Soil fungi are a critical component of agroecosystems and provide ecological services that impact the production of food and bioproducts. Effective management of fungal resources is essential to optimize the productivity and sustainability of agricultural ecosystems. In this review, we (i) highlight the functional groups of fungi that play key roles in agricultural ecosystems, (ii) examine the influence of agronomic practices on these fungi, and (iii) propose ways to improve the management and contribution of soil fungi to annual cropping systems. Many of these key soil fungal organisms (i.e., arbuscular mycorrhizal fungi and fungal root endophytes) interact directly with plants and are determinants of the efficiency of agroecosystems. In turn, plants largely control rhizosphere fungi through the production of carbon and energy rich compounds and of bioactive phytochemicals, making them a powerful tool for the management of soil fungal diversity in agriculture. The use of crop rotations and selection of optimal plant genotypes can be used to improve soil biodiversity and promote beneficial soil fungi. In addition, other agronomic practices (e.g., no-till, microbial inoculants, and biochemical amendments) can be used to enhance the effect of beneficial fungi and increase the health and productivity of cultivated soils.

Increasing evidence supports the existence of variations in the association of plant roots with symbiotic fungi that can improve plant growth and inhibit pathogens. However, it is unclear whether intraspecific variations in the symbiosis exist among plant cultivars and if they can be used to improve crop productivity. In this study, we determined genotype-specific variations in the association of chickpea roots with soil fungal communities and evaluated the effect of root mycota on crop productivity. A 2-year field experiment was conducted in southwestern Saskatchewan, the central zone of the chickpea growing region of the Canadian prairie. The effects of 13 cultivars of chickpea, comprising a wide range of phenotypes and genotypes, were tested on the structure of root-associated fungal communities based on internal transcribed spacer (ITS) and 18S rRNA gene markers using 454 amplicon pyrosequencing. Chickpea cultivar significantly influenced the structure of the root fungal community. The magnitude of the effect varied with the genotypes evaluated, and effects were consistent across years. For example, the roots of CDC Corrine, CDC Cory, and CDC Anna hosted the highest fungal diversity and CDC Alma and CDC Xena the lowest. Fusarium sp. was dominant in chickpea roots but was less abundant in CDC Corrine than the other cultivars. A bioassay showed that certain of these fungal taxa, including Fusarium species, can reduce the productivity of chickpea, whereas Trichoderma harzianum can increase chickpea productivity. The large variation in the profile of chickpea root mycota, which included growth-promoting and -inhibiting species, supports the possibility of improving the productivity of chickpea by improving its root mycota in chickpea genetic improvement programs using traditional breeding techniques.

Trichoderma species are opportunistic plant symbionts that are common in the root and rhizosphere ecosystems. Many Trichoderma species may enhance plant growth, nutrient acquisition, and disease resistance, and for these reasons, they are widely used in agriculture as biofertilizers or biocontrol agents. Host plant genotype and other microorganisms, such as root pathogens, may influence the efficacy of Trichoderma inoculants. Aphanomyces euteiches is an important soil-borne oomycete in western Canada that causes root rot in legume crops such as lentil and pea, and there is not yet any significantly resistant varieties or effective treatments available to control the disease. In this study, the composition of root-associated fungal communities and the abundance of Trichoderma species, T. harzianum strain T-22 and T. virens strain G41, was determined in the roots of eight Lens genotypes based on internal transcribed spacer (ITS) Illumina MiSeq paired-end sequencing, both in the presence and the absence of the root rot pathogen Aphanomyces euteiches. Biocontrol effects of T. harzianum on A. euteiches was also examined. Significant genotypic variations were observed in the composition of root-associated fungal communities and the abundance of the different Trichoderma species in the lentil roots. The presence of A. euteiches altered the composition of Trichoderma found associated to the lentil genotypes. Biocontrol of A. euteiches by T. harzianum T22 species was observed in vitro and positive correlations between the abundance of Trichoderma and plant root and shoot biomass were observed in vivo. These findings revealed that lentil genotype and infection by the phytopathogen A. euteiches greatly influenced the colonization of root-associated fungi and the abundance of the Trichoderma species, as well as the effect on plant growth promotion. The multipartite interactions observed among lentil genotypes, Trichoderma species and A. euteiches suggest possibilities to select compatible host-beneficial microbe combinations in lentil breeding programs and to develop application strategies to harness the beneficial effects of Trichoderma inoculants in sustainable crop production systems.

Biofortification of crops via agricultural interventions represents an excellent way to supply micronutrients in poor rural populations, who highly suffer from these deficiencies. Soil microbes can directly influence plant growth and productivity, e.g., by contrasting plant pathogens or facilitating micronutrient assimilation in harvested crop-food products. Among these microbial communities, Trichoderma fungi are well-known examples of plant symbionts widely used in agriculture as biofertilizers or biocontrol agents. In this work, eleven Trichoderma strains and/or their bioactive metabolites (BAMs) were applied to lentil plants to evaluate their effects on plant growth and mineral content in greenhouse or field experiments. Our results indicated that, depending upon the different combinations of fungal strain and/or BAM, the mode of treatment (seed and/or watering), as well as the supplementary watering with solutions of iron (Fe) and zinc (Zn), the mineral absorption was differentially affected in treated plants compared with the water controls. In greenhouse conditions, the largest increase in Fe and Zn contents occurred when the compounds were applied to the seeds and the strains (in particular, T. afroharzianum T22, T. harzianum TH1, and T. virens GV41) to the soil. In field experiments, Fe and Zn contents increased in plants treated with T. asperellum strain KV906 or the hydrophobin HYTLO1 compared with controls. Both selected fungal strains and BAMs applications improved seed germination and crop yield. This biotechnology may represent an important challenge for natural biofortification of crops, thus reducing the risk of nutrient deficiencies.

Polyphenols comprise the largest group of plant secondary metabolites and have critical roles in plant physiology and response to the biotic and abiotic environment. Changes in the content of polyphenols in the root extracts and root tissues of wild (Lens ervoides) and cultivated (Lens culinaris) lentil genotypes were examined in response to infection by Aphanomyces euteiches using liquid chromatography mass spectrometry (LC-MS). Genotype, infection and their interaction determined the composition of polyphenols in lentil roots. The levels of several polyphenols were lower in the root extract of the low-tannin genotype L. culinaris ZT-4 compared to L. ervoides L01-827A. Kaempferol derivatives including kaempferol dirutinoside and kaempferol 3-robinoside 7-rhamnoside were more concentrated in the healthy root tissues of L. ervoides L01-827A than in L. culinaris genotypes. Infection increased the concentration of kaempferol, apigenin, and naringenin in the root tissues of all genotypes, but had no effect on some polyphenols in the low-tannin genotype L. culinaris ZT-4. The concentrations of apigenin, naringenin, apigenin 4-glucoside, naringenin7-rutinoside, diosmetin, and hesperetin 7-rutinoside were higher in the infected root tissues of L. ervoides L01-827A compared with the L. culinaris genotypes. Organic acids including coumaric acid, vanillic acid, 4-aminosalicylic acid, 4-hydroxybenzoic acid, and 3,4-dihydroxybenzoic acid effectively suppressed the in-vitro hyphal growth of A. euteiches. Some of these bioactive polyphenols were more concentrated in roots of L. ervoides L01-827A but were low to undetectable in ZT-4. This study shows that genotypic differences exist in the composition of root polyphenols in lentil, and is related to the response to infection caused by A. euteiches. Polyphenols, particularly the organic acid content could be useful for selection and breeding of lentil genotypes that are resistant to Aphanomyces root rot (ARR) disease.