Bioactive alkaloids in vertically transmitted fungal endophytes

Authors: PANACCIONE, DANIEL - West Virginia University; BEAULIEU, WESLEY - Indiana University; Cook, Daniel

Submitted to: Functional Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/21/2013
Publication Date: 4/1/2014
Citation: Panaccione, D.G., Beaulieu, W.T., Cook, D. 2014. Bioactive alkaloids in vertically transmitted fungal endophytes. Functional Ecology. 28(2):299-314.

Interpretive Summary: Plants form mutualistic symbioses with endophytic fungi that live inside the plant and cause no symptoms of infection. 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. Grasses frequently form symbioses with endophytic fungi belonging to the family Clavicipitaceae and produce four classes of bioactive alkaloids'ergot alkaloids, lolines, indole-diterpenes, and peramine'that are distributed in different combinations among endophyte taxa, and result in significant impacts on insect and mammalian herbivores. Some plant species in the morning glory family (Convolvulaceae) also form symbioses with endophytic fungi of the Clavicipitaceae that produce ergot alkaloids and some species in this plant family form symbioses with unrelated and undescribed fungi that produces swainsonine, another important but structurally distinct toxin. Lastly, several legumes, including locoweeds, are associated with a toxic symdrome called locoism as a result of their accumulation of swainsonine. Species in two genera were recently found to contain previously undescribed endophytic fungi (Undifilim spp., family Pleosporaceae) that are the source of that toxin. The fungus is strictly vertically transmitted and has a narrow host range. 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.

Technical Abstract: Plants form mutualistic symbioses with a variety of microorganisms, including endophytic fungi that live inside the plant and cause no 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 reduced carbon 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. 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 peramine'that are distributed in different combinations among endophyte taxa. 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 unrelated and undescribed fungi that produce swainsonine, another important but structurally distinct toxin. Several legumes, including locoweeds, are associated with a toxic symdrome called locoism as a result of their accumulation of swainsonine. Species in two genera were recently found to contain previously undescribed endophytic fungi (Undifilim spp., family Pleosporaceae) that are the source of that toxin. The fungus is strictly vertically transmitted and has a narrow host range. 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 are likely to be found as important mutualists in additional plants.