Introduction to Pristionchus pacificus anatomy

Publications

Share / Export Citation / Email / Print / Text size:

Journal of Nematology

Society of Nematologists

Subject: Life Sciences

GET ALERTS DONATE

ISSN: 0022-300X
eISSN: 2640-396X

DESCRIPTION

36
Reader(s)
39
Visit(s)
0
Comment(s)
0
Share(s)

SEARCH WITHIN CONTENT

FIND ARTICLE

Volume / Issue / page

Related articles

Introduction to Pristionchus pacificus anatomy

Nathan E. Schroeder *

Keywords : Cytology, Electron microscopy, Free-living nematode, Morphology, Ultrastructure, WormAtlas

Citation Information : Journal of Nematology. Volume 53, Pages 1-9, DOI: https://doi.org/10.21307/jofnem-2021-091

License : (CC-BY-4.0)

Received Date : 22-September-2021 / Published Online: 03-November-2021

ARTICLE

ABSTRACT

Pristionchus pacificus has emerged as an important nematode species used to understand the evolution of development and behavior. While P. pacificus (Diplogasteridae) is only distantly related to Caenorhabditis elegans (Rhabditidae), both use an identical reproductive strategy, are easily reared on bacteria in Petri dishes and complete their life cycles within a few days. Over the past 25 years, several detailed light and electron microscopy studies have elucidated the anatomy of P. pacificus and have demonstrated clear homology to many cells in C. elegans. Despite this similarity, sufficient anatomical differences between C. elegans and P. pacificus have allowed the latter to be used in comparative evo-devo studies. For example, the stoma of P. pacificus contains a large dorsal tooth used during predation on other nematodes when supplementing its primarily bacterial diet. This review discusses the main anatomical features of P. pacificus with emphasis on comparison to C. elegans.

Graphical ABSTRACT

In 1988, the nematode Pristionchus pacificus was isolated from garden soil in Pasadena, CA (Sommer et al., 1996). P. pacificus was originally studied as a comparative species to Caenorhabditis elegans (Fig. 1). Both species are easily reared in the laboratory on bacterial lawns and have similar anatomies and life cycles (Hong and Sommer, 2006). P. pacificus uses a facultative hermaphroditic reproductive strategy similar to C. elegans. Many of the laboratory tools developed for C. elegans research are readily transferable to P. pacificus (Pires da Silva, 2013). The amenability of P. pacificus to genetic manipulation and analysis has propelled this species forward as an important comparative model for understanding the molecular basis of evolution for diverse traits.

Figure 1:

Pristionchus pacificus (A) and Caenorhabditis elegans (B) adult hermaphrodites have similar sizes and shapes. Scale bar 50 µm.

10.21307_jofnem-2021-091-f001.jpg

Hundreds of P. pacificus isolates and other related Pristionchus species from around the world have been isolated (McGaughran and Morgan, 2015). Due to its cosmopolitan distribution and the diversity of isolated populations, P. pacificus has emerged as a powerful model for studying evolutionary processes at the molecular level. Many P. pacificus isolates are found associated with beetles and data suggests a necromenic relationship wherein the nematode waits for the beetle to die and then feeds off of the rotting cadaver and associated microorganisms (Herrmann et al., 2006). However, others have proposed that the relationship between P. pacificus and beetles is phoretic – the nematodes use beetles as a means of transport to a new nutrient rich environment (Félix et al., 2018).

P. pacificus is androdioecious, comprising both self-fertile hermaphrodites (XX) and occasional males (XO) that fertilize hermaphrodites. Males are usually less than 1% of the population; however, this fraction varies among P. pacificus isolates and environmental conditions (Morgan et al., 2017). The androdioecious system is valuable for genetic studies as selfing by hermaphrodites leads to genetically identical offspring, while the presence of males allows for crosses between distinct genotypes.

Life cycle

P. pacificus is easily maintained on bacterial cultures in the laboratory and frozen stocks can be kept for years (Pires da Silva, 2013). Development from fertilized egg to adult is completed in approximately four days which is only slightly longer than C. elegans (Fig. 2) (Hong and Sommer, 2006). Following exposure to harsh environmental conditions, P. pacificus can form a stress-resistant dauer stage that can survive extended periods without feeding.

Figure 2:

Life cycle of Pristionchus pacificus. Differential interference contrast images of developmental stages. Development from the two-cell stage to adult takes approximately 72 hrs at 20°C. Each post-embryonic stage is positioned with its left side facing the reader, except the J4, which is facing the right side. Scale bar, 50 µm.

10.21307_jofnem-2021-091-f002.jpg

Unlike C. elegans, which hatches as a J1, P. pacificus does not emerge from its egg until J2 (Fig. 2). The presence of a distinct J1 stage in P. pacificus is marked by ecdysis (shedding of the cuticle) within the egg-shell (Fürst von Lieven, 2005) (Fig. 3). The shift in timing of P. pacificus hatch may allow for the development of moveable teeth within the stoma. A similar delay is seen in many plant-parasitic nematodes with moveable stylet mouthparts. Despite the delay in hatching, the generation time for P. pacificus is only slightly longer than C. elegans (Hong and Sommer, 2006). Some events that occur in the post-hatch J1 of C. elegans occur prior to hatching in J1 P. pacificus. For example, migration of the Pn ectoblasts, which contribute to the post-embryonic development of the ventral nerve cord and vulva, occurs in the J1 of both species (Félix et al., 1999; Sulston and Horvitz, 1977). Unfortunately, the additional post-embryonic development and corresponding movement within the eggshell will make it challenging to describe the complete embryonic cell lineage of P. pacificus.

Figure 3:

Unhatched J2. The presence of a shed J1 cuticle (arrowhead) is indicative of the J1 to J2 molt occurring prior to hatching. Scale bar, 10 µm.

10.21307_jofnem-2021-091-f003.jpg

Cuticle

The cuticle of P. pacificus is a tough rigid extracellular matrix likely secreted by the underlying epithelial cells. Similar to C. elegans and other nematodes, collagen is a major biochemical component of the body wall (Kenning et al., 2004; Schlager et al., 2009). The cuticle of P. pacificus contains evenly spaced stippled longitudinal ridges along the length of the body (Fig. 4). Unlike the C. elegans alae, these longitudinal ridges are not restricted to the lateral field of the cuticle. Several tissues open to the outside through the cuticle including the stoma and anus. The excretory pore of P. pacificus lies on the ventral ridge near the terminal bulb of the pharynx. The lateral cuticle of P. pacificus hermaphrodites is also interrupted by a series of small pores that open to gland cells embedded within the lateral hypodermis (Fig. 4) (Ragsdale et al., 2015; Sommer et al., 1996). These lateral gland cells are not present in C. elegans and their lineage in P. pacificus is unknown.

Figure 4:

(A) The cuticle of P. pacificus contains longitudinal stippled lines around the circumference of the animal. Scale bar, 10 µm. (B) In an EM cross section, this stippling can be seen as waves around the animal (arrowheads). Scale bar, 1 µm. Image source: Ralf Sommer Lab, Bumbarger13–1301. (C, D) The cuticle of P. pacificus is interrupted by epithelial gland cell pores. In DIC (C), the small gland cell pores (arrow) are occasionally visible both dorsal and ventral of the midline (deirid, arrowhead). Scale bar, 10 µm. In EM cross sections (D), the epithelial gland cell (purple) is surrounded by the hypodermis. Scale bar, 1 µm. Image Source: Ralf Sommer, Bumbarger14–1955.

10.21307_jofnem-2021-091-f004.jpg

P. pacificus dauers tend to retain their L2 cuticle for extended periods of time. Retention of the L2 cuticle likely assists dauers in survival of adverse environmental conditions. P. pacificus dauers also secrete a waxy ester onto the cuticle surface that facilitates aggregation of dauers and the formation of ‘dauer towers’, which enhance the nematode’s ability to attach to a beetle host (Penkov et al., 2014).

The epithelial system

The main epithelial system of P. pacificus consists of hypodermal syncytia. Similar to C. elegans, the hypodermis wraps around the body wall of the nematode alternating between thick regions with nuclei in the cords and a thin sheet-like region underlying the somatic muscles. The hypodermis is interrupted on the lateral ridges by a linear set of 15 epithelial ‘seam’ cells per side in the adult hermaphrodite, which is slightly less than the 16 homologous seam cells found in C. elegans (Cinkornpumin et al., 2014). Also, differing from C. elegans, the P. pacificus seam cells send processes from the apical membrane that extend away from the lateral midline.

The nervous system

As with C. elegans and other nematodes, the majority of P. pacificus neurons are located in the head and tail. The anterior nervous system of P. pacificus, including the pharynx and anterior amphid sensory neurons, have been reconstructed from serial-section electron microscopy (Bumbarger et al., 2013; Hong et al., 2019). The nervous system of P. pacificus is remarkably similar to that of C. elegans. Both the anterior amphid sensory sensilla and the pharyngeal nervous system have equivalent numbers of neurons in both species and many of these are obvious homologs based on their positions and structures (Bumbarger et al., 2013; Bumbarger and Riebesell, 2015; Hong et al., 2019). While both species have 12 pairs of amphid neurons, the sensory ending shape differs between some homologous neurons. For example, the P. pacificus amphids lack obvious wing-like ciliated dendrites found in the AWA, AWB, and AWC neurons in C. elegans (Hong et al., 2019).

While the pharyngeal nervous system of both species comprises 20 neurons, the synaptic connectivity differs between these species (Bumbarger et al., 2013), although a more recent reanalysis of the C. elegans pharyngeal connectome suggests these differences may not be as great as originally reported (Cook et al., 2020). Wiring differences between the two species in the amphid and pharyngeal circuits may mediate behavioral differences (Bumbarger et al., 2013; Hong et al., 2019). Similarly, slight differences in neurotransmitter expression occur between P. pacificus and C. elegans neurons (Loer and Rivard, 2007). While there are differences reported in the number of neurons within the ventral nerve cord between C. elegans and P. pacificus, additional electron microscopy will be needed to determine the extent of neuronal differences between these species (Han et al., 2016).

The muscle system

The somatic body wall muscle of P. pacificus is platymyarian and similar in overall structure to C. elegans (Fig. 5). A basal lamina separates neurons and hypodermis from the body wall muscle. Typical to all nematodes, innervation of P. pacificus body wall muscles occurs through muscle arm processes extending to neurons (Bird and Bird, 1991). In addition to the body wall, non-striated muscles exist in the pharynx and surrounding the egg-laying apparatus and rectum.

Figure 5:

Transverse EM section through the P. pacificus head showing body wall muscles (green) lying against body wall. Scale bar, 1 µm.

10.21307_jofnem-2021-091-f005.jpg

The excretory system

The P. pacificus excretory system appears very similar to the C. elegans excretory system (Fig. 6). It consists of four cells—two excretory glands, a canal cell with bilaterally symmetrical longitudinal processes, and a duct cell. Similar to C. elegans, the P. pacificus CAN neuron travels alongside the canal cell processes (Carstensen et al., 2021). In P. pacificus, ablation of the CAN results in increased dauer formation, whereas in C. elegans ablation of CAN results in death (Mayer et al., 2015; White et al., 1986).

Figure 6:

Transverse TEM micrograph through junction of excretory glands with canal cell and secretory vesicle being released in gland cell ampulla (arrowhead). Scale bars, 1 µm. Source: Ralf Sommer lab, Bumbarger13_2251.

10.21307_jofnem-2021-091-f006.jpg

The coloemocytes

Both C. elegans and P. pacificus adult hermaphrodites contain six large scavenger cells called coelomocytes that sit within the pseudocoelom body cavity (Jungblut and Sommer, 1998). For both species, two of the coelomocytes are generated post-embryonically (Photos et al., 2006).

The alimentary system

The stoma of P. pacificus comprises a cuticular lined cavity. Consistent with many nematodes in the Diplogastridae family, the P. pacificus stoma contains teeth used for predatory feeding of other nematodes (Fig. 7). The morphology of the stoma varies between two morphotypes called eurystomatous and stenostomatous that are specialized for predatory vs. microbial feeding, respectively (Serobyan et al., 2014). The eurystomatous (wide-mouthed) is characterized by a claw-like dorsal tooth and an opposing subventral tooth. The stenostomatous (narrow-mouthed) form has a less prominent triangle-shaped dorsal tooth and lacks the additional subventral tooth. The specific morphotype is determined through environmental conditions (Bento et al., 2010; Serobyan et al., 2013). P. pacificus dauers isolated from beetle hosts in the wild developed exclusively into eurystomatous adults (Renahan et al., 2021). The teeth of P. pacificus are attached to the anterior-most muscles of the pharynx, allowing for movement during feeding. Similar to C. elegans, the cuticle lined stoma is shed during each molt.

Figure 7:

(A) Longitudinal EM through stoma of eurystomatous form with dorsal tooth (arrowheads). The dorsal tooth attaches to pharyngeal muscle (green) and contains an opening for vesicles from the dorsal pharyngeal gland (purple) to be released into the stoma. A subventral tooth (arrow) is seen on the opposite side. Scale bar, 1 µm. (B) Transverse EM micrograph through a euryostomatous stoma showing dorsal tooth (arrowhead) with lumen for dorsal pharyngeal gland secretions. A subventral tooth (arrow) is found in the subventral sector of the stoma. Scale bar, 1 µm. (Image source: Ralf Sommer Lab, Bumbarger13–154.) C,D. DIC comparison of eurystomatous (C) and stenostomatous (D) forms. The eurystomatous form contains an obvious dorsal tooth (arrowhead). (Image source: Erik Ragsdale.)

10.21307_jofnem-2021-091-f007.jpg

Posterior of the stoma, the P. pacificus pharynx is a muscular pump. While similar in gross morphology to the C. elegans pharynx, the P. pacificus pharynx uses a different pumping sequence to ingest food (Chiang et al., 2006). The P. pacificus pharynx lacks both the grinder and two gland cells found in the C. elegans terminal bulb; however, the three remaining gland cells of P. pacificus have evolved to occupy a larger fraction of the terminal bulb volume (Riebesell and Sommer, 2017).

The intestine connects to the posterior end of the pharynx. The lineage and a detailed description of the P. pacificus intestine are not yet available.

The reproductive system

The first genetic analyses of P. pacificus focused on the molecular genetics of vulva formation (Sommer and Sternberg, 1996). Similar to C. elegans, the reproductive system of P. pacificus consists of a somatic gonad, the germ line, and the egg-laying apparatus; however, there is substantial divergence in the number of cells, overall shape, and developmental timing of the reproductive systems between C. elegans and P. pacificus (Kolotuev and Podbilewicz, 2004; Rudel et al., 2005).

Similar to C. elegans, the P. pacificus vulva is formed through a combination of cell division, migration and fusion from three ectoblastic vulval precursor P cells; however, the molecular signal controlling division differs between the species (Sommer and Sternberg, 1996). Following induction, the P cells undergo divisions to form 20 vulval cells (two less than C. elegans) (Kolotuev and Podbilewicz, 2004). The vulval cells migrate to form a stack of rings at the location of the vulva and undergo cell-cell fusion to form stacked toroids. The timing, sequence and number of toroids differs between C. elegans and P. pacificus (Kolotuev and Podbilewicz, 2004).

The gonad of P. pacificus is didelphic comprising two arms converging on a vulva positioned near the center of the body. The somatic gonad consists of a uterus, spermatheca, sheath, and distal tip cells. The germline is a syncytium connected through a central rachis. Several features of the gonad in P. pacificus distinguish it from that in C. elegans (Rudel et al., 2005). Most obviously distinct in the P. pacificus gonad is the pretzel shape of the gonad arms, which extend from the ventral side to the dorsal side and back again (Fig. 8). The sheath cells wrap the proximal oocytes of both species but differ in number between species (4 pairs in P. pacificus, 5 in C. elegans). While both species have sperm storage organs called spermatheca, P. pacificus does not contain the connective uterine-spermatheca valve cells found in C. elegans and differs in number of cells (Rudel et al., 2005).

Figure 8:

P. pacificus young adult hermaphrodite gonad. Unlike in C. elegans, the distal arms of the P. pacificus gonad extend back to the ventral side. Scale bar, 10 µm.

10.21307_jofnem-2021-091-f008.jpg

Acknowledgments

The author wish to thank Dave Hall, Laura Herndon, Cathy Wolkow, Erik Ragsdale, and Ray Hong for providing critical feedback to this review and thanks to Chris Crocker for illustrations. This review is part of the WormAtlas handbook collection, which is funded by NIH OD 010943.

References


  1. Bento, G. , Ogawa, A. and Sommer, R. J. 2010. Co-option of the hormone-signalling module dafachronic acid-DAF-12 in nematode evolution. Nature. 466:494–497.
  2. Bird, A. F. and Bird, J. 1991. The structure of nematodes, 2nd ed., San Diego: Academic Press.
  3. Bumbarger, D. J. and Riebesell, M. 2015. Anatomy and connectivity in the pharyngeal nervous system. In Sommer, R. J. , Hunt, D. J. and Perry, R. N. (Eds), Pristionchus Pacificus-A Nematode Model for Comparative and Evolutionary Biology. Brill, Leiden, pp. 353–383.
  4. Bumbarger, D. J. , Riebesell, M. , Rödelsperger, C. and Sommer, R. J. 2013. System-wide rewiring underlies behavioral differences in predatory and bacterial-feeding nematodes. Cell. 152:109–119.
  5. Carstensen, H. R. , Villalon, R. M. , Banerjee, N. , Hallem, E. A. and Hong, R. L. 2021. Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus. Genetics 218:iyab071.
  6. Chiang, J.- T. A. , Steciuk, M. , Shtonda, B. and Avery, L. 2006. Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes. Journal of Experimental Biology 209:1859–1873.
  7. Cinkornpumin, J. K. , Wisidagama, D. R. , Rapoport, V. , Go, J. L. , Dieterich, C. and Wang, X. 2014. A host beetle pheromone regulates development and behavior in the nematode Pristionchus pacificus . eLife. 3:1–21..
  8. Cook, S. J. , Crouse, C. M. , Yemini, E. , Hall, D. H. , Emmons, S. W. and Hobert, O. 2020. The connectome of the Caenorhabditis elegans pharynx. Journal of Comparative Neurology 528:2767–2784.
  9. Félix, M.- A. , Ailion, M. , Hsu, J.- C. , Richaud, A. and Wang, J. 2018. Pristionchus nematodes occur frequently in diverse rotting vegetal substrates and are not exclusively necromenic, while Panagrellus redivivoides is found specifically in rotting fruits. PLoS ONE 13:e0200851.
  10. Félix, M. A. , Hill, R. J. , Schwarz, H. , Sternberg, P. W. , Sudhaus, W. and Sommer, R. J. 1999. Pristionchus pacificus, a nematode with only three juvenile stages, displays major heterochronic changes relative to Caenorhabditis elegans. Proceedings of the Royal Society of London. Series B: Biological Sciences 266:1617–1621.
  11. Fürst von Lieven, A. 2005. The embryonic moult in diplogastrids (Nematoda) - Homology of developmental stages and heterochrony as a prerequisite for morphological diversity. Zoologischer Anzeiger 244:79–91.
  12. Han, Z. , Boas, S. and Schroeder, N. E. 2016. Unexpected variation in neuroanatomy among diverse nematode species. Frontiers in Neuroanatomy 9, Available at: https://doi.org/10.3389/fnana.2015.00162.
  13. Herrmann, M. , Mayer, W. E. and Sommer, R. J. 2006. Nematodes of the genus Pristionchus are closely associated with scarab beetles and the Colorado potato beetle in Western Europe. Zoology. 109:96–108.
  14. Hong, R. L. and Sommer, R. J. 2006. Pristionchus pacificus: a well-rounded nematode. BioEssays. 28:651–659.
  15. Hong, R. L. , Riebesell, M. , Bumbarger, D. J. , Cook, S. J. , Carstensen, H. R. and Sarpolaki, T. 2019. Evolution of neuronal anatomy and circuitry in two highly divergent nematode species. eLife. 8:e47155.
  16. Jungblut, B. and Sommer, R. J. 1998. The Pristionchus pacificus mab-5 gene is involved in the regulation of ventral epidermal cell fates. Current Biology 8:775–778.
  17. Kenning, C. , Kipping, I. and Sommer, R. J. 2004. Isolation of mutations with dumpy-like phenotypes and of collagen genes in the nematode Pristionchus pacificus . Genesis. 40:176–183.
  18. Kolotuev, I. and Podbilewicz, B. 2004. Pristionchus pacificus vulva formation: Polarized division, cell migration, cell fusion, and evolution of invagination. Developmental Biology 266:322–333.
  19. Loer, C. M. and Rivard, L. 2007. Evolution of neuronal patterning in free-living Rhabditid nematodes I: Sex-specific serotonin-containing neurons. The Journal of Comparative Neurology 502:736–767.
  20. Mayer, M. G. , Rödelsperger, C. , Witte, H. , Riebesell, M. and Sommer, R. J. 2015. The orphan gene dauerless regulates dauer development and intraspecific competition in nematodes by copy number variation. PLoS Genetics 11:1005146.
  21. McGaughran, A. and Morgan, K. 2015. Population genetics and the La Reunion case study. In Sommer, R. J. (Ed.), Pristionchus pacificus-A Nematode Model for Comparative and Evolutionary Biology, Leiden, pp. 197–219.
  22. Morgan, K. , McGaughran, A. , Rödelsperger, C. and Sommer, R. J. 2017. Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing. BMC Evolutionary Biology 17:1–11.
  23. Penkov, S. , Ogawa, A. , Schmidt, U. , Tate, D. , Zagoriy, V. and Boland, S. 2014. A wax ester promotes collective host finding in the nematode Pristionchus pacificus . Nature Chemical Biology 10:281–285.
  24. Photos, A. , Gutierrez, A. and Sommer, R. J. 2006. sem-4/spalt and egl-17/FGF have a conserved role in sex myoblast specification and migration in P. pacificus and C. elegans . Developmental Biology 293:142–153.
  25. Pires da Silva, A. 2013. Pristionchus pacificus protocols. In Sommer, R. J. (Ed.), The C. elegans Research Community, Wormbook.
  26. Ragsdale, E. J. , Kanzaki, N. and Herrmann, M. 2015. Taxonomy and natural history: the genus Pristionchus. In Sommer, R. J. (Eds), Pristionchus pacificus-A Nematode Model for Comparative and Evolutionary Biology. Brill, Leiden, pp. 77–120.
  27. Renahan, T. , Lo, W.- S. , Werner, M. S. , Rochat, J. , Herrmann, M. and Sommer, R. J. 2021. Nematode biphasic ‘boom and bust’ dynamics are dependent on host bacterial load while linking dauer and mouth-form polyphenisms. Environmental Microbiology 23:5102–5113.
  28. Riebesell, M. and Sommer, R. J. 2017. Three-dimensional reconstruction of the pharyngeal gland cells in the predatory nematode Pristionchus pacificus . Journal of Morphology 278:1656–1666.
  29. Rudel, D. , Riebesell, M. and Sommer, R. J. 2005. Gonadogenesis in Pristionchus pacificus and organ evolution: Development, adult morphology and cell-cell interactions in the hermaphrodite gonad. Developmental Biology 277:200–221.
  30. Schlager, B. , Wang, X. , Braach, G. and Sommer, R. J. 2009. Molecular cloning of a dominant roller mutant and establishment of DNA-mediated transformation in the nematode Pristionchus pacificus . Genesis (New York, N.Y.: 2000) 47:300–4.
  31. Serobyan, V. , Ragsdale, E. J. , Müller, M. R. and Sommer, R. J. 2013. Feeding plasticity in the nematode Pristionchus pacificus is influenced by sex and social context and is linked to developmental speed. Evolution & Development 15:161–170.
  32. Serobyan, V. , Ragsdale, E. J. and Sommer, R. J. 2014. Adaptive value of a predatory mouth-form in a dimorphic nematode. Proceedings of the Royal Society B: Biological Sciences 281:20141334.
  33. Sommer, R. J. and Sternberg, P. W. 1996. Apoptosis and change of competence limit the size of the vulva equivalence group in Pristionchus pacificus: a genetic analysis. Current Biology 6:52–59.
  34. Sommer, R. J. , Carta, L. K. , Kim, S. Y. and Sternberg, P. W. 1996. Morphological, genetic and molecular description of Pristionchus pacificus sp. n. (nematoda: neodiplogastridae). Fundamental and Applied Nematology 19:511–521.
  35. Sulston, J. E. and Horvitz, H. R. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans . Developmental Biology 56:110–156.
  36. White, J. G. , Southgate, E. , Thomson, J. N. and Brenner, S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans . Philosophical Transactions of the Royal Society B: Biological Sciences 314:1–340.
XML PDF Share

FIGURES & TABLES

Figure 1:

Pristionchus pacificus (A) and Caenorhabditis elegans (B) adult hermaphrodites have similar sizes and shapes. Scale bar 50 µm.

Full Size   |   Slide (.pptx)

Figure 2:

Life cycle of Pristionchus pacificus. Differential interference contrast images of developmental stages. Development from the two-cell stage to adult takes approximately 72 hrs at 20°C. Each post-embryonic stage is positioned with its left side facing the reader, except the J4, which is facing the right side. Scale bar, 50 µm.

Full Size   |   Slide (.pptx)

Figure 3:

Unhatched J2. The presence of a shed J1 cuticle (arrowhead) is indicative of the J1 to J2 molt occurring prior to hatching. Scale bar, 10 µm.

Full Size   |   Slide (.pptx)

Figure 4:

(A) The cuticle of P. pacificus contains longitudinal stippled lines around the circumference of the animal. Scale bar, 10 µm. (B) In an EM cross section, this stippling can be seen as waves around the animal (arrowheads). Scale bar, 1 µm. Image source: Ralf Sommer Lab, Bumbarger13–1301. (C, D) The cuticle of P. pacificus is interrupted by epithelial gland cell pores. In DIC (C), the small gland cell pores (arrow) are occasionally visible both dorsal and ventral of the midline (deirid, arrowhead). Scale bar, 10 µm. In EM cross sections (D), the epithelial gland cell (purple) is surrounded by the hypodermis. Scale bar, 1 µm. Image Source: Ralf Sommer, Bumbarger14–1955.

Full Size   |   Slide (.pptx)

Figure 5:

Transverse EM section through the P. pacificus head showing body wall muscles (green) lying against body wall. Scale bar, 1 µm.

Full Size   |   Slide (.pptx)

Figure 6:

Transverse TEM micrograph through junction of excretory glands with canal cell and secretory vesicle being released in gland cell ampulla (arrowhead). Scale bars, 1 µm. Source: Ralf Sommer lab, Bumbarger13_2251.

Full Size   |   Slide (.pptx)

Figure 7:

(A) Longitudinal EM through stoma of eurystomatous form with dorsal tooth (arrowheads). The dorsal tooth attaches to pharyngeal muscle (green) and contains an opening for vesicles from the dorsal pharyngeal gland (purple) to be released into the stoma. A subventral tooth (arrow) is seen on the opposite side. Scale bar, 1 µm. (B) Transverse EM micrograph through a euryostomatous stoma showing dorsal tooth (arrowhead) with lumen for dorsal pharyngeal gland secretions. A subventral tooth (arrow) is found in the subventral sector of the stoma. Scale bar, 1 µm. (Image source: Ralf Sommer Lab, Bumbarger13–154.) C,D. DIC comparison of eurystomatous (C) and stenostomatous (D) forms. The eurystomatous form contains an obvious dorsal tooth (arrowhead). (Image source: Erik Ragsdale.)

Full Size   |   Slide (.pptx)

Figure 8:

P. pacificus young adult hermaphrodite gonad. Unlike in C. elegans, the distal arms of the P. pacificus gonad extend back to the ventral side. Scale bar, 10 µm.

Full Size   |   Slide (.pptx)

REFERENCES

  1. Bento, G. , Ogawa, A. and Sommer, R. J. 2010. Co-option of the hormone-signalling module dafachronic acid-DAF-12 in nematode evolution. Nature. 466:494–497.
  2. Bird, A. F. and Bird, J. 1991. The structure of nematodes, 2nd ed., San Diego: Academic Press.
  3. Bumbarger, D. J. and Riebesell, M. 2015. Anatomy and connectivity in the pharyngeal nervous system. In Sommer, R. J. , Hunt, D. J. and Perry, R. N. (Eds), Pristionchus Pacificus-A Nematode Model for Comparative and Evolutionary Biology. Brill, Leiden, pp. 353–383.
  4. Bumbarger, D. J. , Riebesell, M. , Rödelsperger, C. and Sommer, R. J. 2013. System-wide rewiring underlies behavioral differences in predatory and bacterial-feeding nematodes. Cell. 152:109–119.
  5. Carstensen, H. R. , Villalon, R. M. , Banerjee, N. , Hallem, E. A. and Hong, R. L. 2021. Steroid hormone pathways coordinate developmental diapause and olfactory remodeling in Pristionchus pacificus. Genetics 218:iyab071.
  6. Chiang, J.- T. A. , Steciuk, M. , Shtonda, B. and Avery, L. 2006. Evolution of pharyngeal behaviors and neuronal functions in free-living soil nematodes. Journal of Experimental Biology 209:1859–1873.
  7. Cinkornpumin, J. K. , Wisidagama, D. R. , Rapoport, V. , Go, J. L. , Dieterich, C. and Wang, X. 2014. A host beetle pheromone regulates development and behavior in the nematode Pristionchus pacificus . eLife. 3:1–21..
  8. Cook, S. J. , Crouse, C. M. , Yemini, E. , Hall, D. H. , Emmons, S. W. and Hobert, O. 2020. The connectome of the Caenorhabditis elegans pharynx. Journal of Comparative Neurology 528:2767–2784.
  9. Félix, M.- A. , Ailion, M. , Hsu, J.- C. , Richaud, A. and Wang, J. 2018. Pristionchus nematodes occur frequently in diverse rotting vegetal substrates and are not exclusively necromenic, while Panagrellus redivivoides is found specifically in rotting fruits. PLoS ONE 13:e0200851.
  10. Félix, M. A. , Hill, R. J. , Schwarz, H. , Sternberg, P. W. , Sudhaus, W. and Sommer, R. J. 1999. Pristionchus pacificus, a nematode with only three juvenile stages, displays major heterochronic changes relative to Caenorhabditis elegans. Proceedings of the Royal Society of London. Series B: Biological Sciences 266:1617–1621.
  11. Fürst von Lieven, A. 2005. The embryonic moult in diplogastrids (Nematoda) - Homology of developmental stages and heterochrony as a prerequisite for morphological diversity. Zoologischer Anzeiger 244:79–91.
  12. Han, Z. , Boas, S. and Schroeder, N. E. 2016. Unexpected variation in neuroanatomy among diverse nematode species. Frontiers in Neuroanatomy 9, Available at: https://doi.org/10.3389/fnana.2015.00162.
  13. Herrmann, M. , Mayer, W. E. and Sommer, R. J. 2006. Nematodes of the genus Pristionchus are closely associated with scarab beetles and the Colorado potato beetle in Western Europe. Zoology. 109:96–108.
  14. Hong, R. L. and Sommer, R. J. 2006. Pristionchus pacificus: a well-rounded nematode. BioEssays. 28:651–659.
  15. Hong, R. L. , Riebesell, M. , Bumbarger, D. J. , Cook, S. J. , Carstensen, H. R. and Sarpolaki, T. 2019. Evolution of neuronal anatomy and circuitry in two highly divergent nematode species. eLife. 8:e47155.
  16. Jungblut, B. and Sommer, R. J. 1998. The Pristionchus pacificus mab-5 gene is involved in the regulation of ventral epidermal cell fates. Current Biology 8:775–778.
  17. Kenning, C. , Kipping, I. and Sommer, R. J. 2004. Isolation of mutations with dumpy-like phenotypes and of collagen genes in the nematode Pristionchus pacificus . Genesis. 40:176–183.
  18. Kolotuev, I. and Podbilewicz, B. 2004. Pristionchus pacificus vulva formation: Polarized division, cell migration, cell fusion, and evolution of invagination. Developmental Biology 266:322–333.
  19. Loer, C. M. and Rivard, L. 2007. Evolution of neuronal patterning in free-living Rhabditid nematodes I: Sex-specific serotonin-containing neurons. The Journal of Comparative Neurology 502:736–767.
  20. Mayer, M. G. , Rödelsperger, C. , Witte, H. , Riebesell, M. and Sommer, R. J. 2015. The orphan gene dauerless regulates dauer development and intraspecific competition in nematodes by copy number variation. PLoS Genetics 11:1005146.
  21. McGaughran, A. and Morgan, K. 2015. Population genetics and the La Reunion case study. In Sommer, R. J. (Ed.), Pristionchus pacificus-A Nematode Model for Comparative and Evolutionary Biology, Leiden, pp. 197–219.
  22. Morgan, K. , McGaughran, A. , Rödelsperger, C. and Sommer, R. J. 2017. Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing. BMC Evolutionary Biology 17:1–11.
  23. Penkov, S. , Ogawa, A. , Schmidt, U. , Tate, D. , Zagoriy, V. and Boland, S. 2014. A wax ester promotes collective host finding in the nematode Pristionchus pacificus . Nature Chemical Biology 10:281–285.
  24. Photos, A. , Gutierrez, A. and Sommer, R. J. 2006. sem-4/spalt and egl-17/FGF have a conserved role in sex myoblast specification and migration in P. pacificus and C. elegans . Developmental Biology 293:142–153.
  25. Pires da Silva, A. 2013. Pristionchus pacificus protocols. In Sommer, R. J. (Ed.), The C. elegans Research Community, Wormbook.
  26. Ragsdale, E. J. , Kanzaki, N. and Herrmann, M. 2015. Taxonomy and natural history: the genus Pristionchus. In Sommer, R. J. (Eds), Pristionchus pacificus-A Nematode Model for Comparative and Evolutionary Biology. Brill, Leiden, pp. 77–120.
  27. Renahan, T. , Lo, W.- S. , Werner, M. S. , Rochat, J. , Herrmann, M. and Sommer, R. J. 2021. Nematode biphasic ‘boom and bust’ dynamics are dependent on host bacterial load while linking dauer and mouth-form polyphenisms. Environmental Microbiology 23:5102–5113.
  28. Riebesell, M. and Sommer, R. J. 2017. Three-dimensional reconstruction of the pharyngeal gland cells in the predatory nematode Pristionchus pacificus . Journal of Morphology 278:1656–1666.
  29. Rudel, D. , Riebesell, M. and Sommer, R. J. 2005. Gonadogenesis in Pristionchus pacificus and organ evolution: Development, adult morphology and cell-cell interactions in the hermaphrodite gonad. Developmental Biology 277:200–221.
  30. Schlager, B. , Wang, X. , Braach, G. and Sommer, R. J. 2009. Molecular cloning of a dominant roller mutant and establishment of DNA-mediated transformation in the nematode Pristionchus pacificus . Genesis (New York, N.Y.: 2000) 47:300–4.
  31. Serobyan, V. , Ragsdale, E. J. , Müller, M. R. and Sommer, R. J. 2013. Feeding plasticity in the nematode Pristionchus pacificus is influenced by sex and social context and is linked to developmental speed. Evolution & Development 15:161–170.
  32. Serobyan, V. , Ragsdale, E. J. and Sommer, R. J. 2014. Adaptive value of a predatory mouth-form in a dimorphic nematode. Proceedings of the Royal Society B: Biological Sciences 281:20141334.
  33. Sommer, R. J. and Sternberg, P. W. 1996. Apoptosis and change of competence limit the size of the vulva equivalence group in Pristionchus pacificus: a genetic analysis. Current Biology 6:52–59.
  34. Sommer, R. J. , Carta, L. K. , Kim, S. Y. and Sternberg, P. W. 1996. Morphological, genetic and molecular description of Pristionchus pacificus sp. n. (nematoda: neodiplogastridae). Fundamental and Applied Nematology 19:511–521.
  35. Sulston, J. E. and Horvitz, H. R. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans . Developmental Biology 56:110–156.
  36. White, J. G. , Southgate, E. , Thomson, J. N. and Brenner, S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans . Philosophical Transactions of the Royal Society B: Biological Sciences 314:1–340.

EXTRA FILES

COMMENTS