Functional and phylogenetic implications of septal pore ultrastructure in the ascoma of Neolecta vitellina

Abstract

Neolecta represents the earliest derived extant ascomycete lineage (Taphrinomycotina) to produce ascomata. For this reason the genus has been of interest with regard to ascoma evolution in ascomycetes. However, the evidence is equivocal regarding whether the Neolecta ascoma is homologous or analogous to ascomata produced in the later derived ascomycete lineages (Pezizomycotina). We investigated phylogenetically informative septal pore ultrastructure of Neolecta vitellina to compare with Pezizomycotina. We found that crystalline bodies that block nonascogenous septal pores in Neolecta differ from Woronin bodies, a synapomorphy for the Pezizomycotina, in three ways: (i) vacuolar origin, (ii) associated material and (iii) being loosely membrane bound. We also observed a unique type of membranous material within the septal pore, as well as distant from the septal pore, that appears to be associated with the endoplasmic reticulum. The vacuolar crystals and membranous material might have a function analagous to septal pore structures (e.g. Woronin bodies, lamellate structures) in the Pezizomycotina. Morphological evidence from our study supports an independently derived septal pore-occluding structure in the Neolecta lineage.

Fungal evolution: diversity, taxonomy and phylogeny of the Fungi

“…Pezizomycotina (previously known as Euascomycota) is the most diverse subphylum of Ascomycota. The basic body plan of this subphylum is filamentous and anastomosed, with septa that present a peroxisome‐derived electrodense organelle called the Woronin body (Liu et al ., ; Adl et al ., ; Healy et al ., ). Asci are typically protected and supported by multicellular structures named ascocarps or ascomata.…”

“…The Taphrinomycotina (previously known as Archiascomycota) is a species‐poor but physiologically diverse group of Ascomycota. It currently includes several genera spread over five classes: Taphrinomycetes includes eight genera of biotrophic plant pathogens ( Taphrina , Protomyces ) and saprotrophic yeasts ( Saitoella ) (Sugiyama, Hosaka, & Suh, ; Liu et al ., ; Adl et al ., ; Spatafora et al ., ); Neolectomycetes includes fruiting‐body‐forming species ( Neolecta ) of uncertain lifestyle and multicellular structures that have arisen independently to those found in Pezizomycotina or Agaricomycotina (Landvik et al ., ; Healy et al ., ; Nguyen et al ., ); Schizosaccharomycetes contain a single genus of saprotrophic yeasts ( Schizosaccharomyces ) that include the fission yeast S. pombe , an important model organism (Rhind et al ., ; Kurtzman & Sugiyama, ); Pneumocystidomycetes contain a genus of biotrophic lung parasites of mammals ( Pneumocystis ) (Sugiyama et al ., ; Hauser et al ., ; Porollo et al ., ); and Archaeorhizomycetes, with only two cultivated species of filamentous root endophytes in the genus Archaeorhizomyces (Rosling et al ., ; Menkis et al ., ). Archaeorhizomycetes was first described based on environmental sequences as a cosmopolitan and diverse clade of soil fungi termed the Soil Clone Group I (Porter et al ., ).…”

Research and teaching with the AFTOL SBD: an informatics resource for fungal subcellular and biochemical data

“…Phylogenies can be used to reevaluate characters in order to recognize homologies (Celio et al 2006). Recent recognition of the importance of combined morphological and molecular data for improved phylogenetic analyses highlights the continued significance of structural information (Kumar et al 2012, Padamsee et al 2012, Healy et al 2013). In addition, biochemical pathways such as membrane sterols may be useful in distinguishing certain fungi such as powdery mildews from other ascomycetes or rust fungi from agarics (Weete et al 2010).…”

Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases

“…Specialized structures around septa, including Woronin bodies and the dolipore septum among others, serve to regulate transport between cells in the hyphae of Asco-and Basidiomycota, respectively, although exceptions to this rule exist. Neolecta vitellina, a basal ascomycete (Taphrinomycotina), produces crystalline bodies analogous to Woronin bodies but which are of vacuolar origin and only loosely bound to the membrane (6). Although structurally different, all three solutions provide the means to finely coordinate the transport of goods and to block the diffusion of organelles from one cell to the other.…”

“…Fruiting body-forming members of the Pucciniomycotina (rusts and allies) usually form up to a few millimeters-tall cylindrical or capitate structures (e.g., Phleogena, Gymnosporangium) or crustlike, corticioid layers on the substrate (e.g., Septobasidium). The Taphrinomycotina contain the genus Neolecta, one of the most enigmatic fungi, which forms vividly colored, tongue-like ascocarps (6,43).…”