Bioactive alkaloids in vertically transmitted fungal endophytes

Abstract

Summary1. Plants form mutualistic symbioses with a variety of microorganisms including endophytic fungi that live inside the plant and cause no overt symptoms of infection. Some endophytic fungi form defensive mutualisms based on the production of bioactive metabolites that protect the plant from herbivores in exchange for a protected niche and nutrition from the host plant. Key elements of these symbioses are vertical transmission of the fungus through seed of the host plant, a narrow host range, and production of bioactive metabolites by the fungus. 2. Grasses frequently form symbioses with endophytic fungi belonging to the family Clavicipitaceae. These symbioses have been studied extensively because of their significant impacts on insect and mammalian herbivores. Many of the impacts are likely due to the production of four classes of bioactive alkaloids -ergot alkaloids, lolines, indole-diterpenes and peraminethat are distributed in different combinations among endophyte taxa. 3. Several legumes, including locoweeds, are associated with a toxic syndrome called locoism as a result of their accumulation of swainsonine. Species in two genera were recently found to contain previously undescribed endophytic fungi (Undifilum spp., family Pleosporaceae) that are the source of that toxin. The fungi are strictly vertically transmitted and have narrow host ranges. 4. Some plant species in the morning glory family (Convolvulaceae) also form symbioses with endophytic fungi of the Clavicipitaceae that produce ergot alkaloids and, perhaps in at least one case, lolines. Other species in this plant family form symbioses with undescribed fungi that produce swainsonine. The swainsonine-producing endophytes associated with the Convolvulaceae are distinct from the Undifilum spp. associated with locoweeds and the Clavicipitaceous fungi associated with Convolvulaceae. 5. In the establishment of vertically transmitted symbioses, fungi must have entered the symbiosis with traits that were immediately useful to the plant. Bioactive metabolites are likely candidates for such pre-adapted traits which were likely useful to the free-living fungi as well. With future research, vertically transmitted fungi from diverse clades with narrow host ranges and that produce bioactive compounds are likely to be found as important mutualists in additional plants.

Heterologous Expression of Lysergic Acid and Novel Ergot Alkaloids in Aspergillus fumigatus

“…Agriculturally, ergot alkaloids in forage grasses colonized by endophytic Epichlë spp. (including many fungi recently realigned from the genus Neotyphodium [2]) reduce weight gain and fitness in grazing animals (3,4). Clinically, the structural similarities of ergot alkaloids to neurotransmitters allow ergot alkaloids to treat cognitive and neurological maladies, including dementia, migraines, and Parkinson's disease, in addition to endocrine disorders such as type 2 diabetes and hyperprolactinemia (5)(6)(7)(8).…”

“…Lp1), synthesize lysergic acid-based alkaloids in which the D ring of the ergoline nucleus is unsaturated between carbons 9 and 10 and carbon 17 is highly oxidized (Fig. 1) (4,10,11). Ergot alkaloidproducing fungi in the Trichocomaceae, such as the opportunistic human pathogen Aspergillus fumigatus, produce clavine-based derivatives in which the D ring is saturated and carbon 17 remains reduced as a methyl group (12,13).…”

Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect

“…However, one can speculate whether emitting less volatiles that act as kairomones for insects, and thus being less conspicuous, is the result of coevolution with other soil herbivores in the plant's native range and would thus be part of the defensive mutualism that characterizes fescue and Neotyphodium (Panaccione et al 2014). On the other hand, soil herbivores may have evolved the ability to 'sniff out' plants that harbour specific endophytes.…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…Vertically transmitted fungal endophytes of grasses, for example, produce from amino acid precursors four classes of alkaloids that are toxic to mammals and invertebrates. Among these, insecticidal loline alkaloids are derived from L-proline and L-homoserine, and livestock/ human-intoxicating indole and indole diterpene alkaloids, which interfere with neural and vascular processes, are derived from L-tryptophan (121). Notable toxicoses caused by indole-based alkaloids include "ryegrass staggers" in livestock caused by lolitrem B, and ergotism and related syndromes in humans and animals caused by ergot alkaloids produced by Claviceps purpurea (ergot) and clavicipitaceous grass endophytes.…”