Comparative reconstruction of the predatory feeding structures of the polyphenic nematodePristionchus pacificus

Abstract

Pristionchus pacificus is a nematode model for the developmental genetics of morphological polyphenism, especially at the level of individual cells. Morphological polyphenism in this species includes an evolutionary novelty, moveable teeth, which have enabled predatory feeding in this species and others in its family (Diplogastridae). From transmission electron micrographs of serial thin sections through an adult hermaphrodite of P. pacificus, we three-dimensionally reconstructed all epithelial and myoepithelial cells and syncytia, corresponding to 74 nuclei, of its face, mouth, and pharynx. We found that the epithelia that produce the predatory morphology of P. pacificus are identical to Caenorhabditis elegans in the number of cell classes and nuclei. However, differences in cell form, spatial relationships, and nucleus position correlate with gross morphological differences from C. elegans and outgroups. Moreover, we identified fine-structural features, especially in the anteriormost pharyngeal muscles, that underlie the conspicuous, left-right asymmetry that characterizes the P. pacificus feeding apparatus. Our reconstruction provides an anatomical map for studying the genetics of polyphenism, feeding behavior, and the development of novel form in a satellite model to C. elegans.

Application of ALFA-Tagging in the Nematode Model Organisms Caenorhabditis elegans and Pristionchus pacificus

“…The Ppa-SEUD-1/SULT-1::2xALFA protein was preferentially detected in experimental conditions that promote the St morph (Figure 1B). Ppa-SEUD-1/SULT-1 was present in the cytoplasm of cells of the anterior epidermal (hyp) syncytia, the arcade cells at the interface of the mouth and the pharynx, and the pharyngeal muscle cells that secrete the extracellular teeth of the animal (Figure 3B), as previously observed [30,31,40]. To maximize the expression of the sulfotransferase, sult-1(tu1760sult-1::2xALFA) animals were grown under liquid culture conditions.…”

“…In A, asterisks indicate neuronal projections. In B, cell types were identified based on the reconstruction of the head hypodermis in P. pacificus [ 40 ]. aa: anterior arcade cell, e: epidermal cell, hyp: hypodermal syncytia, pm: pharyngeal muscle cell.…”

The improved genome of the nematode Parapristionchus giblindavisi provides insights into lineage-specific gene family evolution

“…The nematode Pristionchus pacificus had initially been introduced as a satellite model organism for comparative studies with the classical model organism Caenorhabditis elegans ( Sommer 2006 ). This has extended our understanding about the evolution of single genes ( Markov et al 2016 ; Moreno et al 2016 ), developmental networks ( Casasa et al 2021 ; Sun et al 2021 ), and organismal phenotypes such as morphology ( Rudel et al 2005 ; Harry et al 2022 ) and behavior ( Wilecki et al 2015 ; Moreno et al 2016 ). More recently, P. pacificus developed into a stand-alone model organism to study the genetics of phenotypic plasticity ( Sommer et al 2017 ) and the origin of new genes ( Rödelsperger et al 2019 ).…”

Feeding‐structure morphogenesis in “rhabditid” and diplogastrid nematodes is not controlled by a conserved genetic module

“…The four posterior‐most feeding structures are collectively referred to as the stegostom—the part of the buccal capsule that is made by pharyngeal cells. The prostegostom and mesostegostom are each produced by a set of “e” cells (pharyngeal epithelia); the metastegostom and telostegostom are each secreted by a set of “pm” cells (pharyngeal muscles) (De Ley et al, 1995; Harry et al, 2022; Jay Burr & Baldwin, 2016). Interestingly, all of these elements are cuticular; they, just like the body‐wall cuticle, constantly have to be remodeled, degraded, and re‐secreted, during the worm's periodic larval molts.…”

“…Strikingly, the metastegostom of diplogastrids evolved into large hook‐shaped teeth (Figure 1b,d,e) that can actively be moved via pharyngeal muscle contractions and used for predatory feeding (Figure 1c) (Fürst Sommer, 2015; Susoy et al, 2015; von Lieven & Sudhaus, 2000). Additionally, their pro‐ and mesostegostoms are telescoped into the gymnostom, and they evolved into slender and flexible hinges, which facilitate the movement of the teeth relative to the remainder of the buccal capsule (compare Figure 1a,b) (Harry et al, 2022).…”