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Managing the plant microbiome for biocontrol fungi: examples from Hypocreales
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ScienceDirect Managing the plant microbiome for biocontrol fungi: examples from Hypocreales Ryan M Kepler1, Jude E Maul1 and Stephen A Rehner2 Feeding an increasing global population requires continued improvements in agricultural efficiency and productivity. Meeting estimated future production levels requires the adoption of practices that increase output without environmental degradation associated with external inputs to supplement nutrition or control pests. Enriching the community of microbes associated with plants in agricultural systems for those providing ecosystem services such as pest control is one possible component towards achieving sustainable productivity increases. In this review we explore the current state of knowledge for Hypocreales fungi used in biological control. Advances in understanding the field ecology, diversity and genetic determinants of host range and virulence of hypocrealean fungi provide the means to improve their efficacy. Addresses 1 Sustainable Agricultural Systems Laboratory, 10300 Baltimore Ave, Bldg 001, Rm 123, Beltsville, MD 20705, United States 2 USDA-ARS, Mycology and Nematology Genetic Diversity and Biology Laboratory, Beltsville, MD, 20705, United States Corresponding author: Kepler, Ryan M ([email protected])
Current Opinion in Microbiology 2017, 37:48–53 This review comes from a themed issue on Environmental microbiology Edited by Marcio C Silva-Filho and Jorge Vivanco
http://dx.doi.org/10.1016/j.mib.2017.03.006 1369-5274/Published by Elsevier Ltd.
Introduction Increases in modern agricultural output have been achieved through a combination of improved genetics for plants and animals under production and external inputs to supplement nutrition or suppress pests. At the same time the footprint dedicated to agricultural production has increased to include about 35% of all habitable land on Earth [1]. Despite this expansion of capacity, further improvements are required to meet societies needs going forward. Estimates indicate output will need to double by 2050 to accommodate population growth and changes in shifting consumption preferences for more meat and dairy products [2]. Furthermore, such increases will need to do so in a manner that reduces the Current Opinion in Microbiology 2017, 37:48–53
significant negative environmental impacts associated with agricultural production, such as the emission of greenhouse gases and pollution resulting from pesticide and fertilizer run-off [3,4]. Currently, progress towards doubling agricultural output lags behind the pace needed to meet this goal [5]. Most eukaryotes enter into complex relationships with microbes colonizing exterior surfaces as well as internal tissues and organs [6]. In particular, a diverse community of organisms including fungi, archaea, and bacteria persistently and pervasively colonizes plant tissues, although fungi appear to predominate [7]. Fossil records suggest these relationships were established prior to plants moving to land [8,9]. Increasingly, the microbial interactions of plants in agricultural production are being examined for their potential to increase productivity as an alternative to the use of agrochemical amendments that often have negative environmental effects [10]. Colonizing microbes provide a number of services to their host plants, including nutrient transfer [11,12], production of growth promoters and regulation of developmental changes [13]. There are a few major caveats to understanding the relationship between the structure of the microbial community and its observed function; current next generation sequencing technology has allowed us to theoretically account for total metagenomic diversity in an environmental sample but cost and practicality has limited the number of experiments that approach the required depth of analysis to fully capture the ‘total microbial genetic diversity’ [14,15]. Also, the inability to differentiate between active and inactive members of the community in complex environments and biological and environmental eDNA/eRNA can cause under or over estimations of diversity and activity quotients [16,17]. Agricultural systems have a significant advantage in moving forward in uncovering the nuances of plant microbiome interactions due to the natural tendency for fields, farms, and cropping rotations to act as surrogates for landscape level replication [18,19]. Although coordinated landscape level experimentation can be extremely valuable and should be part of our research infrastructure they also can be difficult to manage and expensive to maintain. Because of their ability to closely associate with plants, fungal pathogens of plant pests can be considered extensions of the plant defense system. Biocontrol fungi www.sciencedirect.com
Hypocreales biocontrol fungi Kepler, Maul and Rehner 49
Figure 1
Families with important genera Bionectriaceae Nectriaceae Fusarium Calonectria
Hypocreaceae Trichoderma
Ecological Characteristics Mostly plant associated, with some pathogens. Some species associated with mosses and liverworts Broad range of nutritional modes, including potent plant pathogens. Species of Fusarium cause disease in a number of plants, as well as other organisms.
Broad range of nutritional modes, including decomposition fungal pathogens, and weak insect pathogens. The genus Trichoderma antagonizes plant pathogenic fungi and promotes root growth.
Cordycipitaceae Beauveria Cordyceps Lecanicillium
Broad range of nutritional modes, including potent pathogens of arthropods, nematodes and other fungi. Beauveria species are insect pathogens and facultative plant endophytes.
Clavicipitaceae Epichloe Metarhizium Pochonia
Broad range of nutritional modes including animal (arthropods and nematodes), fungal and plant pathogens. Plant pathogens have evolved multiple times from an animal pathogenic ancestor. The genus Epichloe is a model of plant fungal symbiosis. The genera Metarhizium and Pochonia are facultative endophytes of plant roots.
Ophiocordycipitaceae Ophiocordyceps Purpureocillium Tolypocladium
Broad range of nutritional modes including fungal and animal (arthropods and nematodes) pathogens. P. lilacinum is used for nematode biocontrol, but other species infect insects. Ophiocordyceps displays a tremendous phylosgenetic diversity and also includes insect and nematode pathoges. Some species are also facultative plant root endophytes.
Current Opinion in Microbiology
Representative phylogeny of the major families of Hypocreales (Niessliaceae not shown).
have been employed to suppress populations of a number of different plant pests including insects, nematodes and other fungi. These fungi are primarily drawn from two major clades of fungi: Entomophthorales and Ascomycota. By far, the richest source of biocontrol fungi has been the order Hypocreales in the Ascomycota. Strains of several species are produced commercially, and more receive active research for commercialization (e.g., Trichoderma: T-22, BioWorks Victor, NY 14564 and Rootshield1, Arbico Organics, Oro Valley, AZ 85737-9531; Metarhizium Met52, Novozymes Biologicals). In this paper we review the background knowledge species of Hypocreales relevant to the biological control of plant herbivores and diseases and suggest possible paths to www.sciencedirect.com
improve their efficacy. We do not consider endophytes of cool seasons grasses, which are covered elsewhere [20].
Summary of Hypocreales Species in Hypocreales are notable for their ability to derive nutrition from diverse nutrient sources, and over evolutionary time numerous inter-kingdom host shifts have occurred (Figure 1). The ancestral condition is hypothesized to have been a reliance on plant-based nutrition, either the decomposition of dead plant tissue or as plant pathogens [21]. From this background numerous adaptive shifts have resulted in the acquisition of insect, nematode, rotifer and reptile hosts. However, such shifts have been dynamic and host groups appear to have Current Opinion in Microbiology 2017, 37:48–53
50 Environmental microbiology
been repeatedly gained and lost. In modern agricultural systems Calonectria (=Cylindrocladium) and Fusarium species (Nectriaceae) are examples of major disease agents with diverse plant host ranges [22,23]. The multiple instances of plant pathogenesis in Clavicipitaceae, including ergot fungi infecting cools season grasses, are hypothesized to have evolved from ancestors infecting Hemipteran insects [24,25]. Sexual reproduction features the production of ascospores in an enclosed structure (perithecium) with a pore at the tip that may be embedded in robust, fleshy tissue or produced directly from the substrate. Asexually reproductive forms are often reduced or inconspicuous relative to sexual structures, showing a variety of forms of spore shape, color and presentation. These morphologically divergent reproductive forms are often separated in time and space, resulting in competing taxonomic names for different life stages of the same entity. There may also be differences in the growth requirements for different lifestages, with sexual reproduction limited to specific hosts or geographical ranges while asexual forms may be widespread and utilize many different nutritional sources. Through the use of DNA-based phylogenetic studies, relationships between the different morphological forms for many species have been clarified and taxonomic systems are in the process of being refined to unify divergent morphological forms of the same species under a single name [20,23,26–29].
Insect pathogens Numerous species of Hypocreales are insect pathogens, with a concentration in the families Clavicipitaceae, Cordycipitaceae and Ophiocordycipitaceae [30]. It remains unclear exactly when insect pathogenesis arose, and this ecology may have multiple independent origins [21]. In both natural and managed ecosystems, species of Hypocreales play an important role in the regulation of insect populations [31–33]. Strains from throughout Hypocreales have been registered and are commercially available as mycoinsecticides worldwide [34]. Beauveria and Metarhizium remain two of the most well understood genera of insect pathogens. Robust molecular tools exist for resolving fine scale molecular diversity of the Beauveria bassiana and Metarhizium anisopliae species complexes, containing the primary species currently available commercially for insect control [35,36]. Isolates of B. bassiana and M. anisopliae s.l. exhibit high genetic and virulence diversity [27,36–40]. Comparative genomic analyses for both genera have revealed qualitative differences in gene content that are potentially important in determining host virulence [41–45]. Additional genomic resources for related genera promise to expand the range of inferences possible for the underlying genetics of entomopathogen ecology [46,47]. Current Opinion in Microbiology 2017, 37:48–53
Nematode pathogens Molecular phylogenies reveal that many pathogens of nematodes are closely related to insect pathogens [27,30,48]. The cryptic nature and small size of nematodes and their many pathogens has limited understanding of their biology relative to plant and insect pathogens. Fungi infecting nematodes are found in most families of Hypocreales. Several of these species have been developed for commercially available products including Hirsutella minnesotensis, Pochonia chlamydosporia and Purpureocillium lilacinum [49]. All three of these species are natural inhabitants of soil environments and genome sequence data exists for representative isolates [50–53].
Fungal pathogens Fungal pathogenesis is a less common but widespread ecological trait in Hypocreales apparently gained after shifts from other hosts on multiple occasions [21]. The genus Tolypocladium contains species predominantly infecting false truffles of the genus Elaphomyces, although several species are also insect pathogens [28,46,54]. Thus far, several species of Trichoderma are the only species developed as biocontrol agents against fungi responsible for crop failure [55]. Trichoderma species infect a number of plant pathogenic fungi and oomycetes. When growing in the rhizosphere they also outcompete plant pathogens and secrete plant growth promoters [56–58].
Selecting for a plant microbiome When not infecting other hosts, some hypocrealean fungi are able to interact intimately with plants in a number of ways. Rhizosphere competence has been observed in a number of species including the nematode pathogen P. chlamydosporia [59,60] and Ophiocordyceps sinensis [61]. Tolypocladium species have been found as endophytes in the bark of rubber trees [62] and B. bassiana has been induced to grow as a foliar endophyte [63]. Species of both Metarhizium and Beauveria are commonly isolated from bulk soil and rhizosphere habitats, however it appears that Metarhizium is uniquely adapted to the rhizosphere environment [64,65]. Strains of M. anisopliae have been shown to penetrate root tissues [66] and exchange nitrogen with plants [67]. The ability to attach to plant roots is controlled by the adhesin gene Mad2 [68], and Mad2 knockout strains show diminished persistence in natural landscapes [69]. In contrast, although Metarhizium flavoviride is a dominant species at sites across Denmark, it does not appear to rely heavily on plant associations to maintain population levels [70]. Details remain in understanding the extent of this ability in other Metarhizium species, as well as the host plant range and environmental conditions favoring such relationships. Creating conditions where plants are able to take advantage of naturally occurring populations of biocontrol fungi could proceed along several lines. Corn plants grown today show a marked difference in root architecture www.sciencedirect.com
Hypocreales biocontrol fungi Kepler, Maul and Rehner 51
and reduced microbial community diversity compared to wild teosinte ancestors [71]. Selecting of plant traits that facilitate recruitment of beneficial soil microbes could enhance their effects. Both Metarhizium and Trichoderma have been shown to elicit plant growth promotion when growing in the rhizosphere [69,72]. Variation in abundance has been observed across plant type and farming management practices for some members of the M. anisopliae species complex [19]. The rhizosphere of soybean plants grown in fields under long-term monoculture production systems suppressive to soybean cyst nematode were enriched for P. lilacinum and to a lesser degree P. chlamydosporia [73]. It is unclear if this is the result of selection or evolution for successful strains in this environment or a type of ‘soil memory’ [74]. Experimental selection for functional rhizospheres has been conducted in the lab with model plant systems [75,76]. Cover crops are being explored as a way to boost populations of desired soil microbes, in addition to other benefits of using these crops in rotation schemes [77]. Although diverse genotypes and signatures of reproduction were recovered for natural populations of Metarhizium robertsii and Lecanicillium lecanii in field settings, these species were only composed of a single mating type [19,78]. This suggests studies need to take a broader geographic perspective to understand reproductive biology and landscape genetics of biocontrol fungi. Mating type genes are known to function in regulation of other metabolic processes outside of reproduction [79] and certain environments may select for expression patterns associated with a particular mating type. Understanding the diversity of isolates present will allow assessment as to whether it may be necessary to supplement indigenous fungal communities with additional, outside strains.
Conclusions As the ‘omics’ tools of the third and fourth generation are successfully applied in field situations [80] we should take advantage of agroecosystem research infrastructure to ensure that developed technologies are robust at the appropriate scale for agroecosystem production [81]. The abundance of genome data available for Hypocreales positions this group well for further advances to gain a deep understanding of genotype by environment interactions. A better understanding of reproductive ecology will inform the potential of local populations to adapt to agricultural management practices and crops, as well as assess the risk of sexual crossings between indigenous and introduced strains. The last point is particularly important as genetic modifications become an increasingly attractive way to achieve improvement of biocontrol fungi [82–84]. Although approaches taking into account the broader community of fungi, bacteria, nematodes and other organisms will undoubtedly result in the most productive agricultural outcomes, the Hypocreales present themselves as a model of agriculturally relevant fungi. www.sciencedirect.com
Acknowledgements This work was funded by ARS Project No. 0500-00082-001-00D, National Plant Disease Recovery System and ARS Project No. 8042-22000-279-00D. The mention of trade products or company names or firm names does not imply that the United States Department of Agriculture recommends them over similar products or companies not mentioned.
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Current Opinion in Microbiology 2017, 37:48–53
ScienceDirect Managing the plant microbiome for biocontrol fungi: examples from Hypocreales Ryan M Kepler1, Jude E Maul1 and Stephen A Rehner2 Feeding an increasing global population requires continued improvements in agricultural efficiency and productivity. Meeting estimated future production levels requires the adoption of practices that increase output without environmental degradation associated with external inputs to supplement nutrition or control pests. Enriching the community of microbes associated with plants in agricultural systems for those providing ecosystem services such as pest control is one possible component towards achieving sustainable productivity increases. In this review we explore the current state of knowledge for Hypocreales fungi used in biological control. Advances in understanding the field ecology, diversity and genetic determinants of host range and virulence of hypocrealean fungi provide the means to improve their efficacy. Addresses 1 Sustainable Agricultural Systems Laboratory, 10300 Baltimore Ave, Bldg 001, Rm 123, Beltsville, MD 20705, United States 2 USDA-ARS, Mycology and Nematology Genetic Diversity and Biology Laboratory, Beltsville, MD, 20705, United States Corresponding author: Kepler, Ryan M ([email protected])
Current Opinion in Microbiology 2017, 37:48–53 This review comes from a themed issue on Environmental microbiology Edited by Marcio C Silva-Filho and Jorge Vivanco
http://dx.doi.org/10.1016/j.mib.2017.03.006 1369-5274/Published by Elsevier Ltd.
Introduction Increases in modern agricultural output have been achieved through a combination of improved genetics for plants and animals under production and external inputs to supplement nutrition or suppress pests. At the same time the footprint dedicated to agricultural production has increased to include about 35% of all habitable land on Earth [1]. Despite this expansion of capacity, further improvements are required to meet societies needs going forward. Estimates indicate output will need to double by 2050 to accommodate population growth and changes in shifting consumption preferences for more meat and dairy products [2]. Furthermore, such increases will need to do so in a manner that reduces the Current Opinion in Microbiology 2017, 37:48–53
significant negative environmental impacts associated with agricultural production, such as the emission of greenhouse gases and pollution resulting from pesticide and fertilizer run-off [3,4]. Currently, progress towards doubling agricultural output lags behind the pace needed to meet this goal [5]. Most eukaryotes enter into complex relationships with microbes colonizing exterior surfaces as well as internal tissues and organs [6]. In particular, a diverse community of organisms including fungi, archaea, and bacteria persistently and pervasively colonizes plant tissues, although fungi appear to predominate [7]. Fossil records suggest these relationships were established prior to plants moving to land [8,9]. Increasingly, the microbial interactions of plants in agricultural production are being examined for their potential to increase productivity as an alternative to the use of agrochemical amendments that often have negative environmental effects [10]. Colonizing microbes provide a number of services to their host plants, including nutrient transfer [11,12], production of growth promoters and regulation of developmental changes [13]. There are a few major caveats to understanding the relationship between the structure of the microbial community and its observed function; current next generation sequencing technology has allowed us to theoretically account for total metagenomic diversity in an environmental sample but cost and practicality has limited the number of experiments that approach the required depth of analysis to fully capture the ‘total microbial genetic diversity’ [14,15]. Also, the inability to differentiate between active and inactive members of the community in complex environments and biological and environmental eDNA/eRNA can cause under or over estimations of diversity and activity quotients [16,17]. Agricultural systems have a significant advantage in moving forward in uncovering the nuances of plant microbiome interactions due to the natural tendency for fields, farms, and cropping rotations to act as surrogates for landscape level replication [18,19]. Although coordinated landscape level experimentation can be extremely valuable and should be part of our research infrastructure they also can be difficult to manage and expensive to maintain. Because of their ability to closely associate with plants, fungal pathogens of plant pests can be considered extensions of the plant defense system. Biocontrol fungi www.sciencedirect.com
Hypocreales biocontrol fungi Kepler, Maul and Rehner 49
Figure 1
Families with important genera Bionectriaceae Nectriaceae Fusarium Calonectria
Hypocreaceae Trichoderma
Ecological Characteristics Mostly plant associated, with some pathogens. Some species associated with mosses and liverworts Broad range of nutritional modes, including potent plant pathogens. Species of Fusarium cause disease in a number of plants, as well as other organisms.
Broad range of nutritional modes, including decomposition fungal pathogens, and weak insect pathogens. The genus Trichoderma antagonizes plant pathogenic fungi and promotes root growth.
Cordycipitaceae Beauveria Cordyceps Lecanicillium
Broad range of nutritional modes, including potent pathogens of arthropods, nematodes and other fungi. Beauveria species are insect pathogens and facultative plant endophytes.
Clavicipitaceae Epichloe Metarhizium Pochonia
Broad range of nutritional modes including animal (arthropods and nematodes), fungal and plant pathogens. Plant pathogens have evolved multiple times from an animal pathogenic ancestor. The genus Epichloe is a model of plant fungal symbiosis. The genera Metarhizium and Pochonia are facultative endophytes of plant roots.
Ophiocordycipitaceae Ophiocordyceps Purpureocillium Tolypocladium
Broad range of nutritional modes including fungal and animal (arthropods and nematodes) pathogens. P. lilacinum is used for nematode biocontrol, but other species infect insects. Ophiocordyceps displays a tremendous phylosgenetic diversity and also includes insect and nematode pathoges. Some species are also facultative plant root endophytes.
Current Opinion in Microbiology
Representative phylogeny of the major families of Hypocreales (Niessliaceae not shown).
have been employed to suppress populations of a number of different plant pests including insects, nematodes and other fungi. These fungi are primarily drawn from two major clades of fungi: Entomophthorales and Ascomycota. By far, the richest source of biocontrol fungi has been the order Hypocreales in the Ascomycota. Strains of several species are produced commercially, and more receive active research for commercialization (e.g., Trichoderma: T-22, BioWorks Victor, NY 14564 and Rootshield1, Arbico Organics, Oro Valley, AZ 85737-9531; Metarhizium Met52, Novozymes Biologicals). In this paper we review the background knowledge species of Hypocreales relevant to the biological control of plant herbivores and diseases and suggest possible paths to www.sciencedirect.com
improve their efficacy. We do not consider endophytes of cool seasons grasses, which are covered elsewhere [20].
Summary of Hypocreales Species in Hypocreales are notable for their ability to derive nutrition from diverse nutrient sources, and over evolutionary time numerous inter-kingdom host shifts have occurred (Figure 1). The ancestral condition is hypothesized to have been a reliance on plant-based nutrition, either the decomposition of dead plant tissue or as plant pathogens [21]. From this background numerous adaptive shifts have resulted in the acquisition of insect, nematode, rotifer and reptile hosts. However, such shifts have been dynamic and host groups appear to have Current Opinion in Microbiology 2017, 37:48–53
50 Environmental microbiology
been repeatedly gained and lost. In modern agricultural systems Calonectria (=Cylindrocladium) and Fusarium species (Nectriaceae) are examples of major disease agents with diverse plant host ranges [22,23]. The multiple instances of plant pathogenesis in Clavicipitaceae, including ergot fungi infecting cools season grasses, are hypothesized to have evolved from ancestors infecting Hemipteran insects [24,25]. Sexual reproduction features the production of ascospores in an enclosed structure (perithecium) with a pore at the tip that may be embedded in robust, fleshy tissue or produced directly from the substrate. Asexually reproductive forms are often reduced or inconspicuous relative to sexual structures, showing a variety of forms of spore shape, color and presentation. These morphologically divergent reproductive forms are often separated in time and space, resulting in competing taxonomic names for different life stages of the same entity. There may also be differences in the growth requirements for different lifestages, with sexual reproduction limited to specific hosts or geographical ranges while asexual forms may be widespread and utilize many different nutritional sources. Through the use of DNA-based phylogenetic studies, relationships between the different morphological forms for many species have been clarified and taxonomic systems are in the process of being refined to unify divergent morphological forms of the same species under a single name [20,23,26–29].
Insect pathogens Numerous species of Hypocreales are insect pathogens, with a concentration in the families Clavicipitaceae, Cordycipitaceae and Ophiocordycipitaceae [30]. It remains unclear exactly when insect pathogenesis arose, and this ecology may have multiple independent origins [21]. In both natural and managed ecosystems, species of Hypocreales play an important role in the regulation of insect populations [31–33]. Strains from throughout Hypocreales have been registered and are commercially available as mycoinsecticides worldwide [34]. Beauveria and Metarhizium remain two of the most well understood genera of insect pathogens. Robust molecular tools exist for resolving fine scale molecular diversity of the Beauveria bassiana and Metarhizium anisopliae species complexes, containing the primary species currently available commercially for insect control [35,36]. Isolates of B. bassiana and M. anisopliae s.l. exhibit high genetic and virulence diversity [27,36–40]. Comparative genomic analyses for both genera have revealed qualitative differences in gene content that are potentially important in determining host virulence [41–45]. Additional genomic resources for related genera promise to expand the range of inferences possible for the underlying genetics of entomopathogen ecology [46,47]. Current Opinion in Microbiology 2017, 37:48–53
Nematode pathogens Molecular phylogenies reveal that many pathogens of nematodes are closely related to insect pathogens [27,30,48]. The cryptic nature and small size of nematodes and their many pathogens has limited understanding of their biology relative to plant and insect pathogens. Fungi infecting nematodes are found in most families of Hypocreales. Several of these species have been developed for commercially available products including Hirsutella minnesotensis, Pochonia chlamydosporia and Purpureocillium lilacinum [49]. All three of these species are natural inhabitants of soil environments and genome sequence data exists for representative isolates [50–53].
Fungal pathogens Fungal pathogenesis is a less common but widespread ecological trait in Hypocreales apparently gained after shifts from other hosts on multiple occasions [21]. The genus Tolypocladium contains species predominantly infecting false truffles of the genus Elaphomyces, although several species are also insect pathogens [28,46,54]. Thus far, several species of Trichoderma are the only species developed as biocontrol agents against fungi responsible for crop failure [55]. Trichoderma species infect a number of plant pathogenic fungi and oomycetes. When growing in the rhizosphere they also outcompete plant pathogens and secrete plant growth promoters [56–58].
Selecting for a plant microbiome When not infecting other hosts, some hypocrealean fungi are able to interact intimately with plants in a number of ways. Rhizosphere competence has been observed in a number of species including the nematode pathogen P. chlamydosporia [59,60] and Ophiocordyceps sinensis [61]. Tolypocladium species have been found as endophytes in the bark of rubber trees [62] and B. bassiana has been induced to grow as a foliar endophyte [63]. Species of both Metarhizium and Beauveria are commonly isolated from bulk soil and rhizosphere habitats, however it appears that Metarhizium is uniquely adapted to the rhizosphere environment [64,65]. Strains of M. anisopliae have been shown to penetrate root tissues [66] and exchange nitrogen with plants [67]. The ability to attach to plant roots is controlled by the adhesin gene Mad2 [68], and Mad2 knockout strains show diminished persistence in natural landscapes [69]. In contrast, although Metarhizium flavoviride is a dominant species at sites across Denmark, it does not appear to rely heavily on plant associations to maintain population levels [70]. Details remain in understanding the extent of this ability in other Metarhizium species, as well as the host plant range and environmental conditions favoring such relationships. Creating conditions where plants are able to take advantage of naturally occurring populations of biocontrol fungi could proceed along several lines. Corn plants grown today show a marked difference in root architecture www.sciencedirect.com
Hypocreales biocontrol fungi Kepler, Maul and Rehner 51
and reduced microbial community diversity compared to wild teosinte ancestors [71]. Selecting of plant traits that facilitate recruitment of beneficial soil microbes could enhance their effects. Both Metarhizium and Trichoderma have been shown to elicit plant growth promotion when growing in the rhizosphere [69,72]. Variation in abundance has been observed across plant type and farming management practices for some members of the M. anisopliae species complex [19]. The rhizosphere of soybean plants grown in fields under long-term monoculture production systems suppressive to soybean cyst nematode were enriched for P. lilacinum and to a lesser degree P. chlamydosporia [73]. It is unclear if this is the result of selection or evolution for successful strains in this environment or a type of ‘soil memory’ [74]. Experimental selection for functional rhizospheres has been conducted in the lab with model plant systems [75,76]. Cover crops are being explored as a way to boost populations of desired soil microbes, in addition to other benefits of using these crops in rotation schemes [77]. Although diverse genotypes and signatures of reproduction were recovered for natural populations of Metarhizium robertsii and Lecanicillium lecanii in field settings, these species were only composed of a single mating type [19,78]. This suggests studies need to take a broader geographic perspective to understand reproductive biology and landscape genetics of biocontrol fungi. Mating type genes are known to function in regulation of other metabolic processes outside of reproduction [79] and certain environments may select for expression patterns associated with a particular mating type. Understanding the diversity of isolates present will allow assessment as to whether it may be necessary to supplement indigenous fungal communities with additional, outside strains.
Conclusions As the ‘omics’ tools of the third and fourth generation are successfully applied in field situations [80] we should take advantage of agroecosystem research infrastructure to ensure that developed technologies are robust at the appropriate scale for agroecosystem production [81]. The abundance of genome data available for Hypocreales positions this group well for further advances to gain a deep understanding of genotype by environment interactions. A better understanding of reproductive ecology will inform the potential of local populations to adapt to agricultural management practices and crops, as well as assess the risk of sexual crossings between indigenous and introduced strains. The last point is particularly important as genetic modifications become an increasingly attractive way to achieve improvement of biocontrol fungi [82–84]. Although approaches taking into account the broader community of fungi, bacteria, nematodes and other organisms will undoubtedly result in the most productive agricultural outcomes, the Hypocreales present themselves as a model of agriculturally relevant fungi. www.sciencedirect.com
Acknowledgements This work was funded by ARS Project No. 0500-00082-001-00D, National Plant Disease Recovery System and ARS Project No. 8042-22000-279-00D. The mention of trade products or company names or firm names does not imply that the United States Department of Agriculture recommends them over similar products or companies not mentioned.
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