Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts

Behie, Scott W.; Padilla-Guerrero, Israel Enrique; Bidochka, Michael

doi:10.4161/cib.22321

Cited by 22 publications

(10 citation statements)

References 41 publications

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“…These two lifestyles are linked through reciprocal nutrient exchange with a host plant, whereby the fungus receives carbon in exchange for insect-derived nitrogen. Interestingly, Metarhizium is phylogenetically related to other endophytes26 and we suggest that their evolution as insect pathogens, as well as their ability to translocate nitrogen27, allowed them to effectively barter a specialized nitrogen source (that is, insects) with host plants for photosynthate. While there has been previous work that has indicated the role that root colonizing fungi play in plant nutrient acquisition, the present study provides information on multi-role lifestyles of insect-pathogenic fungi in soil environments.…”

Section: Discussionmentioning

confidence: 89%

Carbon translocation from a plant to an insect-pathogenic endophytic fungus

et al. 2017

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Metarhizium robertsii is a common soil fungus that occupies a specialized ecological niche as an endophyte and an insect pathogen. Previously, we showed that the endophytic capability and insect pathogenicity of Metarhizium are coupled to provide an active method of insect-derived nitrogen transfer to a host plant via fungal mycelia. We speculated that in exchange for this insect-derived nitrogen, the plant would provide photosynthate to the fungus. By using 13CO2, we show the incorporation of 13C into photosynthate and the subsequent translocation of 13C into fungal-specific carbohydrates (trehalose and chitin) in the root/endophyte complex. We determined the amount of 13C present in root-associated fungal biomass over a 21-day period by extracting fungal carbohydrates and analysing their composition using nuclear magnetic resonance (NMR) spectroscopy. These findings are evidence that the host plant is providing photosynthate to the fungus, likely in exchange for insect-derived nitrogen in a tripartite, and symbiotic, interaction.

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Section: Discussionmentioning

confidence: 89%

Carbon translocation from a plant to an insect-pathogenic endophytic fungus

et al. 2017

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“…It has been reported that insect pathogenic fungi and EMF can transport insect-derived organic nitrogen into the plant roots ( Klironomos and Hart, 2001 ; Behie et al, 2012 , 2013 ). More broadly, some rhizobacterial symbionts of plants also secrete proteases and degrade denatured proteins and scavenge organic nitrogen from soil ( White et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Diverse Plant-Associated Pleosporalean Fungi from Saline Areas: Ecological Tolerance and Nitrogen-Status Dependent Effects on Plant Growth

et al. 2017

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Similar to mycorrhizal mutualists, the rhizospheric and endophytic fungi are also considered to act as active regulators of host fitness (e.g., nutrition and stress tolerance). Despite considerable work in selected model systems, it is generally poorly understood how plant-associated fungi are structured in habitats with extreme conditions and to what extent they contribute to improved plant performance. Here, we investigate the community composition of root and seed-associated fungi from six halophytes growing in saline areas of China, and found that the pleosporalean taxa (Ascomycota) were most frequently isolated across samples. A total of twenty-seven representative isolates were selected for construction of the phylogeny based on the multi-locus data (partial 18S rDNA, 28S rDNA, and transcription elongation factor 1-α), which classified them into seven families, one clade potentially representing a novel lineage. Fungal isolates were subjected to growth response assays by imposing temperature, pH, ionic and osmotic conditions. The fungi had a wide pH tolerance, while most isolates showed a variable degree of sensitivity to increasing concentration of either salt or sorbitol. Subsequent plant–fungal co-culture assays indicated that most isolates had only neutral or even adverse effects on plant growth in the presence of inorganic nitrogen. Interestingly, when provided with organic nitrogen sources the majority of the isolates enhanced plant growth especially aboveground biomass. Most of the fungi preferred organic nitrogen over its inorganic counterpart, suggesting that these fungi can readily mineralize organic nitrogen into inorganic nitrogen. Microscopy revealed that several isolates can successfully colonize roots and form melanized hyphae and/or microsclerotia-like structures within cortical cells suggesting a phylogenetic assignment as dark septate endophytes. This work provides a better understanding of the symbiotic relationship between plants and pleosporalean fungi, and initial evidence for the use of this fungal group in benefiting plant production.

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“…The intimacy of this association was potentially driven by fungal acquisition of plant-fixed carbon. Plants can fix carbon dioxide and are a carbon reservoir, a valuable commodity to fungi [ 77 ]. Plants would allow carbon exchange to a partner that could provide nutrients.…”

Section: Evolutionary Implication Of Nitrogen Transfer By Fungal Smentioning

confidence: 99%

“…The traditional paradigm concerning the population structure of insect pathogenic fungi has focused on the insect host as the driving force. However, the fact that some pathogenic fungi are endophytes ( Beauveria and Metarhizium ) suggests that plant host symbiosis may be a major evolutionary influence [ 77 ]. Insect pathogenic fungi that are incapable of forming plant associations would be more likely to evolve insect host specificity and, in this case, fungal evolution would be driven most influentially by the range of insect hosts.…”

Section: Evolutionary Implication Of Nitrogen Transfer By Fungal Smentioning

confidence: 99%

Insects as a Nitrogen Source for Plants

Behie

Bidochka

2013

Insects

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Many plants have evolved adaptations in order to survive in low nitrogen environments. One of the best-known adaptations is that of plant symbiosis with nitrogen-fixing bacteria; this is the major route by which nitrogen is incorporated into plant biomass. A portion of this plant-associated nitrogen is then lost to insects through herbivory, and insects represent a nitrogen reservoir that is generally overlooked in nitrogen cycles. In this review we show three specialized plant adaptations that allow for the recovery of insect nitrogen; that is, plants gaining nitrogen from insects. First, we show specialized adaptations by carnivorous plants in low nitrogen habitats. Insect carnivorous plants such as pitcher plants and sundews (Nepenthaceae/Sarraceniaceae and Drosera respectively) are able to obtain substantial amounts of nitrogen from the insects that they capture. Secondly, numerous plants form associations with mycorrhizal fungi that can provide soluble nitrogen from the soil, some of which may be insect-derived nitrogen, obtained from decaying insects or insect frass. Finally, a specialized group of endophytic, insect-pathogenic fungi (EIPF) provide host plants with insect-derived nitrogen. These soil-inhabiting fungi form a remarkable symbiosis with certain plant species. They can infect a wide range of insect hosts and also form endophytic associations in which they transfer insect-derived nitrogen to the plant. Root colonizing fungi are found in disparate fungal phylogenetic lineages, indicating possible convergent evolutionary strategies between taxa, evolution potentially driven by access to carbon-containing root exudates.

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Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts

Cited by 22 publications

References 41 publications

Carbon translocation from a plant to an insect-pathogenic endophytic fungus

Carbon translocation from a plant to an insect-pathogenic endophytic fungus

Diverse Plant-Associated Pleosporalean Fungi from Saline Areas: Ecological Tolerance and Nitrogen-Status Dependent Effects on Plant Growth

Insects as a Nitrogen Source for Plants

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