Contributions of arbuscular mycorrhizas to soil biological fertility

David D. Douds, Nancy Johnson

Research output: Chapter in Book/Report/Conference proceedingChapter

14 Citations (Scopus)

Abstract

Mycorrhizas are ubiquitous plant-fungal associations that are important components of soil fertility (Table 1). Roots of most crops are normally inhabited by arbuscular mycorrhizal (AM) fungi. These Zygomycota in the order Glomales, function at the interface between plants and soils by greatly expanding the area from which plants can gather soil resources. Extensive networks of as much as 160 m of AM hyphae per g of soil (Degens et al. 1994) function as conduits for nutrient uptake. Crops with coarse root systems generally benefit greatly from AM associations, while mycorrhizal benefits in crops with more fibrous root systems tend to be determined by soil mineral availability (Baylis 1975, Hetrick et al. 1992). Only a few crops, such as lupines and members of the Brassicaceae and Chenopodiaceae, do not regularly form AM associations. In addition to their direct effects on nutrient uptake, AM fungi also contribute to soil fertility by enhancing soil structure and protecting crops from root pathogens. AM fungi form structures inside (intraradical) and outside (extraradical) the host root. After an infective soil borne hypha contacts a host root, it forms an appressorium, penetrates the epidermis, and grows in the space between the cells into the root cortex. Once in the cortex, the intraradical hyphae penetrate the cells and produce arbuscules. These highly branched structures are surrounded by the host cells' membranes and are thought to be where nutrients are exchanged between the partners: i.e. glucose from host to fungus and phosphorus (P) from fungus to host (Blee and Anderson 1998). Once the source of carbohydrate nourishment is secured, the extraradical hyphae can proliferate in the soil. New spores are produced typically on hyphae in the soil in response to achievement of a critical amount of root length colonised, senescence of the host, or other factors. There are clear differences in the effectiveness of AM fungal species to improve soil fertility (Abbott and Robson 1982, 1985, Graham and Abbott 2000), and these differences are likely to be related to differences in allocation to intraradical and extraradical structures (Abbott and Gazey 1994, Dodd et al. 2000). (table presented) The partnership between plants and AM fungi has a long history. Fossil and molecular evidence indicates that AM fungi were associated with the earliest land plants, and that the symbiosis evolved concurrently with the evolution of roots (Malloch et al. 1980, Stubblefield et al. 1987, Simon et al. 1993, Redecker et al. 2000). The intimacy of this association is reflected in the fact that Glomalean fungi are obligate biotrophs that have not yet been successfully cultured in the absence of root tissues. Although the Glomales are asexual and include fewer than 160 species (INVAM 2001), a surprising level of genetic diversity is maintained within populations of these fungi (Hijri et al. 1999, Hosny et al. 1999). Sanders (1999) suggested that, in genetic terms, an individual aseptate AM fungus is actually a population of discrete nuclei. This genetic variance within taxa corroborates physiological variance between geographic isolates of the same species. For example, Bethlenfalvay et al. (1989) found that Glomus mosseae isolated from an arid site improved the photosynthetic water use efficiency of soybean more than G. mosseae isolated from a mesic site. Other studies also have shown that different isolates of the same species can elicit different plant responses under identical conditions (e.g. Stahl and Smith 1984, Stahl and Christensen 1990, Sylvia et al. 1993-a). Mycorrhizal function is strongly influenced by the soil environment, particularly those factors that control mineral fertility (Abbott and Robson 1982). Generally, mycorrhizal benefits are greater in phosphorus-poor soils than in phosphorus-rich ones (Koide 1991). Furthermore, crop species and even different cultivars of the same species interact with AM fungi differently (Hetrick et al. 1993, Hetrick et al. 1996). It is useful to envision mycorrhizas as dynamic systems controlled by interactions among plants, fungi, soil microbes, and soil properties. Bethlenfalvay and Sch üepp (1994) suggested that sustainable agroecosystems require management to generate a stable community of soil biota that functions effectively with abiotic conditions to maximise crop productivity and minimise inputs and soil erosion. Cultural practices have been shown to influence the species composition of AM fungal communities (see below). Certain taxa increase in abundance in agricultural systems relative to other taxa. Furthermore, species diversity of AM fungi is consistently lower in agricultural systems than in nearby natural areas (Sieverding 1990, Helgason et al. 1998-b). The consequences of this on crop production have not yet been carefully studied. Sieverding (1990) suggested that a few well selected AM fungi could increase yields if they are the best mutualists. Alternatively, if the proliferating fungi are simply the most aggressive colonists, and not the best at improving nutrient uptake, pathogen resistance, or soil structure, then this agriculture-induced reduction in diversity is cause for concern. The potential for agricultural management of mycorrhizas to reduce reliance on inorganic fertilisers and develop more sustainable agricultural systems has long been recognised and has already been reviewed (e.g. Sanders et al. 1975, Azcon-Aguilar et al. 1979, Bethlenfalvay and Linderman 1992, Pfleger and Linderman 1994, Gianinazzi and Sch üepp 1994). But, "promises of the applied value of AM fungi in agriculture, forestry and horticulture have been more rhetorical than deliverable" (Miller and Jastrow 1992). A much better understanding of the ecological and evolutionary mechanisms responsible for generating positive, neutral or negative mycorrhizal functioning in field environments is necessary before mycorrhizas can be effectively managed to maximise their contribution to soil fertility in sustainable systems. This chapter has a twofold emphasis. First, it describes the fundamental ways in which AM fungi contribute to the biological fertility of the soil (Table 1). We discuss how AM fungi directly affect plant growth and soil structure and how their interactions with other soil organisms indirectly affect crop yields and nutrient cycling. We will see that these are not independent effects and that feedbacks between plants, fungi, and biotic and abiotic soil properties ultimately determine mycorrhizal effects on plant growth. Second, we discuss how agricultural management practices affect indigenous communities of these fungi. We show that management practices positively and negatively affect AM fungi, and that these have ramifications upon plant growth. Throughout we will point out key topics where further research is needed.

Original languageEnglish (US)
Title of host publicationSoil Biological Fertility: A Key to Sustainable Land Use in Agriculture
PublisherSpringer Netherlands
Pages129-162
Number of pages34
ISBN (Print)9781402066184
DOIs
StatePublished - 2007

Fingerprint

fertility
fungus
soil
crop
soil fertility
nutrient uptake
soil structure
farming system
agricultural management
phosphorus
root system
management practice
soil property
pathogen
agriculture
plant and fungus
soil biota
horticulture
mineral
senescence

ASJC Scopus subject areas

  • Environmental Science(all)
  • Earth and Planetary Sciences(all)

Cite this

Douds, D. D., & Johnson, N. (2007). Contributions of arbuscular mycorrhizas to soil biological fertility. In Soil Biological Fertility: A Key to Sustainable Land Use in Agriculture (pp. 129-162). Springer Netherlands. https://doi.org/10.1007/978-1-4020-6619-1_7

Contributions of arbuscular mycorrhizas to soil biological fertility. / Douds, David D.; Johnson, Nancy.

Soil Biological Fertility: A Key to Sustainable Land Use in Agriculture. Springer Netherlands, 2007. p. 129-162.

Research output: Chapter in Book/Report/Conference proceedingChapter

Douds, DD & Johnson, N 2007, Contributions of arbuscular mycorrhizas to soil biological fertility. in Soil Biological Fertility: A Key to Sustainable Land Use in Agriculture. Springer Netherlands, pp. 129-162. https://doi.org/10.1007/978-1-4020-6619-1_7
Douds DD, Johnson N. Contributions of arbuscular mycorrhizas to soil biological fertility. In Soil Biological Fertility: A Key to Sustainable Land Use in Agriculture. Springer Netherlands. 2007. p. 129-162 https://doi.org/10.1007/978-1-4020-6619-1_7
Douds, David D. ; Johnson, Nancy. / Contributions of arbuscular mycorrhizas to soil biological fertility. Soil Biological Fertility: A Key to Sustainable Land Use in Agriculture. Springer Netherlands, 2007. pp. 129-162
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abstract = "Mycorrhizas are ubiquitous plant-fungal associations that are important components of soil fertility (Table 1). Roots of most crops are normally inhabited by arbuscular mycorrhizal (AM) fungi. These Zygomycota in the order Glomales, function at the interface between plants and soils by greatly expanding the area from which plants can gather soil resources. Extensive networks of as much as 160 m of AM hyphae per g of soil (Degens et al. 1994) function as conduits for nutrient uptake. Crops with coarse root systems generally benefit greatly from AM associations, while mycorrhizal benefits in crops with more fibrous root systems tend to be determined by soil mineral availability (Baylis 1975, Hetrick et al. 1992). Only a few crops, such as lupines and members of the Brassicaceae and Chenopodiaceae, do not regularly form AM associations. In addition to their direct effects on nutrient uptake, AM fungi also contribute to soil fertility by enhancing soil structure and protecting crops from root pathogens. AM fungi form structures inside (intraradical) and outside (extraradical) the host root. After an infective soil borne hypha contacts a host root, it forms an appressorium, penetrates the epidermis, and grows in the space between the cells into the root cortex. Once in the cortex, the intraradical hyphae penetrate the cells and produce arbuscules. These highly branched structures are surrounded by the host cells' membranes and are thought to be where nutrients are exchanged between the partners: i.e. glucose from host to fungus and phosphorus (P) from fungus to host (Blee and Anderson 1998). Once the source of carbohydrate nourishment is secured, the extraradical hyphae can proliferate in the soil. New spores are produced typically on hyphae in the soil in response to achievement of a critical amount of root length colonised, senescence of the host, or other factors. There are clear differences in the effectiveness of AM fungal species to improve soil fertility (Abbott and Robson 1982, 1985, Graham and Abbott 2000), and these differences are likely to be related to differences in allocation to intraradical and extraradical structures (Abbott and Gazey 1994, Dodd et al. 2000). (table presented) The partnership between plants and AM fungi has a long history. Fossil and molecular evidence indicates that AM fungi were associated with the earliest land plants, and that the symbiosis evolved concurrently with the evolution of roots (Malloch et al. 1980, Stubblefield et al. 1987, Simon et al. 1993, Redecker et al. 2000). The intimacy of this association is reflected in the fact that Glomalean fungi are obligate biotrophs that have not yet been successfully cultured in the absence of root tissues. Although the Glomales are asexual and include fewer than 160 species (INVAM 2001), a surprising level of genetic diversity is maintained within populations of these fungi (Hijri et al. 1999, Hosny et al. 1999). Sanders (1999) suggested that, in genetic terms, an individual aseptate AM fungus is actually a population of discrete nuclei. This genetic variance within taxa corroborates physiological variance between geographic isolates of the same species. For example, Bethlenfalvay et al. (1989) found that Glomus mosseae isolated from an arid site improved the photosynthetic water use efficiency of soybean more than G. mosseae isolated from a mesic site. Other studies also have shown that different isolates of the same species can elicit different plant responses under identical conditions (e.g. Stahl and Smith 1984, Stahl and Christensen 1990, Sylvia et al. 1993-a). Mycorrhizal function is strongly influenced by the soil environment, particularly those factors that control mineral fertility (Abbott and Robson 1982). Generally, mycorrhizal benefits are greater in phosphorus-poor soils than in phosphorus-rich ones (Koide 1991). Furthermore, crop species and even different cultivars of the same species interact with AM fungi differently (Hetrick et al. 1993, Hetrick et al. 1996). It is useful to envision mycorrhizas as dynamic systems controlled by interactions among plants, fungi, soil microbes, and soil properties. Bethlenfalvay and Sch {\"u}epp (1994) suggested that sustainable agroecosystems require management to generate a stable community of soil biota that functions effectively with abiotic conditions to maximise crop productivity and minimise inputs and soil erosion. Cultural practices have been shown to influence the species composition of AM fungal communities (see below). Certain taxa increase in abundance in agricultural systems relative to other taxa. Furthermore, species diversity of AM fungi is consistently lower in agricultural systems than in nearby natural areas (Sieverding 1990, Helgason et al. 1998-b). The consequences of this on crop production have not yet been carefully studied. Sieverding (1990) suggested that a few well selected AM fungi could increase yields if they are the best mutualists. Alternatively, if the proliferating fungi are simply the most aggressive colonists, and not the best at improving nutrient uptake, pathogen resistance, or soil structure, then this agriculture-induced reduction in diversity is cause for concern. The potential for agricultural management of mycorrhizas to reduce reliance on inorganic fertilisers and develop more sustainable agricultural systems has long been recognised and has already been reviewed (e.g. Sanders et al. 1975, Azcon-Aguilar et al. 1979, Bethlenfalvay and Linderman 1992, Pfleger and Linderman 1994, Gianinazzi and Sch {\"u}epp 1994). But, {"}promises of the applied value of AM fungi in agriculture, forestry and horticulture have been more rhetorical than deliverable{"} (Miller and Jastrow 1992). A much better understanding of the ecological and evolutionary mechanisms responsible for generating positive, neutral or negative mycorrhizal functioning in field environments is necessary before mycorrhizas can be effectively managed to maximise their contribution to soil fertility in sustainable systems. This chapter has a twofold emphasis. First, it describes the fundamental ways in which AM fungi contribute to the biological fertility of the soil (Table 1). We discuss how AM fungi directly affect plant growth and soil structure and how their interactions with other soil organisms indirectly affect crop yields and nutrient cycling. We will see that these are not independent effects and that feedbacks between plants, fungi, and biotic and abiotic soil properties ultimately determine mycorrhizal effects on plant growth. Second, we discuss how agricultural management practices affect indigenous communities of these fungi. We show that management practices positively and negatively affect AM fungi, and that these have ramifications upon plant growth. Throughout we will point out key topics where further research is needed.",
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N2 - Mycorrhizas are ubiquitous plant-fungal associations that are important components of soil fertility (Table 1). Roots of most crops are normally inhabited by arbuscular mycorrhizal (AM) fungi. These Zygomycota in the order Glomales, function at the interface between plants and soils by greatly expanding the area from which plants can gather soil resources. Extensive networks of as much as 160 m of AM hyphae per g of soil (Degens et al. 1994) function as conduits for nutrient uptake. Crops with coarse root systems generally benefit greatly from AM associations, while mycorrhizal benefits in crops with more fibrous root systems tend to be determined by soil mineral availability (Baylis 1975, Hetrick et al. 1992). Only a few crops, such as lupines and members of the Brassicaceae and Chenopodiaceae, do not regularly form AM associations. In addition to their direct effects on nutrient uptake, AM fungi also contribute to soil fertility by enhancing soil structure and protecting crops from root pathogens. AM fungi form structures inside (intraradical) and outside (extraradical) the host root. After an infective soil borne hypha contacts a host root, it forms an appressorium, penetrates the epidermis, and grows in the space between the cells into the root cortex. Once in the cortex, the intraradical hyphae penetrate the cells and produce arbuscules. These highly branched structures are surrounded by the host cells' membranes and are thought to be where nutrients are exchanged between the partners: i.e. glucose from host to fungus and phosphorus (P) from fungus to host (Blee and Anderson 1998). Once the source of carbohydrate nourishment is secured, the extraradical hyphae can proliferate in the soil. New spores are produced typically on hyphae in the soil in response to achievement of a critical amount of root length colonised, senescence of the host, or other factors. There are clear differences in the effectiveness of AM fungal species to improve soil fertility (Abbott and Robson 1982, 1985, Graham and Abbott 2000), and these differences are likely to be related to differences in allocation to intraradical and extraradical structures (Abbott and Gazey 1994, Dodd et al. 2000). (table presented) The partnership between plants and AM fungi has a long history. Fossil and molecular evidence indicates that AM fungi were associated with the earliest land plants, and that the symbiosis evolved concurrently with the evolution of roots (Malloch et al. 1980, Stubblefield et al. 1987, Simon et al. 1993, Redecker et al. 2000). The intimacy of this association is reflected in the fact that Glomalean fungi are obligate biotrophs that have not yet been successfully cultured in the absence of root tissues. Although the Glomales are asexual and include fewer than 160 species (INVAM 2001), a surprising level of genetic diversity is maintained within populations of these fungi (Hijri et al. 1999, Hosny et al. 1999). Sanders (1999) suggested that, in genetic terms, an individual aseptate AM fungus is actually a population of discrete nuclei. This genetic variance within taxa corroborates physiological variance between geographic isolates of the same species. For example, Bethlenfalvay et al. (1989) found that Glomus mosseae isolated from an arid site improved the photosynthetic water use efficiency of soybean more than G. mosseae isolated from a mesic site. Other studies also have shown that different isolates of the same species can elicit different plant responses under identical conditions (e.g. Stahl and Smith 1984, Stahl and Christensen 1990, Sylvia et al. 1993-a). Mycorrhizal function is strongly influenced by the soil environment, particularly those factors that control mineral fertility (Abbott and Robson 1982). Generally, mycorrhizal benefits are greater in phosphorus-poor soils than in phosphorus-rich ones (Koide 1991). Furthermore, crop species and even different cultivars of the same species interact with AM fungi differently (Hetrick et al. 1993, Hetrick et al. 1996). It is useful to envision mycorrhizas as dynamic systems controlled by interactions among plants, fungi, soil microbes, and soil properties. Bethlenfalvay and Sch üepp (1994) suggested that sustainable agroecosystems require management to generate a stable community of soil biota that functions effectively with abiotic conditions to maximise crop productivity and minimise inputs and soil erosion. Cultural practices have been shown to influence the species composition of AM fungal communities (see below). Certain taxa increase in abundance in agricultural systems relative to other taxa. Furthermore, species diversity of AM fungi is consistently lower in agricultural systems than in nearby natural areas (Sieverding 1990, Helgason et al. 1998-b). The consequences of this on crop production have not yet been carefully studied. Sieverding (1990) suggested that a few well selected AM fungi could increase yields if they are the best mutualists. Alternatively, if the proliferating fungi are simply the most aggressive colonists, and not the best at improving nutrient uptake, pathogen resistance, or soil structure, then this agriculture-induced reduction in diversity is cause for concern. The potential for agricultural management of mycorrhizas to reduce reliance on inorganic fertilisers and develop more sustainable agricultural systems has long been recognised and has already been reviewed (e.g. Sanders et al. 1975, Azcon-Aguilar et al. 1979, Bethlenfalvay and Linderman 1992, Pfleger and Linderman 1994, Gianinazzi and Sch üepp 1994). But, "promises of the applied value of AM fungi in agriculture, forestry and horticulture have been more rhetorical than deliverable" (Miller and Jastrow 1992). A much better understanding of the ecological and evolutionary mechanisms responsible for generating positive, neutral or negative mycorrhizal functioning in field environments is necessary before mycorrhizas can be effectively managed to maximise their contribution to soil fertility in sustainable systems. This chapter has a twofold emphasis. First, it describes the fundamental ways in which AM fungi contribute to the biological fertility of the soil (Table 1). We discuss how AM fungi directly affect plant growth and soil structure and how their interactions with other soil organisms indirectly affect crop yields and nutrient cycling. We will see that these are not independent effects and that feedbacks between plants, fungi, and biotic and abiotic soil properties ultimately determine mycorrhizal effects on plant growth. Second, we discuss how agricultural management practices affect indigenous communities of these fungi. We show that management practices positively and negatively affect AM fungi, and that these have ramifications upon plant growth. Throughout we will point out key topics where further research is needed.

AB - Mycorrhizas are ubiquitous plant-fungal associations that are important components of soil fertility (Table 1). Roots of most crops are normally inhabited by arbuscular mycorrhizal (AM) fungi. These Zygomycota in the order Glomales, function at the interface between plants and soils by greatly expanding the area from which plants can gather soil resources. Extensive networks of as much as 160 m of AM hyphae per g of soil (Degens et al. 1994) function as conduits for nutrient uptake. Crops with coarse root systems generally benefit greatly from AM associations, while mycorrhizal benefits in crops with more fibrous root systems tend to be determined by soil mineral availability (Baylis 1975, Hetrick et al. 1992). Only a few crops, such as lupines and members of the Brassicaceae and Chenopodiaceae, do not regularly form AM associations. In addition to their direct effects on nutrient uptake, AM fungi also contribute to soil fertility by enhancing soil structure and protecting crops from root pathogens. AM fungi form structures inside (intraradical) and outside (extraradical) the host root. After an infective soil borne hypha contacts a host root, it forms an appressorium, penetrates the epidermis, and grows in the space between the cells into the root cortex. Once in the cortex, the intraradical hyphae penetrate the cells and produce arbuscules. These highly branched structures are surrounded by the host cells' membranes and are thought to be where nutrients are exchanged between the partners: i.e. glucose from host to fungus and phosphorus (P) from fungus to host (Blee and Anderson 1998). Once the source of carbohydrate nourishment is secured, the extraradical hyphae can proliferate in the soil. New spores are produced typically on hyphae in the soil in response to achievement of a critical amount of root length colonised, senescence of the host, or other factors. There are clear differences in the effectiveness of AM fungal species to improve soil fertility (Abbott and Robson 1982, 1985, Graham and Abbott 2000), and these differences are likely to be related to differences in allocation to intraradical and extraradical structures (Abbott and Gazey 1994, Dodd et al. 2000). (table presented) The partnership between plants and AM fungi has a long history. Fossil and molecular evidence indicates that AM fungi were associated with the earliest land plants, and that the symbiosis evolved concurrently with the evolution of roots (Malloch et al. 1980, Stubblefield et al. 1987, Simon et al. 1993, Redecker et al. 2000). The intimacy of this association is reflected in the fact that Glomalean fungi are obligate biotrophs that have not yet been successfully cultured in the absence of root tissues. Although the Glomales are asexual and include fewer than 160 species (INVAM 2001), a surprising level of genetic diversity is maintained within populations of these fungi (Hijri et al. 1999, Hosny et al. 1999). Sanders (1999) suggested that, in genetic terms, an individual aseptate AM fungus is actually a population of discrete nuclei. This genetic variance within taxa corroborates physiological variance between geographic isolates of the same species. For example, Bethlenfalvay et al. (1989) found that Glomus mosseae isolated from an arid site improved the photosynthetic water use efficiency of soybean more than G. mosseae isolated from a mesic site. Other studies also have shown that different isolates of the same species can elicit different plant responses under identical conditions (e.g. Stahl and Smith 1984, Stahl and Christensen 1990, Sylvia et al. 1993-a). Mycorrhizal function is strongly influenced by the soil environment, particularly those factors that control mineral fertility (Abbott and Robson 1982). Generally, mycorrhizal benefits are greater in phosphorus-poor soils than in phosphorus-rich ones (Koide 1991). Furthermore, crop species and even different cultivars of the same species interact with AM fungi differently (Hetrick et al. 1993, Hetrick et al. 1996). It is useful to envision mycorrhizas as dynamic systems controlled by interactions among plants, fungi, soil microbes, and soil properties. Bethlenfalvay and Sch üepp (1994) suggested that sustainable agroecosystems require management to generate a stable community of soil biota that functions effectively with abiotic conditions to maximise crop productivity and minimise inputs and soil erosion. Cultural practices have been shown to influence the species composition of AM fungal communities (see below). Certain taxa increase in abundance in agricultural systems relative to other taxa. Furthermore, species diversity of AM fungi is consistently lower in agricultural systems than in nearby natural areas (Sieverding 1990, Helgason et al. 1998-b). The consequences of this on crop production have not yet been carefully studied. Sieverding (1990) suggested that a few well selected AM fungi could increase yields if they are the best mutualists. Alternatively, if the proliferating fungi are simply the most aggressive colonists, and not the best at improving nutrient uptake, pathogen resistance, or soil structure, then this agriculture-induced reduction in diversity is cause for concern. The potential for agricultural management of mycorrhizas to reduce reliance on inorganic fertilisers and develop more sustainable agricultural systems has long been recognised and has already been reviewed (e.g. Sanders et al. 1975, Azcon-Aguilar et al. 1979, Bethlenfalvay and Linderman 1992, Pfleger and Linderman 1994, Gianinazzi and Sch üepp 1994). But, "promises of the applied value of AM fungi in agriculture, forestry and horticulture have been more rhetorical than deliverable" (Miller and Jastrow 1992). A much better understanding of the ecological and evolutionary mechanisms responsible for generating positive, neutral or negative mycorrhizal functioning in field environments is necessary before mycorrhizas can be effectively managed to maximise their contribution to soil fertility in sustainable systems. This chapter has a twofold emphasis. First, it describes the fundamental ways in which AM fungi contribute to the biological fertility of the soil (Table 1). We discuss how AM fungi directly affect plant growth and soil structure and how their interactions with other soil organisms indirectly affect crop yields and nutrient cycling. We will see that these are not independent effects and that feedbacks between plants, fungi, and biotic and abiotic soil properties ultimately determine mycorrhizal effects on plant growth. Second, we discuss how agricultural management practices affect indigenous communities of these fungi. We show that management practices positively and negatively affect AM fungi, and that these have ramifications upon plant growth. Throughout we will point out key topics where further research is needed.

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