Influence of Seed Endophyte Amounts on Swainsonine Concentrations in Astragalus and Oxytropis Locoweeds

Abstract

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.

Bioactive alkaloids in vertically transmitted fungal endophytes

“…Finally, swainsonine concentrations are greatest in floral parts and seeds (Grum et al . ), consistent with the optimal defence theory.…”

“…); (v) plants derived from embryos that were inoculated with Undifilum have swainsonine concentrations greater than 0·01% (Grum et al . ); and (vi) rats fed U. oxytropis developed lesions and clinical signs similar to those fed swainsonine‐containing Oxytropis lambertii (McLain‐Romero et al . ).…”

“…; Grum et al . ); (iii) plants derived from fungicide‐treated Astragalus and Oxytropis seeds have no detectable swainsonine or have concentrations less than 0·001% (Grum et al . ); (iv) Undifilum species isolated from locoweeds produce swainsonine in pure culture (Braun et al .…”

“…); (iii) plants derived from fungicide‐treated Astragalus and Oxytropis seeds have no detectable swainsonine or have concentrations less than 0·001% (Grum et al . ); (iv) Undifilum species isolated from locoweeds produce swainsonine in pure culture (Braun et al . ); (v) plants derived from embryos that were inoculated with Undifilum have swainsonine concentrations greater than 0·01% (Grum et al .…”

Vertical transmission of fungal endophytes is widespread in forbs

“…The fact that some seedlings contain endophytes and others do not could have far-reaching consequences for plant population dynamics. Indeed, the vertically transmitted endophyte Undifilum oxytropis can confer high levels of alkaloid content in the tissues of some seeds and seedlings of locoweeds Grum et al 2012). Of the fungi studied here, Alternaria alternata may have negative effects on insect herbivores (Abbas and Mulrooney 1994) and on plant pathogenic fungi (Musetti et al 2006) or be negatively associated with other endophytes .…”