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Review

Arbuscular Mycorrhizal Fungi and Microbes Interaction in Rice Mycorrhizosphere

by
Xiaozhe Bao
1,2,
Jixiang Zou
1,2,
Bin Zhang
1,2,*,
Longmei Wu
1,2,
Taotao Yang
1,2 and
Qing Huang
1,2
1
Rice Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China
2
Guangdong Key Laboratory of New Technology in Rice Breeding, Guangzhou 510640, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(6), 1277; https://doi.org/10.3390/agronomy12061277
Submission received: 1 May 2022 / Revised: 22 May 2022 / Accepted: 22 May 2022 / Published: 26 May 2022
Browse Figure
Versions Notes

Abstract

:
Rice (Oryza sativa L.) is the most widely consumed staple crop for approximately half of the world’s population. Many interactions take place in paddy soil, particularly in the rice mycorrhizosphere region. Arbuscular mycorrhizal fungi (AMF) and soil microbe interactions are among the most important and influential processes that occur, as they significantly influence the plant growth and soil structure properties. Their interactions may be of crucial importance to the sustainable, low-input productivity of paddy ecosystems. In this study, we summarize the major groups of microbial communities interacting with arbuscular mycorrhizal fungi in the rice mycorrhizosphere, and discuss the mechanisms involved in these arbuscular mycorrhizal fungi and microbe interactions. We further highlight the potential application of arbuscular mycorrhizal mutualism in paddy fields, which will be helpful for the production of bioinoculants in the future.

1. Introduction

As one of the most important agricultural crops, rice (Oryza sativa L.) feeds more than 50% of the world’s population (https://www.irri.org/, accessed on 25 April 2022). The demand for rice production is growing due to the increasing global population [1]. There are a large number of microorganisms in the rhizosphere that interact with rice roots, playing an important role in crop health and sustainable productivity [2]. Arbuscular mycorrhizal fungi (AMF), belonging to Glomeromycota, are among the most important symbionts of rice plants, as they provide a range of soil nutrients (e.g., P and N) to plants in exchange for plant carbohydrates [3,4]. In addition, AMF can also improve the biotic and abiotic resistance of rice plants [5,6]. Furthermore, the extensive extraradical hyphae produced by AMF in the paddy soil are a habitat for other microbes, including both the microbes in the rhizosphere and the microbes in the cytoplasm of some fungal species [7,8]. However, to date, there is a lack of studies which focus on the interactions between AMF and microbes in the mycorrhizosphere of rice.
In this study, we first introduce the microbial diversity of the rice mycorrhizosphere interacting with AMF, including bacteria, fungi, and other microbes, etc. We then discuss the mechanisms involved in the interactions between rice plants and AMF mutualisms. Finally, we present the potential application of AMF mutualism in paddy fields and provide an outlook on future research priorities. This review has important implications, not only underscoring the diversity of the microbes inhabiting the rice mycorrhizosphere interacting with AMF, but also highlighting the potential application of AMF mutualism for the improvement of rice plant performance.

2. AMF in the Paddy Fields

AMF are one of the most important rhizosphere fungi, colonizing nearly 80% of terrestrial plants [9]. They provide the host with water, nutrients, and pathogen protection in exchange for photosynthetic products [10,11]. Globally, rice production is mostly conducted in wetland ecosystems, characterized by anaerobic environment [1], where AMF find it difficult to survive. Some studies have reported that AMF are rare or absent in the rice roots of flooded paddy fields [12,13], while an increasing number of studies have demonstrated the presence of AMF colonization inside rice roots in paddy fields [14,15,16,17]. The mycorrhizal growth response of rice plants differs, ranging from positive to negative [4,18,19,20,21,22,23,24].
The mycorrhizosphere is defined as the zone influenced by both the root and the mycorrhizal fungus, and includes the more specific term “hyphosphere”, which refers only to the zone surrounding individual fungal hyphae [25,26]. This narrow region is characterized by increased microbial activity stimulated by the leakage and exudation of organic substances from the root and mycorrhiza, which are different from the bulk soil [27,28]. There are different types of microbial functional groups in the rice “mycorrhizosphere” interacting with AMF, which may be involved in plant response variation [29,30]. These microorganisms may directly increase mycorrhizal colonization and the abundance of fungal propagules [31]; meanwhile, rice mycorrhizal response could be influenced indirectly by the change in soil microbial communities caused by agriculture practices [32,33]. In addition, soil pathogens are also involved in AMF and rice interaction. Plant growth response to the soil microbial community is therefore a result of the balance between the negative effects of pathogens and the positive effects of AMF [34,35]. Despite the fact that plants have been interacting with AMF for 450 million years, the functional consequences of AMF integrating with the rice mycorrhizosphere microbes are only just beginning to be appreciated.

3. Major Groups of Bacteria Interacting with AMF

Bacteria populations have been found to be dominant in the rice rhizosphere, exerting a great influence over rice growth and production [36]. Different groups of soil bacteria have been reported to interact with AMF, including plant-growth-promoting bacteria (PGPR), endo-bacteria, mycorrhiza helper bacteria (MHB), and deleterious bacteria (DB), etc. [37,38,39] (Figure 1). Knowledge of such interactions is vital for enhancing the tripartite symbiosis between AMF, bacteria, and host plants.

3.1. PGPR

PGPR are among the most important soil bacteria, as they significantly enhance rice yield and reduce the need for chemical fertilizers [40]. The mechanisms involved include: (1) enhancing the solubility of soil nutrients by producing enzymes and siderophores; (2) producing phytohormones; (3) controlling pathogens and alleviating the adverse effects of stress; and (4) interacting with other soil microbes [41,42,43,44]. A variety of PGPR have been reported to interact with AMF, including Pseudomonas, Bacillus, Azospirillum, Herbaspirillum, Paenibacillus, rhizobia, etc. [41,45,46,47]. In paddy fields, there are several different enhanced combinations of bacterial strains and AMF species that could promote rice growth and development (Table 1). Bacterial strains include Bacillus, Pseudomonas, Azospirillum, and Herbaspirillum, while AMF species include Rhizophagus irregularis (renamed from Glomus intraradices) and Funneliformis mosseae [48,49,50,51]. The abbreviations for AMF and PGPR can be seen in Table 2. Their synergistic stimulating effects include the solubilization of phosphate, nitrogen fixing, rice growth promotion, and the suppression of pathogens [41]. For example, Hoseinzade et al. [52] observed that the interaction of AMF (F. mosseae) with nitrogen-fixing bacteria (Herbaspirillum seropedicae) together with urea (nitrogen source) and triple super phosphate (phosphorus source) fertilizers promoted the growth of rice plants. Norouzinia et al. [51] showed that the co-inoculation of Pseudomonas putida strain S34, Pseudomonas fluorescens strain R167 and R. irregularis alleviated the adverse effects of salinity and significantly increased the grain yield of rice.

3.2. Endo-Bacteria

Some endo-bacteria inside AMF cytoplasms are also regarded as PGPR, establishing an intimate interaction with AMF. The endobacteria of Glomeromycota are the most thoroughly investigated bacterial endosymbionts [58]. Two types of endosymbionts are known in Glomeromycota: (i) a rod-shaped, Gram-negative beta-proteobacterium Candidatus Glomeribacter gigasporarum (CaGg), limited members of the Gigasporaceae family [59]; (ii) a coccoid bacterium displaying a homogeneous Gram-positive-like wall structure, Mollicutes-related endobacteria (Mre), widely distributed across Glomeromycota [60]. It is also well accepted that some actinobacteria are considered potential PGPR [61,62], and evidence obtained from Lasudee et al. [54] showed that Streptomyces thermocarboxydus isolate S3 isolated from spores of F. mosseae promoted the growth of rice plants grown in low-nutritional soil under drought-induced stress (Table 1). The abbreviations for AMF and endo-bacteria can be seen in Table 2. According to Bonfante et al. [63] and Salvioli et al. [64], the mechanisms involved in the endo-bacteria affecting fungal performance are as follows: (1) release of substances, e.g., volatiles, which affects fungal gene expression; (2) production of lectins which attach to the fungal surface; (3) degradation of fungal cell wall; and (4) injection of molecules into the fungal spore.

3.3. MHB

MHB were first identified by Garbaye (1994), and mostly include Proteobacteria such as Pseudomonas, Oxalobacteraceae, Actinomycetes such as Streptomyces, and Firmicutes such as Bacillus [37,65,66]. A number of studies have stated the synergistic effect of AMF and MHB, including some which focused on rice crops. MHB may play an important role in enhancing the activity and development of AMF, providing nutrients to plants and AMF, as well as promoting their defenses [67,68]. For example, the co-inoculation of Azospirillum lipoferum, Bacillus megaterium and AMF increased the growth and grain yield of rice, at the nursery and in the main field, under the System of Rice Intensification (SRI) [50]. There have also been studies that showed the opposite effects of AMF, where the use of two fluorescent Pseudomonas strains (Pseudomonas jessenii R62; Pseudomonas synxantha R81) on rice yields was far less pronounced over two cropping seasons [48] (Table 1). The abbreviations for AMF and MHB can be seen in Table 2. It is reported that MHB are usually fungal-specific but not plant-specific [69], which means that MHB can promote the growth of specific AMF, even if in symbiosis with their non-specific host plant. Therefore, the opposite conclusions above were possibly found because of the use of inappropriate bacterial types and AMF species. Moreover, since there are relatively few studies of AMF and MHB in the rice rhizosphere, the common unresolved issues (such as whether increased AMF growth and survival by MHB are due to the production of growth factors, the detoxification of soil allelochemicals, or the antagonism of competitors and/or parasites) remain unresolved in rice [70].

3.4. DB

DB, which adversely affects plant growth, are also found to be interactive with AMF. Their unfavorable effects on plant growth are probably due to the production of harmful substances such as phytotoxins, competition for food resources with other soil microorganisms, and their inhibitory effects on AM fungal activities [38]. Various mechanisms have been demonstrated to explain biocontrol activity by AMF, including: (1) parasitizing pathogen, (2) higher competition for colonization sites and host photosynthates, (3) secondary metabolites production, (4) the modification of the microbial community, (5) promoting plant nutrient uptake and anatomical changes in the root system, and (6) inducting plant systemic resistance [71,72]. Although some deleterious bacteria reside in the rice rhizosphere, few studies have reported the effect of AMF on the DB control.
Interestingly, PGPR may be detrimental for mycorrhizal colonization, implying the probable existence of ‘functional competition’ between beneficial microorganisms [73,74]. This depends on the mycorrhizosphere conditions, such as AM growth and development, microbial growth stage, and environmental conditions [75]. Such characteristics indicate the importance of the choice of AMF and rhizobacteria used for inoculum production to achieve sustainable agriculture [76,77].

4. Interactions between AMF and Other Fungi

Fungi are another important group in the mycorrhizosphere, playing significant roles in ecosystem function, such as phosphorus (P) solubilization, nitrogen fixation, and the synthesis of indole acetic acid (IAA) for plant growth promotion [78]. In the rice mycorrhizosphere, fungi communities are commonly composed of Penicillium, Aspergillus, Talaromyces, and Trichoderma, etc [2]. Pathogenic fungi can also reside in the rice mycorrhizosphere, interacting with AMF such as Rhizoctonia solani, a phytopathogenic fungus that causes rice sheath blight. AMF could establish direct interaction with other fungi, which could in turn affect rice growth (Table 1, Figure 1). The abbreviations for AMF and other fungi can be seen in Table 2. Baby et al. [55] showed that an increase in AMF spore density and infection decreased the sheath blight disease in rice; however, Bernaola et al. [56] indicated that lesion lengths and susceptibility to sheath blight infection were higher in rice plants colonized by AMF. Different types of fungi can affect the level of symbiotic efficiency between AMF and rice performance. Furthermore, parameters such as microbial growth stage, environmental factors, and AMF growth and development can also affect their interaction. Studies have also shown that pathogenic fungi can interact with AMF through their effects on plant growth [38]. Although there are examples of interaction between AMF and other fungi in other kinds of plants, such as soybean, tomato, Brassica juncea L, Oil Palm, etc., there are relatively few studies concerning AMF and other fungi interaction in the rice mycorrhizosphere.

5. Interactions between AMF and Other Microorganisms

In addition to the rhizobacteria and fungi, AMF also interact with other soil fauna in paddy fields, e.g., protozoa and small nematodes [79,80] (Table 1, Figure 1). The abbreviations for AMF and soil fauna can be seen in Table 2. Although protozoa (18–250 lb/ac live weight) and soil nematodes (10–260 lb/ac live weight) comprise a relatively small part of the soil biomass, they perform essential functions in the soil environment [81]. Protozoa and small nematodes feeding on bacteria and fungi, collectively known as microbial grazers, release plant-available nutrients and suppress disease [82]. Soil protozoa are reported to interact with AMF species, and collembola are among the soil protozoa which interact with soil fungi [83], however this interaction is not detected in paddy fields. In fact there were few studies concerning AMF and protozoa in the paddy fields.
Not all nematodes are beneficial in agricultural soils. About 10% of soil nematodes feed on plant roots, causing root rot or wilting problems [84]. Therefore, AMF not only synergistically interact with soil nematodes, but also play a role in the biocontrol against plant-parasitic nematodes. Studies have reported that F. mossae exhibited suppression of the Meloidogyne graminicola multiplication in rice, while R. irregularis did not [32]. The direct effects of AMF species on the pathogens include competition for limited space or nutrients, and the indirect effects include alteration of plant root morphology and exudation, as well as induced plant systemic resistance. The detailed mechanisms involved in AMF against pathogens will be described below, either directly or indirectly. However, although AMF are one of the most important components of the soil ecosystem and large numbers of soil fauna are found in the paddy fields, little is known about the interactions between AMF species, and thus further research should pay more attention to this aspect.
Interestingly, AMF could also cooperate with Cyanobacteria (blue-green algae) (Table 1, Figure 1). The abbreviations for AMF and BGA can be seen in Table 2. BGA are the main components of the microbial community in rice paddy fields, contributing to the fertility of agricultural ecosystems [85]. Their beneficial effects on the crop growth, yield, and nitrogen fixation of such ecosystems have been reported [86]. Rice may respond favorably to the combined application of BGA, AMF, and N fertilizer, such as through improvements in grain yield, straw yield, nutrient availability, soil structure, and alkali soil reclamation. The combined effect of biological N2 fixation by BGA and the plant growth regulators produced by AMF resulted in increased grain and straw yield [72].

6. AMF and Soil Microbial Community

It is universally acknowledged that soil microorganisms efficiently participate in the decomposition of organic materials and indirectly affect the nutrient cycling and pathogen resistance of plants [87]. In paddy soil, AMF and soil microbial communities could affect each other, and thus influence the efficiency of soil production and increase rice yield (Table 1, Figure 1). Interactions between AMF and soil microorganisms may be inhibitory or stimulatory, as described by Fitter and Garbaye [88] and Ye et al. [89]. The relationship may be positive when AMF cooperate with PGPR and MHB, while the effect is adverse when AMF interact with soil-borne pathogens such as parasitic nematodes. AMF can positively affect the microbial communities through the following: (1) supplying C compounds via hyphae, (2) stimulating root growth, (3) changing root exudates, and (4) producing glomalin and hence improving soil structure [90,91]. Accordingly, soil microbial communities can exert positive effects on AMF by: (1) producing plant hormones, (2) improving the bioavailability of soil nutrients, (3) affecting the germination of fungal propagules and fungal growth, and (4) affecting plant growth [92,93]. Their adverse effects are probably due to: (1) competing for nutrients, (2) reducing plant growth, and (3) producing unfavorable chemicals [76,94]. As AMF and soil microbes play important roles in affecting soil properties and plant growth, understanding such interactions is of great significance from a sustainable perspective.

7. Mechanisms Involved in Interactions between AMF and Other Soil Microbes

The co-inoculation of AMF and other soil microbes allows plants, including rice, to improve the absorption of nutrients such as nitrogen, phosphorus, and other macro and micro-nutrients, as well as to enhance system resistance [53,95,96,97,98]. It is well known that nutritional exchange is a cornerstone for the above-ground plant and below-ground microorganism interactions [99]. Carbon metabolites secreted by rice roots promote the growth and activity of microbes residing in the rhizosphere [100,101,102]. In return, the microbes benefit the plants by supplying nutrients and plant hormones and enhancing tolerance to biotic (e.g., phytopathogens) and abiotic stress (e.g., drought, salt, heat, and frost) [103,104]. Nutritional exchange does not only exist in the interactions between rice plants and AMF mutualism, but also in those between AMF and microbes (although the amount of carbon metabolite produced by AMF hyphae is small relative to the rhizosphere) [105]. AMF can transfer plant-derived carbon compounds through the extensive extraradical hyphae to the attached soil and then provide them to soil microbes. At the same time, microbes residing in the soil transfer mineral nutrients back to AMF. These tripartite symbiosis of rice plants, AMF, and microbes are essential for the ecological function of paddy ecosystems.
Rice plants can exude a wide range of root exudates into the rhizosphere that attract and sustain microorganisms, establishing mutualistic associations, meanwhile improving soil structure and controlling plant pathogens in soil [106,107]. The compounds originate from photosynthates, and mainly include organic acids, amino acids, polysaccharides, hormones, and other primary and/or secondary metabolites [108]. Among these, strigolactones (SLs) serve as important bioactive molecules, stimulating the branching and metabolism of pre-symbiotic hyphae in AMF [109]. At the same time, SLs also influence the growth of several plant pathogens [110]. Flavonoids also play a significant role in AMF spore germination, hyphal growth, differentiation, and root colonization in AMF–plant interactions, as well as in promoting the growth of host-specific rhizobia by serving as chemoattractants [111].
Microbes can produce a series of signaling molecules that can promote rice growth and AMF organic nutrient utilization, such as phytohormones, volatile organic compounds (VOCs), 1-aminocyclopropane-1-carboxylate deaminase (ACCD), and polysaccharides. Some microbes can synthesize phytohormones (e.g., auxin (IAA), cytokinin (CTK), jasmonic acid (JA), and abscisic acid (ABA)), which will be beneficial for plant growth and pathogens control [112,113]. Some are able to produce extracellular enzymes such as cellulases, chitinases, β-1-3 glucanases, lipases, and proteases, which can hydrolyze a wide variety of cell wall compounds, including cellulose, chitin, hemicellulose, and protein [114,115]. Soil microorganisms can also enhance plant growth and protect plants from environmental stress through the synthesis of ethylene production inhibitors, e.g., ACC and rhizobitoxine; [116], VOCs [117]; and polysaccharides, e.g., exopolysaccharides and extracellular polymeric substances (EPSs) [118]. Furthermore, a number of microbial-mediated processes, pathways, and proteins are related to the establishment of associative symbiosis and colonization. Quorum sensing (QS) is a bacterial cell-to-cell communication mechanism whereby bacterial population density is controlled by diffusible signaling molecules produced by individual bacterial cells [119]. N-acyl-L-homoserine lactones (AHLs) are the essential components of this communication system [120]. The microbial chemotaxis toward particular root-exuded compounds is an important trait for the plant-driven selection of microbes and their colonization. The diversity of microbe-associated molecular patterns (MAMPs) evades the recognition of plant immune responses and helps microbes form endophytic microbial communities in plants [121]. Eukaryotic-like plants resembling plant-associated and root-associated domains (PREPARADOs) could evade MAMP-triggered immunity by binding to extracellular MAMP molecules, thus acting as decoys to circumvent plant defenses and gain entry into plant tissues [121]. For PGPRs, their adherence to AMF is determined by the formation of biofilms, which exist as a sheet of bacterial cells in association with AMF structures, embedded within a self-produced exopolysaccharide matrix [65]. In addition, the bacterium could increase the fungal sporulation success, raise the fungal bioenergetic capacity, increase ATP production, elicit mechanisms to detoxify reactive oxygen species, and prime mitochondrial metabolic pathways to improve AMF ecological fitness [122]. Interestingly, AMF lack the ability to secrete phosphatases, which means that they cannot utilize organic nutrients directly, rather, their organic nutrients mainly come from mineralization driven by soil microbes [122]. The compounds produced by microbes will enhance the attachment of microbes to mycorrhizal roots and AMF structures and is also important for the effective production of microbial inoculums.
In conclusion, the synergetic microorganisms that reside in the rhizosphere assist plants in many ways, including the mobilization, immobilization, and weathering of minerals [123]; the degradation of recalcitrant organic matter [124]; preventing pathogens [125]; modulating host immunity through mycorrhiza-induced resistance (MIR) and induced systemic resistance (ISR) [126,127,128]; and enhancing host abiotic stress resistance by regulating osmoregulation substance and active oxygen metabolism [49,51].

8. Potential Application of AMF Mutualism in Paddy Fields

The practical aspects of microbial consortia in the field have been attracting attention for a long time. At present, there is a patented commercial product named ‘Micosat F’ (MF) which contains a mixture of AMF (Glomus coronatum, Glomus caledonium, R. irregularis, F. mosseae, Glomus viscosum) and helper bacteria (Pseudomonas spp., Bacillus spp., actinobacteria Streptomyces spp., and the saprophytic fungi Trichoderma spp.) [127]. The application of beneficial microbes in crop production has been suggested as a cornerstone for the next “Green Revolution” in agriculture [129]. Recent advances have shown that microbial consortia containing mycorrhizal inoculant are effective [130,131]. Microbial consortia showed increased growth and yield of rice compared to the control [132,133]. The interaction effect of consortium of Azospirillum, PSB, and AMF fungus could reduce levels of N and P fertilizers in the growth of directly seeded rice [134]. Improved soil structure is also another benefit resulting from the presence of AMF in the soil [92]. Moreover, the use of microbial consortia in agriculture could alleviate different soil stresses including salinity, drought, acidity, compaction, and heavy metals [135], but the actual and specific mechanisms for this need to be investigated further. Some studies have also shown that Bacillus subtilis UTSP40 was the most effective isolate against Magnaporthe oryzae FR1, but the presence of R. irregularis significantly reduced the biocontrol potential of B. subtilis UTSP40 [136]. Certainly, microbial consortia do not always have a positive effect on rice growth and an inappropriate combination is likely to inhibit rice performance. Therefore, the identification of appropriate combinations of PGPR and AMF is vital for microbial development and the optimization of supportable agriculture systems.
There are several different factors affecting AM mutualism functioning in the paddy field including AM species, microbe strains, soil tillage, chemical fertilization, biocides, and climate properties [115]. Soil modifications due to soil tillage, chemical fertilization, biocides, etc., are regarded as the adverse factors influencing microbial consortia function. Organic farming may be a useful alternative to alleviate the unfavorable effects of the above-mentioned practices on AMF symbiosis in the field. Therefore, the selection of appropriate agricultural practices is vitally important for the enhanced efficiency of microbial consortia in the field [38,137].

9. Conclusions and Future Prospects

AMF and rice mycorrhizosphere microbe interactions are among the most important and influential processes significantly influencing rice growth and soil structure properties. There are many groups of microbial communities interacting with arbuscular mycorrhizal fungi in the rice mycorrhizosphere, including bacteria, fungi, faunas, and other microbes, etc. Nutritional exchange is vitally important for the tripartite symbiosis of rice plants, AMF, and other microbes. The compounds exuded from rice root (e.g., organic acids, amino acids, polysaccharides, and hormones) and microbes (e.g., VOCs, ACCD, and polysaccharides) can also sustain the symbiotic relationships among rice plants, AMF, and soil microorganisms. Furthermore, a number of microbial-mediated processes, pathways, and proteins are related to the establishment of associative symbiosis and colonization. Although some kinds of microbial consortia containing mycorrhizal inoculants are applied in crop production, we are only at the beginning of understanding the complexity of the interaction between AMF and microbes in the rice mycorrhizosphere. We recommend that, in the future, attention should be paid to the following issues:
(1) Because of the limitation in isolating microorganisms through conventional cultivation methods (such as the isolation of soil archaea), studies concerning the interactions between AMF and these kinds of microorganisms are still rare. Therefore, the application of metaproteomic and metagenomic techniques with higher resolutions and broader coverage to investigate the rice rhizosphere microbiome will be a useful tool.
(2) It is important to determine the most efficient microbe population, in association with AMF, which will then maximize the benefits of the co-inoculation.
(3) Although some research has been carried out on the interactive activities between AMF and soil microorganisms in rice, more research should be concentrated on the mechanisms involved in the interactions between AMF and other soil microorganisms.

Author Contributions

Writing—original draft preparation, X.B.; writing—review and editing, B.Z.; validation, J.Z., L.W., T.Y. and Q.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (grant number 32101827); Natural Science Foundation of Guangdong Province, China (grant number 2022A1515010822); special fund for scientific innovation strategy-construction of high level Academy of Agriculture Science (grant number R2019YJ-YB2002); key project of The Rice Research Institute of Guangdong Academy of Agricultural Sciences (grant number 2021YG03); the Key-Area Research and Development Program of Guangdong Province (grant number 2020B0202010006); and Guangdong Provincial Key Laboratory of New Technology in Rice Breeding (grant number 2020B1212060047).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the writing of the manuscript or in the decision to publish it.

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Agronomy 12 01277 g001 550
Figure 1. Schematic view of interactions between AMF and different components of the mycorrhizosphere.
Figure 1. Schematic view of interactions between AMF and different components of the mycorrhizosphere.
Agronomy 12 01277 g001
Table
Table 1. List of major microorganisms interacting with AMF in rice mycorrhizosphere.
Table 1. List of major microorganisms interacting with AMF in rice mycorrhizosphere.
Type of MicroorganismsMicrobe SpeciesAMF SpeciesEffectsReference
BacteriaA. Lipoferum,
B. megaterium		Glomus sp., Gigasporasp sp. and Acaulospora sp.Rice growth↑,
grain yield↑		[50]
A. brasilense,
B. cepacia		F. mosseaeRice growth↑,
grain yield↑,
P uptake↑		[53]
H. seropedicaeF. mosseaeRice growth↑[52]
P. fluorescens, P. putidaR. irregularisGrain yield↑, salinity↓[51]
P. jessenii, P. synxanthaA natural AMF consortium (Mnat) and a single-spore AMF strain (Mss2)No change[48]
S. thermocarboxydusF. mosseaeRice growth↑[54]
FungiR. solaniR. fasciculatum,
F. mosseae,
G. aggregatum,
G. fulvum,
G. candida, and
G. gigantea		AMF spore density and infection↑,
sheath blight↓		[55]
R. irregularis,
F. mosseae,
G. deserticola,
R. fasciculatum,
S. dussii, and
G. microaggregatum		Sheath blight↑[56]
Soil faunas and other microbesM. graminicolaR. irregularis,
F. mossae		F. mossae decreased
M. graminicola multiplication, while
R. irregularis did not		[32]
Blue-Green AlgaeG. microcarpiumRice growth↑,
grain yield↑		[57]
Table
Table 2. List of abbreviations for AMF and other microorganisms.
Table 2. List of abbreviations for AMF and other microorganisms.
Type of MicroorganismsFull NameAbbreviations
AMFRhizophagus irregularisR. irregularis
Funneliformis mosseaeF. mosseae
Gigaspora candidaG. candida
Glomus aggregatumG. aggregatum
Glomus caledoniumG. caledonium
Glomus coronatumG. coronatum
Glomus deserticolaG. deserticola
Glomus fulvumG. fulvum
Gigaspora giganteaG. gigantea
Glomus microaggregatumG. microaggregatum
Glomus viscosumG. viscosum
Rhizophagus fasciculatumR. fasciculatum
Sclerocystis dussiiS.dussii
BacteriaAzospirillum brasilenseBrasilense
Azospirillum lipoferumA. lipoferum
Bacillus megateriumB. megaterium
Bacillus subtilisB. subtilis
Burkholderia cepaciaB. cepacia
Herbaspirillum seropedicaeH. seropedicae
Pseudomonas fluorescensP. fluorescens
Pseudomonas jesseniiP. jessenii
Pseudomonas putidaP. putida
Pseudomonas synxanthaP. synxantha
Streptomyces thermocarboxydusS. thermocarboxydus
FungiRhizoctonia solaniR. solani
Magnaporthe oryzaeM. oryzae
Soil faunaMeloidogyne graminicolaM. graminicola
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Bao, X.; Zou, J.; Zhang, B.; Wu, L.; Yang, T.; Huang, Q. Arbuscular Mycorrhizal Fungi and Microbes Interaction in Rice Mycorrhizosphere. Agronomy 2022, 12, 1277. https://doi.org/10.3390/agronomy12061277

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Bao X, Zou J, Zhang B, Wu L, Yang T, Huang Q. Arbuscular Mycorrhizal Fungi and Microbes Interaction in Rice Mycorrhizosphere. Agronomy. 2022; 12(6):1277. https://doi.org/10.3390/agronomy12061277

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Bao, Xiaozhe, Jixiang Zou, Bin Zhang, Longmei Wu, Taotao Yang, and Qing Huang. 2022. "Arbuscular Mycorrhizal Fungi and Microbes Interaction in Rice Mycorrhizosphere" Agronomy 12, no. 6: 1277. https://doi.org/10.3390/agronomy12061277

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