Production of the Alkaloid Swainsonine by a Fungal Endosymbiont of the Ascomycete Order Chaetothyriales in the Host Ipomoea carnea

Abstract

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.

Swainsonine Biosynthesis Genes in Diverse Symbiotic and Pathogenic Fungi

“…The genome of ICE (Cook et al 2013) was sequenced and annotated to model its genes. Inferred protein sequences from this genome and the published genome of M. robertsii ARSEF 23 (Gao et al 2011) were searched by hidden Markov models (HMM) with InterProScan to identify putative functional domains.…”

“…The source and culturing conditions for the Ipomoea carnea endophyte (ICE) are described in Cook et al (2013). Slafractonia leguminicola (= Rhizoctonia leguminicola ) ATCC 26280 was obtained from the American Type Culture Collection (ATCC), and cultured as described by Alhawatema et al (2015).…”

“…Wildlife and livestock that feed on these plants can exhibit toxicosis (“locoism” or “pea struck”) characterized by weight loss, altered behavior, depression, decreased libido, infertility, abortion, birth defects, and death. Swainsonine is also produced by a recently discovered endophyte of the morning glory species, Ipomoea carnea (Cook et al 2013). This I. carnea endophyte (ICE) has phylogenetic affinity to the order Chaetothyriales, but is of an undescribed species.…”

A Review on Ipomoea Carnea: An Exploration

“…Different extracts of I. carnea plant showed significant antibacterial, anti-fungal, anti-oxidant, anti-cancer, anti-convulsant, immunomodulatory, anti-inflammatory, hepatoprotective, wound healing, anti-diabetic sedative and anxiolytic activities 33 .…”

Genomes of Plant-Associated Clavicipitaceae

“…In particular, many cool-season grasses (Poaceae subfamily Po€ oideae) possess seed-borne Epichloe¨species (including Neotyphodium species) (Schardl, 2010), and many morning glories (Convolvulaceae tribe Ipomoeeae) have seed-borne Periglandula species (Steiner, Leibner, Schardl, Leuchtmann, & Leistner, 2011). These same plant groups can possess other heritable symbionts (An et al, 1993;Cook et al, 2013), but the associations with Clavicipitaceae are particularly common and are the best-documented defensive mutualisms. Symbiotic and parasitic Clavicipitaceae often produce a wide array of alkaloids that antagonize invertebrate and sometimes vertebrate herbivores (Schardl, Young, Faulkner, Florea, & Pan, 2012;Schardl, Young, Hesse, et al, 2013).…”