1016/j.biocontrol.2023.105223 Received 30 January 2023; Received in revised form 17 March 2023; Accepted 4 April 2023 Biological Control 182 (2023) 105223 2 (Cramer et al., 2022). These phenomena can lead to water shortages, soil degradation or even the disruption of the biosphere. For example, the distribution patterns of certain pests, which act as vectors for the transmission of plant pathogens, can be altered, posing a threat to crops (Shipley et al., 2020). The agricultural system has to be able to cope with all these issues by increasing production, respecting the carrying capacity of the planet and avoiding overexploitation of soils and water sources (Gerten et al., 2020). During the green revolution, world production increased considerably, partly as a result of the indiscriminate use of agrochemicals (mainly fertilizers and pesticides). Although in those decades it was a great advance, today it has generated problems of immense depth. It is essential to modify the use we make of agrochemicals. It is evident that new fertilization strategies must be formulated, since the application rate is usually higher than the optimum, leading to an excess of fertilizer that contaminates the soil and water (Ullah et al., 2019). As an example, there are efforts to improve nitrogen use efficiency (NUE) since the excessive use of fertilizers rich in phosphorus and nitrogen can produce accumulation of these, generating human and animal toxicity (Mandal et al., 2020). In addition, the leaching of fertilizers from the soil is considered a global phenomenon that generates eutrophication and mortality of aquatic organisms (Khanna and Gupta, 2018). Moreover, nitrate in drinking water produces adverse health effects on population (Kotopoulou et al., 2021). The imbalance of mineral nutrients in the soil can generate a toxic impact on the edaphic microbiota. Alterations in the microbiome can affect the cycle of nutrients and, ultimately, the yield of crops (Mandal et al., 2020). On the other hand, pesticides contaminate the soil and water, generating wide-ranging concerns, since some heavy metals have been generated as residues, which have accumulated in the food chain, affecting the environment and human health (Parr´ on et al., 2014). Therefore, the agricultural system must move towards more sustainable and context-sensitive solutions. New biocontrol strategies must be based on specific microorganisms that affect the target organisms, without harming other beneficial organisms such as insects or plantsymbiotic microorganisms. Similarly, biostimulants must specifically supplement the necessary nutrients, avoiding surpluses that may be toxic or harmful to the environment (Mandal et al., 2020). One proposal to try to reduce the use of agrochemicals is the use of microbial bioinoculants, products formulated with the strains of interest of one or more microorganisms. These microorganisms can be bacteria or fungi that induce immune response against pathogens and pests, promote growth (producing phytohormones, improving the absorption of nutrients, mobilizing or solubilizing them) or generating tolerance to abiotic stresses (Chaudhary et al., 2020). In addition to improving plant performance, bioinoculants can also be used to improve the physicochemical properties of the soil and decontaminate or detoxify the soil (Maitra et al., 2022). For microorganisms to fulfil their function, they must be included in a uniform matrix (carrier) that allows their storage, transport and protection. The ideal carrier would be the one that allows the desired purpose to be fulfilled without polluting the environment. There are different types of carriers, among which we find: solid, liquid, metabolite and polymeric formulation. The ideal material should provide the necessary nutrients, be sterilizable, non-toxic and adaptable to different microorganisms (Chaudhary et al., 2020). The benefit of mycorrhizal fungi (MF) in agriculture, either individually (Benami et al., 2020; Ejersa, 2021) or in co-inoculation with other microorganisms (Yadav et al., 2020; Santoyo et al., 2021), is well established. However, although numerous studies have demonstrated the efficacy of co-inoculation between MF and endophytic filamentous fungi (EFF), there was no review addressing the physiological responses of plant species to MF-EFF colonization. Therefore, the aim of this review is to gather the literature on the use of bio-inoculants based on filamentous endophytic fungi, mycorrhizal fungi, and their combination. In order to develop tools for sustainable agriculture that promote growth, increase crop yield and quality, promote tolerance to abiotic stresses and induce plant defense responses against pathogens and pests. In addition, including information on their formulation and being critical of their efficacy, highlighting the weaknesses of this technology and proposing possible solutions. 2. Agricultural bio-inoculants based on mycorrhizal fungi (MF) Mycorrhizae are defined as soil fungi associated with plant roots and establishing a symbiotic relationship with them. However, not all fungi associated with plants are mycorrhizas. Generally, mycorrhizas meet a number of distinctive structural (forming arbuscules, coils, pelotons, Hartig net, mantle…), functional (facilitating nutrient supply) and developmental synchronisation requirements with the host (Brundrett, 2006). In addition, the relationship is usually mutualistic, with the host plant benefiting from the supply of nutrients, such as phosphorus or nitrogen, and the fungus benefiting from a protected environment and carbon-derived compounds. Therefore, this definition must be understood within a broad spectrum of fungi that differ in function and structure from each other and may not strictly fit the definition. Within this amalgam of symbiont fungi we find various types of mycorrhizae, which have different origins, anatomy and ecology and, generating differences in their ability to protect against biotic or abiotic stresses, nutrient acquisition, carbon cycling and other nutrients (Tedersoo et al., 2020). They are usually classified by making a general division between ectomycorrhizae (ECM) and endomycorrhizae, among which we find orchid mycorrhizae (ORM), arbuscular mycorrhizae (AM) and ericoid mycorrhizae (ERM) (Genre et al., 2020). 2.1. MF as biostimulants Mycorrhizal fungi (MF) can be used in agriculture for a wide variety of purposes. The most common way is to find them as biostimulants, because they increase nutrient uptake, mainly of phosphorus and other inorganic nutrients as nitrogen (Anand et al., 2022). In addition, crops associated with MF usually have in their tissues increased amount of some micronutrients, such as Cu, Zn, Fe or Mn (Baslam et al., 2011), essential for the human health but frequently scarce in the daily food intake, which induces the phenomenon termed ‘hidden hunger’. In fact, there are numerous patents covering the use of MF as biostimulants. The most patented genus is Glomus, which accounts for 82.5% of all patented MF between 2000 and 2020, followed by the genera Rhizophagus (3.9%), Sclerocystis (3.9%) and Gigaspora. 2.2. Other benefits of AMF MF can reduce the amount of fertiliser used, allowing a reduction in nutrient losses (Cavagnaro et al., 2015). These edaphic fungi favour soil aggregation through hyphal enmeshment and production of glomalinrelated proteins, accelerate the decomposition of fresh N-rich residues and enhance the retention of organic C into soil aggregates in the longer term (Wei et al., 2019). The use of biostimulants is often linked to increasing yield in the form of dry and fresh weight, or/and grain weight, although this is not always correlated. In addition, some MF can increase grain quality (Tran et al., 2019), in wheat being this beneficial effect more evident when plants are exposed to water deficit (Goicoechea et al., 2016). Another of their main utilities is their use as bioprotectors against biotic stresses such as pests, plant diseases and weeds. They reduce crop diseases as they can activate plant defence systems and generate induced systemic resistance, as in the case of Glomus sp. which confers protection to tomato and pepper against Phytophthora (Nevalainen, 2021). This bioprotective effect, however, can be dependent on the species of MF as reported by Garmendia et al. (2004) working with pepper affected by Verticillium dahliae. Likewise, MF species can affect the competitive relationships between crops and weeds (Rashidi et al., 2021). In addition, MF have been shown to improve plant performance under abiotic stress conditions, such as high salinity, alkaline soils, low or elevated temperatures or high M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 3 concentrations of heavy metals. Therefore they can be used in bioremediation or recovery of natural areas (deserts, mines…) (Anand et al., 2022) and appear as a promising tool for increasing the resilience and quality of crops facing climate change scenarios (Torres et al., 2018a). MF also favour system performance and yield stability. Although not directly related to yield or short-term production, MF enhance plant stability by adding soil particles, promoting water acquisition, sequestering carbon and increasing soil organic matter, improving soil structure (Rillig et al., 2019). Finally, MF can induce the accumulation of mineral nutrients and antioxidant compounds in plant tissues and organs usually discarded as crop residuals, thus turning these vegetable wastes in an interesting material with potential use, not only as fertilizers, but also for human nutrition (Torres et al., 2018b) or even for biomedicine (Torres et al., 2019). 2.3. Co-inoculants: MF and other microorganisms They were frequently co-inoculated with other microorganisms to enhance their effect. Bacteria were the most common microorganisms with which MF were associated. Co-inoculations with nitrogen fixing bacteria, phosphate solubilising bacteria and plant growth promoting rhizobacteria were predominant. The most predominant ones were Bacillus licheniformis, B. subtilis, Bradyrhizobium japonicum, Pseudomonas fluorescens and Rhizobium meliloti (Srivastava et al., 2021). 3. Agricultural bio-inoculants based on endophytic filamentous fungi (EFF) Endophytic filamentous fungi (EFF) are microorganisms that colonize, partly or throughout their lifespan, the plant internal tissues or organs, such as roots, stems, seeds, leaves and fruits without causing any symptoms of disease (Petrini, 1991; Kumar et al., 2021). They are found in all plants on the planet and there is a great diversity of them. Some are specifically associated with certain species, while others are generalists. They can also occur in a specific tissue or colonise several different tissues (Zabalgogeazcoa, 2008). Depending on the tissue or organ, the abundance and diversity of EFF varies according to plant’s genotype, nutrient availability, presence of other microorganisms and environmental conditions (soil characteristics, climate, agricultural management practices…) (Pozo et al., 2021). Different types of endophytes have been identified and are generally grouped into: clavicipitaceous endophytes associated with grasses, and non-clavicipitaceous endophytes associated with non-vascular plants, conifers and angiosperms (Rodriguez et al., 2009). The phylum with the greatest presence of endophytes is Ascomycota, followed by Basidiomycota, Zygomycota and Glomeromycota. Plant colonization can occur vertically, remaining through the seed, or horizontally, in which case it must recognize and colonize the host (Lugtenberg et al., 2016). 3.1. Benefits of EFF inoculation Some EFF can maintain a mutualistic relationship with crops and provide them with certain advantages over uncolonized plants. Endophytes can increase yield or quality directly, by promoting growth, improving the uptake or use of the nutrient. They can also improve yield indirectly, by improving the plant’s response to abiotic (drought, salinity, heavy metals…) or biotic stresses (plant pathogens such as viruses, bacteria, nematodes and fungi, herbivory…) (Poveda et al., 2022). The most popular and cost-effective strategy is the direct use of EFF by incorporating them into crops and allowing them to establish in plants. To a lesser extent, it has also been studied how exogenous application of compounds generated by EFF can improve plant performance. This is because EFF can produce antimicrobial compounds or activators of the plant’s defence system, which could be applied to different crops like a traditional agrochemical (Khan et al., 2014; Numponsak et al., 2018). 3.1.1. EFF promote plant growth To promote growth, they act as biostimulants, improving the uptake of nutrients that are difficult for the plant to access (Umesha et al., 2018; Poveda et al., 2021). Some examples are: Trichoderma, Penicillium or Beauveria sp. that increase nitrogen, phosphorus or iron uptake, respectively in various crops such as maize, wheat or habanero peppers (Wakelin et al., 2011; Rinu et al., 2014; Toscano-Verduzco et al., 2020). On the other hand, they can also promote growth by modifying the plant’s hormone levels. Some endophytes produce hormone-like compounds that act as phytostimulators (auxins, cytokinins, gibberellins, etc.) (Chagas et al., 2018). As an example, Aspergillus japonicus and A. niger produces auxins and gibberellins that increases the growth of soybean, sunflower or rice (Asaf et al., 2018). In order to improve plant performance in stressful conditions, endophytes present several strategies. According to Dastogeer and Wylie (2017), they can improve water uptake, the photosynthesis, the osmotic adjustment, reactive oxygen species (ROS) removal and hormone modulation. In addition, it has also been documented that endophytes can activate induced systemic tolerance (IST) (Chagas et al., 2018; Khan et al., 2013). Examples are Exophiala pisciphila which gives maize tolerance to cadmium at concentrations that would be phytotoxic or Piriformospora indica which protects against drought in Chinese cabbage (Sun et al., 2010) and against salinity in barley (Baltruschat et al., 2008). 3.1.2. EFF as biocontrol agents Finally, endophytic fungi can increase resistance to pathogens, either locally or systemically. In this case, the formulated bioinoculant act as a biological control agent (BCA). Endophytes have been shown to protect plants against disease by reducing or suppressing the growth of the plant pathogen. To achieve this protection, endophytes activate induced systemic resistance (ISR), preventing pathogen colonization, compete for space and nutrients or synthesize defensive metabolites such as alkaloids, flavonoids, phenols, steroids, terpenoids or volatile organic compounds (VOCs) that inhibit the growth of certain plant pathogens. The latter strategy is also valid against herbivory, as has been demonstrated by some endophytic fungi of the genus Epichlo¨ e (Brem and Leuchtmann, 2001). Another type of plant protection mediated by endophytic fungi may come from nematophagous or entomopathogens fungi which can inhabit plant roots as endophytes (Zabalgogeazcoa, 2008; Poveda et al., 2020; Pozo et al., 2021). As an example, genus Trichoderma, act as BCA for nematode control (Poveda et al., 2020). Other examples of endophytes acting as BCAs are Trichoderma asperellum that protects against Pseudomonas syringae pv. lachrymans in cucumber, Epichlo¨ e festucae that generates an antifungal protein against Sclerotinia homoeocarpa (Tian et al., 2017) and Heteroconium chaetospira which reduces the symptoms of clubroot disease in oilseed roots (Adeleke et al., 2022). Trichoderma-based products are the most marketed ones. A large number of species within this genus have been shown to have fungicidal, fertilizer, insecticidal and inductors of ISR. As an example, products containing different Trichoderma species (T. polysporum, T. harzianum, T. gamsii, T. atroviride o T. asperellum, among others) have been registered in Europe. Some of these products are marketed as TUSAL WG, Trichomic, BioFlower, Sani-Root or Bioten and are formulated with one or more Trichoderma species. In addition, Trichoderma can appear associated with other microorganisms (Poveda and Eugui, 2022), as in the products Compete Plus and Suma Grow in which it appears combined with Bacillus spp. and Streptomyces in the former (Woo et al., 2014), or Rhizobium spp., Pseudomonas spp. and Bacillus spp. in the latter (Pirttil¨ a et al., 2021). 3.2. Co-inoculants: EFF and other microorganisms In general terms, these products consist of a microorganism, or a set of organisms (microbial consortium), associated with a carrier. Usually the microbial consortia offer better results than single-strain inoculants both as biostimulants (Kenneth Odoh et al., 2020) and in biological M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 4 control (Kumar et al., 2012; Whipps, 2001) especially in adverse environmental conditions. Although microbial consortia can potentially be made with a multitude of microorganisms (viruses, algae, archaea, oomycetes), the most commercialized products are the consortium between bacteria and fungi (Pirttil¨ a et al., 2021; Poveda et al., 2022). This is probably due to the fact that most commercially available products are based on bacteria and are already accepted by the consumer and the regulation (EU, 2019; Kowalska et al., 2020). Moreover, bacteria have been shown to play a key role in biostimulation as they fix nitrogen (Rhizobium, Azospirillum, Azotobacter…), solubilise phosphorus (Penicillium, Fusarium, Aspergillus…), mobilise phosphate… And they are also used as biocontrol tools as they produce antibiotics, enzymes that degrade the cell wall of certain fungi and induce systemic resistance in plants (Tripathi et al., 2015; Vyas, 2018). Using them in combination can have a synergistic effect (Seenivasagan and Babalola, 2021), as an example Pririformospora indica and Azotobacter chroococcum promotes plant growth (Arora et al., 2020). In addition to the microorganisms that form the product, it is essential that the bioinoculants developed are cheap, easy to apply, easy to handle and remain effective throughout their useful life, which should be as long as possible. For this purpose, solid formulations (granules, microcapsules, emulsions or powder) and liquid formulations have been developed (Tripathi et al., 2015). In the case of biostimulants, they can also be different types of soils, either natural (peat and coal, soya bean oil, compost…) or inert (perlite, talcum, clay, vermiculite…). In general, the material must be non-toxic to micro-organisms, plants, animals and the environment. These tools are intended to be more environmentally friendly, safer for human health and the environment. In addition, bioinoculants are used in small quantities and their proliferation is controlled by the native microbiota and the plant (Baron and Rigobelo, 2022). The forms of application depend on the formulation. Usually, the most desirable form of application requires no additional material, either by the irrigation system itself or by spraying. Seed coating or dispersion by spreader centrifuges is also common. Crops that are transplanted, such as rice, onions or many ornamental plants can be dipped into this solution for several hours and then transplanted (Misra et al., 2020). It must be highlighted that EU Regulation allows only the drying or freeze-drying processes in the formulation of the product, limiting the range of micro-organisms that can be used to those that survive these processes (Kowalska et al., 2020). 4. Combined use mycorrhizal fungi-endophytic filamentous fungi The plant-fungus relationship is never an isolated interaction, since both members interact in turn with the rest of organisms present (microorganisms, plants and animals). In the case of fungus-plant root interaction, the enormous complexity of interactions is encompassed under the concept of mycorrhizosphere. This includes the proportion of soil occupied by the roots and the fungal hyphae that interact with them, also colonizing the internal-plant tissues, together with all organisms present there (Kothe and Turnau, 2018). In the plant-MF-EFF tripartite interaction we find a complex network of molecular dialogues that not only have effects on its members, but also on the rest of the organisms in the agro-system. Directly, it has been reported how different EFFs are capable of reducing or eliminating the ability of MF to colonize roots. In different grasses it has been possible to verify how the endophyte Neotyphodium coenophialum produces various allelochemical compounds that reduce the ability of MF to colonize the roots of these plants by 90% (Antunes et al., 2008). These antifungal allochemical compounds against MF have been identified as alkaloids produced by the endophyte Acremonium coenophiulum in Festuca arundinacea plants (Chu-Chou et al., 1992). On the other hand, MF can also act indirectly on endophytic fungi populations in different plant organs. It has been possible to describe how the root colonization of Cirsium arvense by different MF actively modifies the quantity and diversity of EFF present in leaves and stems (Eschen et al., 2010). In turn, these EFF in the aerial part can also favor root colonization by MF, how has been reported in the grass Poa bonariensis with the endophyte Neotyphodium sp. (Victoria-Novas et al., 2009). Simultaneous root colonization by MF and EFF has been described in a wide diversity of plant species, such as pteridophytes (Fern´ andez et al., 2013), desert plants (Wagg et al., 2008; Wu et al., 2009), pines (Kernaghan et al., 2003), oaks (Toju et al., 2013; Yamamoto et al., 2014), orchids (Wang et al., 2017), medicinal and aromatic plants (Muthukumar et al., 2006; Dang et al., 2021), ginger (Pandey et al., 2020), switchgrass (Lee and Hawkes, 2021), rice (Vallino et al., 2009) or alfalfa (Saravesi et al., 2014). However, diversity and root/rhizosphere colonization of each fungal group can be very different depending on various factors, being the main: host phylogeny, geographic distance, soil and climate (Gooden et al., 2020; Wang et al., 2020). Within climatic factors, the most influential for MF and EFF are rainfall, sunlight hours and temperature (Olsson et al., 2004; Lingfei et al., 2005; Huo et al., 2021). Regarding the soil, the main conditioning factors are nutritional content (mainly, N and P), pH and the presence of heavy metals (Postma et al., 2007; G¨ oransson et al., 2008; Bueno de Mesquita et al., 2018). Of course, the host conditions both directly and indirectly can modify the diversity and quantity of MF and EFF that colonize its roots. Differences have been reported at genotype level within the same species (Karli´ nski et al., 2010; Bazghaleh et al., 2018), between different species within the same place (Fuchs and Haselwandter, 2004; John et al., 2014; Surendirakumar et al., 2021), and in different places with the same host (Chaudhry et al., 2009). On the other hand, it has also been described how this simultaneous root colonization by MF and EFF is modified according to the stage of plant development, with EFF being more present during the early part of the growing season, and MF during the peak growing season (Mandyam and Jumpponen, 2008). In the next sections, all the studies carried out on the combined and directed use of MF and EFF in different crops, in order to promote their growth and yield, increase their tolerance to abiotic stresses and/or protect them from biotic stresses, are presented and discussed. In Fig. 1 we can find a summary infographic about the different effects and mechanisms of action reported with MF-EFF co-inoculation in plants. 4.1. Promotion of plant growth, yield and quality of crops The ability of MF and EFF in isolation to promote plant growth and crop productivity is widely known. In this sense, the combination of both fungal tools can increase (even synergistically) the isolated effects of each microorganism. Table 1 compiles all MF-EFF co-inoculation studies related to plant growth promotion, yield and quality of crops. There are numerous descriptive studies where only the effects of MFEFF co-inoculation are reported, without identifying the mechanisms of action involved. In this sense, the promotion of plant growth has been reported additively with both types of fungi combined compared to each one in isolation. For example, in Elymus hystrix co-inoculated with different MF (Glomus claroideum and G. mosseae) and the EFF Epichlo¨ e elymi (Larimer et al., 2012); or in cucumber with G. mosseae and Fusarium equiseti (Saldajeno and Hyakumachi, 2011). Synergistic plant growth promotion effects have also been reported, such as in tomato coinoculated with MF and Trichoderma spp. (Commatteo et al., 2019). And even at a productive level, as is the case with the increase in tuber yield in Helianthus tuberosus plants co-inoculated with Glomus etunicatum and Exserohilum rostratum (Khaekhum et al., 2021). In isolation, MF and EFF promote plant growth through various mechanisms of action, always dependent on the degree of root colonization (Jansa et al., 2008; Poveda et al., 2021). In this sense, it has been reported in several studies how MF-EFF co-inoculation increases root colonization by one or both fungi, significantly promoting the growth of the host plant. One of the mechanisms of action involved may be the production of exudates by EFF, favoring the growth and development of MF and the colonization of the host plant. In Bromus auleticus plants, the M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 5 exudates produced by Epichlo¨ e tembladerae promoted the growth and development of the MF Rhizophagus intraradices and Gigaspora rosea, significantly promoting plant growth (Vignale et al., 2018). These plant growth promotion effects, as a consequence of greater root colonization by MF, caused by its co-inoculation with EFF, have been reported with very different crops and fungal species. For example, in soybean with G. mosseae and Fusarium spp. (Garcia-Romera et al., 1998), or in blueberry with the co-inoculations Glomus viscosum-Phanerochaete chrysosporium and Glomus intraradices-Trametes versicolor (Arriagada et al., 2012). However, these plant growth promotion effects because of a greater MF-root colonization are totally dependent on the MF-EFF combination performed. In this sense, co-inoculation with G. mosseae with Trichoderma harzianum in cucumber plants is effective, but when EFF is modified by Penicillium simplicissimum, the beneficial effect is not obtained (Chandanie et al., 2009). In a similar way, it occurs when the species MF is modified, having been observed how T. harzianum promotes root colonization of melon plants by Glomus constrictum, G. claraideum and G. intraradices, but not by G. mosseae (Martínez- Medina et al., 2009). This same mechanism of action has been reported with ectomycorrhizae, promoting plant growth of Picea abies due to greater root colonization by Laccaria bicolor when co-inoculated with the EFF Phialocephala fortinii and Acephala applanata (Reininger and Sieber, 2012). In addition to the promotion of plant growth, the increase in root colonization by MF can lead to an increase in the nutritional content of plant tissues. These results have been reported in very diverse crops and MF-EFF combinations, with the main nutrients quantified differentially being N, P, K, Ca, Na, Mg, Cu and Zn (Fracchia et al., 2000; Vaz et al., 2012; Zhou et al., 2018). Finally, both the promotion of plant growth and the increase in the acquisition of nutrients by the plant lead to an increase in crop yield and crop quality. In onions, MF-Trichoderma viride co-inoculation increases bulb yield by up to 20% (Metwally and Al- Amri, 2020), along with total free amino acids, and soluble protein content (Metwally et al., 2021). Similar increases reported in tuber yield of potato plants co-inoculated with Rhizophagus irregularis and T. harzianum (Buysens et al., 2016). Fig. 1. Summary infographic about the different effects and mechanisms of action reported with mycorrhizal fungi (MF) and endophytic filamentous fungi (EFF) coinoculation in plants. The acronyms PPO, PAL, POD, APX, SOD refer to the polyphenol oxidase, phenylalanine amino lyase, peroxidase, ascorbate peroxidase and superoxide dismutase enzymes, respectively. M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 6 Table 1 Effect of promoting plant growth and increasing yield in crops by co-inoculations with mycorrhizal fungi (MF) and endophytic filamentous fungi (EFF). MF SPECIES EFF SPECIES EXPERIMENT CROP BENEFICIAL EFFECTS MECHANISMS OF ACTION REFERENCE Acaulospora laevis Trichoderma viride In greenhouse Sunflower Plant growth promotion Improved oil yield Increased MF root colonizationIncreased P supply (MF) Yadav et al., 2015 Phoma leveillei In greenhouse Cucumber Plant growth promotion Increased yield Increased fungi root colonization Gao et al., 2016 T. viride In greenhouse Onion Plant growth promotion Increased bulb yield Increased MF root colonization Metwally and Al- Amri, 2020 Dentiscutata nigra T. viride In greenhouse Onion Plant growth promotion Increased bulb yield Increased MF root colonization Metwally and Al- Amri, 2020 Diversispora spurca Piriformospora indica In field Orange Improved fruit quality Increased P and water content in soil Cheng et al., 2022 D. versiformis P. indica In field Orange Improved fruit quality Increased P and water content in soil Cheng et al., 2022 Epulorhiza repens Umbelopsis nana In greenhouse Cymbidium hybridum Plant growth promotion Increased nutrients content in plant tissues Increased P, K, Ca, Mg and Zn supply (E. repens)Increased N, P and Ca supply (U. nana) Liu et al., 2021 Funneliformis constrictum (=Septoglomus constrictum) (= Glomus constrictum) Trichoderma harzianum In greenhouse Melon Plant growth promotion Increased MF root colonization Martínez-Medina et al., 2009 T. viride In greenhouse Onion Plant growth promotion Improved bulbs quality Increased MF root colonization Metwally et al., 2021 Gigaspora margarita T. harzianum In greenhouse Bean Plant growth promotion Increased nutrients content in plant tissues Increased P and Zn supplyP solubilization (T. harzianum) Eke et al., 2019 T. viride In greenhouse Onion Plant growth promotion Improved bulbs quality Increased MF root colonization Metwally et al., 2021 G. rosea Phialocephala turiciensis P. glacialis In growth chamber Trifolium repens Increased nutrients content in plant tissues Increased P content in soil Della Monica et al., 2015 Epichlo¨ e tembladerae In greenhouse Bromus auleticus Plant growth promotion Increased MF root colonization Vignale et al., 2018 Glomus aggregatum Mortierella sp. In greenhouse Leucaena Plant growth promotion Increased nutrients content in plant tissues P solubilization (Mortierella sp.) Increased P supply (G. aggregatum) Osorio and Habte, 2001 T. harzianum In greenhouse Rapeseed Arabidopsis Increased siliques yield Increased T. harzianum root colonization MF root colonization Poveda et al., 2019 G. claroideum (=Claroideoglomus claroideum) T. harzianum In greenhouse Melon Plant growth promotion Increased MF root colonization Martínez-Medina et al., 2009 Epichlo¨ e elymi In greenhouse Elymus hystrix Plant growth promotion Unidentified Larimer et al., 2012 Mortierella sp. In greenhouse Leucaena Plant growth promotion Increased nutrients content in plant tissues P solubilization (Mortierella sp.) Increased P supply (C. claroideum) Osorio and Habte, 2015 T. harzianum In greenhouse Rapeseed Arabidopsis Increased siliques yield Increased T. harzianum root colonization MF root colonization Poveda et al., 2019 G. clarum Fusarium oxysporum In greenhouse In field Pea Sorghum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Fracchia et al., 2000 G. deserticola F. oxysporum In greenhouse In field Pea Sorghum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Fracchia et al., 2000 (continued on next page) M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 7 Table 1 (continued) MF SPECIES EFF SPECIES EXPERIMENT CROP BENEFICIAL EFFECTS MECHANISMS OF ACTION REFERENCE G. etunicatum (=Claroideoglomus etunicatum) Epichlo¨ e sp. In field Achnatherum sibiricum Increased nutrients content in plant tissues Increased P supply Zhou et al., 2016 Epichlo¨ e gansuensis E. sibirica In field Achnatherum sibiricum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Zhou et al., 2018 Penicillium pinophilum In growth chamber Tomato Lettuce Plant growth promotion P solubilization (P. pinophilum) Siderophore production (P. pinophilum)Increased root colonization (both) Ibiang et al., 2020 Exserohilum rostratum In field Helianthus tuberosus Increased tuber yield Unidentified Khaekhum et al., 2021 G. fistulosum Mortierella sp. In greenhouse Leucaena Plant growth promotion Increased nutrients content in plant tissues P solubilization (Mortierella sp.) Increased P supply (G. fistulosum) Osorio and Habte, 2013 G. hoi (=Simiglomus hoi) Epichlo¨ e occultans In greenhouse Lolium multiflorum Plant growth promotion Increased P supply (MF) García-Parisi and Omacini, 2017 T. harzianum In greenhouse Bean Plant growth promotion Increased nutrients content in plant tissues Increased P and Zn supplyP solubilization (T. harzianum) Eke et al., 2019 G. monosporum (=Funneliformis monosporus) T. viride In greenhouse Onion Plant growth promotion Increased bulb yield Increased MF root colonization Metwally and Al- Amri, 2020 G. mosseae (=Funneliformis mosseae) F. oxysporum F. stilboide F. solani In greenhouse Soybean Plant growth promotion Increased MF root colonization Garcia-Romera et al., 1998 F. oxysporum In greenhouse In field Pea Sorghum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Fracchia et al., 2000 T. harzianum In growth chamber Cucumber Plant growth promotion Increased MF root colonization Chandanie et al., 2009 T. harzianum In greenhouse Melon Plant growth promotion Increased MF root colonization Martínez-Medina et al., 2009 Fusarium equiseti In growth chamber Cucumber Plant growth promotion Unidentified Saldajeno and Hyakumachi, 2011 E. elymi In greenhouse E. hystrix Plant growth promotion Unidentified Larimer et al., 2012 P. indica In field Maize Plant growth promotion Unidentified Rane et al., 2015 T. viride In greenhouse Sunflower Plant growth promotion Improved oil yield Increased MF root colonizationIncreased P supply (MF) Yadav et al., 2015 P. leveillei In greenhouse Cucumber Plant growth promotion Increased yield Increased fungi root colonization Gao et al., 2016 Epichlo¨ e sp. In field A. sibiricum Plant growth promotion Increased nutrients content in plant tissues Increased P and N supply Zhou et al., 2016 E. occultans In greenhouse Lolium multiflorum Plant growth promotion Increased P supply (MF) García-Parisi and Omacini, 2017 E. gansuensis E. sibirica In field A. sibiricum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Zhou et al., 2018 T. harzianum In greenhouse Rapeseed Arabidopsis Increased siliques yield Increased T. harzianum root colonization MF root colonization Poveda et al., 2019 Serendipita williamsii In growth chamber Tomato Increased nutrients content in plant tissues Increased N supply (both) Hallasgo et al., 2020 (continued on next page) M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 8 Table 1 (continued) MF SPECIES EFF SPECIES EXPERIMENT CROP BENEFICIAL EFFECTS MECHANISMS OF ACTION REFERENCE T. viride In greenhouse Onion Plant growth promotion Improved bulbs quality Increased MF root colonization Metwally et al., 2021 G. versiforme (=Diversispora epigaea) P. leveillei In greenhouse Cucumber Plant growth promotion Increased yield Increased fungi root colonization Gao et al., 2016 Alternaria sp. In greenhouse Maize Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Increased P and K supply Xie et al., 2021 G. viscosum Phanerochaete chrysosporium In greenhouse Blueberry Plant growth promotion Increased MF root colonization Arriagada et al., 2012 Glomus sp. Cylindrocarpon destructans C. pauciseptatum Eucasphaeria sp. Phoma schachtii P. columnaris In greenhouse Sorghum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Vaz et al., 2012 Laccaria bicolor Phialocephala fortinii Acephala applanata In growth chamber Picea abies Plant growth promotion Increased ectomycorrhizae root colonization Reininger and Sieber, 2012 Rhizophagus intraradices (=Glomus intraradices) F. oxysporum In greenhouse In field Pea Sorghum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Fracchia et al., 2000 T. harzianum In greenhouse Melon Plant growth promotion Increased MF root colonization Martínez-Medina et al., 2009 Trametes versicolor In greenhouse Blueberry Plant growth promotion Increased MF root colonization Arriagada et al., 2012 E. occultans In greenhouse Lolium multiflorum Plant growth promotion Increased P supply (MF) García-Parisi and Omacini, 2017 P. indica In greenhouse Miscanthus giganteus Plant growth promotion Modification of hormonal content in plant tissues Schmidt et al., 2017 E. tembladerae In greenhouse B. auleticus Plant growth promotion Increased MF root colonization Vignale et al., 2018 P. pinophilum In growth chamber Tomato Lettuce Plant growth promotion P solubilization (P. pinophilum) Siderophore production (P. pinophilum)Increased root colonization (both) Ibiang et al., 2020 R. irregularis (=Glomus irregulare) T. harzianum In field Potato Increased tuber yield Increased MF root colonization Buysens et al., 2016 T. harzianum In greenhouse Rapeseed Arabidopsis Increased siliques yield Increased T. harzianum root colonization MF root colonization Poveda et al., 2019 P. pinophilum In growth chamber Tomato Lettuce Plant growth promotion P solubilization (P. pinophilum) Siderophore production (P. pinophilum)Increased root colonization (both) Ibiang et al., 2020 T. viride In greenhouse Onion Plant growth promotion Improved bulbs quality Increased MF root colonization Metwally et al., 2021 Rhizoglomus clarum (=Rhizophagus clarus) T. viride In greenhouse Onion Plant growth promotion Increased bulb yield Increased MF root colonization Metwally and Al- Amri, 2020 R. fasciculatum (=Glomus fasciculatum) F. oxysporum In greenhouse In field Pea Sorghum Plant growth promotion Increased nutrients content in plant tissues Increased MF root colonization Fracchia et al., 2000 Mortierella sp. In greenhouse Avocado Plant growth promotion Increased nutrients content in plant tissues P solubilization (Mortierella sp.) Increased P supply (R. fasciculatum) Tamayo-Velez and Osorio, 2016 (continued on next page) M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 9 However, MF-EFF co-inoculation is not able to promote plant growth only through increased colonization by MF, but also EFF can promote their growth, development and colonization of host roots. The coinoculation of cucumber plants with different MF and Phoma leveillei significantly promotes the plant height, stem diameter, dry mass and yield per plant, due to greater root colonization by both types of fungi (Gao et al., 2016). Something even more innovative has been the work carried out by Poveda et al. (2019). Starting from the problem that the Brassicaceae family plants cannot form symbiosis with MF, since they have lost this ability evolutionarily, they formulated the hypothesis that using an EFF capable of colonizing the roots of these plants could facilitate colonization by MF. They co-inoculated Arabidopsis and rapeseed plants with different MF species and the endophyte T. harzianum, quantifying a significant increase in siliques yield. This was a consequence of an increase in root colonization by T. harzianum, by mycoparasitizing MF and using them as an energy resource, and the existence of colonization by MF. This colonization of the Brassicaceae roots by MF represents an enormous scientific advance in achieving the effective mycorrhization of important crops within this family of plants, being possible thanks to the modification of the root defenses by T. harzianum, “opening the door” for the entry of MF (Poveda et al., 2019). Together with a greater root colonization, MF and EFF promote plant growth due to a direct supply of nutrients to the roots. With respect to N, both MF and EFF act as powerful decomposers of the organic matter present in the soil, making assimilable forms of the nutrient available to the plant (Dighton et al., 1987; Giesemann et al., 2020; Hallasgo et al., 2020). However, the main nutrient provided by both groups of fungi is P. It has been reported that greater root colonization by MF is related to a greater supply of P to the host plant, as occurs with Acaulospora laevis- T. viride co-inoculation in sunflower (Yadav et al., 2015), or Glomus etunicatum-Epichlo¨ e sp. in Achnatherum sibiricum (Zhou et al., 2016). In this sense, a complementary action between both fungi has been described, very important for the nutritional contribution to the plant: the solubilization of P by EFF and its greater supply to the plant by MF. Through these mechanisms of action, it has been possible to promote plant growth and increase the tissue content of P in various crops, such as leucaena and avocado with MF-Mortierella sp. co-inoculations (Osorio and Habte, 2001, 2013, 2015; Tamayo-Velez and Osorio, 2016), or bean with MF-T. harzianum (Eke et al., 2019). In addition, together with P supply, these fungi can favor the acquisition of other important nutrients by their host plant, such as K (Xie et al., 2021), Fe (Ibiang et al., 2020), Ca, Mg or Zn (Liu et al., 2021), and even improve the acquisition of water by the roots (Cheng et al., 2022). On the other hand, it is widely known that rhizospheric fungi can promote plant growth through the production of plant hormones or the modification of the tissue contents of their host plant (Poveda et al., 2021). In this sense, it has been reported how root colonization of Miscanthus giganteus by Glomus intraradices and Piriformospora indica leads to plant growth promotion as a consequence of an increase in leaf concentrations of abscisic acid (ABA) derivatives, auxin (indole-3-acetic acid) precursors and catabolites and numerous cytokinins (Schmidt et al., 2017). Indirectly, root colonization by MF and/or EFF can also act on the fungal endophytic microbiota of the aerial part, and vice versa, modifying plant growth. For example, the foliar presence of EFF significantly reduces root colonization by MF, P uptake and shoot growth in several plant species (Park and Eom, 2007; Liu et al., 2020). But they can also have important positive effects on their host plant. In the wild grass Bromus auleticus, the presence of certain foliar EFFs, such as Epichlo¨ e sp., increases rhizosphere diversity and root colonization of P-solubilizing EFF and MF (Arrieta et al., 2015). 4.2. Abiotic stress tolerance Environmental conditions, such as atmospheric CO 2 , soil warming or drought, can significantly modify the diversity and quantity of MF and EFF that colonize plant roots (Staddon et al., 2004). It has even been possible to describe species of these filamentous fungi that are only present in situations of strong abiotic stress, such as salinity or pollution, and may play a key role in the ability of their host plants to survive in these extreme environments (Muthukumar and Vediyappan, 2010; Likar et al., 2011; Thiem et al., 2018). Table 2 compiles all the studies carried out to date where the MF-EFF co-inoculation has led to an improvement in the plant tolerance of crops to abiotic stresses. 4.2.1. MF-EFF inoculum against water stress Drought is an increasing abiotic stress due to climate change and global warming. It is caused by a massive loss of soil moisture, causing serious losses in three quarters of the globally harvested land (Mishra et al., 2021). The co-inoculation of crops with MF and EFF has reported important results in improving plant tolerance under drought situations, although each type of fungus can by itself promote plant tolerance very effectively (Tyagi et al., 2017). As described above, co-inoculation can cause an increase in root colonization by one or both types of fungi. In a drought situation, the co-inoculation with Gigaspora margarita and Phomopsis liquidambaris in peanut plants caused a significant increase in root colonization by MF and a greater development of the extraradical mycelium, increasing the volume of soil where the plant can acquire water, and the plant tolerance to stress (Xu et al., 2020). Other mechanisms of action derived from co-inoculation under drought stress are the increase in the nutritional contribution to the plant, specifically P, facilitating the accumulation of osmoregulatory substances in plant Table 1 (continued) MF SPECIES EFF SPECIES EXPERIMENT CROP BENEFICIAL EFFECTS MECHANISMS OF ACTION REFERENCE T. harzianum In greenhouse Rapeseed Arabidopsis Increased siliques yield Increased T. harzianum root colonization MF root colonization Poveda et al., 2019 Scutellospora aurigloba P. leveillei In greenhouse Cucumber Plant growth promotion Increased yield Increased fungi root colonization Gao et al., 2016 S. gigantea T. harzianum In greenhouse Bean Plant growth promotion Increased nutrients content in plant tissues Increased P and Zn supplyP solubilization (T. harzianum) Eke et al., 2019 Suillus luteus Mycena galopus In growth chamber Pinus contorta Plant growth promotion Increased N supply Dighton et al., 1987 Unidentified Trichoderma spp. In growth chamber Tomato Plant growth promotion Unidentified Commatteo et al., 2019 Unidentified In field Equisetum arvense E. sylvaticum Increased nutrients content in plant tissues Increased N supply Giesemann et al., 2020 M. Díaz-Urbano et al. Biological Control 182 (2023) 105223 16 BCA and biostimulants depends on the degree of colonization of the roots by the microorganism, its ability to displace the existing microbiota to establish itself or the environmental conditions at the time of product application. Very low temperatures, lack of moisture and high ultraviolet radiation can compromise the efficacy of the product (Babalola and Glick, 2012). Therefore, it is of utmost importance to study plant-microorganism, micro-organism-microorganism and microorganism-environment interactions in the agricultural context in order to develop appropriate formulations. Small changes in the formulation, the timing of application or the introduction of auxiliary microorganisms, which modulate the rhizosphere, can make the difference between a successful or unsuccessful bioinoculant. Author contributions JP proposed the review structure and content, and coordinated the work of all authors. 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