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Arbuscular Mycorrhizal Fungi in Intercropping Systems: Roles and Performance

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Yunjian Xu and Fang Liu

Submitted: 04 January 2024 Reviewed: 10 January 2024 Published: 01 July 2024

DOI: 10.5772/intechopen.114186

Unveiling the Mycorrhizal World IntechOpen
Unveiling the Mycorrhizal World Edited by Everlon Rigobelo

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Unveiling the Mycorrhizal World [Working Title]

Prof. Everlon Cid Rigobelo

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Abstract

Arbuscular mycorrhizal fungi (AMF) have attracted significant interest in the field of sustainable agriculture. Intercropping is another sustainable practice improving the nutrient utilization efficiency. In an AMF-colonized intercropping system, intercropping has been found to increase the mycorrhization rate, including root colonization and spore population in the rhizosphere of plants. Root colonization of one plant by AMF is clearly influenced by their intercropping partners. Therefore, the selection of appropriate intercropping partners can be used to improve the activity of mycorrhizal symbiosis in crops. Furthermore, intercropping with different plant species can alter arbuscular mycorrhizal (AM) fungal diversity, and these different AM genera have distinct functions and benefits for plants in intercropping systems. Additionally, in certain intercropping systems, perennial plants serve as reservoirs of AMF inoculum for intercrops. In return, AM symbiosis enhances nutrient availability in the intercropping system, leading to positive effects of intercrops. Moreover, AMF exhibit bioprotective effects in intercropping systems, reducing the severity of plant diseases and/or compensating for plant biomass loss. However, these bioprotective effects depend on the intercropping partner rather than the degree of AM colonization. In conclusion, the combination of AMF benefits with intercropping holds great promise for improving nutrient utilization efficiency and plant health.

Keywords

  • arbuscular mycorrhizal fungi
  • intercropping system
  • symbiosis
  • nutrient
  • sustainable agriculture

1. Introduction

Arbuscular mycorrhizal fungi (AMF) are beneficial soil microorganisms that can form symbiosis with more than 80% of plants [1]. The beneficial functions of AMF in the field are important in sustainable agriculture. The formation of AM symbiosis is considered important in improving plant nutrition and resistance to plant diseases (especially soil-borne diseases) [2, 3, 4]. In mycorrhizal roots, nutrient and some chemical signal transfer are dependent on common mycorrhizal networks (CMN), which are formed by AMF hyphae enlarging the area for roots [5, 6] and linking the neighboring plants [7]. In addition, AMF have effects on different plant growth in a field by altering interspecific or intraspecific competitive situations [8, 9]. In return, the arbuscular mycorrhizal (AM) fungal community can be influenced by the host plants [10, 11, 12].

In a field, two or more crops are simultaneously cultivated called intercropping systems, and is receiving increasing global interest as an agricultural sustainable practice [13, 14]. Many crop combinations have been reported in intercropping systems, especially those cultivated with legume species as intercrops [15], such as sugarcane/soybean [16], maize/faba bean [17], maize/soybean [18, 19], and maize/peanut [19]. In the intercropping system, the intercrops were connected via CMN, in which nutrients and signaling compounds can be exchanged between the connected plants.

In intercropping systems, AMF symbiosis further improves plant growth by increasing nutrient uptake, improving soil condition, or improving disease resistance. In return, AMF colonization, diversity, and reservoir are related to interactions between different intercrops. The aim of this chapter is to review information on AMF function and its response to intercrops interactions in intercropping systems.

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2. Benefits of AMF for plants

Arbuscular mycorrhizal fungi (AMF), belonging to the phylum Mucoromycota [20], can form mutualistic symbionts with more than 80% of land plants, including many agricultural crops [21]. A meta-analysis of 215 cases (involving 21 nurse species and 29 facilitated species) with/without AMF inoculation has shown that mycorrhizal fungi significantly improve plant facilitation mainly by increasing plant biomass (aboveground parts) and nutrient content [22]. AMF have a global impact on plant mineral nutrition, such as phosphorus (P) and nitrogen (N). AMF improves the uptake of mineral nutrients by increasing the surface area of absorbing and mobilizing sparsely available nutrients, which depends on AM fungal hyphae. In the root, the hyphae grow into root cortical cells, forming highly branched structures called arbuscules, which provide a large interface for nutrient exchange [1]. Mineral nutrients such as P and N are transported from AMF to plant hosts across the symbiotic interface [23]. In the soil, the extracellular hyphae form a fine network growing from colonized roots into the soil to expand the area for absorbing mineral nutrients from soil [24]. Mycorrhizal networks extend the absorbing surface area up to 40 times growing in every direction [25, 26], efficiently exploring the soil and increasing plant uptake of nutrients and water [27, 28]. This makes them essential for the establishment and productivity of plants in nutrient-limited soils and for the mitigation of plant stress [29]. Recent studies have shown that AMF also attracts other soil microorganisms helping them facilitate plant access to nutrients [30]. The intraradical AM fungal hyphae access carbon from the root and this fuels the growth of extraradical hyphae (ERH) in the surrounding soil, which feed on mineral nutrients essential for fungal growth and for delivery to the plant [31, 32, 33]. At the same time, growth of ERH increases the flow of carbon into the soil [34, 35, 36], which further recruits some special microorganisms to the rhizosphere.

Additionally, AMF increases plant resistance to biotic and abiotic stresses. For biotic stresses, in a biocontrol way, AMF plays a vital role in protecting the host from pathogens, which is one of the important strategies for ecologically sound management of plant diseases [37, 38]. For example, AMF inoculation suppresses tomato Ralstonia wilt and yield damage under the attack of Ralstonia solanacearum (soilborne pathogens), mainly through improved soil quality and alleviation of plant metabolic pressure [39]. AMF as a biocontrol for pepper Phytophthora blight has also been well reported [38, 40]. AMF Funneliformis caledonium significantly increased nutrient acquisition (N, P, and K), plant biomass, and pepper fruit yield under Phytophthora capsici inoculation [38]. Abiotic stress, such as drought, salinity, extreme temperatures, and pollution, present serious threats to agriculture. Fortunately, AMF have the ability to overcome adverse effects and improve plant performance in stressful environments. For example, AMF contributes to the production of low-Cd fruiting vegetables in Cd-contaminated fields: AMF symbiosis increase the P acquisition and biomass of cucumber plants, but reduce Cd concentrations in the plant by decreasing the efficiency of Cd acquisition by root [41].

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3. Contributions of intercrops in intercropping systems

Intercropping is the cultivation of two or more crop species, or genotypes, in a field simultaneously, which is receiving increasing global interest as an agricultural practice [13]. Intercropping can be one of the ways to achieve “sustainable intensification” by achieving a real increase in yields without increasing inputs or by improving the stability of yields with fewer inputs [42]. For example, cereal/legume intercropping systems can reduce fertilizer inputs and have a positive impact on the environment [19, 43]. In legumes involved in intercropping cultivation, N fixed by legumes can be transferred to companion species [44], thus, the maize/soybean and maize/peanut intercropping systems show yield advantages compared to monocultures [19].

In addition to fixing N by legume, intercropping systems always increase yield and improve grain nutritional quality and ultimately human health, mainly due to intercropping contributing to increased nutrient (P, Fe, and Zn) uptake [45], which is associated with the rhizosphere processes. Intercropping may have a potential facilitating mechanism whereby some crop species can chemically mobilize unavailable forms of one or more limiting soil nutrients, such as P and micronutrients (iron (Fe), zinc (Zn), and manganese (Mn)). The P, Fe, and Zn-mobilizing crop species improve the nutrition of P, Fe, and Zn for themselves and neighboring non-mobilizing species with P, Fe, or Zn by releasing acid phosphatases, protons, and/or carboxylates, chelating substances in the rhizosphere, increasing the concentration of soluble inorganic P, Fe or Zn in the soil [46]. In cereal/legume intercropping, direct interspecific facilitation involves such processes, in which cereals increase Fe and Zn bioavailability while companion legumes benefit [45]. In terms of interspecific promotion, maize improves Fe nutrition in intercropped peanuts, faba beans improve N and P uptake by intercropped maize, and chickpea promotes P uptake by companion wheat [47]. Other intercropping systems, such as wheat/faba bean, which is also efficient in P utilization, but the reasons are not only due to positive interactions of rhizosphere processes but also due to complementary P uptake in the early growth stage [48].

A study of a maize and soybean intercropping system showed that root interactions are important to improve the soil microbiological environment, increase microbial populations and enzyme activities in the soil, and increase crop yields [49]. In addition to root interactions, studies in wheat/maize and wheat/soybean intercropping systems have shown that a positive impact of the border row and inner rows of the intercropped plants and more efficient use of soil nutrients than the monocrops result in both dominant and subordinate species in intercropped crops, which then produce higher yields than the corresponding wheat, maize, or soybean monocrops [47]. Additionally, intercropping improved plant resistance to some pathogens to improve yield. For example, intercropping with maize can provide relief to peppers against both wind-dispersed and soilborne pathogens [50]. Furthermore, intercropping systems largely impacted soil microbial functionalities and mycorrhizal soil infectivity, improving crop productivity [51]. These benefits resulting from intercrop should be closely related to changes recorded in soil microbial functionalities.

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4. Advantages of the intercropping systems with AMF colonization in agriculture

4.1 Roles of AMF in agricultural intercropping system

AMF plays an important role in intercropping systems in two main ways: protecting plant health and improving plant growth and yield. Specifically, it involves the following: regulating the transfer, distribution, and acquisition of resources (e.g., nitrogen and phosphorus); influencing crop interactions; and resisting biotic (plant pathogens) and abiotic stresses (metals, drought) (Figure 1).

Figure 1.

Potential benefits of intercropping systems in symbiosis with arbuscular mycorrhizal fungi (AMF).

AMF play a vital role in optimizing resource use in the agricultural intercropping system, especially in resource-limited soils. Intercropping systems show a growth advantage for intercrop plants over those in monoculture systems [52, 53], while inoculation of AMF in intercropping systems, such as rice/mungbean, further increased the biomass of intercrop (mungbean) [54]. AMF can interconnect different individuals and even different plant species by forming a below-ground mycelial network from their hyphal branches [55, 56]. Such mycorrhizal networks can influence the distribution of nutrients among intercropped crops [57], and feedback in protecting plant health.

In low-input agriculture, AMF-inoculated cereal/legume intercropping typically provides over-yielding. Mycorrhizal networks contribute to the over-yielding in intercropping by improving the nutrient uptake of mycorrhiza-dependent plant species. Fungal hyphal networks AM could transfer nutrients among intercrops, increasing plant P uptake, and when the AMF was absent in intercropping eggplant (Solanum melongena L.) with maize, the expected advantages disappeared [58]. In a maize-grass pea intercropping system, inoculation with AMF resulted in mutual reinforcement of maize and grass pea under low P and low water conditions, but as the availability of resources increased, maize was facilitated, but grass pea had a neutral role or facilitator [59]. In the wheat and faba bean intercropping system, the inoculation of AMF Funneliformis mosseae enhances the complementary resource for intercrops under N and P limiting conditions [60]. In addition, AMF show different responses to different forms of P [Ca10(OH)2(PO4)6 (Ca-P), sodium phytate (Na-P) and KH2PO4 (K-P)] in coix (Coix lacryma-jobi L.)/faba bean (Vicia faba L.) intercropping systems for the intercrops, indicated the differences in the strategies utilized in the forms P of coix and faba bean, which improve intercropping productivity [61]. Except for nutrients, AMF inoculation alleviates the negative effects of drought conditions on finger millet in finger millet/pigeon pea intercropping systems [62].

AMF play an important role in mediating interactions among neighboring plants. In intercropping systems, mycorrhizal networks showed different effects on intraspecific and interspecific interactions. In the presence of AMF, maize and faba bean benefited from mycorrhizal networks and intermingling root systems, but weeds (foxtail) were inhibited by interspecific interactions [63]. AMF can change the competitive relationships between intercrops by modifying plants’ nutritional levels [64]. In the maize/chili pepper intercropping system, AMF form a better symbiotic relationship with maize, which also supply part of photosynthetic C to increase AM fungal propagules in the chili pepper compartment, increasing the competitive capacity of P of pepper against maize and increasing pepper fruit yield [57]. In the faba bean/wheat intercropping system, the colonization of AMF favored the stronger competitor in the mixture (wheat) without negatively affecting the companion species (faba bean), including positive effects on root biomass, specific root length, root density, and uptake of P, Fe, and Zn [17]. Additionally, AMF colonization and AMF species can also affect the competitive relationships between crops and weeds [65]. The colonization of the AM root of tomato was clearly affected by its intercropping partners: The tomato intercropped with leek showed a higher AM colonization rate than intercropped with itself [66].

4.2 Resource transfer between intercrops through CMNs

AMF extend the root surface by more than 10 cm per gram of soil [67], and such mycelial network plays a significant role in mediating the flow of mineral nutrients from the soil to the host plants. These mycelial networks can be supported by several host plants of either the same or even different plant species, thereby forming common mycorrhizal networks (CMN) [68]. The formation of CMN affects the distribution and transfer of resources from a plant to other plants, such as nutrients (N, P, C) [69, 70] and defense signals [71, 72], which may affect plant competitive outcomes and community composition through differential resource allocation. The study has shown that flax acquired 80 and 94% of total N and P by CMN, respectively, while neighboring sorghum (Sorghum bicolor L.) acquired 20 and 6% of N and P by the CMN [73]. N transfer through direct and indirect pathways in cereal/legume intercropping systems [74, 75]. The direct pathway is N fixed in legumes transferred to related cereal plants through CMN, and the indirect pathway is that legume residues and root exudates release N into the rhizosphere, which is then absorbed by the intercropped cereal or mycorrhizal hyphae. In non-mycorrhizal roots, N was only transferred by the root network, while AMF symbiosis can provide a mycorrhizal pathway for N transferred by the hyphae network, which increases contact between plants and contact with roots, increasing N transport [76]. In the faba bean/wheat intercropping system, the AMF symbiosis increased N transfer from the faba bean to wheat by 20% [17].

In addition to N and P, CMN can mediate K trade to benefit individuals in intercropping system, but maybe there exists an asymmetry between intercrops. In the AMF inoculated tomato/potato-onion system, intercropping increased the dry weight of the plant and the K content of tomato, but decreased those of potato-onion, because K transfer between plants has a strong asymmetry: more K was transferred from potato-onion to tomato than from tomato to potato-onion [73]. Reasons for asymmetry in nutrient gains between plants have been studied in the cereal/legume intercropping system. They reveal the asymmetry in nutrient gains by a mixture of millet (Setaria italica L.) and chickpea (Cicer arietinum L.), dependent on which plant species was the donor or receiver: chickpea inoculation increased the acquisition of N and P and the biomass of both chickpea (donor) and millet (receiver), leading to overyielding of the mixture [77]. Therefore, they suggest that the introduction of mycorrhizal networks by legumes in intercropping could be an important factor contributing to the magnitude of the intercropping effect. It’s worth noting that different AMF show different contributions to plant growth and nutrient uptake through CMN. For example, the CMN formed by Funneliformis mosseae was greater than those of F. intraradices [78].

The establishment of CMNs appears to influence intraspecific and interspecific interactions between donor and receiver plants [78]. Mycorrhization decreased the proportion of N transferred from pea to wheat but increased the proportion transferred to flax and chicory, suggesting that AM symbiosis influences the distribution of N, and thus affects competition between neighboring plants of different species [70]. In Arctic tundra, belowground carbon (C) transfer by CMNs is enough to potentially alter plant interactions, increasing the competitive ability and monodominance of dwarf birch (Betula nana L.) [64]. The different plant-plant interactions that result from the symbiosis of AMF will provide different outcomes based on the two processes: the diversity of resources provided by AMF to its host (resource dissimilarity) and different ways of allocating these resources (resource allocation) [79].

4.3 Effects of intercropping on AMF colonization

Intercropping has an impact on the community and the functions of AMF in soils in many aspects (Figure 1). Alter AM fungal diversity. Conventional agricultural practices have been shown to have a negative impact on the abundance and diversity of AM fungi [12], but intercropping has shown the potential to reduce the negative impact. Increased plant diversity can alter the diversity of species of fungi [80]. In intercropping systems, such as maize/soybeans and oat/pea, the AMF diversity was higher in an intercropped system compared to their respective monocropping system [11, 81]. Tree-based intercropping systems support a more abundant and diverse AM fungal community compared to conventionally managed systems [12]. However, some studies intend to show zero or negative significant effects on the fungal community of AMF due to the incorporation of trees into agricultural systems, which may be a function of different cultivation techniques, climatic variation, or various tree-crop combinations used within different tree-based intercropping systems [82, 83, 84]. Furthermore, the amount of growth of fungal species of AMF also depends on the associated host plant species [85, 86]. In intercropping systems, such as the maize/soybean intercropping system, different N applications also change the AMF diversity and community: Glomus_f_Glomeraceae in maize soil and roots increased significantly with increasing N application levels, but decreased with increasing N application levels in soybean soil and roots [18]. In the maize/soybean strip intercropping systems, both N application and the cropping pattern affect the diversity of the AM fungal community, but the N application had a stronger influence than the cropping pattern: Lower N application shows significantly higher diversity and co-occurring species than higher N application [87].

Improve mycorrhizal symbiosis activity. Intercropping can improve AM symbiosis activity among intercrops, such as increasing mycorrhization, including root colonization and spore population in the rhizosphere. In intercropping systems of sorghum/ana tree (Faidherbia albida) and soybean/peacock flower (Albizia gummifera) or broad-leaved croton (Croton macrostachyus), both root colonization and soil sporulation of AMF are increased [88, 89]. Increases in mycorrhizal colonization in intercropped systems consistent with more than two plant species have also been found in groundnuts and sweet potato as intercrops of banana [90], wheat and maize intercropped with faba bean [91]. In the maize/soybean intercropping system, AMF-secreted glomalin-related soil protein (GRSP) concentrations are generally increased in the soil of the rhizosphere of the crop compared to monoculture [81]. Intercropping promotes the release of a wide range of organic compounds that contribute to the activity of the soil microbiota, including AMF, increasing the colonization and species diversity of these fungi [80]. However, the study also finds that AMF colonization of tomato is increased, not changed, or decreased when intercropped with leek, cucumber/basil, and fennel, respectively [66], which indicated a neighbor effect on plant-AM fungal interactions [92].

Perennial plants severed as reservoirs of inoculum in intercropping systems. In the tree-based intercropping system (Agroforestry), perennial trees play a role in maintaining active populations and mycelial networks of AMF [12]. These trees always acted as reservoirs for the AMF inoculum for the intercrops. AMF are always nonspecific in their selection of host [93], and thus the AMF soil habitat could serve as potential inoculants for the implantation of plant species [94]. Alternatively, native AMF which undergo a variety of modifications to survive in their habitats can be isolated and used as potential inoculants for inoculation into plant species of interest [95].

Improvement of disease resistance in host plants in intercropping systems. Continuous monoculture of pepper often leads to increases in soil pathogen populations [96], especially the most economically destructive soilborne diseases. Phytophthora blight causes severe plant disease and thus enormous yield loss [97]. By elevating root mycorrhization, intercropping with maize could suppress pepper Phytophthora blight and increase fruit biomass [98]. However, not all intercropping plants have a positive effect on disease resistance after AMF colonization. With different intercropping partners (leek, cucumber, basil, fennel, or tomato itself), only in tomato/leek and tomato/basil combinations, AMF inoculation reduces the negative effects of F. oxysporum f. sp. lycopersici on tomato biomass [66]. Therefore, the bioprotective effect of AMF resulting in reduced disease severity of F. oxysporum f. sp. lycopersici and/or compensation of plant biomass does not depend on the extent of AM colonization, but more on the intercropping partner [66].

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5. Conclusions

Combining arbuscular mycorrhizal fungi (AMF) and intercropping can improve resource utilization efficiency in the field of sustainable agriculture. In the AMF-colonized intercropping system, the root colonization of one plant by AMF is influenced by its intercrops. Furthermore, different intercropping species can alter the arbuscular mycorrhizal (AM) fungal community. Moreover, the bioprotective effects of AMF depend on the intercropping partner rather than the degree of AM colonization. Thus, in agricultural practice, the application of intercropping in combination with AMF needs to be tested for each intercropping arrangement separately, and the appropriate selection of intercropping partners can be beneficial for each intercrop. Additionally, the characterization of native AMF communities and their application to intercropping systems may be a useful tool for agricultural development.

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (31902104, 32101358), the Yunnan Fundamental Research Projects (202301AT070106), the Double Top University Fund of Yunnan University and the Yunnan Revitalization Talent Support Program.

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Conflict of interest

The authors declare no conflict of interest.

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Statements and declarations

The authors declare that the research was conducted in the absence of commercial or financial relationships that could be construed as a potential conflict of interest.

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Written By

Yunjian Xu and Fang Liu

Submitted: 04 January 2024 Reviewed: 10 January 2024 Published: 01 July 2024

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