Localization of the Swainsonine-Producing Chaetothyriales Symbiont in the Seed and Shoot Apical Meristem in Its Host Ipomoea carnea

Abstract

Several species of fungi from the orders Chaetothyriales and Pleosporales have been reported to produce swainsonine and be associated as symbionts with plants of the Convolvulaceae and Fabaceae, respectively. An endosymbiont belonging to the Chaetothyriales produces swainsonine and grows as an epibiont on the adaxial leaf surfaces of Ipomoea carnea, but how the symbiont passes through plant growth and development is unknown. Herein, different types of microscopy were used to localize the symbiont in seeds and in cross sections of plant parts. The symbiont was found in several tissues including the hilum, the sclereids, and the hypocotyl of seeds. In five-day old seedlings and mature plants, the symbiont was found in the shoot apical meristem (SAM) and the adaxial surface of immature folded leaves. The mycelia generally formed a close association with peltate glandular trichomes. This report provides further data explaining the relationship between the seed transmitted Chaetothyriales symbiont and Ipomoea carnea. These results provide a possible explanation for how this symbiont, and others like Periglandula may persist and are transmitted over time.

Characterization of the Root-Associated Microbiome Provides Insights into Endemism ofThymusSpecies Growing in the Kazdagi National Park

“…chaubardii (LS) while Comoclathris and unclassified Chaetothyriales were enriched in the rhizosphere soil of endemic T. pulvinatus. Chaetothyriales have been reported as plant symbionts and transmitted by seed (37). Chaetothyriales are capable of producing swainsonine which is an indolizidine alkaloid that causes severe toxicity in livestock feeding with swainsonine containing plants (38).…”

Phylogenetic patterns of bioactive secondary metabolites produced by fungal endosymbionts in morning glories (Ipomoeeae, Convolvulaceae)

“…Closely related legumes in the Astragalus , Oxytropis , and Swainsona genera (locoweeds) are symbiotic with related, SWN‐producing Alternaria endosymbionts (Cook et al ., 2014). In diverse morning glory species (defined as members of the large tribe Ipomoeeae with spiny pollen, family Convolvulaceae), distinct fungal endosymbionts producing SWN and EA are detectable in many host species through hyphal growth on adaxial leaf surfaces associated with oil‐secreting glandular trichomes as well as between tissue types and cell layers (Neyaz et al ., 2022; Olaranont et al ., 2022; Fig. 1).…”

“…In most symbiotic species, both the Periglandula and Chaeotothyriales symbionts are found tightly associated with the glandular trichomes on the adaxial leaf surfaces of taxa containing EAs, IDTs, and SWN (Fig. 1; Steiner et al ., 2015; Noor et al ., 2021; Neyaz et al ., 2022; Olaranont et al ., 2022). Glandular trichomes in I. pes‐caprae and I. asarifolia , which are both EA+ and IDT+, have been found to secrete polysaccharides, terpenes, and fatty acids (Martins et al ., 2012; Steiner et al ., 2015; Kuster et al ., 2016), which might act as an energy source for the endosymbiotic fungi.…”

“…Molecular genetic studies have identified and characterized an orthologous SWN gene cluster shown to be required for SWN biosynthesis (Cook et al ., 2017a). Six additional orders of fungi have been found to contain the SWN biosynthetic gene cluster although the representative species have not been tested for SWN (Neyaz et al ., 2022). Two Sida species of the plant family Malvaceae (cotton family) have also been reported to contain SWN but their association with a heritable endosymbiont has not yet been investigated (Colodel et al ., 2002; Micheloud et al ., 2017).…”

“…Ipomoea carnea , a SWN‐containing morning glory, is associated with a yet unnamed fungal symbiont belonging to the order Chaetothyriales (Cook et al ., 2013). Similar to the Periglandula symbiosis, I. carnea has observable epiphytic growth on leaves, and the fungus can be detected in parts of the host seeds, and in the shoot apical meristem of seedlings (Neyaz et al ., 2022). However, unlike Periglandula spp.…”