Some plant species within the Convolvulaceae (morning glory family) from South America, Africa, and Australia cause a neurologic disease in grazing livestock caused by swainsonine. These convolvulaceous species including Ipomoea carnea contain the indolizidine alkaloid swainsonine, an inhibitor of α-mannosidase and mannosidase II, and polyhydroxy nortropane alkaloids, the calystegines which are glycosidase inhibitors. Swainsonine has been shown to be produced by a fungal endosymbiont in legumes of the Astragalus and Oxytropis genera, where it causes a similar neurologic disease in grazing livestock called locoism. Here we demonstrate that I. carnea plants are infected with a fungal endosymbiont that was cultured from its seeds and which produced swainsonine in pure culture but not the calystegines. The same fungal endosymbiont was detected by PCR and by culturing in I. carnea plants containing swainsonine. The fungal endosymbiont belongs to the Ascomycete order Chaetothyriales. Plants derived from fungicide-treated seeds lacked swainsonine, but calystegine concentrations were unaltered.
Locoweeds are defined as Astragalus and Oxytropis species that induce locoism due to the toxic alkaloid swainsonine. Swainsonine was detected in all parts of Astragalus lentiginosus and Astragalus mollissimus , with greater concentrations found in the aboveground parts. Undifilum oxytropis , a fungal endophyte responsible for the synthesis of swainsonine, was detected in all plant parts of A. lentiginosus and A. mollissimus. The amount of endophyte within a plant part does not always correspond to the concentration of swainsonine in the same part. Plants of A. mollissimus and A. lentiginosus can be divided into two chemotypes: those that contain swainsonine (>0.1%; chemotype 1) and those that contain little or no detectable swainsonine (<0.01%; chemotype 2). Chemotype 1 plants in both species had quantitatively higher amounts of endophyte compared to chemotype 2 plants. Swainsonine and endophyte amounts were not uniformly distributed within stalks of the same plant. For that reason, repeated sampling of stalks from the same plant during one growing season may provide misleading results. Sequence variants of U. oxytropis exist within populations of A. mollissimus, A. lentiginosus, and Oxytropis sericea and do not correlate with chemotype. These findings suggest several possible reasons for differential concentrations of swainsonine that will be tested in future work.
Legumes belonging to the Astragalus, Oxytropis, and Swainsona genera have been noted by ranchers in the Americas, Asia, and Australia to cause a neurologic disease often referred to as locoism or peastruck. The toxin in these legumes is swainsonine, an α-mannosidase and mannosidase II inhibitor. Recent research has shown that in Astragalus and Oxytropis species swainsonine is produced by a fungal endophyte belonging to the Undifilum genus. Here Swainsona canescens is shown to harbor an endophyte that is closely related to Undifilum species previously cultured from locoweeds of North America and Asia. The endophyte produces swainsonine in vitro and was detected by PCR and culturing in S. canescens. The endophyte isolated from S. canescens was characterized as an Undifilum species using morphological and phylogenetic analyses.
Locoism is a toxic syndrome of livestock caused by the ingestion of a subset of legumes known as locoweeds endemic to arid and semiarid regions of the western United States. Locoweeds contain the toxic alkaloid swainsonine, which is produced by the endophytic fungi Undifilum species. Two chemotypes of plants can coexist within toxic populations of locoweeds: chemotype 1 plants are defined as individuals containing swainsonine concentrations greater than 0.01% and quantitatively greater amounts of Undifilum, while chemotype 2 plants are defined as individuals containing less than 0.01% swainsonine and quantitatively smaller amounts of Undifilum. To elucidate the mechanisms that govern chemotypes, the amount of Undifilum in seeds/embryos was manipulated, thus altering subsequent swainsonine concentrations in three locoweed species: Astragalus mollissimus, Astragalus lentiginosus, and Oxytropis sericea. Chemotype 1 seeds that were fungicide-treated or had the seed coat removed resulted in plants with swainsonine concentrations comparable to those in chemotype 2 plants. Conversely, embryos from seeds of chemotypes 1 and 2 that were inoculated with the endophyte resulted in plants with swainsonine concentrations comparable to those of chemotype 1 plants. This reproducible interconversion between the two swainsonine chemotypes suggests that the quantity of endophyte present in the seed at the time of germination is a key determinant of the eventual chemotype. Additionally, this is the first report of the inoculation of locoweeds with the endophyte Undifilum species.
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